Abstract

The use of a focused laser beam to create a sub-micron hole in the plasma membrane of a cell (photoporation), for the selective introduction of membrane impermeable substances (optical injection) including nucleic acids (optical transfection), is a powerful technique most commonly applied to treat single cells. However, particularly for femtosecond photoporation, these studies have been limited to low throughput, small-scale studies, because they require sequential dosing of individual cells. Herein, we describe a microfluidic photoporation system for increased throughput and automated optical injection of cells. Hydrodynamic focusing is employed to direct a flow of single-file cells through a focused femtosecond laser beam for photoporation. Upon traversing the beam, a number of transient pores potentially open across the extracellular membrane, which allows the uptake of the surrounding fluid media into the cytoplasm, also containing the chosen injection agent. The process is entirely automated and a rate of 1 cell/sec could readily be obtained, enabling several thousand cells to be injected per hour using this system. The efficiency of optically injecting propidium iodide into HEK293 mammalian cells was found to be 42 ± 8%, or 28 ± 4% taking into account the requirement of post-injection viability, as tested using Calcein AM. This work now opens the way for combining photoporation with microfluidic analyses, sorting, purification or on-chip cell culture studies.

© 2010 OSA

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  2. L. Paterson, B. Agate, M. Comrie, R. Ferguson, T. K. Lake, J. E. Morris, A. E. Carruthers, C. T. A. Brown, W. Sibbett, P. E. Bryant, F. Gunn-Moore, A. C. Riches, and K. Dholakia, “Photoporation and cell transfection using a violet diode laser,” Opt. Express 13(2), 595–600 (2005).
  3. M. L. Torres-Mapa, L. Angus, M. Ploschner, K. Dholakia, and F. J. Gunn-Moore, “Transient transfection of mammalian cells using a violet diode laser,” J. Biomed. Opt. 15(4), 041506 (2010).
  4. H. Schneckenburger, A. Hendinger, R. Sailer, W. S. L. Strauss, and M. Schmitt, “Laser-assisted optoporation of single cells,” J. Biomed. Opt. 7(3), 410–416 (2002).
  5. A. V. Nikolskaya, V. P. Nikolski, and I. R. Efimov, “Gene printer: laser-scanning targeted transfection of cultured cardiac neonatal rat cells,” Cell Commun. Adhes. 13(4), 217–222 (2006).
  6. G. Palumbo, M. Caruso, E. Crescenzi, M. F. Tecce, G. Roberti, and A. Colasanti, “Targeted gene transfer in eucaryotic cells by dye-assisted laser optoporation,” J. Photochem. Photobiol. B 36(1), 41–46 (1996).
  7. I. B. Clark, E. G. Hanania, J. Stevens, M. Gallina, A. Fieck, R. Brandes, B. O. Palsson, and M. R. Koller, “Optoinjection for efficient targeted delivery of a broad range of compounds and macromolecules into diverse cell types,” J. Biomed. Opt. 11(1), 014034 (2006).
  8. T. Knoll, L. Trojan, S. Langbein, S. Sagi, P. Alken, and M. S. Michel, “Impact of holmium:YAG and neodymium:YAG lasers on the efficacy of DNA delivery in transitional cell carcinoma,” Lasers Med. Sci. 19(1), 33–36 (2004).
  9. H. Schinkel, P. Jacobs, S. Schillberg, and M. Wehner, “Infrared picosecond laser for perforation of single plant cells,” Biotechnol. Bioeng. 99(1), 244–248 (2008).
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  12. M. Lei, H. Xu, H. Yang, and B. Yao, “Femtosecond laser-assisted microinjection into living neurons,” J. Neurosci. Methods 174(2), 215–218 (2008).
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  18. A. Uchugonova, K. König, R. Bueckle, A. Isemann, and G. Tempea, “Targeted transfection of stem cells with sub-20 femtosecond laser pulses,” Opt. Express 16(13), 9357–9364 (2008).
  19. A. Yamaguchi, Y. Hosokawa, G. Louit, T. Asahi, C. Shukunami, Y. Hiraki, and H. Masuhara, “Nanoparticle injection to single animal cells using femtosecond laser-induced impulsive force,” Adv. Mater. (Deerfield Beach Fla.) 93, 39–43 (2008).
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  27. T. Cizmár, V. Kollárová, X. Tsampoula, F. Gunn-Moore, W. Sibbett, Z. Bouchal, and K. Dholakia, “Generation of multiple Bessel beams for a biophotonics workstation,” Opt. Express 16(18), 14024–14035 (2008).
  28. A. Noori, P. R. Selvaganapathy, and J. Wilson, “Microinjection in a microfluidic format using flexible and compliant channels and electroosmotic dosage control,” Lab Chip 9(22), 3202–3211 (2009).
  29. A. Adamo and K. F. Jensen, “Microfluidic based single cell microinjection,” Lab Chip 8(8), 1258–1261 (2008).
  30. N. Bao, Y. Zhan, and C. Lu, “Microfluidic electroporative flow cytometry for studying single-cell biomechanics,” Anal. Chem. 80(20), 7714–7719 (2008).
  31. J. Wang, M. J. Stine, and C. Lu, “Microfluidic cell electroporation using a mechanical valve,” Anal. Chem. 79(24), 9584–9587 (2007).
  32. Y. Zhan, J. Wang, N. Bao, and C. Lu, “Electroporation of cells in microfluidic droplets,” Anal. Chem. 81(5), 2027–2031 (2009).
  33. T. Zhu, C. Luo, J. Huang, C. Xiong, Q. Ouyang, and J. Fang, “Electroporation based on hydrodynamic focusing of microfluidics with low dc voltage,” Biomed. Microdevices 12(1), 35–40 (2010).
  34. R. Ziv, Y. Steinhardt, G. Pelled, D. Gazit, and B. Rubinsky, “Micro-electroporation of mesenchymal stem cells with alternating electrical current pulses,” Biomed. Microdevices 11(1), 95–101 (2009).
  35. E. Neumann, M. Schaefer-Ridder, Y. Wang, and P. H. Hofschneider, “Gene transfer into mouse lyoma cells by electroporation in high electric fields,” EMBO J. 1(7), 841–845 (1982).
  36. J. A. Wolff, R. W. Malone, P. Williams, W. Chong, G. Acsadi, A. Jani, and P. L. Felgner, “Direct gene transfer into mouse muscle in vivo,” Science 247(4949 Pt 1), 1465–1468 (1990).
  37. N. S. Yang, J. Burkholder, B. Roberts, B. Martinell, and D. McCabe, “In vivo and in vitro gene transfer to mammalian somatic cells by particle bombardment,” Proc. Natl. Acad. Sci. U.S.A. 87(24), 9568–9572 (1990).
  38. P. L. Felgner, T. R. Gadek, M. Holm, R. Roman, H. W. Chan, M. Wenz, J. P. Northrop, G. M. Ringold, and M. Danielsen, “Lipofection: a highly efficient, lipid-mediated DNA-transfection procedure,” Proc. Natl. Acad. Sci. U.S.A. 84(21), 7413–7417 (1987).
  39. K. L. Douglas, “Toward development of artificial viruses for gene therapy: a comparative evaluation of viral and non-viral transfection,” Biotechnol. Prog. 24(4), 871–883 (2008).
  40. M. M. Wang, E. Tu, D. E. Raymond, J. M. Yang, H. Zhang, N. Hagen, B. Dees, E. M. Mercer, A. H. Forster, I. Kariv, P. J. Marchand, and W. F. Butler, “Microfluidic sorting of mammalian cells by optical force switching,” Nat. Biotechnol. 23(1), 83–87 (2005).
  41. A. Y. Lau, L. P. Lee, and J. W. Chan, “An integrated optofluidic platform for Raman-activated cell sorting,” Lab Chip 8(7), 1116–1120 (2008).
  42. R. F. Marchington, M. Mazilu, S. Kuriakose, V. Garcés-Chávez, P. J. Reece, T. F. Krauss, M. Gu, and K. Dholakia, “Optical deflection and sorting of microparticles in a near-field optical geometry,” Opt. Express 16(6), 3712–3726 (2008).
  43. K. Dholakia, W. M. Lee, L. Paterson, M. P. Macdonald, R. Mcdonald, I. Andreev, P. Mthunzi, C. T. A. Brown, R. F. Marchington, and A. C. Riches, “Optical separation of cells on potential energy landscapes: enhancement with dielectric tagging,” IEEE J. Sel. Top. Quantum Electron. 13(6), 1646–1654 (2007).
  44. J. C. McDonald and G. M. Whitesides, “Poly(dimethylsiloxane) as a material for fabricating microfluidic devices,” Acc. Chem. Res. 35(7), 491–499 (2002).
  45. K. Haubert, T. Drier, and D. Beebe, “PDMS bonding by means of a portable, low-cost corona system,” Lab Chip 6(12), 1548–1549 (2006).
  46. G.-B. Lee, C.-C. Chang, S.-B. Huang, and R.-J. Yang, “The hydrodynamic focusing effect inside rectangular microchannels,” J. Micromech. Microeng. 16(5), 1024–1032 (2006).
  47. C. M. Pitsillides, E. K. Joe, X. Wei, R. R. Anderson, and C. P. Lin, “Selective cell targeting with light-absorbing microparticles and nanoparticles,” Biophys. J. 84(6), 4023–4032 (2003).
  48. W. M. Lee, P. J. Reece, R. F. Marchington, N. K. Metzger, and K. Dholakia, “Construction and calibration of an optical trap on a fluorescence optical microscope,” Nat. Protoc. 2(12), 3226–3238 (2007).
  49. P. B. Howell, J. P. Golden, L. R. Hilliard, J. S. Erickson, D. R. Mott, and F. S. Ligler, “Two simple and rugged designs for creating microfluidic sheath flow,” Lab Chip 8(7), 1097–1103 (2008).

2010 (3)

M. L. Torres-Mapa, L. Angus, M. Ploschner, K. Dholakia, and F. J. Gunn-Moore, “Transient transfection of mammalian cells using a violet diode laser,” J. Biomed. Opt. 15(4), 041506 (2010).

P. Mthunzi, K. Dholakia, and F. Gunn-Moore, “Photo-transfection of mammalian cells using femtosecond laser pulses: optimisation and applicability to stem cell differentiation,” J. Biomed. Opt. 15(4), 041507 (2010).

T. Zhu, C. Luo, J. Huang, C. Xiong, Q. Ouyang, and J. Fang, “Electroporation based on hydrodynamic focusing of microfluidics with low dc voltage,” Biomed. Microdevices 12(1), 35–40 (2010).

2009 (4)

R. Ziv, Y. Steinhardt, G. Pelled, D. Gazit, and B. Rubinsky, “Micro-electroporation of mesenchymal stem cells with alternating electrical current pulses,” Biomed. Microdevices 11(1), 95–101 (2009).

A. Noori, P. R. Selvaganapathy, and J. Wilson, “Microinjection in a microfluidic format using flexible and compliant channels and electroosmotic dosage control,” Lab Chip 9(22), 3202–3211 (2009).

C. McDougall, D. J. Stevenson, C. T. A. Brown, F. Gunn-Moore, and K. Dholakia, “Targeted optical injection of gold nanoparticles into single mammalian cells,” J Biophotonics 2(12), 736–743 (2009).

Y. Zhan, J. Wang, N. Bao, and C. Lu, “Electroporation of cells in microfluidic droplets,” Anal. Chem. 81(5), 2027–2031 (2009).

2008 (15)

P. B. Howell, J. P. Golden, L. R. Hilliard, J. S. Erickson, D. R. Mott, and F. S. Ligler, “Two simple and rugged designs for creating microfluidic sheath flow,” Lab Chip 8(7), 1097–1103 (2008).

A. Y. Lau, L. P. Lee, and J. W. Chan, “An integrated optofluidic platform for Raman-activated cell sorting,” Lab Chip 8(7), 1116–1120 (2008).

R. F. Marchington, M. Mazilu, S. Kuriakose, V. Garcés-Chávez, P. J. Reece, T. F. Krauss, M. Gu, and K. Dholakia, “Optical deflection and sorting of microparticles in a near-field optical geometry,” Opt. Express 16(6), 3712–3726 (2008).

K. L. Douglas, “Toward development of artificial viruses for gene therapy: a comparative evaluation of viral and non-viral transfection,” Biotechnol. Prog. 24(4), 871–883 (2008).

J. Baumgart, W. Bintig, A. Ngezahayo, S. Willenbrock, H. Murua Escobar, W. Ertmer, H. Lubatschowski, and A. Heisterkamp, “Quantified femtosecond laser based opto-perforation of living GFSHR-17 and MTH53 a cells,” Opt. Express 16(5), 3021–3031 (2008).

X. Tsampoula, K. Taguchi, T. Cizmár, V. Garces-Chavez, N. Ma, S. Mohanty, K. Mohanty, F. Gunn-Moore, and K. Dholakia, “Fibre based cellular transfection,” Opt. Express 16(21), 17007–17013 (2008).

A. Uchugonova, K. König, R. Bueckle, A. Isemann, and G. Tempea, “Targeted transfection of stem cells with sub-20 femtosecond laser pulses,” Opt. Express 16(13), 9357–9364 (2008).

A. Yamaguchi, Y. Hosokawa, G. Louit, T. Asahi, C. Shukunami, Y. Hiraki, and H. Masuhara, “Nanoparticle injection to single animal cells using femtosecond laser-induced impulsive force,” Adv. Mater. (Deerfield Beach Fla.) 93, 39–43 (2008).

A. Vogel, N. Linz, S. Freidank, and G. U. Paltauf, “Femtosecond-laser-induced nanocavitation in water: implications for optical breakdown threshold and cell surgery,” Phys. Rev. Lett. 100(3), 038102 (2008).

T. Cizmár, V. Kollárová, X. Tsampoula, F. Gunn-Moore, W. Sibbett, Z. Bouchal, and K. Dholakia, “Generation of multiple Bessel beams for a biophotonics workstation,” Opt. Express 16(18), 14024–14035 (2008).

A. Adamo and K. F. Jensen, “Microfluidic based single cell microinjection,” Lab Chip 8(8), 1258–1261 (2008).

N. Bao, Y. Zhan, and C. Lu, “Microfluidic electroporative flow cytometry for studying single-cell biomechanics,” Anal. Chem. 80(20), 7714–7719 (2008).

H. Schinkel, P. Jacobs, S. Schillberg, and M. Wehner, “Infrared picosecond laser for perforation of single plant cells,” Biotechnol. Bioeng. 99(1), 244–248 (2008).

C. T. A. Brown, D. J. Stevenson, X. Tsampoula, C. McDougall, A. A. Lagatsky, W. Sibbett, F. J. Gunn-Moore, and K. Dholakia, “Enhanced operation of femtosecond lasers and applications in cell transfection,” J Biophotonics 1(3), 183–199 (2008).

M. Lei, H. Xu, H. Yang, and B. Yao, “Femtosecond laser-assisted microinjection into living neurons,” J. Neurosci. Methods 174(2), 215–218 (2008).

2007 (5)

X. Tsampoula, V. Garces-Chavez, M. Comrie, D. J. Stevenson, B. Agate, C. T. A. Brown, F. Gunn-Moore, and K. Dholakia, “Femtosecond cellular transfection using a nondiffracting light beam,” Appl. Phys. Lett. 91(5), 053902–053903 (2007).

C. Peng, R. E. Palazzo, and I. Wilke, “Laser intensity dependence of femtosecond near-infrared optoinjection,” Phys. Rev. E Stat. Nonlin. Soft Matter Phys. 75(4 Pt 1), 041903 (2007).

J. Wang, M. J. Stine, and C. Lu, “Microfluidic cell electroporation using a mechanical valve,” Anal. Chem. 79(24), 9584–9587 (2007).

K. Dholakia, W. M. Lee, L. Paterson, M. P. Macdonald, R. Mcdonald, I. Andreev, P. Mthunzi, C. T. A. Brown, R. F. Marchington, and A. C. Riches, “Optical separation of cells on potential energy landscapes: enhancement with dielectric tagging,” IEEE J. Sel. Top. Quantum Electron. 13(6), 1646–1654 (2007).

W. M. Lee, P. J. Reece, R. F. Marchington, N. K. Metzger, and K. Dholakia, “Construction and calibration of an optical trap on a fluorescence optical microscope,” Nat. Protoc. 2(12), 3226–3238 (2007).

2006 (6)

K. Haubert, T. Drier, and D. Beebe, “PDMS bonding by means of a portable, low-cost corona system,” Lab Chip 6(12), 1548–1549 (2006).

G.-B. Lee, C.-C. Chang, S.-B. Huang, and R.-J. Yang, “The hydrodynamic focusing effect inside rectangular microchannels,” J. Micromech. Microeng. 16(5), 1024–1032 (2006).

D. Stevenson, B. Agate, X. Tsampoula, P. Fischer, C. T. A. Brown, W. Sibbett, A. Riches, F. Gunn-Moore, and K. Dholakia, “Femtosecond optical transfection of cells: viability and efficiency,” Opt. Express 14(16), 7125–7133 (2006).

L. E. Barrett, J. Y. Sul, H. Takano, E. J. Van Bockstaele, P. G. Haydon, and J. H. Eberwine, “Region-directed phototransfection reveals the functional significance of a dendritically synthesized transcription factor,” Nat. Methods 3(6), 455–460 (2006).

A. V. Nikolskaya, V. P. Nikolski, and I. R. Efimov, “Gene printer: laser-scanning targeted transfection of cultured cardiac neonatal rat cells,” Cell Commun. Adhes. 13(4), 217–222 (2006).

I. B. Clark, E. G. Hanania, J. Stevens, M. Gallina, A. Fieck, R. Brandes, B. O. Palsson, and M. R. Koller, “Optoinjection for efficient targeted delivery of a broad range of compounds and macromolecules into diverse cell types,” J. Biomed. Opt. 11(1), 014034 (2006).

2005 (2)

L. Paterson, B. Agate, M. Comrie, R. Ferguson, T. K. Lake, J. E. Morris, A. E. Carruthers, C. T. A. Brown, W. Sibbett, P. E. Bryant, F. Gunn-Moore, A. C. Riches, and K. Dholakia, “Photoporation and cell transfection using a violet diode laser,” Opt. Express 13(2), 595–600 (2005).

M. M. Wang, E. Tu, D. E. Raymond, J. M. Yang, H. Zhang, N. Hagen, B. Dees, E. M. Mercer, A. H. Forster, I. Kariv, P. J. Marchand, and W. F. Butler, “Microfluidic sorting of mammalian cells by optical force switching,” Nat. Biotechnol. 23(1), 83–87 (2005).

2004 (1)

T. Knoll, L. Trojan, S. Langbein, S. Sagi, P. Alken, and M. S. Michel, “Impact of holmium:YAG and neodymium:YAG lasers on the efficacy of DNA delivery in transitional cell carcinoma,” Lasers Med. Sci. 19(1), 33–36 (2004).

2003 (3)

E. Zeira, A. Manevitch, A. Khatchatouriants, O. Pappo, E. Hyam, M. Darash-Yahana, E. Tavor, A. Honigman, A. Lewis, and E. Galun, “Femtosecond infrared laser-an efficient and safe in vivo gene delivery system for prolonged expression,” Mol. Ther. 8(2), 342–350 (2003).

S. Sagi, T. Knoll, L. Trojan, A. Schaaf, P. Alken, and M. S. Michel, “Gene delivery into prostate cancer cells by holmium laser application,” Prostate Cancer Prostatic Dis. 6(2), 127–130 (2003).

C. M. Pitsillides, E. K. Joe, X. Wei, R. R. Anderson, and C. P. Lin, “Selective cell targeting with light-absorbing microparticles and nanoparticles,” Biophys. J. 84(6), 4023–4032 (2003).

2002 (3)

J. C. McDonald and G. M. Whitesides, “Poly(dimethylsiloxane) as a material for fabricating microfluidic devices,” Acc. Chem. Res. 35(7), 491–499 (2002).

H. Schneckenburger, A. Hendinger, R. Sailer, W. S. L. Strauss, and M. Schmitt, “Laser-assisted optoporation of single cells,” J. Biomed. Opt. 7(3), 410–416 (2002).

U. K. Tirlapur and K. König, “Targeted transfection by femtosecond laser,” Nature 418(6895), 290–291 (2002).

1996 (1)

G. Palumbo, M. Caruso, E. Crescenzi, M. F. Tecce, G. Roberti, and A. Colasanti, “Targeted gene transfer in eucaryotic cells by dye-assisted laser optoporation,” J. Photochem. Photobiol. B 36(1), 41–46 (1996).

1990 (2)

J. A. Wolff, R. W. Malone, P. Williams, W. Chong, G. Acsadi, A. Jani, and P. L. Felgner, “Direct gene transfer into mouse muscle in vivo,” Science 247(4949 Pt 1), 1465–1468 (1990).

N. S. Yang, J. Burkholder, B. Roberts, B. Martinell, and D. McCabe, “In vivo and in vitro gene transfer to mammalian somatic cells by particle bombardment,” Proc. Natl. Acad. Sci. U.S.A. 87(24), 9568–9572 (1990).

1987 (1)

P. L. Felgner, T. R. Gadek, M. Holm, R. Roman, H. W. Chan, M. Wenz, J. P. Northrop, G. M. Ringold, and M. Danielsen, “Lipofection: a highly efficient, lipid-mediated DNA-transfection procedure,” Proc. Natl. Acad. Sci. U.S.A. 84(21), 7413–7417 (1987).

1984 (1)

M. Tsukakoshi, S. Kurata, Y. Nomiya, Y. Ikawa, and T. Kasuya, “A novel method of DNA transfection by laser microbeam cell surgery,” Appl. Phys. B 35(3), 135–140 (1984).

1982 (1)

E. Neumann, M. Schaefer-Ridder, Y. Wang, and P. H. Hofschneider, “Gene transfer into mouse lyoma cells by electroporation in high electric fields,” EMBO J. 1(7), 841–845 (1982).

Acsadi, G.

J. A. Wolff, R. W. Malone, P. Williams, W. Chong, G. Acsadi, A. Jani, and P. L. Felgner, “Direct gene transfer into mouse muscle in vivo,” Science 247(4949 Pt 1), 1465–1468 (1990).

Adamo, A.

A. Adamo and K. F. Jensen, “Microfluidic based single cell microinjection,” Lab Chip 8(8), 1258–1261 (2008).

Agate, B.

Alken, P.

T. Knoll, L. Trojan, S. Langbein, S. Sagi, P. Alken, and M. S. Michel, “Impact of holmium:YAG and neodymium:YAG lasers on the efficacy of DNA delivery in transitional cell carcinoma,” Lasers Med. Sci. 19(1), 33–36 (2004).

S. Sagi, T. Knoll, L. Trojan, A. Schaaf, P. Alken, and M. S. Michel, “Gene delivery into prostate cancer cells by holmium laser application,” Prostate Cancer Prostatic Dis. 6(2), 127–130 (2003).

Anderson, R. R.

C. M. Pitsillides, E. K. Joe, X. Wei, R. R. Anderson, and C. P. Lin, “Selective cell targeting with light-absorbing microparticles and nanoparticles,” Biophys. J. 84(6), 4023–4032 (2003).

Andreev, I.

K. Dholakia, W. M. Lee, L. Paterson, M. P. Macdonald, R. Mcdonald, I. Andreev, P. Mthunzi, C. T. A. Brown, R. F. Marchington, and A. C. Riches, “Optical separation of cells on potential energy landscapes: enhancement with dielectric tagging,” IEEE J. Sel. Top. Quantum Electron. 13(6), 1646–1654 (2007).

Angus, L.

M. L. Torres-Mapa, L. Angus, M. Ploschner, K. Dholakia, and F. J. Gunn-Moore, “Transient transfection of mammalian cells using a violet diode laser,” J. Biomed. Opt. 15(4), 041506 (2010).

Asahi, T.

A. Yamaguchi, Y. Hosokawa, G. Louit, T. Asahi, C. Shukunami, Y. Hiraki, and H. Masuhara, “Nanoparticle injection to single animal cells using femtosecond laser-induced impulsive force,” Adv. Mater. (Deerfield Beach Fla.) 93, 39–43 (2008).

Bao, N.

Y. Zhan, J. Wang, N. Bao, and C. Lu, “Electroporation of cells in microfluidic droplets,” Anal. Chem. 81(5), 2027–2031 (2009).

N. Bao, Y. Zhan, and C. Lu, “Microfluidic electroporative flow cytometry for studying single-cell biomechanics,” Anal. Chem. 80(20), 7714–7719 (2008).

Barrett, L. E.

L. E. Barrett, J. Y. Sul, H. Takano, E. J. Van Bockstaele, P. G. Haydon, and J. H. Eberwine, “Region-directed phototransfection reveals the functional significance of a dendritically synthesized transcription factor,” Nat. Methods 3(6), 455–460 (2006).

Baumgart, J.

Beebe, D.

K. Haubert, T. Drier, and D. Beebe, “PDMS bonding by means of a portable, low-cost corona system,” Lab Chip 6(12), 1548–1549 (2006).

Bintig, W.

Bouchal, Z.

Brandes, R.

I. B. Clark, E. G. Hanania, J. Stevens, M. Gallina, A. Fieck, R. Brandes, B. O. Palsson, and M. R. Koller, “Optoinjection for efficient targeted delivery of a broad range of compounds and macromolecules into diverse cell types,” J. Biomed. Opt. 11(1), 014034 (2006).

Brown, C. T. A.

C. McDougall, D. J. Stevenson, C. T. A. Brown, F. Gunn-Moore, and K. Dholakia, “Targeted optical injection of gold nanoparticles into single mammalian cells,” J Biophotonics 2(12), 736–743 (2009).

C. T. A. Brown, D. J. Stevenson, X. Tsampoula, C. McDougall, A. A. Lagatsky, W. Sibbett, F. J. Gunn-Moore, and K. Dholakia, “Enhanced operation of femtosecond lasers and applications in cell transfection,” J Biophotonics 1(3), 183–199 (2008).

K. Dholakia, W. M. Lee, L. Paterson, M. P. Macdonald, R. Mcdonald, I. Andreev, P. Mthunzi, C. T. A. Brown, R. F. Marchington, and A. C. Riches, “Optical separation of cells on potential energy landscapes: enhancement with dielectric tagging,” IEEE J. Sel. Top. Quantum Electron. 13(6), 1646–1654 (2007).

X. Tsampoula, V. Garces-Chavez, M. Comrie, D. J. Stevenson, B. Agate, C. T. A. Brown, F. Gunn-Moore, and K. Dholakia, “Femtosecond cellular transfection using a nondiffracting light beam,” Appl. Phys. Lett. 91(5), 053902–053903 (2007).

D. Stevenson, B. Agate, X. Tsampoula, P. Fischer, C. T. A. Brown, W. Sibbett, A. Riches, F. Gunn-Moore, and K. Dholakia, “Femtosecond optical transfection of cells: viability and efficiency,” Opt. Express 14(16), 7125–7133 (2006).

L. Paterson, B. Agate, M. Comrie, R. Ferguson, T. K. Lake, J. E. Morris, A. E. Carruthers, C. T. A. Brown, W. Sibbett, P. E. Bryant, F. Gunn-Moore, A. C. Riches, and K. Dholakia, “Photoporation and cell transfection using a violet diode laser,” Opt. Express 13(2), 595–600 (2005).

Bryant, P. E.

Bueckle, R.

Burkholder, J.

N. S. Yang, J. Burkholder, B. Roberts, B. Martinell, and D. McCabe, “In vivo and in vitro gene transfer to mammalian somatic cells by particle bombardment,” Proc. Natl. Acad. Sci. U.S.A. 87(24), 9568–9572 (1990).

Butler, W. F.

M. M. Wang, E. Tu, D. E. Raymond, J. M. Yang, H. Zhang, N. Hagen, B. Dees, E. M. Mercer, A. H. Forster, I. Kariv, P. J. Marchand, and W. F. Butler, “Microfluidic sorting of mammalian cells by optical force switching,” Nat. Biotechnol. 23(1), 83–87 (2005).

Carruthers, A. E.

Caruso, M.

G. Palumbo, M. Caruso, E. Crescenzi, M. F. Tecce, G. Roberti, and A. Colasanti, “Targeted gene transfer in eucaryotic cells by dye-assisted laser optoporation,” J. Photochem. Photobiol. B 36(1), 41–46 (1996).

Chan, H. W.

P. L. Felgner, T. R. Gadek, M. Holm, R. Roman, H. W. Chan, M. Wenz, J. P. Northrop, G. M. Ringold, and M. Danielsen, “Lipofection: a highly efficient, lipid-mediated DNA-transfection procedure,” Proc. Natl. Acad. Sci. U.S.A. 84(21), 7413–7417 (1987).

Chan, J. W.

A. Y. Lau, L. P. Lee, and J. W. Chan, “An integrated optofluidic platform for Raman-activated cell sorting,” Lab Chip 8(7), 1116–1120 (2008).

Chang, C.-C.

G.-B. Lee, C.-C. Chang, S.-B. Huang, and R.-J. Yang, “The hydrodynamic focusing effect inside rectangular microchannels,” J. Micromech. Microeng. 16(5), 1024–1032 (2006).

Chong, W.

J. A. Wolff, R. W. Malone, P. Williams, W. Chong, G. Acsadi, A. Jani, and P. L. Felgner, “Direct gene transfer into mouse muscle in vivo,” Science 247(4949 Pt 1), 1465–1468 (1990).

Cizmár, T.

Clark, I. B.

I. B. Clark, E. G. Hanania, J. Stevens, M. Gallina, A. Fieck, R. Brandes, B. O. Palsson, and M. R. Koller, “Optoinjection for efficient targeted delivery of a broad range of compounds and macromolecules into diverse cell types,” J. Biomed. Opt. 11(1), 014034 (2006).

Colasanti, A.

G. Palumbo, M. Caruso, E. Crescenzi, M. F. Tecce, G. Roberti, and A. Colasanti, “Targeted gene transfer in eucaryotic cells by dye-assisted laser optoporation,” J. Photochem. Photobiol. B 36(1), 41–46 (1996).

Comrie, M.

X. Tsampoula, V. Garces-Chavez, M. Comrie, D. J. Stevenson, B. Agate, C. T. A. Brown, F. Gunn-Moore, and K. Dholakia, “Femtosecond cellular transfection using a nondiffracting light beam,” Appl. Phys. Lett. 91(5), 053902–053903 (2007).

L. Paterson, B. Agate, M. Comrie, R. Ferguson, T. K. Lake, J. E. Morris, A. E. Carruthers, C. T. A. Brown, W. Sibbett, P. E. Bryant, F. Gunn-Moore, A. C. Riches, and K. Dholakia, “Photoporation and cell transfection using a violet diode laser,” Opt. Express 13(2), 595–600 (2005).

Crescenzi, E.

G. Palumbo, M. Caruso, E. Crescenzi, M. F. Tecce, G. Roberti, and A. Colasanti, “Targeted gene transfer in eucaryotic cells by dye-assisted laser optoporation,” J. Photochem. Photobiol. B 36(1), 41–46 (1996).

Danielsen, M.

P. L. Felgner, T. R. Gadek, M. Holm, R. Roman, H. W. Chan, M. Wenz, J. P. Northrop, G. M. Ringold, and M. Danielsen, “Lipofection: a highly efficient, lipid-mediated DNA-transfection procedure,” Proc. Natl. Acad. Sci. U.S.A. 84(21), 7413–7417 (1987).

Darash-Yahana, M.

E. Zeira, A. Manevitch, A. Khatchatouriants, O. Pappo, E. Hyam, M. Darash-Yahana, E. Tavor, A. Honigman, A. Lewis, and E. Galun, “Femtosecond infrared laser-an efficient and safe in vivo gene delivery system for prolonged expression,” Mol. Ther. 8(2), 342–350 (2003).

Dees, B.

M. M. Wang, E. Tu, D. E. Raymond, J. M. Yang, H. Zhang, N. Hagen, B. Dees, E. M. Mercer, A. H. Forster, I. Kariv, P. J. Marchand, and W. F. Butler, “Microfluidic sorting of mammalian cells by optical force switching,” Nat. Biotechnol. 23(1), 83–87 (2005).

Dholakia, K.

P. Mthunzi, K. Dholakia, and F. Gunn-Moore, “Photo-transfection of mammalian cells using femtosecond laser pulses: optimisation and applicability to stem cell differentiation,” J. Biomed. Opt. 15(4), 041507 (2010).

M. L. Torres-Mapa, L. Angus, M. Ploschner, K. Dholakia, and F. J. Gunn-Moore, “Transient transfection of mammalian cells using a violet diode laser,” J. Biomed. Opt. 15(4), 041506 (2010).

C. McDougall, D. J. Stevenson, C. T. A. Brown, F. Gunn-Moore, and K. Dholakia, “Targeted optical injection of gold nanoparticles into single mammalian cells,” J Biophotonics 2(12), 736–743 (2009).

C. T. A. Brown, D. J. Stevenson, X. Tsampoula, C. McDougall, A. A. Lagatsky, W. Sibbett, F. J. Gunn-Moore, and K. Dholakia, “Enhanced operation of femtosecond lasers and applications in cell transfection,” J Biophotonics 1(3), 183–199 (2008).

X. Tsampoula, K. Taguchi, T. Cizmár, V. Garces-Chavez, N. Ma, S. Mohanty, K. Mohanty, F. Gunn-Moore, and K. Dholakia, “Fibre based cellular transfection,” Opt. Express 16(21), 17007–17013 (2008).

T. Cizmár, V. Kollárová, X. Tsampoula, F. Gunn-Moore, W. Sibbett, Z. Bouchal, and K. Dholakia, “Generation of multiple Bessel beams for a biophotonics workstation,” Opt. Express 16(18), 14024–14035 (2008).

R. F. Marchington, M. Mazilu, S. Kuriakose, V. Garcés-Chávez, P. J. Reece, T. F. Krauss, M. Gu, and K. Dholakia, “Optical deflection and sorting of microparticles in a near-field optical geometry,” Opt. Express 16(6), 3712–3726 (2008).

K. Dholakia, W. M. Lee, L. Paterson, M. P. Macdonald, R. Mcdonald, I. Andreev, P. Mthunzi, C. T. A. Brown, R. F. Marchington, and A. C. Riches, “Optical separation of cells on potential energy landscapes: enhancement with dielectric tagging,” IEEE J. Sel. Top. Quantum Electron. 13(6), 1646–1654 (2007).

X. Tsampoula, V. Garces-Chavez, M. Comrie, D. J. Stevenson, B. Agate, C. T. A. Brown, F. Gunn-Moore, and K. Dholakia, “Femtosecond cellular transfection using a nondiffracting light beam,” Appl. Phys. Lett. 91(5), 053902–053903 (2007).

W. M. Lee, P. J. Reece, R. F. Marchington, N. K. Metzger, and K. Dholakia, “Construction and calibration of an optical trap on a fluorescence optical microscope,” Nat. Protoc. 2(12), 3226–3238 (2007).

D. Stevenson, B. Agate, X. Tsampoula, P. Fischer, C. T. A. Brown, W. Sibbett, A. Riches, F. Gunn-Moore, and K. Dholakia, “Femtosecond optical transfection of cells: viability and efficiency,” Opt. Express 14(16), 7125–7133 (2006).

L. Paterson, B. Agate, M. Comrie, R. Ferguson, T. K. Lake, J. E. Morris, A. E. Carruthers, C. T. A. Brown, W. Sibbett, P. E. Bryant, F. Gunn-Moore, A. C. Riches, and K. Dholakia, “Photoporation and cell transfection using a violet diode laser,” Opt. Express 13(2), 595–600 (2005).

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K. L. Douglas, “Toward development of artificial viruses for gene therapy: a comparative evaluation of viral and non-viral transfection,” Biotechnol. Prog. 24(4), 871–883 (2008).

Drier, T.

K. Haubert, T. Drier, and D. Beebe, “PDMS bonding by means of a portable, low-cost corona system,” Lab Chip 6(12), 1548–1549 (2006).

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L. E. Barrett, J. Y. Sul, H. Takano, E. J. Van Bockstaele, P. G. Haydon, and J. H. Eberwine, “Region-directed phototransfection reveals the functional significance of a dendritically synthesized transcription factor,” Nat. Methods 3(6), 455–460 (2006).

Efimov, I. R.

A. V. Nikolskaya, V. P. Nikolski, and I. R. Efimov, “Gene printer: laser-scanning targeted transfection of cultured cardiac neonatal rat cells,” Cell Commun. Adhes. 13(4), 217–222 (2006).

Erickson, J. S.

P. B. Howell, J. P. Golden, L. R. Hilliard, J. S. Erickson, D. R. Mott, and F. S. Ligler, “Two simple and rugged designs for creating microfluidic sheath flow,” Lab Chip 8(7), 1097–1103 (2008).

Ertmer, W.

Fang, J.

T. Zhu, C. Luo, J. Huang, C. Xiong, Q. Ouyang, and J. Fang, “Electroporation based on hydrodynamic focusing of microfluidics with low dc voltage,” Biomed. Microdevices 12(1), 35–40 (2010).

Felgner, P. L.

J. A. Wolff, R. W. Malone, P. Williams, W. Chong, G. Acsadi, A. Jani, and P. L. Felgner, “Direct gene transfer into mouse muscle in vivo,” Science 247(4949 Pt 1), 1465–1468 (1990).

P. L. Felgner, T. R. Gadek, M. Holm, R. Roman, H. W. Chan, M. Wenz, J. P. Northrop, G. M. Ringold, and M. Danielsen, “Lipofection: a highly efficient, lipid-mediated DNA-transfection procedure,” Proc. Natl. Acad. Sci. U.S.A. 84(21), 7413–7417 (1987).

Ferguson, R.

Fieck, A.

I. B. Clark, E. G. Hanania, J. Stevens, M. Gallina, A. Fieck, R. Brandes, B. O. Palsson, and M. R. Koller, “Optoinjection for efficient targeted delivery of a broad range of compounds and macromolecules into diverse cell types,” J. Biomed. Opt. 11(1), 014034 (2006).

Fischer, P.

Forster, A. H.

M. M. Wang, E. Tu, D. E. Raymond, J. M. Yang, H. Zhang, N. Hagen, B. Dees, E. M. Mercer, A. H. Forster, I. Kariv, P. J. Marchand, and W. F. Butler, “Microfluidic sorting of mammalian cells by optical force switching,” Nat. Biotechnol. 23(1), 83–87 (2005).

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A. Vogel, N. Linz, S. Freidank, and G. U. Paltauf, “Femtosecond-laser-induced nanocavitation in water: implications for optical breakdown threshold and cell surgery,” Phys. Rev. Lett. 100(3), 038102 (2008).

Gadek, T. R.

P. L. Felgner, T. R. Gadek, M. Holm, R. Roman, H. W. Chan, M. Wenz, J. P. Northrop, G. M. Ringold, and M. Danielsen, “Lipofection: a highly efficient, lipid-mediated DNA-transfection procedure,” Proc. Natl. Acad. Sci. U.S.A. 84(21), 7413–7417 (1987).

Gallina, M.

I. B. Clark, E. G. Hanania, J. Stevens, M. Gallina, A. Fieck, R. Brandes, B. O. Palsson, and M. R. Koller, “Optoinjection for efficient targeted delivery of a broad range of compounds and macromolecules into diverse cell types,” J. Biomed. Opt. 11(1), 014034 (2006).

Galun, E.

E. Zeira, A. Manevitch, A. Khatchatouriants, O. Pappo, E. Hyam, M. Darash-Yahana, E. Tavor, A. Honigman, A. Lewis, and E. Galun, “Femtosecond infrared laser-an efficient and safe in vivo gene delivery system for prolonged expression,” Mol. Ther. 8(2), 342–350 (2003).

Garces-Chavez, V.

X. Tsampoula, K. Taguchi, T. Cizmár, V. Garces-Chavez, N. Ma, S. Mohanty, K. Mohanty, F. Gunn-Moore, and K. Dholakia, “Fibre based cellular transfection,” Opt. Express 16(21), 17007–17013 (2008).

X. Tsampoula, V. Garces-Chavez, M. Comrie, D. J. Stevenson, B. Agate, C. T. A. Brown, F. Gunn-Moore, and K. Dholakia, “Femtosecond cellular transfection using a nondiffracting light beam,” Appl. Phys. Lett. 91(5), 053902–053903 (2007).

Garcés-Chávez, V.

Gazit, D.

R. Ziv, Y. Steinhardt, G. Pelled, D. Gazit, and B. Rubinsky, “Micro-electroporation of mesenchymal stem cells with alternating electrical current pulses,” Biomed. Microdevices 11(1), 95–101 (2009).

Golden, J. P.

P. B. Howell, J. P. Golden, L. R. Hilliard, J. S. Erickson, D. R. Mott, and F. S. Ligler, “Two simple and rugged designs for creating microfluidic sheath flow,” Lab Chip 8(7), 1097–1103 (2008).

Gu, M.

Gunn-Moore, F.

P. Mthunzi, K. Dholakia, and F. Gunn-Moore, “Photo-transfection of mammalian cells using femtosecond laser pulses: optimisation and applicability to stem cell differentiation,” J. Biomed. Opt. 15(4), 041507 (2010).

C. McDougall, D. J. Stevenson, C. T. A. Brown, F. Gunn-Moore, and K. Dholakia, “Targeted optical injection of gold nanoparticles into single mammalian cells,” J Biophotonics 2(12), 736–743 (2009).

X. Tsampoula, K. Taguchi, T. Cizmár, V. Garces-Chavez, N. Ma, S. Mohanty, K. Mohanty, F. Gunn-Moore, and K. Dholakia, “Fibre based cellular transfection,” Opt. Express 16(21), 17007–17013 (2008).

T. Cizmár, V. Kollárová, X. Tsampoula, F. Gunn-Moore, W. Sibbett, Z. Bouchal, and K. Dholakia, “Generation of multiple Bessel beams for a biophotonics workstation,” Opt. Express 16(18), 14024–14035 (2008).

X. Tsampoula, V. Garces-Chavez, M. Comrie, D. J. Stevenson, B. Agate, C. T. A. Brown, F. Gunn-Moore, and K. Dholakia, “Femtosecond cellular transfection using a nondiffracting light beam,” Appl. Phys. Lett. 91(5), 053902–053903 (2007).

D. Stevenson, B. Agate, X. Tsampoula, P. Fischer, C. T. A. Brown, W. Sibbett, A. Riches, F. Gunn-Moore, and K. Dholakia, “Femtosecond optical transfection of cells: viability and efficiency,” Opt. Express 14(16), 7125–7133 (2006).

L. Paterson, B. Agate, M. Comrie, R. Ferguson, T. K. Lake, J. E. Morris, A. E. Carruthers, C. T. A. Brown, W. Sibbett, P. E. Bryant, F. Gunn-Moore, A. C. Riches, and K. Dholakia, “Photoporation and cell transfection using a violet diode laser,” Opt. Express 13(2), 595–600 (2005).

Gunn-Moore, F. J.

M. L. Torres-Mapa, L. Angus, M. Ploschner, K. Dholakia, and F. J. Gunn-Moore, “Transient transfection of mammalian cells using a violet diode laser,” J. Biomed. Opt. 15(4), 041506 (2010).

C. T. A. Brown, D. J. Stevenson, X. Tsampoula, C. McDougall, A. A. Lagatsky, W. Sibbett, F. J. Gunn-Moore, and K. Dholakia, “Enhanced operation of femtosecond lasers and applications in cell transfection,” J Biophotonics 1(3), 183–199 (2008).

Hagen, N.

M. M. Wang, E. Tu, D. E. Raymond, J. M. Yang, H. Zhang, N. Hagen, B. Dees, E. M. Mercer, A. H. Forster, I. Kariv, P. J. Marchand, and W. F. Butler, “Microfluidic sorting of mammalian cells by optical force switching,” Nat. Biotechnol. 23(1), 83–87 (2005).

Hanania, E. G.

I. B. Clark, E. G. Hanania, J. Stevens, M. Gallina, A. Fieck, R. Brandes, B. O. Palsson, and M. R. Koller, “Optoinjection for efficient targeted delivery of a broad range of compounds and macromolecules into diverse cell types,” J. Biomed. Opt. 11(1), 014034 (2006).

Haubert, K.

K. Haubert, T. Drier, and D. Beebe, “PDMS bonding by means of a portable, low-cost corona system,” Lab Chip 6(12), 1548–1549 (2006).

Haydon, P. G.

L. E. Barrett, J. Y. Sul, H. Takano, E. J. Van Bockstaele, P. G. Haydon, and J. H. Eberwine, “Region-directed phototransfection reveals the functional significance of a dendritically synthesized transcription factor,” Nat. Methods 3(6), 455–460 (2006).

Heisterkamp, A.

Hendinger, A.

H. Schneckenburger, A. Hendinger, R. Sailer, W. S. L. Strauss, and M. Schmitt, “Laser-assisted optoporation of single cells,” J. Biomed. Opt. 7(3), 410–416 (2002).

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P. B. Howell, J. P. Golden, L. R. Hilliard, J. S. Erickson, D. R. Mott, and F. S. Ligler, “Two simple and rugged designs for creating microfluidic sheath flow,” Lab Chip 8(7), 1097–1103 (2008).

Hiraki, Y.

A. Yamaguchi, Y. Hosokawa, G. Louit, T. Asahi, C. Shukunami, Y. Hiraki, and H. Masuhara, “Nanoparticle injection to single animal cells using femtosecond laser-induced impulsive force,” Adv. Mater. (Deerfield Beach Fla.) 93, 39–43 (2008).

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E. Neumann, M. Schaefer-Ridder, Y. Wang, and P. H. Hofschneider, “Gene transfer into mouse lyoma cells by electroporation in high electric fields,” EMBO J. 1(7), 841–845 (1982).

Holm, M.

P. L. Felgner, T. R. Gadek, M. Holm, R. Roman, H. W. Chan, M. Wenz, J. P. Northrop, G. M. Ringold, and M. Danielsen, “Lipofection: a highly efficient, lipid-mediated DNA-transfection procedure,” Proc. Natl. Acad. Sci. U.S.A. 84(21), 7413–7417 (1987).

Honigman, A.

E. Zeira, A. Manevitch, A. Khatchatouriants, O. Pappo, E. Hyam, M. Darash-Yahana, E. Tavor, A. Honigman, A. Lewis, and E. Galun, “Femtosecond infrared laser-an efficient and safe in vivo gene delivery system for prolonged expression,” Mol. Ther. 8(2), 342–350 (2003).

Hosokawa, Y.

A. Yamaguchi, Y. Hosokawa, G. Louit, T. Asahi, C. Shukunami, Y. Hiraki, and H. Masuhara, “Nanoparticle injection to single animal cells using femtosecond laser-induced impulsive force,” Adv. Mater. (Deerfield Beach Fla.) 93, 39–43 (2008).

Howell, P. B.

P. B. Howell, J. P. Golden, L. R. Hilliard, J. S. Erickson, D. R. Mott, and F. S. Ligler, “Two simple and rugged designs for creating microfluidic sheath flow,” Lab Chip 8(7), 1097–1103 (2008).

Huang, J.

T. Zhu, C. Luo, J. Huang, C. Xiong, Q. Ouyang, and J. Fang, “Electroporation based on hydrodynamic focusing of microfluidics with low dc voltage,” Biomed. Microdevices 12(1), 35–40 (2010).

Huang, S.-B.

G.-B. Lee, C.-C. Chang, S.-B. Huang, and R.-J. Yang, “The hydrodynamic focusing effect inside rectangular microchannels,” J. Micromech. Microeng. 16(5), 1024–1032 (2006).

Hyam, E.

E. Zeira, A. Manevitch, A. Khatchatouriants, O. Pappo, E. Hyam, M. Darash-Yahana, E. Tavor, A. Honigman, A. Lewis, and E. Galun, “Femtosecond infrared laser-an efficient and safe in vivo gene delivery system for prolonged expression,” Mol. Ther. 8(2), 342–350 (2003).

Ikawa, Y.

M. Tsukakoshi, S. Kurata, Y. Nomiya, Y. Ikawa, and T. Kasuya, “A novel method of DNA transfection by laser microbeam cell surgery,” Appl. Phys. B 35(3), 135–140 (1984).

Isemann, A.

Jacobs, P.

H. Schinkel, P. Jacobs, S. Schillberg, and M. Wehner, “Infrared picosecond laser for perforation of single plant cells,” Biotechnol. Bioeng. 99(1), 244–248 (2008).

Jani, A.

J. A. Wolff, R. W. Malone, P. Williams, W. Chong, G. Acsadi, A. Jani, and P. L. Felgner, “Direct gene transfer into mouse muscle in vivo,” Science 247(4949 Pt 1), 1465–1468 (1990).

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A. Adamo and K. F. Jensen, “Microfluidic based single cell microinjection,” Lab Chip 8(8), 1258–1261 (2008).

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C. M. Pitsillides, E. K. Joe, X. Wei, R. R. Anderson, and C. P. Lin, “Selective cell targeting with light-absorbing microparticles and nanoparticles,” Biophys. J. 84(6), 4023–4032 (2003).

Kariv, I.

M. M. Wang, E. Tu, D. E. Raymond, J. M. Yang, H. Zhang, N. Hagen, B. Dees, E. M. Mercer, A. H. Forster, I. Kariv, P. J. Marchand, and W. F. Butler, “Microfluidic sorting of mammalian cells by optical force switching,” Nat. Biotechnol. 23(1), 83–87 (2005).

Kasuya, T.

M. Tsukakoshi, S. Kurata, Y. Nomiya, Y. Ikawa, and T. Kasuya, “A novel method of DNA transfection by laser microbeam cell surgery,” Appl. Phys. B 35(3), 135–140 (1984).

Khatchatouriants, A.

E. Zeira, A. Manevitch, A. Khatchatouriants, O. Pappo, E. Hyam, M. Darash-Yahana, E. Tavor, A. Honigman, A. Lewis, and E. Galun, “Femtosecond infrared laser-an efficient and safe in vivo gene delivery system for prolonged expression,” Mol. Ther. 8(2), 342–350 (2003).

Knoll, T.

T. Knoll, L. Trojan, S. Langbein, S. Sagi, P. Alken, and M. S. Michel, “Impact of holmium:YAG and neodymium:YAG lasers on the efficacy of DNA delivery in transitional cell carcinoma,” Lasers Med. Sci. 19(1), 33–36 (2004).

S. Sagi, T. Knoll, L. Trojan, A. Schaaf, P. Alken, and M. S. Michel, “Gene delivery into prostate cancer cells by holmium laser application,” Prostate Cancer Prostatic Dis. 6(2), 127–130 (2003).

Kollárová, V.

Koller, M. R.

I. B. Clark, E. G. Hanania, J. Stevens, M. Gallina, A. Fieck, R. Brandes, B. O. Palsson, and M. R. Koller, “Optoinjection for efficient targeted delivery of a broad range of compounds and macromolecules into diverse cell types,” J. Biomed. Opt. 11(1), 014034 (2006).

König, K.

Krauss, T. F.

Kurata, S.

M. Tsukakoshi, S. Kurata, Y. Nomiya, Y. Ikawa, and T. Kasuya, “A novel method of DNA transfection by laser microbeam cell surgery,” Appl. Phys. B 35(3), 135–140 (1984).

Kuriakose, S.

Lagatsky, A. A.

C. T. A. Brown, D. J. Stevenson, X. Tsampoula, C. McDougall, A. A. Lagatsky, W. Sibbett, F. J. Gunn-Moore, and K. Dholakia, “Enhanced operation of femtosecond lasers and applications in cell transfection,” J Biophotonics 1(3), 183–199 (2008).

Lake, T. K.

Langbein, S.

T. Knoll, L. Trojan, S. Langbein, S. Sagi, P. Alken, and M. S. Michel, “Impact of holmium:YAG and neodymium:YAG lasers on the efficacy of DNA delivery in transitional cell carcinoma,” Lasers Med. Sci. 19(1), 33–36 (2004).

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C. McDougall, D. J. Stevenson, C. T. A. Brown, F. Gunn-Moore, and K. Dholakia, “Targeted optical injection of gold nanoparticles into single mammalian cells,” J Biophotonics 2(12), 736–743 (2009).

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T. Knoll, L. Trojan, S. Langbein, S. Sagi, P. Alken, and M. S. Michel, “Impact of holmium:YAG and neodymium:YAG lasers on the efficacy of DNA delivery in transitional cell carcinoma,” Lasers Med. Sci. 19(1), 33–36 (2004).

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S. Sagi, T. Knoll, L. Trojan, A. Schaaf, P. Alken, and M. S. Michel, “Gene delivery into prostate cancer cells by holmium laser application,” Prostate Cancer Prostatic Dis. 6(2), 127–130 (2003).

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A. Noori, P. R. Selvaganapathy, and J. Wilson, “Microinjection in a microfluidic format using flexible and compliant channels and electroosmotic dosage control,” Lab Chip 9(22), 3202–3211 (2009).

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A. Yamaguchi, Y. Hosokawa, G. Louit, T. Asahi, C. Shukunami, Y. Hiraki, and H. Masuhara, “Nanoparticle injection to single animal cells using femtosecond laser-induced impulsive force,” Adv. Mater. (Deerfield Beach Fla.) 93, 39–43 (2008).

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I. B. Clark, E. G. Hanania, J. Stevens, M. Gallina, A. Fieck, R. Brandes, B. O. Palsson, and M. R. Koller, “Optoinjection for efficient targeted delivery of a broad range of compounds and macromolecules into diverse cell types,” J. Biomed. Opt. 11(1), 014034 (2006).

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Stevenson, D. J.

C. McDougall, D. J. Stevenson, C. T. A. Brown, F. Gunn-Moore, and K. Dholakia, “Targeted optical injection of gold nanoparticles into single mammalian cells,” J Biophotonics 2(12), 736–743 (2009).

C. T. A. Brown, D. J. Stevenson, X. Tsampoula, C. McDougall, A. A. Lagatsky, W. Sibbett, F. J. Gunn-Moore, and K. Dholakia, “Enhanced operation of femtosecond lasers and applications in cell transfection,” J Biophotonics 1(3), 183–199 (2008).

X. Tsampoula, V. Garces-Chavez, M. Comrie, D. J. Stevenson, B. Agate, C. T. A. Brown, F. Gunn-Moore, and K. Dholakia, “Femtosecond cellular transfection using a nondiffracting light beam,” Appl. Phys. Lett. 91(5), 053902–053903 (2007).

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J. Wang, M. J. Stine, and C. Lu, “Microfluidic cell electroporation using a mechanical valve,” Anal. Chem. 79(24), 9584–9587 (2007).

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H. Schneckenburger, A. Hendinger, R. Sailer, W. S. L. Strauss, and M. Schmitt, “Laser-assisted optoporation of single cells,” J. Biomed. Opt. 7(3), 410–416 (2002).

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G. Palumbo, M. Caruso, E. Crescenzi, M. F. Tecce, G. Roberti, and A. Colasanti, “Targeted gene transfer in eucaryotic cells by dye-assisted laser optoporation,” J. Photochem. Photobiol. B 36(1), 41–46 (1996).

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M. L. Torres-Mapa, L. Angus, M. Ploschner, K. Dholakia, and F. J. Gunn-Moore, “Transient transfection of mammalian cells using a violet diode laser,” J. Biomed. Opt. 15(4), 041506 (2010).

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T. Knoll, L. Trojan, S. Langbein, S. Sagi, P. Alken, and M. S. Michel, “Impact of holmium:YAG and neodymium:YAG lasers on the efficacy of DNA delivery in transitional cell carcinoma,” Lasers Med. Sci. 19(1), 33–36 (2004).

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C. T. A. Brown, D. J. Stevenson, X. Tsampoula, C. McDougall, A. A. Lagatsky, W. Sibbett, F. J. Gunn-Moore, and K. Dholakia, “Enhanced operation of femtosecond lasers and applications in cell transfection,” J Biophotonics 1(3), 183–199 (2008).

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M. M. Wang, E. Tu, D. E. Raymond, J. M. Yang, H. Zhang, N. Hagen, B. Dees, E. M. Mercer, A. H. Forster, I. Kariv, P. J. Marchand, and W. F. Butler, “Microfluidic sorting of mammalian cells by optical force switching,” Nat. Biotechnol. 23(1), 83–87 (2005).

Uchugonova, A.

Van Bockstaele, E. J.

L. E. Barrett, J. Y. Sul, H. Takano, E. J. Van Bockstaele, P. G. Haydon, and J. H. Eberwine, “Region-directed phototransfection reveals the functional significance of a dendritically synthesized transcription factor,” Nat. Methods 3(6), 455–460 (2006).

Vogel, A.

A. Vogel, N. Linz, S. Freidank, and G. U. Paltauf, “Femtosecond-laser-induced nanocavitation in water: implications for optical breakdown threshold and cell surgery,” Phys. Rev. Lett. 100(3), 038102 (2008).

Wang, J.

Y. Zhan, J. Wang, N. Bao, and C. Lu, “Electroporation of cells in microfluidic droplets,” Anal. Chem. 81(5), 2027–2031 (2009).

J. Wang, M. J. Stine, and C. Lu, “Microfluidic cell electroporation using a mechanical valve,” Anal. Chem. 79(24), 9584–9587 (2007).

Wang, M. M.

M. M. Wang, E. Tu, D. E. Raymond, J. M. Yang, H. Zhang, N. Hagen, B. Dees, E. M. Mercer, A. H. Forster, I. Kariv, P. J. Marchand, and W. F. Butler, “Microfluidic sorting of mammalian cells by optical force switching,” Nat. Biotechnol. 23(1), 83–87 (2005).

Wang, Y.

E. Neumann, M. Schaefer-Ridder, Y. Wang, and P. H. Hofschneider, “Gene transfer into mouse lyoma cells by electroporation in high electric fields,” EMBO J. 1(7), 841–845 (1982).

Wehner, M.

H. Schinkel, P. Jacobs, S. Schillberg, and M. Wehner, “Infrared picosecond laser for perforation of single plant cells,” Biotechnol. Bioeng. 99(1), 244–248 (2008).

Wei, X.

C. M. Pitsillides, E. K. Joe, X. Wei, R. R. Anderson, and C. P. Lin, “Selective cell targeting with light-absorbing microparticles and nanoparticles,” Biophys. J. 84(6), 4023–4032 (2003).

Wenz, M.

P. L. Felgner, T. R. Gadek, M. Holm, R. Roman, H. W. Chan, M. Wenz, J. P. Northrop, G. M. Ringold, and M. Danielsen, “Lipofection: a highly efficient, lipid-mediated DNA-transfection procedure,” Proc. Natl. Acad. Sci. U.S.A. 84(21), 7413–7417 (1987).

Whitesides, G. M.

J. C. McDonald and G. M. Whitesides, “Poly(dimethylsiloxane) as a material for fabricating microfluidic devices,” Acc. Chem. Res. 35(7), 491–499 (2002).

Wilke, I.

C. Peng, R. E. Palazzo, and I. Wilke, “Laser intensity dependence of femtosecond near-infrared optoinjection,” Phys. Rev. E Stat. Nonlin. Soft Matter Phys. 75(4 Pt 1), 041903 (2007).

Willenbrock, S.

Williams, P.

J. A. Wolff, R. W. Malone, P. Williams, W. Chong, G. Acsadi, A. Jani, and P. L. Felgner, “Direct gene transfer into mouse muscle in vivo,” Science 247(4949 Pt 1), 1465–1468 (1990).

Wilson, J.

A. Noori, P. R. Selvaganapathy, and J. Wilson, “Microinjection in a microfluidic format using flexible and compliant channels and electroosmotic dosage control,” Lab Chip 9(22), 3202–3211 (2009).

Wolff, J. A.

J. A. Wolff, R. W. Malone, P. Williams, W. Chong, G. Acsadi, A. Jani, and P. L. Felgner, “Direct gene transfer into mouse muscle in vivo,” Science 247(4949 Pt 1), 1465–1468 (1990).

Xiong, C.

T. Zhu, C. Luo, J. Huang, C. Xiong, Q. Ouyang, and J. Fang, “Electroporation based on hydrodynamic focusing of microfluidics with low dc voltage,” Biomed. Microdevices 12(1), 35–40 (2010).

Xu, H.

M. Lei, H. Xu, H. Yang, and B. Yao, “Femtosecond laser-assisted microinjection into living neurons,” J. Neurosci. Methods 174(2), 215–218 (2008).

Yamaguchi, A.

A. Yamaguchi, Y. Hosokawa, G. Louit, T. Asahi, C. Shukunami, Y. Hiraki, and H. Masuhara, “Nanoparticle injection to single animal cells using femtosecond laser-induced impulsive force,” Adv. Mater. (Deerfield Beach Fla.) 93, 39–43 (2008).

Yang, H.

M. Lei, H. Xu, H. Yang, and B. Yao, “Femtosecond laser-assisted microinjection into living neurons,” J. Neurosci. Methods 174(2), 215–218 (2008).

Yang, J. M.

M. M. Wang, E. Tu, D. E. Raymond, J. M. Yang, H. Zhang, N. Hagen, B. Dees, E. M. Mercer, A. H. Forster, I. Kariv, P. J. Marchand, and W. F. Butler, “Microfluidic sorting of mammalian cells by optical force switching,” Nat. Biotechnol. 23(1), 83–87 (2005).

Yang, N. S.

N. S. Yang, J. Burkholder, B. Roberts, B. Martinell, and D. McCabe, “In vivo and in vitro gene transfer to mammalian somatic cells by particle bombardment,” Proc. Natl. Acad. Sci. U.S.A. 87(24), 9568–9572 (1990).

Yang, R.-J.

G.-B. Lee, C.-C. Chang, S.-B. Huang, and R.-J. Yang, “The hydrodynamic focusing effect inside rectangular microchannels,” J. Micromech. Microeng. 16(5), 1024–1032 (2006).

Yao, B.

M. Lei, H. Xu, H. Yang, and B. Yao, “Femtosecond laser-assisted microinjection into living neurons,” J. Neurosci. Methods 174(2), 215–218 (2008).

Zeira, E.

E. Zeira, A. Manevitch, A. Khatchatouriants, O. Pappo, E. Hyam, M. Darash-Yahana, E. Tavor, A. Honigman, A. Lewis, and E. Galun, “Femtosecond infrared laser-an efficient and safe in vivo gene delivery system for prolonged expression,” Mol. Ther. 8(2), 342–350 (2003).

Zhan, Y.

Y. Zhan, J. Wang, N. Bao, and C. Lu, “Electroporation of cells in microfluidic droplets,” Anal. Chem. 81(5), 2027–2031 (2009).

N. Bao, Y. Zhan, and C. Lu, “Microfluidic electroporative flow cytometry for studying single-cell biomechanics,” Anal. Chem. 80(20), 7714–7719 (2008).

Zhang, H.

M. M. Wang, E. Tu, D. E. Raymond, J. M. Yang, H. Zhang, N. Hagen, B. Dees, E. M. Mercer, A. H. Forster, I. Kariv, P. J. Marchand, and W. F. Butler, “Microfluidic sorting of mammalian cells by optical force switching,” Nat. Biotechnol. 23(1), 83–87 (2005).

Zhu, T.

T. Zhu, C. Luo, J. Huang, C. Xiong, Q. Ouyang, and J. Fang, “Electroporation based on hydrodynamic focusing of microfluidics with low dc voltage,” Biomed. Microdevices 12(1), 35–40 (2010).

Ziv, R.

R. Ziv, Y. Steinhardt, G. Pelled, D. Gazit, and B. Rubinsky, “Micro-electroporation of mesenchymal stem cells with alternating electrical current pulses,” Biomed. Microdevices 11(1), 95–101 (2009).

Acc. Chem. Res. (1)

J. C. McDonald and G. M. Whitesides, “Poly(dimethylsiloxane) as a material for fabricating microfluidic devices,” Acc. Chem. Res. 35(7), 491–499 (2002).

Adv. Mater. (Deerfield Beach Fla.) (1)

A. Yamaguchi, Y. Hosokawa, G. Louit, T. Asahi, C. Shukunami, Y. Hiraki, and H. Masuhara, “Nanoparticle injection to single animal cells using femtosecond laser-induced impulsive force,” Adv. Mater. (Deerfield Beach Fla.) 93, 39–43 (2008).

Anal. Chem. (3)

N. Bao, Y. Zhan, and C. Lu, “Microfluidic electroporative flow cytometry for studying single-cell biomechanics,” Anal. Chem. 80(20), 7714–7719 (2008).

J. Wang, M. J. Stine, and C. Lu, “Microfluidic cell electroporation using a mechanical valve,” Anal. Chem. 79(24), 9584–9587 (2007).

Y. Zhan, J. Wang, N. Bao, and C. Lu, “Electroporation of cells in microfluidic droplets,” Anal. Chem. 81(5), 2027–2031 (2009).

Appl. Phys. B (1)

M. Tsukakoshi, S. Kurata, Y. Nomiya, Y. Ikawa, and T. Kasuya, “A novel method of DNA transfection by laser microbeam cell surgery,” Appl. Phys. B 35(3), 135–140 (1984).

Appl. Phys. Lett. (1)

X. Tsampoula, V. Garces-Chavez, M. Comrie, D. J. Stevenson, B. Agate, C. T. A. Brown, F. Gunn-Moore, and K. Dholakia, “Femtosecond cellular transfection using a nondiffracting light beam,” Appl. Phys. Lett. 91(5), 053902–053903 (2007).

Biomed. Microdevices (2)

T. Zhu, C. Luo, J. Huang, C. Xiong, Q. Ouyang, and J. Fang, “Electroporation based on hydrodynamic focusing of microfluidics with low dc voltage,” Biomed. Microdevices 12(1), 35–40 (2010).

R. Ziv, Y. Steinhardt, G. Pelled, D. Gazit, and B. Rubinsky, “Micro-electroporation of mesenchymal stem cells with alternating electrical current pulses,” Biomed. Microdevices 11(1), 95–101 (2009).

Biophys. J. (1)

C. M. Pitsillides, E. K. Joe, X. Wei, R. R. Anderson, and C. P. Lin, “Selective cell targeting with light-absorbing microparticles and nanoparticles,” Biophys. J. 84(6), 4023–4032 (2003).

Biotechnol. Bioeng. (1)

H. Schinkel, P. Jacobs, S. Schillberg, and M. Wehner, “Infrared picosecond laser for perforation of single plant cells,” Biotechnol. Bioeng. 99(1), 244–248 (2008).

Biotechnol. Prog. (1)

K. L. Douglas, “Toward development of artificial viruses for gene therapy: a comparative evaluation of viral and non-viral transfection,” Biotechnol. Prog. 24(4), 871–883 (2008).

Cell Commun. Adhes. (1)

A. V. Nikolskaya, V. P. Nikolski, and I. R. Efimov, “Gene printer: laser-scanning targeted transfection of cultured cardiac neonatal rat cells,” Cell Commun. Adhes. 13(4), 217–222 (2006).

EMBO J. (1)

E. Neumann, M. Schaefer-Ridder, Y. Wang, and P. H. Hofschneider, “Gene transfer into mouse lyoma cells by electroporation in high electric fields,” EMBO J. 1(7), 841–845 (1982).

IEEE J. Sel. Top. Quantum Electron. (1)

K. Dholakia, W. M. Lee, L. Paterson, M. P. Macdonald, R. Mcdonald, I. Andreev, P. Mthunzi, C. T. A. Brown, R. F. Marchington, and A. C. Riches, “Optical separation of cells on potential energy landscapes: enhancement with dielectric tagging,” IEEE J. Sel. Top. Quantum Electron. 13(6), 1646–1654 (2007).

J Biophotonics (2)

C. McDougall, D. J. Stevenson, C. T. A. Brown, F. Gunn-Moore, and K. Dholakia, “Targeted optical injection of gold nanoparticles into single mammalian cells,” J Biophotonics 2(12), 736–743 (2009).

C. T. A. Brown, D. J. Stevenson, X. Tsampoula, C. McDougall, A. A. Lagatsky, W. Sibbett, F. J. Gunn-Moore, and K. Dholakia, “Enhanced operation of femtosecond lasers and applications in cell transfection,” J Biophotonics 1(3), 183–199 (2008).

J. Biomed. Opt. (4)

P. Mthunzi, K. Dholakia, and F. Gunn-Moore, “Photo-transfection of mammalian cells using femtosecond laser pulses: optimisation and applicability to stem cell differentiation,” J. Biomed. Opt. 15(4), 041507 (2010).

I. B. Clark, E. G. Hanania, J. Stevens, M. Gallina, A. Fieck, R. Brandes, B. O. Palsson, and M. R. Koller, “Optoinjection for efficient targeted delivery of a broad range of compounds and macromolecules into diverse cell types,” J. Biomed. Opt. 11(1), 014034 (2006).

M. L. Torres-Mapa, L. Angus, M. Ploschner, K. Dholakia, and F. J. Gunn-Moore, “Transient transfection of mammalian cells using a violet diode laser,” J. Biomed. Opt. 15(4), 041506 (2010).

H. Schneckenburger, A. Hendinger, R. Sailer, W. S. L. Strauss, and M. Schmitt, “Laser-assisted optoporation of single cells,” J. Biomed. Opt. 7(3), 410–416 (2002).

J. Micromech. Microeng. (1)

G.-B. Lee, C.-C. Chang, S.-B. Huang, and R.-J. Yang, “The hydrodynamic focusing effect inside rectangular microchannels,” J. Micromech. Microeng. 16(5), 1024–1032 (2006).

J. Neurosci. Methods (1)

M. Lei, H. Xu, H. Yang, and B. Yao, “Femtosecond laser-assisted microinjection into living neurons,” J. Neurosci. Methods 174(2), 215–218 (2008).

J. Photochem. Photobiol. B (1)

G. Palumbo, M. Caruso, E. Crescenzi, M. F. Tecce, G. Roberti, and A. Colasanti, “Targeted gene transfer in eucaryotic cells by dye-assisted laser optoporation,” J. Photochem. Photobiol. B 36(1), 41–46 (1996).

Lab Chip (5)

A. Noori, P. R. Selvaganapathy, and J. Wilson, “Microinjection in a microfluidic format using flexible and compliant channels and electroosmotic dosage control,” Lab Chip 9(22), 3202–3211 (2009).

A. Adamo and K. F. Jensen, “Microfluidic based single cell microinjection,” Lab Chip 8(8), 1258–1261 (2008).

P. B. Howell, J. P. Golden, L. R. Hilliard, J. S. Erickson, D. R. Mott, and F. S. Ligler, “Two simple and rugged designs for creating microfluidic sheath flow,” Lab Chip 8(7), 1097–1103 (2008).

K. Haubert, T. Drier, and D. Beebe, “PDMS bonding by means of a portable, low-cost corona system,” Lab Chip 6(12), 1548–1549 (2006).

A. Y. Lau, L. P. Lee, and J. W. Chan, “An integrated optofluidic platform for Raman-activated cell sorting,” Lab Chip 8(7), 1116–1120 (2008).

Lasers Med. Sci. (1)

T. Knoll, L. Trojan, S. Langbein, S. Sagi, P. Alken, and M. S. Michel, “Impact of holmium:YAG and neodymium:YAG lasers on the efficacy of DNA delivery in transitional cell carcinoma,” Lasers Med. Sci. 19(1), 33–36 (2004).

Mol. Ther. (1)

E. Zeira, A. Manevitch, A. Khatchatouriants, O. Pappo, E. Hyam, M. Darash-Yahana, E. Tavor, A. Honigman, A. Lewis, and E. Galun, “Femtosecond infrared laser-an efficient and safe in vivo gene delivery system for prolonged expression,” Mol. Ther. 8(2), 342–350 (2003).

Nat. Biotechnol. (1)

M. M. Wang, E. Tu, D. E. Raymond, J. M. Yang, H. Zhang, N. Hagen, B. Dees, E. M. Mercer, A. H. Forster, I. Kariv, P. J. Marchand, and W. F. Butler, “Microfluidic sorting of mammalian cells by optical force switching,” Nat. Biotechnol. 23(1), 83–87 (2005).

Nat. Methods (1)

L. E. Barrett, J. Y. Sul, H. Takano, E. J. Van Bockstaele, P. G. Haydon, and J. H. Eberwine, “Region-directed phototransfection reveals the functional significance of a dendritically synthesized transcription factor,” Nat. Methods 3(6), 455–460 (2006).

Nat. Protoc. (1)

W. M. Lee, P. J. Reece, R. F. Marchington, N. K. Metzger, and K. Dholakia, “Construction and calibration of an optical trap on a fluorescence optical microscope,” Nat. Protoc. 2(12), 3226–3238 (2007).

Nature (1)

U. K. Tirlapur and K. König, “Targeted transfection by femtosecond laser,” Nature 418(6895), 290–291 (2002).

Opt. Express (7)

J. Baumgart, W. Bintig, A. Ngezahayo, S. Willenbrock, H. Murua Escobar, W. Ertmer, H. Lubatschowski, and A. Heisterkamp, “Quantified femtosecond laser based opto-perforation of living GFSHR-17 and MTH53 a cells,” Opt. Express 16(5), 3021–3031 (2008).

X. Tsampoula, K. Taguchi, T. Cizmár, V. Garces-Chavez, N. Ma, S. Mohanty, K. Mohanty, F. Gunn-Moore, and K. Dholakia, “Fibre based cellular transfection,” Opt. Express 16(21), 17007–17013 (2008).

D. Stevenson, B. Agate, X. Tsampoula, P. Fischer, C. T. A. Brown, W. Sibbett, A. Riches, F. Gunn-Moore, and K. Dholakia, “Femtosecond optical transfection of cells: viability and efficiency,” Opt. Express 14(16), 7125–7133 (2006).

A. Uchugonova, K. König, R. Bueckle, A. Isemann, and G. Tempea, “Targeted transfection of stem cells with sub-20 femtosecond laser pulses,” Opt. Express 16(13), 9357–9364 (2008).

L. Paterson, B. Agate, M. Comrie, R. Ferguson, T. K. Lake, J. E. Morris, A. E. Carruthers, C. T. A. Brown, W. Sibbett, P. E. Bryant, F. Gunn-Moore, A. C. Riches, and K. Dholakia, “Photoporation and cell transfection using a violet diode laser,” Opt. Express 13(2), 595–600 (2005).

R. F. Marchington, M. Mazilu, S. Kuriakose, V. Garcés-Chávez, P. J. Reece, T. F. Krauss, M. Gu, and K. Dholakia, “Optical deflection and sorting of microparticles in a near-field optical geometry,” Opt. Express 16(6), 3712–3726 (2008).

T. Cizmár, V. Kollárová, X. Tsampoula, F. Gunn-Moore, W. Sibbett, Z. Bouchal, and K. Dholakia, “Generation of multiple Bessel beams for a biophotonics workstation,” Opt. Express 16(18), 14024–14035 (2008).

Phys. Rev. E Stat. Nonlin. Soft Matter Phys. (1)

C. Peng, R. E. Palazzo, and I. Wilke, “Laser intensity dependence of femtosecond near-infrared optoinjection,” Phys. Rev. E Stat. Nonlin. Soft Matter Phys. 75(4 Pt 1), 041903 (2007).

Phys. Rev. Lett. (1)

A. Vogel, N. Linz, S. Freidank, and G. U. Paltauf, “Femtosecond-laser-induced nanocavitation in water: implications for optical breakdown threshold and cell surgery,” Phys. Rev. Lett. 100(3), 038102 (2008).

Proc. Natl. Acad. Sci. U.S.A. (2)

N. S. Yang, J. Burkholder, B. Roberts, B. Martinell, and D. McCabe, “In vivo and in vitro gene transfer to mammalian somatic cells by particle bombardment,” Proc. Natl. Acad. Sci. U.S.A. 87(24), 9568–9572 (1990).

P. L. Felgner, T. R. Gadek, M. Holm, R. Roman, H. W. Chan, M. Wenz, J. P. Northrop, G. M. Ringold, and M. Danielsen, “Lipofection: a highly efficient, lipid-mediated DNA-transfection procedure,” Proc. Natl. Acad. Sci. U.S.A. 84(21), 7413–7417 (1987).

Prostate Cancer Prostatic Dis. (1)

S. Sagi, T. Knoll, L. Trojan, A. Schaaf, P. Alken, and M. S. Michel, “Gene delivery into prostate cancer cells by holmium laser application,” Prostate Cancer Prostatic Dis. 6(2), 127–130 (2003).

Science (1)

J. A. Wolff, R. W. Malone, P. Williams, W. Chong, G. Acsadi, A. Jani, and P. L. Felgner, “Direct gene transfer into mouse muscle in vivo,” Science 247(4949 Pt 1), 1465–1468 (1990).

Other (1)

D. J. Stevenson, F. J. Gunn-Moore, P. Campbell, and K. Dholakia, “The Handbook of Photonics for Medical Science,” 1 ed., V. V. Tuchin, ed. (CRC Press, USA, 2010), pp. 87–117.

Supplementary Material (1)

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Figures (6)

Fig. 1
Fig. 1

(a) Image of the PDMS chip showing micro-centrifuge tubes for cell insertion and collection, and the two inlet pipes on the left for buffer and sample flow and a single outlet pipe on the right. (b) Microfluidic channel layout on the PDMS chip (not to scale). The cells are first inserted directly into chip via an adapted micro-centrifuge tube (left-most). The three syringe pumps then drive the fluid as indicated by the arrows. Cells pass into the hydrodynamic focusing junction, forcing them to flow one at a time through the femtosecond laser beam (as focused into the chip via the objective lens), where optical injection occurs. The beam is positioned approximately 300 μm downstream of the hydrodynamic focusing junction. Cells come to rest under the second micro-centrifuge tube, ready for collection with a pipette for culture and/or analysis.

Fig. 2
Fig. 2

Fluidic setup required for cleaning, sterilizing and flowing cells. Cleaning, sterilizing and filling of the fluidics with cell medium is conducted using the peristaltic pump. Syringe pumps are used for flowing of the cells for optical injection, and operate in a “push-pull” configuration to obtain stable fluid flow. Layout of the PDMS microfluidic chip is also shown, which matches with Fig. 1. The injection agent is added the Opti-MEM® before filling the chip and piping at the start of the experiment.

Fig. 3
Fig. 3

Schematic of the optical setup, showing the Ti: Sapphire laser, power attenuators (2x half-wave plate and polarizing beam-splitter), spectrum analyzer (SA), beam expanding telescope, and the microscope containing: a high-NA objective lens for focusing the optical injection beam, and condenser lens, 800 nm high reflector (HR) and CCD camera. The PDMS microfluidic chip sits on the microscope stage and the fluid pumps are housed on adjacent raised platforms.

Fig. 4
Fig. 4

(Media 1) Frames from the accompanying video, from within the PDMS microfluidic chip shown schematically in Fig. 1(b). (a) Sample injection port after the insertion of cells into the chip. (b) Cells flowing from left to right out of the injection reservoir and towards (c) the hydrodynamic focusing junction, where cells (circled) can be seen flowing single file down the center of the channel after the junction. The focused femtosecond laser beam for optical injection was situated 300 μm downstream of the junction. (d) Cell collection port after 10 minutes showing several hundred optically injected cells that have come to rest due to the drop in flow velocity in this region of the chip.

Fig. 5
Fig. 5

Collected cells 24 hours after microfluidic photoporation, including viable optically injected cells (arrowed and circled). (a) Bright field microscope image showing cell attachment to the base of the well plate. (b) The same cells exhibiting varying levels of PI fluorescence. Strongly red fluorescing cells have uptaken large quantities of PI indicating permanently compromised dead or dying cells. Weakly fluorescing red cells are optically injected. (c) Fluorescence of CAM showing the viable cells in this field of view. The combination of PI fluorescence in (b) and CAM indicates a cell that has been optically injected with PI and has remained viable (arrowed and circled).

Fig. 6
Fig. 6

Optical injection efficiencies for HEK293 cells in a microfluidic flow. The percentage of cells exhibiting fluorescence of PI and those that exhibit both PI and CAM is plotted here against those observed in the control samples. Cells exhibiting both PI and CAM are viable after optical injection of PI. Data was obtained 1.5 hours after collection from the chip and error bars are the standard error in the mean of three experimental runs.

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