Abstract

Femtosecond (fs) laser-based intracellular nanosurgery has become an important tool in cell biology, albeit the mechanisms in the so-called low-density plasma regime are largely unknown. Previous calculations of free-electron densities for intracellular surgery used water as a model substance for biological media and neglected the presence of dye and biomolecules. In addition, it is still unclear on which time scales free-electron and free-radical induced chemical effects take place in a cellular environment. Here, we present our experimental study on the influence of laser parameters and staining on the intracellular ablation threshold in the low-density plasma regime. We found that the ablation effect of fs laser pulse trains resulted from the accumulation of single-shot multiphoton-induced photochemical effects finished within a few nanoseconds. At the threshold, the number of applied pulses was inversely proportional to a higher order of the irradiance, depending on the laser repetition rate and wavelength. Furthermore, fluorescence staining of subcellular structures before surgery significantly decreased the ablation threshold. Based on our findings, we propose that dye molecules are the major source for providing seed electrons for the ionization cascade. Consequently, future calculations of free-electron densities for intracellular nanosurgery have to take them into account, especially in the calculations of multiphoton ionization rates.

© 2010 Optical Society of America

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  2. K. Koenig, I. Riemann, and W. Fritzsche, “Nanodissection of human chromosomes with near-infrared femtosecond laser pulses,” Opt. Lett. 26, 819–821 (2001).
  3. U. K. Tirlapur and K. Koenig, “Targeted transfection by femtosecond laser,” Nature 418, 290–291 (2002).
  4. W. Watanabe, N. Arakawa, T. Higashi, K. Fukui, K. Isobe, K. Itoh, and S. Matsunaga, “Femtosecond laser disruption of subcellular organelles in a living cell,” Opt. Express 12, 4203–4213 (2004).
  5. I. Maxwell, S. Chung, and E. Mazur, “Nanoprocessing of subcellular targets using femtosecond laser pulses,” Med. Laser Appl. 20, 193–200 (2005).
  6. M. F. Yanik, H. Cinar, H. N. Cinar, A. D. Chisholm, Y. Jin, and A. Ben-Yakar, “Functional regeneration after laser axotomy,” Nature 432, 822–822 (2004).
  7. W. Supatto, D. Debarre, B. Moulia, E. Brouzes, J. L. Martin, E. Farge, and E. Beaurepaire, “In vivo modulation of morphogenetic movements in Drosophila embryos with femtosecond laser pulses,” Proc. Natl. Acad. Sci. USA 102, 1047–1052 (2005).
  8. L. Sacconi, R. P. O’Connor, A. Jasaitis, A. Masi, M. Buffelli, and F. S. Pavone, “In vivo multiphoton nanosurgery on cortical neurons,” J. Biomed. Opt. 12, 050502 (2007).
  9. A. L. Allegra Mascaro, L. Sacconi, and F. S. Pavone, “Multi-photon nanosurgery in live brain,” Front. Neuroen-erg. 2, 21 (2010).
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  12. L. Sacconi, I. M. Tolic-Norrelykke, R. Antolini, and F. S. Pavone, “Combined intracellular three-dimensional imaging and selective nanosurgery by a nonlinear microscope,” J. Biomed. Opt. 10, 014002 (2005).
  13. S. Kumar, I. Z. Maxwell, A. Heisterkamp, T. R. Polte, T. P. Lele, M. Salanga, E. Mazur, and D. E. Ingber, “Viscoelastic retraction of single living stress fibers and its impact on cell shape, cytoskeletal organization, and extracellular matrix mechanics,” Biophys. J. 90, 3762–3773 (2006).
  14. T. Shimada, W. Watanabe, S. Matsunaga, T. Higashi, H. Ishii, K. Fukui, K. Isobe, and K. Itoh, “Intracellular disruption of mitochondria in a living HeLa cell with a 76-MHz femtosecond laser oscillator,” Opt. Express 13, 9869–9880 (2005).
  15. K. Kuetemeyer, A. Lucas-Hahn, B. Petersen, E. Lemme, P. Hassel, H. Niemann, and A. Heisterkamp, “Combined multiphoton imaging and automated functional enucleation of porcine oocytes using femtosecond laser pulses,” J. Biomed. Opt. 15, 046006 (2010).
  16. F. Bourgeois and A. Ben-Yakar, “Femtosecond laser nanoaxotomy properties and their effect on axonal recovery in C.elegans,” Opt. Express 15, 8521–8531 (2007).
  17. P. K. Kennedy, S. A. Boppart, D. X. Hammer, B. A. Rockwell, G. D. Noojin, and W.P. Roach, “A first-order model for computation of laser-induced breakdown thresholds in ocular and aqueous-media: part II - comparison to experiment,” IEEE J. Quantum Electron. 31, 2250–2257 (1995).
  18. A. Vogel, N. Linz, S. Freidank, and G. Paltauf, “Femtosecond-laser-induced nanocavitation in water: Implications for optical breakdown threshold and cell surgery,” Phys. Rev. Lett. 100, 038102 (2008).
  19. B. Boudaiffa, P. Cloutier, D. Hunting, M. A. Huels, and L. Sanche, “Resonant formation of DNA strand breaks by low-energy (3 to 20 eV) electrons,” Science 287, 1658–1660 (2000).
  20. L. Sanche, “Low energy electron-driven damage in biomolecules,” Eur. Phys. J. D 35, 367–390 (2005).
  21. D. N. Nikogosyan, A. A. Oraevsky, and V. I. Rupasov, “Two-photon ionization and dissociation of liquid water by powerful laser UV radiation,” Chem. Phys. 77, 131–143 (1983).
  22. F. Hutchinson, “Chemical-changes induced in DNA by ionizing-radiation,” Prog. Nucleic Acid Res. Mol. Biol. 32, 115–154 (1985).
  23. A. A. Oraevsky and D. N. Nikogosyan, “Picosecond two-quantum UV photochemistry of thymine in aqueous-solution,” Chem. Phys. 100, 429–445 (1985).
  24. U. K. Tirlapur, K. Koenig, C. Peuckert, R. Krieg, and K. J. Halbhuber, “Femtosecond near-infrared laser pulses elicit generation of reactive oxygen species in mammalian cells leading to apoptosis-like death,” Exp. Cell Res. 263, 88–97 (2001).
  25. J. Baumgart, K. Kuetemeyer, W. Bintig, A. Ngezahayo, W. Ertmer, H. Lubatschowski, and A. Heisterkamp, “Repetition rate dependency of reactive oxygen species formation during femtosecond laser-based cell surgery,” J. Biomed. Opt. 14, 054040 (2009).
  26. K. Kuetemeyer, J. Baumgart, H. Lubatschowski, and A. Heisterkamp, “Repetition rate dependency of low-density plasma effects during femtosecond-laser-based surgery of biological tissue,” Appl. Phys. B 97, 695–699 (2009).
  27. F. Bestvater, E. Spiess, G. Stobrawa, M. Hacker, T. Feurer, T. Porwol, U. Berchner-Pfannschmidt, C. Wotzlaw, and H. Acker, “Two-photon fluorescence absorption and emission spectra of dyes relevant for cell imaging,” J. Microsc-Oxford 208, 108–115 (2002).
  28. F. Helmchen and W. Denk, “Deep tissue two-photon microscopy,” Nat. Met. 2, 932–940 (2005).
  29. J. L. Boulnois, “Photophysical processes in recent medical laser developments: a review,” Laser Med. Sci. 1, 47–66 (1986).
  30. A. P. Reuvers, C. L. Greenstock, J. Borsa, and J. D. Chapman, “Studies on mechanism of chemical radioprotec-tion by dimethyl sulfoxide,” Int. J. Radiat. Biol. 24, 533–536 (1973).
  31. R. Roots and S. Okada, “Estimation of life times and diffusion distances of radicals involved in X-ray-induced DNA strand breaks or killing of mammalian cells,” Radiat. Res. 64, 306–320 (1975).
  32. J. F. Ward, “DNA damage produced by ionizing radiation in mammalian cells: identities, mechanisms of formation, and reparability,” Prog. Nucleic Acid Res. Mol. Biol. 35, 95–125 (1988).
  33. E. S. Williams, J. Stap, J. Essers, B. Ponnaiya, M. S. Luijsterburg, P. M. Krawczyk, R. L. Ullrich, J. A. Aten, and S. M. Bailey, “DNA double-strand breaks are not sufficient to initiate recruitment of TRF2,” Nat. Genet. 39, 696–698 (2007).
  34. C. Dinant, M. de Jager, J. Essers, W. A. van Cappellen, R. Kanaar, A. B. Houtsmuller, and W. Vermeulen, “Activation of multiple DNA repair pathways by subnuclear damage induction methods,” J. Cell Sci. 120, 2731–2740 (2007).
  35. J. E. Downing, W. M. Christopherson, and W. L. Broghamer, “Nuclear water content during carcinogenesis,” Cancer 15, 1176–1180 (1962).
  36. H. M. Golomb and G. F. Bahr, “Electron-microscopy of human interphase nuclei - determination of total dry mass and DNA-packing ratio,” Chromosoma 46, 233–245 (1974).
  37. F. G. Loontiens, P. Regenfuss, A. Zechel, L. Dumortier, and R. M. Clegg, “Binding characteristics of Hoechst 33258 with calf thymus DNA, Poly[d(A-T)], and d(CCGGAATTCCGG): multiple stoichiometries and determination of tight binding with a wide spectrum of site affinities,” Biochemistry-US 29, 9029–9039 (1990).
  38. I. Cohanoschi and F. E. Hernandez, “Surface plasmon enhancement of two- and three-photon absorption of Hoechst 33 258 dye in activated gold colloid solution,” J. Phys. Chem. B 109, 14506–14512 (2005).
  39. A. Rosenfeld, M. Lorenz, R. Stoian, and D. Ashkenasi, “Ultrashort-laser-pulse damage threshold of transparent materials and the role of incubation,” Appl. Phys. A 69, S373–S376 (1999).
  40. Y. Jee, M. F. Becker, and R. M. Walser, “Laser-induced damage on single-crystal metal surfaces,” J. Opt. Soc. Am. B 5, 648–659 (1988).
  41. F. Williams, S. P. Varma, and S. Hillenius, “Liquid water as a lone-pair amorphous-semiconductor,” J. Chem. Phys. 64, 1549–1554(1976).
  42. H. Goerner, “Direct and sensitized photoprocesses of bis-benzimidazole dyes and the effects of surfactants and DNA,” Photochem. Photobiol. 73, 339–348 (2001).
  43. E. Amouyal, A. Bernas, and D. Grand, “On the photoionization energy threshold of tryptophan in aqueous solutions,” Photochem. Photobiol. 29, 1071–1077 (1979).

2010 (2)

A. L. Allegra Mascaro, L. Sacconi, and F. S. Pavone, “Multi-photon nanosurgery in live brain,” Front. Neuroen-erg. 2, 21 (2010).

K. Kuetemeyer, A. Lucas-Hahn, B. Petersen, E. Lemme, P. Hassel, H. Niemann, and A. Heisterkamp, “Combined multiphoton imaging and automated functional enucleation of porcine oocytes using femtosecond laser pulses,” J. Biomed. Opt. 15, 046006 (2010).

2009 (2)

J. Baumgart, K. Kuetemeyer, W. Bintig, A. Ngezahayo, W. Ertmer, H. Lubatschowski, and A. Heisterkamp, “Repetition rate dependency of reactive oxygen species formation during femtosecond laser-based cell surgery,” J. Biomed. Opt. 14, 054040 (2009).

K. Kuetemeyer, J. Baumgart, H. Lubatschowski, and A. Heisterkamp, “Repetition rate dependency of low-density plasma effects during femtosecond-laser-based surgery of biological tissue,” Appl. Phys. B 97, 695–699 (2009).

2008 (1)

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

2007 (4)

E. S. Williams, J. Stap, J. Essers, B. Ponnaiya, M. S. Luijsterburg, P. M. Krawczyk, R. L. Ullrich, J. A. Aten, and S. M. Bailey, “DNA double-strand breaks are not sufficient to initiate recruitment of TRF2,” Nat. Genet. 39, 696–698 (2007).

C. Dinant, M. de Jager, J. Essers, W. A. van Cappellen, R. Kanaar, A. B. Houtsmuller, and W. Vermeulen, “Activation of multiple DNA repair pathways by subnuclear damage induction methods,” J. Cell Sci. 120, 2731–2740 (2007).

F. Bourgeois and A. Ben-Yakar, “Femtosecond laser nanoaxotomy properties and their effect on axonal recovery in C.elegans,” Opt. Express 15, 8521–8531 (2007).

L. Sacconi, R. P. O’Connor, A. Jasaitis, A. Masi, M. Buffelli, and F. S. Pavone, “In vivo multiphoton nanosurgery on cortical neurons,” J. Biomed. Opt. 12, 050502 (2007).

2006 (1)

S. Kumar, I. Z. Maxwell, A. Heisterkamp, T. R. Polte, T. P. Lele, M. Salanga, E. Mazur, and D. E. Ingber, “Viscoelastic retraction of single living stress fibers and its impact on cell shape, cytoskeletal organization, and extracellular matrix mechanics,” Biophys. J. 90, 3762–3773 (2006).

2005 (9)

T. Shimada, W. Watanabe, S. Matsunaga, T. Higashi, H. Ishii, K. Fukui, K. Isobe, and K. Itoh, “Intracellular disruption of mitochondria in a living HeLa cell with a 76-MHz femtosecond laser oscillator,” Opt. Express 13, 9869–9880 (2005).

A. Vogel, J. Noack, G. Huettman, and G. Paltauf, “Mechanisms of femtosecond laser nanosurgery of cells and tissues,” Appl. Phys. B 81, 1015–1047 (2005).

A. Heisterkamp, I. Z. Maxwell, J. M. Underwood, J. A. Nickerson, S. Kumar, D. E. Ingber, and E. Mazur, “Pulse energy dependence of subcellular dissection by femtosecond laser pulses,” Opt. Express 13, 3690–3696 (2005).

L. Sacconi, I. M. Tolic-Norrelykke, R. Antolini, and F. S. Pavone, “Combined intracellular three-dimensional imaging and selective nanosurgery by a nonlinear microscope,” J. Biomed. Opt. 10, 014002 (2005).

W. Supatto, D. Debarre, B. Moulia, E. Brouzes, J. L. Martin, E. Farge, and E. Beaurepaire, “In vivo modulation of morphogenetic movements in Drosophila embryos with femtosecond laser pulses,” Proc. Natl. Acad. Sci. USA 102, 1047–1052 (2005).

I. Maxwell, S. Chung, and E. Mazur, “Nanoprocessing of subcellular targets using femtosecond laser pulses,” Med. Laser Appl. 20, 193–200 (2005).

F. Helmchen and W. Denk, “Deep tissue two-photon microscopy,” Nat. Met. 2, 932–940 (2005).

L. Sanche, “Low energy electron-driven damage in biomolecules,” Eur. Phys. J. D 35, 367–390 (2005).

I. Cohanoschi and F. E. Hernandez, “Surface plasmon enhancement of two- and three-photon absorption of Hoechst 33 258 dye in activated gold colloid solution,” J. Phys. Chem. B 109, 14506–14512 (2005).

2004 (2)

M. F. Yanik, H. Cinar, H. N. Cinar, A. D. Chisholm, Y. Jin, and A. Ben-Yakar, “Functional regeneration after laser axotomy,” Nature 432, 822–822 (2004).

W. Watanabe, N. Arakawa, T. Higashi, K. Fukui, K. Isobe, K. Itoh, and S. Matsunaga, “Femtosecond laser disruption of subcellular organelles in a living cell,” Opt. Express 12, 4203–4213 (2004).

2002 (2)

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

F. Bestvater, E. Spiess, G. Stobrawa, M. Hacker, T. Feurer, T. Porwol, U. Berchner-Pfannschmidt, C. Wotzlaw, and H. Acker, “Two-photon fluorescence absorption and emission spectra of dyes relevant for cell imaging,” J. Microsc-Oxford 208, 108–115 (2002).

2001 (3)

U. K. Tirlapur, K. Koenig, C. Peuckert, R. Krieg, and K. J. Halbhuber, “Femtosecond near-infrared laser pulses elicit generation of reactive oxygen species in mammalian cells leading to apoptosis-like death,” Exp. Cell Res. 263, 88–97 (2001).

K. Koenig, I. Riemann, and W. Fritzsche, “Nanodissection of human chromosomes with near-infrared femtosecond laser pulses,” Opt. Lett. 26, 819–821 (2001).

H. Goerner, “Direct and sensitized photoprocesses of bis-benzimidazole dyes and the effects of surfactants and DNA,” Photochem. Photobiol. 73, 339–348 (2001).

2000 (1)

B. Boudaiffa, P. Cloutier, D. Hunting, M. A. Huels, and L. Sanche, “Resonant formation of DNA strand breaks by low-energy (3 to 20 eV) electrons,” Science 287, 1658–1660 (2000).

1999 (2)

K. Koenig, I. Riemann, P. Fischer, and K. H. Halbhuber, “Intracellular nanosurgery with near infrared femtosecond laser pulses,” Cell Mol. Biol. 45, 195–201 (1999).

A. Rosenfeld, M. Lorenz, R. Stoian, and D. Ashkenasi, “Ultrashort-laser-pulse damage threshold of transparent materials and the role of incubation,” Appl. Phys. A 69, S373–S376 (1999).

1995 (1)

P. K. Kennedy, S. A. Boppart, D. X. Hammer, B. A. Rockwell, G. D. Noojin, and W.P. Roach, “A first-order model for computation of laser-induced breakdown thresholds in ocular and aqueous-media: part II - comparison to experiment,” IEEE J. Quantum Electron. 31, 2250–2257 (1995).

1990 (1)

F. G. Loontiens, P. Regenfuss, A. Zechel, L. Dumortier, and R. M. Clegg, “Binding characteristics of Hoechst 33258 with calf thymus DNA, Poly[d(A-T)], and d(CCGGAATTCCGG): multiple stoichiometries and determination of tight binding with a wide spectrum of site affinities,” Biochemistry-US 29, 9029–9039 (1990).

1988 (2)

Y. Jee, M. F. Becker, and R. M. Walser, “Laser-induced damage on single-crystal metal surfaces,” J. Opt. Soc. Am. B 5, 648–659 (1988).

J. F. Ward, “DNA damage produced by ionizing radiation in mammalian cells: identities, mechanisms of formation, and reparability,” Prog. Nucleic Acid Res. Mol. Biol. 35, 95–125 (1988).

1986 (1)

J. L. Boulnois, “Photophysical processes in recent medical laser developments: a review,” Laser Med. Sci. 1, 47–66 (1986).

1985 (2)

F. Hutchinson, “Chemical-changes induced in DNA by ionizing-radiation,” Prog. Nucleic Acid Res. Mol. Biol. 32, 115–154 (1985).

A. A. Oraevsky and D. N. Nikogosyan, “Picosecond two-quantum UV photochemistry of thymine in aqueous-solution,” Chem. Phys. 100, 429–445 (1985).

1983 (1)

D. N. Nikogosyan, A. A. Oraevsky, and V. I. Rupasov, “Two-photon ionization and dissociation of liquid water by powerful laser UV radiation,” Chem. Phys. 77, 131–143 (1983).

1979 (1)

E. Amouyal, A. Bernas, and D. Grand, “On the photoionization energy threshold of tryptophan in aqueous solutions,” Photochem. Photobiol. 29, 1071–1077 (1979).

1976 (1)

F. Williams, S. P. Varma, and S. Hillenius, “Liquid water as a lone-pair amorphous-semiconductor,” J. Chem. Phys. 64, 1549–1554(1976).

1975 (1)

R. Roots and S. Okada, “Estimation of life times and diffusion distances of radicals involved in X-ray-induced DNA strand breaks or killing of mammalian cells,” Radiat. Res. 64, 306–320 (1975).

1974 (1)

H. M. Golomb and G. F. Bahr, “Electron-microscopy of human interphase nuclei - determination of total dry mass and DNA-packing ratio,” Chromosoma 46, 233–245 (1974).

1973 (1)

A. P. Reuvers, C. L. Greenstock, J. Borsa, and J. D. Chapman, “Studies on mechanism of chemical radioprotec-tion by dimethyl sulfoxide,” Int. J. Radiat. Biol. 24, 533–536 (1973).

1962 (1)

J. E. Downing, W. M. Christopherson, and W. L. Broghamer, “Nuclear water content during carcinogenesis,” Cancer 15, 1176–1180 (1962).

Acker, H.

F. Bestvater, E. Spiess, G. Stobrawa, M. Hacker, T. Feurer, T. Porwol, U. Berchner-Pfannschmidt, C. Wotzlaw, and H. Acker, “Two-photon fluorescence absorption and emission spectra of dyes relevant for cell imaging,” J. Microsc-Oxford 208, 108–115 (2002).

Amouyal, E.

E. Amouyal, A. Bernas, and D. Grand, “On the photoionization energy threshold of tryptophan in aqueous solutions,” Photochem. Photobiol. 29, 1071–1077 (1979).

Antolini, R.

L. Sacconi, I. M. Tolic-Norrelykke, R. Antolini, and F. S. Pavone, “Combined intracellular three-dimensional imaging and selective nanosurgery by a nonlinear microscope,” J. Biomed. Opt. 10, 014002 (2005).

Arakawa, N.

Ashkenasi, D.

A. Rosenfeld, M. Lorenz, R. Stoian, and D. Ashkenasi, “Ultrashort-laser-pulse damage threshold of transparent materials and the role of incubation,” Appl. Phys. A 69, S373–S376 (1999).

Aten, J. A.

E. S. Williams, J. Stap, J. Essers, B. Ponnaiya, M. S. Luijsterburg, P. M. Krawczyk, R. L. Ullrich, J. A. Aten, and S. M. Bailey, “DNA double-strand breaks are not sufficient to initiate recruitment of TRF2,” Nat. Genet. 39, 696–698 (2007).

Bahr, G. F.

H. M. Golomb and G. F. Bahr, “Electron-microscopy of human interphase nuclei - determination of total dry mass and DNA-packing ratio,” Chromosoma 46, 233–245 (1974).

Bailey, S. M.

E. S. Williams, J. Stap, J. Essers, B. Ponnaiya, M. S. Luijsterburg, P. M. Krawczyk, R. L. Ullrich, J. A. Aten, and S. M. Bailey, “DNA double-strand breaks are not sufficient to initiate recruitment of TRF2,” Nat. Genet. 39, 696–698 (2007).

Baumgart, J.

J. Baumgart, K. Kuetemeyer, W. Bintig, A. Ngezahayo, W. Ertmer, H. Lubatschowski, and A. Heisterkamp, “Repetition rate dependency of reactive oxygen species formation during femtosecond laser-based cell surgery,” J. Biomed. Opt. 14, 054040 (2009).

K. Kuetemeyer, J. Baumgart, H. Lubatschowski, and A. Heisterkamp, “Repetition rate dependency of low-density plasma effects during femtosecond-laser-based surgery of biological tissue,” Appl. Phys. B 97, 695–699 (2009).

Beaurepaire, E.

W. Supatto, D. Debarre, B. Moulia, E. Brouzes, J. L. Martin, E. Farge, and E. Beaurepaire, “In vivo modulation of morphogenetic movements in Drosophila embryos with femtosecond laser pulses,” Proc. Natl. Acad. Sci. USA 102, 1047–1052 (2005).

Becker, M. F.

Y. Jee, M. F. Becker, and R. M. Walser, “Laser-induced damage on single-crystal metal surfaces,” J. Opt. Soc. Am. B 5, 648–659 (1988).

Ben-Yakar, A.

F. Bourgeois and A. Ben-Yakar, “Femtosecond laser nanoaxotomy properties and their effect on axonal recovery in C.elegans,” Opt. Express 15, 8521–8531 (2007).

M. F. Yanik, H. Cinar, H. N. Cinar, A. D. Chisholm, Y. Jin, and A. Ben-Yakar, “Functional regeneration after laser axotomy,” Nature 432, 822–822 (2004).

Berchner-Pfannschmidt, U.

F. Bestvater, E. Spiess, G. Stobrawa, M. Hacker, T. Feurer, T. Porwol, U. Berchner-Pfannschmidt, C. Wotzlaw, and H. Acker, “Two-photon fluorescence absorption and emission spectra of dyes relevant for cell imaging,” J. Microsc-Oxford 208, 108–115 (2002).

Bernas, A.

E. Amouyal, A. Bernas, and D. Grand, “On the photoionization energy threshold of tryptophan in aqueous solutions,” Photochem. Photobiol. 29, 1071–1077 (1979).

Bestvater, F.

F. Bestvater, E. Spiess, G. Stobrawa, M. Hacker, T. Feurer, T. Porwol, U. Berchner-Pfannschmidt, C. Wotzlaw, and H. Acker, “Two-photon fluorescence absorption and emission spectra of dyes relevant for cell imaging,” J. Microsc-Oxford 208, 108–115 (2002).

Bintig, W.

J. Baumgart, K. Kuetemeyer, W. Bintig, A. Ngezahayo, W. Ertmer, H. Lubatschowski, and A. Heisterkamp, “Repetition rate dependency of reactive oxygen species formation during femtosecond laser-based cell surgery,” J. Biomed. Opt. 14, 054040 (2009).

Boppart, S. A.

P. K. Kennedy, S. A. Boppart, D. X. Hammer, B. A. Rockwell, G. D. Noojin, and W.P. Roach, “A first-order model for computation of laser-induced breakdown thresholds in ocular and aqueous-media: part II - comparison to experiment,” IEEE J. Quantum Electron. 31, 2250–2257 (1995).

Borsa, J.

A. P. Reuvers, C. L. Greenstock, J. Borsa, and J. D. Chapman, “Studies on mechanism of chemical radioprotec-tion by dimethyl sulfoxide,” Int. J. Radiat. Biol. 24, 533–536 (1973).

Boudaiffa, B.

B. Boudaiffa, P. Cloutier, D. Hunting, M. A. Huels, and L. Sanche, “Resonant formation of DNA strand breaks by low-energy (3 to 20 eV) electrons,” Science 287, 1658–1660 (2000).

Boulnois, J. L.

J. L. Boulnois, “Photophysical processes in recent medical laser developments: a review,” Laser Med. Sci. 1, 47–66 (1986).

Bourgeois, F.

Broghamer, W. L.

J. E. Downing, W. M. Christopherson, and W. L. Broghamer, “Nuclear water content during carcinogenesis,” Cancer 15, 1176–1180 (1962).

Brouzes, E.

W. Supatto, D. Debarre, B. Moulia, E. Brouzes, J. L. Martin, E. Farge, and E. Beaurepaire, “In vivo modulation of morphogenetic movements in Drosophila embryos with femtosecond laser pulses,” Proc. Natl. Acad. Sci. USA 102, 1047–1052 (2005).

Buffelli, M.

L. Sacconi, R. P. O’Connor, A. Jasaitis, A. Masi, M. Buffelli, and F. S. Pavone, “In vivo multiphoton nanosurgery on cortical neurons,” J. Biomed. Opt. 12, 050502 (2007).

Chapman, J. D.

A. P. Reuvers, C. L. Greenstock, J. Borsa, and J. D. Chapman, “Studies on mechanism of chemical radioprotec-tion by dimethyl sulfoxide,” Int. J. Radiat. Biol. 24, 533–536 (1973).

Chisholm, A. D.

M. F. Yanik, H. Cinar, H. N. Cinar, A. D. Chisholm, Y. Jin, and A. Ben-Yakar, “Functional regeneration after laser axotomy,” Nature 432, 822–822 (2004).

Christopherson, W. M.

J. E. Downing, W. M. Christopherson, and W. L. Broghamer, “Nuclear water content during carcinogenesis,” Cancer 15, 1176–1180 (1962).

Chung, S.

I. Maxwell, S. Chung, and E. Mazur, “Nanoprocessing of subcellular targets using femtosecond laser pulses,” Med. Laser Appl. 20, 193–200 (2005).

Cinar, H.

M. F. Yanik, H. Cinar, H. N. Cinar, A. D. Chisholm, Y. Jin, and A. Ben-Yakar, “Functional regeneration after laser axotomy,” Nature 432, 822–822 (2004).

Cinar, H. N.

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K. Koenig, I. Riemann, and W. Fritzsche, “Nanodissection of human chromosomes with near-infrared femtosecond laser pulses,” Opt. Lett. 26, 819–821 (2001).

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Figures (6)

Fig. 1.
Fig. 1.

Schematic setup for multiphoton imaging and manipulation of single cells.

Fig. 2.
Fig. 2.

(a,b) Multiphoton microscopy images of live Hoechst stained cell nuclei directly after and two minutes after line cutting (indicated by black triangles) and after re-staining. At pulse energies in the photobleaching regime, a clear dip in fluorescence could be observed after a few minutes. Above the ablation threshold, the dip in fluorescence occurred directly after irradiation. Scale bar: 3 μm. (c) Ablation probability as a function of the pulse energy at a fixed repetition rate of 40 kHz, a central wavelength of 720 nm and 200 pulses per micrometer (n ≥ 20 for each data point).

Fig. 3.
Fig. 3.

(a) Ablation threshold pulse energy for line cuts in live Hoechst stained cell nuclei as a function of the repetition rate at different numbers of pulses per micrometer. No significant influence of the repetition rate was observed. (b) Ablation threshold irradiance as a function of the exposure time per micrometer at a fixed repetition rate of 40 kHz. The exposure time was inversely proportional to approximately the fourth power of irradiance (solid line). A central wavelength of 720 nm was used in all cases. Each data point represents the mean ± standard deviation of at least five experiments.

Fig. 4.
Fig. 4.

Influence of Hoechst staining on the ablation threshold for line cuts in fixed cell nuclei. A central wavelength of 720 nm and 20,000 pulses per micrometer were used. Multiphoton microscopy images of (a) Hoechst / FM4-64 stained and (b) FM4-64 stained cell nuclei (a1;b1) before and (a2;b2) after line cutting at 1.5 nJ pulse energy (indicated by black triangles) and Hoechst re-staining. Scale bar: 3 μm. (c) Ablation probability as a function of the logarithmic pulse energy with and without Hoechst staining before line cutting. The ablation threshold was a factor four lower with Hoechst staining (n=3 experiments for each data point, the values represent the means ± standard deviation).

Fig. 5.
Fig. 5.

(a) Wavelength dependence of the ablation threshold pulse energy as a function of the number of applied pulses on a single spot in live Hoechst stained cell nuclei at repetition rates in the kHz regime. Solid lines show the power-law fits for each wavelength. Between 840 and 950 nm, the scaling exponent increased from k=4 to k=5. (b) Scaling exponent k as a function of the laser wavelength at different repetition rates in the kHz regime and 80 MHz. Each data point represents the mean ± standard deviation of at least three experiments.

Fig. 6.
Fig. 6.

FWHM-widths of the damaged region in live Hoechst stained cell nuclei as a function of the pulse energy at a central wavelength of 720 nm and different repetition rates. The dashed lines indicate the ablation threshold. Each data point represents the mean ± standard deviation of at least ten cells. (a) 2,000 pulses per micrometer and (b) 40,000 pulses per micrometer were used. No significant influence of the repetition rate was observed up to 4 MHz. The increase of the FWHM-width was significantly stronger at 80 MHz.

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