Abstract

Single cell isolation is a prerequisite for the analysis of rare or small cell subtypes. Here, we selectively detach single cells in a heterogeneous population comprised of different morphological subtypes whose sizes vary in body and extension. Such a cellular environment is first accommodated for by a photomechanical method in which pulsed laser irradiation produces microbubbles from a polymer substrate, thus pushing out and detaching cultured cells in an intact, viable, and spatially tailored way. While this has previously only bene used at a very low cell density with lack of quantitative characterization, we determine optimal detachment conditions for different cell sizes in terms of an optical fluence and the number of laser pulses. Importantly, our approach is employed to isolate cancer cells with inherent size variation and elucidate cellular heterogeneity in drug sensitivity: i.e., higher resistance for larger cell size. For cells detached by laser-induced microbubbles, morphology, proliferation, and viability are compared with those of conventional trypsin-treated cells detached without any spatial selectivity. These results support the suitability of our photomechanical method for biochemical screen and secondary analysis of cells with unusual responses.

© 2019 Optical Society of America under the terms of the OSA Open Access Publishing Agreement

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References

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2018 (1)

J. Chen, N. Niu, J. Zhang, L. Qi, W. Shen, K. Donkena, Z. Feng, and J. Liu, “Polyploid Giant Cancer Cells (PGCCs): The Evil Roots of Cancer,” Curr. Cancer Drug Targets 18, 1–8 (2018).
[PubMed]

2017 (3)

Y. C. Chen, H. W. Baac, K. T. Lee, S. Fouladdel, K. Teichert, J. G. Ok, Y. H. Cheng, P. N. Ingram, A. J. Hart, E. Azizi, L. J. Guo, M. S. Wicha, and E. Yoon, “Selective photomechanical detachment and retrieval of divided sister cells from enclosed microfluidics for downstream analyses,” ACS Nano 11(5), 4660–4668 (2017).
[Crossref] [PubMed]

N. McGranahan and C. Swanton, “Clonal heterogeneity and tumor evolution: past, present, and the future,” Cell 168(4), 613–628 (2017).
[Crossref] [PubMed]

Y. Song, A. K. Kaster, J. Vollmers, Y. Song, P. A. Davison, M. Frentrup, G. M. Preston, I. P. Thompson, J. C. Murrell, H. Yin, C. N. Hunter, and W. E. Huang, “Single-cell genomics based on Raman sorting reveals novel carotenoid-containing bacteria in the Red Sea,” Microb. Biotechnol. 10(1), 125–137 (2017).
[Crossref] [PubMed]

2016 (3)

J. Han, Y. Jun, S. H. Kim, H.-H. Hoang, Y. Jung, S. Kim, J. Kim, R. H. Austin, S. Lee, and S. Park, “Rapid emergence and mechanisms of resistance by U87 glioblastoma cells to doxorubicin in an in vitro tumor microfluidic ecology,” Proc. Natl. Acad. Sci. U.S.A. 113(50), 14283–14288 (2016).
[Crossref] [PubMed]

P. Hu, W. Zhang, H. Xin, and G. Deng, “Single cell isolation and analysis,” Front. Cell Dev. Biol. 4, 116 (2016).
[Crossref] [PubMed]

L. R. Rau, W. Y. Huang, J. W. Liaw, and S. W. Tsai, “Photothermal effects of laser-activated surface plasmonic gold nanoparticles on the apoptosis and osteogenesis of osteoblast-like cells,” Int. J. Nanomedicine 11, 3461–3473 (2016).
[Crossref] [PubMed]

2015 (6)

A. K. Velichko, N. V. Petrova, S. V. Razin, and O. L. Kantidze, “Mechanism of heat stress-induced cellular senescence elucidates the exclusive vulnerability of early S-phase cells to mild genotoxic stress,” Nucleic Acids Res. 43(13), 6309–6320 (2015).
[Crossref] [PubMed]

A. Gross, J. Schoendube, S. Zimmermann, M. Steeb, R. Zengerle, and P. Koltay, “Technologies for single-cell isolation,” Int. J. Mol. Sci. 16(8), 16897–16919 (2015).
[Crossref] [PubMed]

N. E. Navin, “The first five years of single-cell cancer genomics and beyond,” Genome Res. 25(10), 1499–1507 (2015).
[Crossref] [PubMed]

C. W. Shields, C. D. Reyes, and G. P. López, “Microfluidic cell sorting: a review of the advances in the separation of cells from debulking to rare cell isolation,” Lab Chip 15(5), 1230–1249 (2015).
[Crossref] [PubMed]

Y. Ebihara, R. Ota, T. Noriki, M. Shimojo, and K. Kajikawa, “Biometamaterials: Black Ultrathin Gold Film Fabricated on Lotus Leaf,” Sci. Rep. 5(1), 15992 (2015).
[Crossref] [PubMed]

S. Datta, L. Malhotra, R. Dickerson, S. Chaffee, C. K. Sen, and S. Roy, “Laser capture microdissection: Big data from small samples,” Histol. Histopathol. 30(11), 1255–1269 (2015).
[PubMed]

2014 (2)

P. C. Blainey and S. R. Quake, “Dissecting genomic diversity, one cell at a time,” Nat. Methods 11(1), 19–21 (2014).
[Crossref] [PubMed]

S. Zhang, I. Mercado-Uribe, Z. Xing, B. Sun, J. Kuang, and J. Liu, “Generation of cancer stem-like cells through the formation of polyploid giant cancer cells,” Oncogene 33(1), 116–128 (2014).
[Crossref] [PubMed]

2013 (2)

P. Duesberg and A. McCormack, “Immortality of cancers: a consequence of inherent karyotypic variations and selections for autonomy,” Cell Cycle 12(5), 783–802 (2013).
[Crossref] [PubMed]

Y. Wang, Y. Ji, E. S. Wharfe, R. S. Meadows, P. March, R. Goodacre, J. Xu, and W. E. Huang, “Raman activated cell ejection for isolation of single cells,” Anal. Chem. 85(22), 10697–10701 (2013).
[Crossref] [PubMed]

2012 (1)

H. W. Baac, J. G. Ok, A. Maxwell, K. T. Lee, Y. C. Chen, A. J. Hart, Z. Xu, E. Yoon, and L. J. Guo, “Carbon-nanotube optoacoustic lens for focused ultrasound generation and high-precision targeted therapy,” Sci. Rep. 2(1), 989 (2012).
[Crossref] [PubMed]

2011 (3)

T. H. Wu, T. Teslaa, S. Kalim, C. T. French, S. Moghadam, R. Wall, J. F. Miller, O. N. Witte, M. A. Teitell, and P. Y. Chiou, “Photothermal nanoblade for large cargo delivery into mammalian cells,” Anal. Chem. 83(4), 1321–1327 (2011).
[Crossref] [PubMed]

K. K. Elineni and N. D. Gallant, “Regulation of cell adhesion strength by peripheral focal adhesion distribution,” Biophys. J. 101(12), 2903–2911 (2011).
[Crossref] [PubMed]

T. Sada, T. Fujigaya, Y. Niidome, K. Nakazawa, and N. Nakashima, “Near-IR laser-triggered target cell collection using a carbon nanotube-based cell-cultured substrate,” ACS Nano 5(6), 4414–4421 (2011).
[Crossref] [PubMed]

2010 (4)

E. Y. Lukianova-Hleb, L. J. Anderson, S. Lee, J. H. Hafner, and D. O. Lapotko, “Hot plasmonic interactions: a new look at the photothermal efficacy of gold nanoparticles,” Phys. Chem. Chem. Phys. 12(38), 12237–12244 (2010).
[Crossref] [PubMed]

A. Marusyk and K. Polyak, “Tumor heterogeneity: causes and consequences,” Biochim. Biophys. Acta 1805(1), 105–117 (2010).
[PubMed]

H. Won Baac, J. G. Ok, H. J. Park, T. Ling, S.-L. Chen, A. J. Hart, and L. J. Guo, “Carbon nanotube composite optoacoustic transmitters for strong and high frequency ultrasound generation,” Appl. Phys. Lett. 97(23), 234104 (2010).
[Crossref] [PubMed]

D. R. Gossett, W. M. Weaver, A. J. Mach, S. C. Hur, H. T. Tse, W. Lee, H. Amini, and D. Di Carlo, “Label-free cell separation and sorting in microfluidic systems,” Anal. Bioanal. Chem. 397(8), 3249–3267 (2010).
[Crossref] [PubMed]

2008 (1)

B. A. Weaver and D. W. Cleveland, “The aneuploidy paradox in cell growth and tumorigenesis,” Cancer Cell 14(6), 431–433 (2008).
[Crossref] [PubMed]

2007 (1)

V. Espina, M. Heiby, M. Pierobon, and L. A. Liotta, “Laser capture microdissection technology,” Expert Rev. Mol. Diagn. 7(5), 647–657 (2007).
[Crossref] [PubMed]

2006 (1)

G. M. Whitesides, “The origins and the future of microfluidics,” Nature 442(7101), 368–373 (2006).
[Crossref] [PubMed]

2004 (1)

S. P. Perfetto, P. K. Chattopadhyay, and M. Roederer, “Seventeen-colour flow cytometry: unravelling the immune system,” Nat. Rev. Immunol. 4(8), 648–655 (2004).
[Crossref] [PubMed]

2000 (1)

N. J. Sucher, D. L. Deitcher, D. J. Baro, R. M. Warrick, and E. Guenther, “Genes and channels: patch/voltage-clamp analysis and single-cell RT-PCR,” Cell Tissue Res. 302(3), 295–307 (2000).
[Crossref] [PubMed]

1998 (2)

Y. Xia and G. M. Whitesides, “Soft lithography,” Angew. Chem. Int. Ed. Engl. 37(5), 550–575 (1998).
[Crossref] [PubMed]

K. K. Karukstis, E. H. Thompson, J. A. Whiles, and R. J. Rosenfeld, “Deciphering the fluorescence signature of daunomycin and doxorubicin,” Biophys. Chem. 73(3), 249–263 (1998).
[Crossref] [PubMed]

1995 (1)

G. P. Dimri, X. Lee, G. Basile, M. Acosta, G. Scott, C. Roskelley, E. E. Medrano, M. Linskens, I. Rubelj, and O. Pereira-Smith, “A biomarker that identifies senescent human cells in culture and in aging skin in vivo,” Proc. Natl. Acad. Sci. U.S.A. 92(20), 9363–9367 (1995).
[Crossref] [PubMed]

1987 (1)

1977 (1)

R. S. Molday, S. P. Yen, and A. Rembaum, “Application of magnetic microspheres in labelling and separation of cells,” Nature 268(5619), 437–438 (1977).
[Crossref] [PubMed]

Acosta, M.

G. P. Dimri, X. Lee, G. Basile, M. Acosta, G. Scott, C. Roskelley, E. E. Medrano, M. Linskens, I. Rubelj, and O. Pereira-Smith, “A biomarker that identifies senescent human cells in culture and in aging skin in vivo,” Proc. Natl. Acad. Sci. U.S.A. 92(20), 9363–9367 (1995).
[Crossref] [PubMed]

Amini, H.

D. R. Gossett, W. M. Weaver, A. J. Mach, S. C. Hur, H. T. Tse, W. Lee, H. Amini, and D. Di Carlo, “Label-free cell separation and sorting in microfluidic systems,” Anal. Bioanal. Chem. 397(8), 3249–3267 (2010).
[Crossref] [PubMed]

Anderson, L. J.

E. Y. Lukianova-Hleb, L. J. Anderson, S. Lee, J. H. Hafner, and D. O. Lapotko, “Hot plasmonic interactions: a new look at the photothermal efficacy of gold nanoparticles,” Phys. Chem. Chem. Phys. 12(38), 12237–12244 (2010).
[Crossref] [PubMed]

Austin, R. H.

J. Han, Y. Jun, S. H. Kim, H.-H. Hoang, Y. Jung, S. Kim, J. Kim, R. H. Austin, S. Lee, and S. Park, “Rapid emergence and mechanisms of resistance by U87 glioblastoma cells to doxorubicin in an in vitro tumor microfluidic ecology,” Proc. Natl. Acad. Sci. U.S.A. 113(50), 14283–14288 (2016).
[Crossref] [PubMed]

Azizi, E.

Y. C. Chen, H. W. Baac, K. T. Lee, S. Fouladdel, K. Teichert, J. G. Ok, Y. H. Cheng, P. N. Ingram, A. J. Hart, E. Azizi, L. J. Guo, M. S. Wicha, and E. Yoon, “Selective photomechanical detachment and retrieval of divided sister cells from enclosed microfluidics for downstream analyses,” ACS Nano 11(5), 4660–4668 (2017).
[Crossref] [PubMed]

Baac, H. W.

Y. C. Chen, H. W. Baac, K. T. Lee, S. Fouladdel, K. Teichert, J. G. Ok, Y. H. Cheng, P. N. Ingram, A. J. Hart, E. Azizi, L. J. Guo, M. S. Wicha, and E. Yoon, “Selective photomechanical detachment and retrieval of divided sister cells from enclosed microfluidics for downstream analyses,” ACS Nano 11(5), 4660–4668 (2017).
[Crossref] [PubMed]

H. W. Baac, J. G. Ok, A. Maxwell, K. T. Lee, Y. C. Chen, A. J. Hart, Z. Xu, E. Yoon, and L. J. Guo, “Carbon-nanotube optoacoustic lens for focused ultrasound generation and high-precision targeted therapy,” Sci. Rep. 2(1), 989 (2012).
[Crossref] [PubMed]

Baro, D. J.

N. J. Sucher, D. L. Deitcher, D. J. Baro, R. M. Warrick, and E. Guenther, “Genes and channels: patch/voltage-clamp analysis and single-cell RT-PCR,” Cell Tissue Res. 302(3), 295–307 (2000).
[Crossref] [PubMed]

Basile, G.

G. P. Dimri, X. Lee, G. Basile, M. Acosta, G. Scott, C. Roskelley, E. E. Medrano, M. Linskens, I. Rubelj, and O. Pereira-Smith, “A biomarker that identifies senescent human cells in culture and in aging skin in vivo,” Proc. Natl. Acad. Sci. U.S.A. 92(20), 9363–9367 (1995).
[Crossref] [PubMed]

Blainey, P. C.

P. C. Blainey and S. R. Quake, “Dissecting genomic diversity, one cell at a time,” Nat. Methods 11(1), 19–21 (2014).
[Crossref] [PubMed]

Chaffee, S.

S. Datta, L. Malhotra, R. Dickerson, S. Chaffee, C. K. Sen, and S. Roy, “Laser capture microdissection: Big data from small samples,” Histol. Histopathol. 30(11), 1255–1269 (2015).
[PubMed]

Chattopadhyay, P. K.

S. P. Perfetto, P. K. Chattopadhyay, and M. Roederer, “Seventeen-colour flow cytometry: unravelling the immune system,” Nat. Rev. Immunol. 4(8), 648–655 (2004).
[Crossref] [PubMed]

Chen, J.

J. Chen, N. Niu, J. Zhang, L. Qi, W. Shen, K. Donkena, Z. Feng, and J. Liu, “Polyploid Giant Cancer Cells (PGCCs): The Evil Roots of Cancer,” Curr. Cancer Drug Targets 18, 1–8 (2018).
[PubMed]

Chen, S.-L.

H. Won Baac, J. G. Ok, H. J. Park, T. Ling, S.-L. Chen, A. J. Hart, and L. J. Guo, “Carbon nanotube composite optoacoustic transmitters for strong and high frequency ultrasound generation,” Appl. Phys. Lett. 97(23), 234104 (2010).
[Crossref] [PubMed]

Chen, Y. C.

Y. C. Chen, H. W. Baac, K. T. Lee, S. Fouladdel, K. Teichert, J. G. Ok, Y. H. Cheng, P. N. Ingram, A. J. Hart, E. Azizi, L. J. Guo, M. S. Wicha, and E. Yoon, “Selective photomechanical detachment and retrieval of divided sister cells from enclosed microfluidics for downstream analyses,” ACS Nano 11(5), 4660–4668 (2017).
[Crossref] [PubMed]

H. W. Baac, J. G. Ok, A. Maxwell, K. T. Lee, Y. C. Chen, A. J. Hart, Z. Xu, E. Yoon, and L. J. Guo, “Carbon-nanotube optoacoustic lens for focused ultrasound generation and high-precision targeted therapy,” Sci. Rep. 2(1), 989 (2012).
[Crossref] [PubMed]

Cheng, Y. H.

Y. C. Chen, H. W. Baac, K. T. Lee, S. Fouladdel, K. Teichert, J. G. Ok, Y. H. Cheng, P. N. Ingram, A. J. Hart, E. Azizi, L. J. Guo, M. S. Wicha, and E. Yoon, “Selective photomechanical detachment and retrieval of divided sister cells from enclosed microfluidics for downstream analyses,” ACS Nano 11(5), 4660–4668 (2017).
[Crossref] [PubMed]

Chiou, P. Y.

T. H. Wu, T. Teslaa, S. Kalim, C. T. French, S. Moghadam, R. Wall, J. F. Miller, O. N. Witte, M. A. Teitell, and P. Y. Chiou, “Photothermal nanoblade for large cargo delivery into mammalian cells,” Anal. Chem. 83(4), 1321–1327 (2011).
[Crossref] [PubMed]

Cleveland, D. W.

B. A. Weaver and D. W. Cleveland, “The aneuploidy paradox in cell growth and tumorigenesis,” Cancer Cell 14(6), 431–433 (2008).
[Crossref] [PubMed]

Datta, S.

S. Datta, L. Malhotra, R. Dickerson, S. Chaffee, C. K. Sen, and S. Roy, “Laser capture microdissection: Big data from small samples,” Histol. Histopathol. 30(11), 1255–1269 (2015).
[PubMed]

Davison, P. A.

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T. Sada, T. Fujigaya, Y. Niidome, K. Nakazawa, and N. Nakashima, “Near-IR laser-triggered target cell collection using a carbon nanotube-based cell-cultured substrate,” ACS Nano 5(6), 4414–4421 (2011).
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Y. C. Chen, H. W. Baac, K. T. Lee, S. Fouladdel, K. Teichert, J. G. Ok, Y. H. Cheng, P. N. Ingram, A. J. Hart, E. Azizi, L. J. Guo, M. S. Wicha, and E. Yoon, “Selective photomechanical detachment and retrieval of divided sister cells from enclosed microfluidics for downstream analyses,” ACS Nano 11(5), 4660–4668 (2017).
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H. W. Baac, J. G. Ok, A. Maxwell, K. T. Lee, Y. C. Chen, A. J. Hart, Z. Xu, E. Yoon, and L. J. Guo, “Carbon-nanotube optoacoustic lens for focused ultrasound generation and high-precision targeted therapy,” Sci. Rep. 2(1), 989 (2012).
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H. Won Baac, J. G. Ok, H. J. Park, T. Ling, S.-L. Chen, A. J. Hart, and L. J. Guo, “Carbon nanotube composite optoacoustic transmitters for strong and high frequency ultrasound generation,” Appl. Phys. Lett. 97(23), 234104 (2010).
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Y. Ebihara, R. Ota, T. Noriki, M. Shimojo, and K. Kajikawa, “Biometamaterials: Black Ultrathin Gold Film Fabricated on Lotus Leaf,” Sci. Rep. 5(1), 15992 (2015).
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H. Won Baac, J. G. Ok, H. J. Park, T. Ling, S.-L. Chen, A. J. Hart, and L. J. Guo, “Carbon nanotube composite optoacoustic transmitters for strong and high frequency ultrasound generation,” Appl. Phys. Lett. 97(23), 234104 (2010).
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S. P. Perfetto, P. K. Chattopadhyay, and M. Roederer, “Seventeen-colour flow cytometry: unravelling the immune system,” Nat. Rev. Immunol. 4(8), 648–655 (2004).
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A. K. Velichko, N. V. Petrova, S. V. Razin, and O. L. Kantidze, “Mechanism of heat stress-induced cellular senescence elucidates the exclusive vulnerability of early S-phase cells to mild genotoxic stress,” Nucleic Acids Res. 43(13), 6309–6320 (2015).
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A. Marusyk and K. Polyak, “Tumor heterogeneity: causes and consequences,” Biochim. Biophys. Acta 1805(1), 105–117 (2010).
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Y. Song, A. K. Kaster, J. Vollmers, Y. Song, P. A. Davison, M. Frentrup, G. M. Preston, I. P. Thompson, J. C. Murrell, H. Yin, C. N. Hunter, and W. E. Huang, “Single-cell genomics based on Raman sorting reveals novel carotenoid-containing bacteria in the Red Sea,” Microb. Biotechnol. 10(1), 125–137 (2017).
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J. Chen, N. Niu, J. Zhang, L. Qi, W. Shen, K. Donkena, Z. Feng, and J. Liu, “Polyploid Giant Cancer Cells (PGCCs): The Evil Roots of Cancer,” Curr. Cancer Drug Targets 18, 1–8 (2018).
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L. R. Rau, W. Y. Huang, J. W. Liaw, and S. W. Tsai, “Photothermal effects of laser-activated surface plasmonic gold nanoparticles on the apoptosis and osteogenesis of osteoblast-like cells,” Int. J. Nanomedicine 11, 3461–3473 (2016).
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A. K. Velichko, N. V. Petrova, S. V. Razin, and O. L. Kantidze, “Mechanism of heat stress-induced cellular senescence elucidates the exclusive vulnerability of early S-phase cells to mild genotoxic stress,” Nucleic Acids Res. 43(13), 6309–6320 (2015).
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R. S. Molday, S. P. Yen, and A. Rembaum, “Application of magnetic microspheres in labelling and separation of cells,” Nature 268(5619), 437–438 (1977).
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C. W. Shields, C. D. Reyes, and G. P. López, “Microfluidic cell sorting: a review of the advances in the separation of cells from debulking to rare cell isolation,” Lab Chip 15(5), 1230–1249 (2015).
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S. P. Perfetto, P. K. Chattopadhyay, and M. Roederer, “Seventeen-colour flow cytometry: unravelling the immune system,” Nat. Rev. Immunol. 4(8), 648–655 (2004).
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K. K. Karukstis, E. H. Thompson, J. A. Whiles, and R. J. Rosenfeld, “Deciphering the fluorescence signature of daunomycin and doxorubicin,” Biophys. Chem. 73(3), 249–263 (1998).
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G. P. Dimri, X. Lee, G. Basile, M. Acosta, G. Scott, C. Roskelley, E. E. Medrano, M. Linskens, I. Rubelj, and O. Pereira-Smith, “A biomarker that identifies senescent human cells in culture and in aging skin in vivo,” Proc. Natl. Acad. Sci. U.S.A. 92(20), 9363–9367 (1995).
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A. Gross, J. Schoendube, S. Zimmermann, M. Steeb, R. Zengerle, and P. Koltay, “Technologies for single-cell isolation,” Int. J. Mol. Sci. 16(8), 16897–16919 (2015).
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J. Chen, N. Niu, J. Zhang, L. Qi, W. Shen, K. Donkena, Z. Feng, and J. Liu, “Polyploid Giant Cancer Cells (PGCCs): The Evil Roots of Cancer,” Curr. Cancer Drug Targets 18, 1–8 (2018).
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C. W. Shields, C. D. Reyes, and G. P. López, “Microfluidic cell sorting: a review of the advances in the separation of cells from debulking to rare cell isolation,” Lab Chip 15(5), 1230–1249 (2015).
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Y. Ebihara, R. Ota, T. Noriki, M. Shimojo, and K. Kajikawa, “Biometamaterials: Black Ultrathin Gold Film Fabricated on Lotus Leaf,” Sci. Rep. 5(1), 15992 (2015).
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Y. Song, A. K. Kaster, J. Vollmers, Y. Song, P. A. Davison, M. Frentrup, G. M. Preston, I. P. Thompson, J. C. Murrell, H. Yin, C. N. Hunter, and W. E. Huang, “Single-cell genomics based on Raman sorting reveals novel carotenoid-containing bacteria in the Red Sea,” Microb. Biotechnol. 10(1), 125–137 (2017).
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Y. Song, A. K. Kaster, J. Vollmers, Y. Song, P. A. Davison, M. Frentrup, G. M. Preston, I. P. Thompson, J. C. Murrell, H. Yin, C. N. Hunter, and W. E. Huang, “Single-cell genomics based on Raman sorting reveals novel carotenoid-containing bacteria in the Red Sea,” Microb. Biotechnol. 10(1), 125–137 (2017).
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A. Gross, J. Schoendube, S. Zimmermann, M. Steeb, R. Zengerle, and P. Koltay, “Technologies for single-cell isolation,” Int. J. Mol. Sci. 16(8), 16897–16919 (2015).
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N. J. Sucher, D. L. Deitcher, D. J. Baro, R. M. Warrick, and E. Guenther, “Genes and channels: patch/voltage-clamp analysis and single-cell RT-PCR,” Cell Tissue Res. 302(3), 295–307 (2000).
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S. Zhang, I. Mercado-Uribe, Z. Xing, B. Sun, J. Kuang, and J. Liu, “Generation of cancer stem-like cells through the formation of polyploid giant cancer cells,” Oncogene 33(1), 116–128 (2014).
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N. McGranahan and C. Swanton, “Clonal heterogeneity and tumor evolution: past, present, and the future,” Cell 168(4), 613–628 (2017).
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Y. C. Chen, H. W. Baac, K. T. Lee, S. Fouladdel, K. Teichert, J. G. Ok, Y. H. Cheng, P. N. Ingram, A. J. Hart, E. Azizi, L. J. Guo, M. S. Wicha, and E. Yoon, “Selective photomechanical detachment and retrieval of divided sister cells from enclosed microfluidics for downstream analyses,” ACS Nano 11(5), 4660–4668 (2017).
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T. H. Wu, T. Teslaa, S. Kalim, C. T. French, S. Moghadam, R. Wall, J. F. Miller, O. N. Witte, M. A. Teitell, and P. Y. Chiou, “Photothermal nanoblade for large cargo delivery into mammalian cells,” Anal. Chem. 83(4), 1321–1327 (2011).
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T. H. Wu, T. Teslaa, S. Kalim, C. T. French, S. Moghadam, R. Wall, J. F. Miller, O. N. Witte, M. A. Teitell, and P. Y. Chiou, “Photothermal nanoblade for large cargo delivery into mammalian cells,” Anal. Chem. 83(4), 1321–1327 (2011).
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K. K. Karukstis, E. H. Thompson, J. A. Whiles, and R. J. Rosenfeld, “Deciphering the fluorescence signature of daunomycin and doxorubicin,” Biophys. Chem. 73(3), 249–263 (1998).
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Y. Song, A. K. Kaster, J. Vollmers, Y. Song, P. A. Davison, M. Frentrup, G. M. Preston, I. P. Thompson, J. C. Murrell, H. Yin, C. N. Hunter, and W. E. Huang, “Single-cell genomics based on Raman sorting reveals novel carotenoid-containing bacteria in the Red Sea,” Microb. Biotechnol. 10(1), 125–137 (2017).
[Crossref] [PubMed]

Tsai, S. W.

L. R. Rau, W. Y. Huang, J. W. Liaw, and S. W. Tsai, “Photothermal effects of laser-activated surface plasmonic gold nanoparticles on the apoptosis and osteogenesis of osteoblast-like cells,” Int. J. Nanomedicine 11, 3461–3473 (2016).
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D. R. Gossett, W. M. Weaver, A. J. Mach, S. C. Hur, H. T. Tse, W. Lee, H. Amini, and D. Di Carlo, “Label-free cell separation and sorting in microfluidic systems,” Anal. Bioanal. Chem. 397(8), 3249–3267 (2010).
[Crossref] [PubMed]

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A. K. Velichko, N. V. Petrova, S. V. Razin, and O. L. Kantidze, “Mechanism of heat stress-induced cellular senescence elucidates the exclusive vulnerability of early S-phase cells to mild genotoxic stress,” Nucleic Acids Res. 43(13), 6309–6320 (2015).
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Vollmers, J.

Y. Song, A. K. Kaster, J. Vollmers, Y. Song, P. A. Davison, M. Frentrup, G. M. Preston, I. P. Thompson, J. C. Murrell, H. Yin, C. N. Hunter, and W. E. Huang, “Single-cell genomics based on Raman sorting reveals novel carotenoid-containing bacteria in the Red Sea,” Microb. Biotechnol. 10(1), 125–137 (2017).
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T. H. Wu, T. Teslaa, S. Kalim, C. T. French, S. Moghadam, R. Wall, J. F. Miller, O. N. Witte, M. A. Teitell, and P. Y. Chiou, “Photothermal nanoblade for large cargo delivery into mammalian cells,” Anal. Chem. 83(4), 1321–1327 (2011).
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Y. Wang, Y. Ji, E. S. Wharfe, R. S. Meadows, P. March, R. Goodacre, J. Xu, and W. E. Huang, “Raman activated cell ejection for isolation of single cells,” Anal. Chem. 85(22), 10697–10701 (2013).
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N. J. Sucher, D. L. Deitcher, D. J. Baro, R. M. Warrick, and E. Guenther, “Genes and channels: patch/voltage-clamp analysis and single-cell RT-PCR,” Cell Tissue Res. 302(3), 295–307 (2000).
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B. A. Weaver and D. W. Cleveland, “The aneuploidy paradox in cell growth and tumorigenesis,” Cancer Cell 14(6), 431–433 (2008).
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D. R. Gossett, W. M. Weaver, A. J. Mach, S. C. Hur, H. T. Tse, W. Lee, H. Amini, and D. Di Carlo, “Label-free cell separation and sorting in microfluidic systems,” Anal. Bioanal. Chem. 397(8), 3249–3267 (2010).
[Crossref] [PubMed]

Wharfe, E. S.

Y. Wang, Y. Ji, E. S. Wharfe, R. S. Meadows, P. March, R. Goodacre, J. Xu, and W. E. Huang, “Raman activated cell ejection for isolation of single cells,” Anal. Chem. 85(22), 10697–10701 (2013).
[Crossref] [PubMed]

Whiles, J. A.

K. K. Karukstis, E. H. Thompson, J. A. Whiles, and R. J. Rosenfeld, “Deciphering the fluorescence signature of daunomycin and doxorubicin,” Biophys. Chem. 73(3), 249–263 (1998).
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G. M. Whitesides, “The origins and the future of microfluidics,” Nature 442(7101), 368–373 (2006).
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Y. Xia and G. M. Whitesides, “Soft lithography,” Angew. Chem. Int. Ed. Engl. 37(5), 550–575 (1998).
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Y. C. Chen, H. W. Baac, K. T. Lee, S. Fouladdel, K. Teichert, J. G. Ok, Y. H. Cheng, P. N. Ingram, A. J. Hart, E. Azizi, L. J. Guo, M. S. Wicha, and E. Yoon, “Selective photomechanical detachment and retrieval of divided sister cells from enclosed microfluidics for downstream analyses,” ACS Nano 11(5), 4660–4668 (2017).
[Crossref] [PubMed]

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T. H. Wu, T. Teslaa, S. Kalim, C. T. French, S. Moghadam, R. Wall, J. F. Miller, O. N. Witte, M. A. Teitell, and P. Y. Chiou, “Photothermal nanoblade for large cargo delivery into mammalian cells,” Anal. Chem. 83(4), 1321–1327 (2011).
[Crossref] [PubMed]

Won Baac, H.

H. Won Baac, J. G. Ok, H. J. Park, T. Ling, S.-L. Chen, A. J. Hart, and L. J. Guo, “Carbon nanotube composite optoacoustic transmitters for strong and high frequency ultrasound generation,” Appl. Phys. Lett. 97(23), 234104 (2010).
[Crossref] [PubMed]

Wu, T. H.

T. H. Wu, T. Teslaa, S. Kalim, C. T. French, S. Moghadam, R. Wall, J. F. Miller, O. N. Witte, M. A. Teitell, and P. Y. Chiou, “Photothermal nanoblade for large cargo delivery into mammalian cells,” Anal. Chem. 83(4), 1321–1327 (2011).
[Crossref] [PubMed]

Xia, Y.

Y. Xia and G. M. Whitesides, “Soft lithography,” Angew. Chem. Int. Ed. Engl. 37(5), 550–575 (1998).
[Crossref] [PubMed]

Xin, H.

P. Hu, W. Zhang, H. Xin, and G. Deng, “Single cell isolation and analysis,” Front. Cell Dev. Biol. 4, 116 (2016).
[Crossref] [PubMed]

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S. Zhang, I. Mercado-Uribe, Z. Xing, B. Sun, J. Kuang, and J. Liu, “Generation of cancer stem-like cells through the formation of polyploid giant cancer cells,” Oncogene 33(1), 116–128 (2014).
[Crossref] [PubMed]

Xu, J.

Y. Wang, Y. Ji, E. S. Wharfe, R. S. Meadows, P. March, R. Goodacre, J. Xu, and W. E. Huang, “Raman activated cell ejection for isolation of single cells,” Anal. Chem. 85(22), 10697–10701 (2013).
[Crossref] [PubMed]

Xu, Z.

H. W. Baac, J. G. Ok, A. Maxwell, K. T. Lee, Y. C. Chen, A. J. Hart, Z. Xu, E. Yoon, and L. J. Guo, “Carbon-nanotube optoacoustic lens for focused ultrasound generation and high-precision targeted therapy,” Sci. Rep. 2(1), 989 (2012).
[Crossref] [PubMed]

Yen, S. P.

R. S. Molday, S. P. Yen, and A. Rembaum, “Application of magnetic microspheres in labelling and separation of cells,” Nature 268(5619), 437–438 (1977).
[Crossref] [PubMed]

Yin, H.

Y. Song, A. K. Kaster, J. Vollmers, Y. Song, P. A. Davison, M. Frentrup, G. M. Preston, I. P. Thompson, J. C. Murrell, H. Yin, C. N. Hunter, and W. E. Huang, “Single-cell genomics based on Raman sorting reveals novel carotenoid-containing bacteria in the Red Sea,” Microb. Biotechnol. 10(1), 125–137 (2017).
[Crossref] [PubMed]

Yoon, E.

Y. C. Chen, H. W. Baac, K. T. Lee, S. Fouladdel, K. Teichert, J. G. Ok, Y. H. Cheng, P. N. Ingram, A. J. Hart, E. Azizi, L. J. Guo, M. S. Wicha, and E. Yoon, “Selective photomechanical detachment and retrieval of divided sister cells from enclosed microfluidics for downstream analyses,” ACS Nano 11(5), 4660–4668 (2017).
[Crossref] [PubMed]

H. W. Baac, J. G. Ok, A. Maxwell, K. T. Lee, Y. C. Chen, A. J. Hart, Z. Xu, E. Yoon, and L. J. Guo, “Carbon-nanotube optoacoustic lens for focused ultrasound generation and high-precision targeted therapy,” Sci. Rep. 2(1), 989 (2012).
[Crossref] [PubMed]

Zengerle, R.

A. Gross, J. Schoendube, S. Zimmermann, M. Steeb, R. Zengerle, and P. Koltay, “Technologies for single-cell isolation,” Int. J. Mol. Sci. 16(8), 16897–16919 (2015).
[Crossref] [PubMed]

Zhang, J.

J. Chen, N. Niu, J. Zhang, L. Qi, W. Shen, K. Donkena, Z. Feng, and J. Liu, “Polyploid Giant Cancer Cells (PGCCs): The Evil Roots of Cancer,” Curr. Cancer Drug Targets 18, 1–8 (2018).
[PubMed]

Zhang, S.

S. Zhang, I. Mercado-Uribe, Z. Xing, B. Sun, J. Kuang, and J. Liu, “Generation of cancer stem-like cells through the formation of polyploid giant cancer cells,” Oncogene 33(1), 116–128 (2014).
[Crossref] [PubMed]

Zhang, W.

P. Hu, W. Zhang, H. Xin, and G. Deng, “Single cell isolation and analysis,” Front. Cell Dev. Biol. 4, 116 (2016).
[Crossref] [PubMed]

Zimmermann, S.

A. Gross, J. Schoendube, S. Zimmermann, M. Steeb, R. Zengerle, and P. Koltay, “Technologies for single-cell isolation,” Int. J. Mol. Sci. 16(8), 16897–16919 (2015).
[Crossref] [PubMed]

ACS Nano (2)

T. Sada, T. Fujigaya, Y. Niidome, K. Nakazawa, and N. Nakashima, “Near-IR laser-triggered target cell collection using a carbon nanotube-based cell-cultured substrate,” ACS Nano 5(6), 4414–4421 (2011).
[Crossref] [PubMed]

Y. C. Chen, H. W. Baac, K. T. Lee, S. Fouladdel, K. Teichert, J. G. Ok, Y. H. Cheng, P. N. Ingram, A. J. Hart, E. Azizi, L. J. Guo, M. S. Wicha, and E. Yoon, “Selective photomechanical detachment and retrieval of divided sister cells from enclosed microfluidics for downstream analyses,” ACS Nano 11(5), 4660–4668 (2017).
[Crossref] [PubMed]

Anal. Bioanal. Chem. (1)

D. R. Gossett, W. M. Weaver, A. J. Mach, S. C. Hur, H. T. Tse, W. Lee, H. Amini, and D. Di Carlo, “Label-free cell separation and sorting in microfluidic systems,” Anal. Bioanal. Chem. 397(8), 3249–3267 (2010).
[Crossref] [PubMed]

Anal. Chem. (2)

T. H. Wu, T. Teslaa, S. Kalim, C. T. French, S. Moghadam, R. Wall, J. F. Miller, O. N. Witte, M. A. Teitell, and P. Y. Chiou, “Photothermal nanoblade for large cargo delivery into mammalian cells,” Anal. Chem. 83(4), 1321–1327 (2011).
[Crossref] [PubMed]

Y. Wang, Y. Ji, E. S. Wharfe, R. S. Meadows, P. March, R. Goodacre, J. Xu, and W. E. Huang, “Raman activated cell ejection for isolation of single cells,” Anal. Chem. 85(22), 10697–10701 (2013).
[Crossref] [PubMed]

Angew. Chem. Int. Ed. Engl. (1)

Y. Xia and G. M. Whitesides, “Soft lithography,” Angew. Chem. Int. Ed. Engl. 37(5), 550–575 (1998).
[Crossref] [PubMed]

Appl. Phys. Lett. (1)

H. Won Baac, J. G. Ok, H. J. Park, T. Ling, S.-L. Chen, A. J. Hart, and L. J. Guo, “Carbon nanotube composite optoacoustic transmitters for strong and high frequency ultrasound generation,” Appl. Phys. Lett. 97(23), 234104 (2010).
[Crossref] [PubMed]

Biochim. Biophys. Acta (1)

A. Marusyk and K. Polyak, “Tumor heterogeneity: causes and consequences,” Biochim. Biophys. Acta 1805(1), 105–117 (2010).
[PubMed]

Biophys. Chem. (1)

K. K. Karukstis, E. H. Thompson, J. A. Whiles, and R. J. Rosenfeld, “Deciphering the fluorescence signature of daunomycin and doxorubicin,” Biophys. Chem. 73(3), 249–263 (1998).
[Crossref] [PubMed]

Biophys. J. (1)

K. K. Elineni and N. D. Gallant, “Regulation of cell adhesion strength by peripheral focal adhesion distribution,” Biophys. J. 101(12), 2903–2911 (2011).
[Crossref] [PubMed]

Cancer Cell (1)

B. A. Weaver and D. W. Cleveland, “The aneuploidy paradox in cell growth and tumorigenesis,” Cancer Cell 14(6), 431–433 (2008).
[Crossref] [PubMed]

Cell (1)

N. McGranahan and C. Swanton, “Clonal heterogeneity and tumor evolution: past, present, and the future,” Cell 168(4), 613–628 (2017).
[Crossref] [PubMed]

Cell Cycle (1)

P. Duesberg and A. McCormack, “Immortality of cancers: a consequence of inherent karyotypic variations and selections for autonomy,” Cell Cycle 12(5), 783–802 (2013).
[Crossref] [PubMed]

Cell Tissue Res. (1)

N. J. Sucher, D. L. Deitcher, D. J. Baro, R. M. Warrick, and E. Guenther, “Genes and channels: patch/voltage-clamp analysis and single-cell RT-PCR,” Cell Tissue Res. 302(3), 295–307 (2000).
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Figures (7)

Fig. 1
Fig. 1 A Cancer Drug Resistance Accelerator (CDRA) chip. (A) Schematic diagram of the chip and its dimensions. Filled arrow indicates the flow of 1.5 μM DOX and nutrients, whereas empty arrow represents the flow of nutrients only. (B) An optical image of the concentration gradient with red and blue ink. (C) The actual image of the CDRA chip.
Fig. 2
Fig. 2 (A) The pulsed laser setup to generate microbubbles and detach cells. The configuration for laser irradiation was combined with an inverted optical microscope which visualizes an image from the bottom side. (B) A schematic for LIMB generation and cell detachment. Pulsed laser irradiation onto the Au film leads to instantaneous heating of the PDMS overlayer in contact. This merges nanoscale voids readily embedded within PDMS into a single microbubble. Then, the microbubble ejects through the PDMS layer to the overlaying culture medium, thus breaking the cell contact formed physically with the PDMS substrate. In the schematic, the pulsed laser beam is given (green arrow) onto cells initially forming physical adhesion with the PDMS substrate (top left). A LIMB is produced at the location near the right edge of the right cell (top right). Then, the cell loses its contact due to the LIMB ejection. The cell shrinks changing its morphology (bottom right). Due to the subsequent laser irradiation, the cell loses its contact formed at other locations. In this manner, entire cell-substrate contacts can be removed, resulting in cell detachment.
Fig. 3
Fig. 3 Optimization of NLP conditions for selective and viable detachment of normal-sized cells (MDA-MB-231 WT). (A) Laser spot diameters (n = 3) at different laser fluences (1.3−19.9 mJ/cm2). (B) Effects of laser fluence and hit number (N) on cell death. Each bar represents the average death rate of cells (n = 30) at each detachment condition. Student’s t-test, ***p < 0.001, N: the number of laser pulses. The cell death rate was measured by staining detached cells with tryptophan blue. (C) Microbubble generation capable of detaching a target cell (marked by a dotted line) according to the number (N) of laser pulses. The dashed line in red in Fig. 2(C) (N0) shows the target cell before laser irradiation. The cell was then irradiated with a single laser pulse (N1) in the region near the cell body. From this aiming location, laser irradiation was continued into the upper region of the cellular extension using 18 laser pulses (N18). At N23, microbubbles could push the cells to complete detachment, and the cells were then swept away by the flow. The blue arrow denotes a microbubble surrounding the laser spot in white (scale bar = 50 μm). (D) The aspect ratio of detached cells (n = 20) by either trypsin or LIMBs. Cell doubling time and viability of detached cells (n = 30) were determined. Student’s t-test was used for statistical analysis; ND = not determined.
Fig. 4
Fig. 4 MDA-MB-231 WT cells detached by (a) LIMBs and (b) trypsin, after β-Gal staining. For both cases, the cells were not stained, manifesting healthy states of cells. Scale bar = 100 μm.
Fig. 5
Fig. 5 Isolation of very large cells (231 RL) using the photomechanical method. (A) Accumulation of DOX in 231 WT (A) and 231 R (B) cells. Cells were treated with DOX (0.5 μM) for 72 h. DOX intrinsically fluoresced red. 231 R cells consisted of normal-sized cells (231 RN, denoted by blue arrow) and large cells (231 RL, denoted by green arrow). (C) Cell area distribution of 231 R cells (n = 135). The insets are the merged images of optical and fluorescent images (blue: DAPI). (D) Schematic of the subcellular detachment of 231 RL cells from the PDMS layer using multiple NLPs. (E) Number of laser pulses at 2 mJ/cm2 for the detachment of cells (n = 23) with different sizes.
Fig. 6
Fig. 6 The cell area distribution of wild type MDA-MB-231 cells (n = 135 and average area = 3,007 μm2).
Fig. 7
Fig. 7 Isolation of very large cells (231 RL) using the photomechanical method. (A) Accumulation of DOX in 231 WT (A) and 231 R (B) cells. Cells were treated with DOX (0.5 μM) for 72 h. DOX intrinsically fluoresced red. 231 R cells consisted of normal-sized cells (231 RN, denoted by blue arrow) and large cells (231 RL, denoted by green arrow). (C) Cell area distribution of 231 R cells (n = 135). The insets are the merged images of optical and fluorescent images (blue: DAPI). (D) Schematic of the subcellular detachment of 231 RL cells from the PDMS layer using multiple NLPs. (E) Number of laser pulses at 2 mJ/cm2 for the detachment of cells (n = 23) with different sizes.

Tables (1)

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Table 1 Comparison of the features of LIMB and other cell isolation techniques

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