Abstract

Laser-exposed plasmonic substrates permeabilize the plasma membrane of cells when in close contact to deliver cell-impermeable cargo. While studies have determined the cargo delivery efficiency and viability of laser-exposed plasmonic substrates, morphological changes in a cell have not been quantified. We porated myoblast C2C12 cells on a plasmonic pyramid array using a 532-nm laser with 850-ps pulse length and time-lapse fluorescence imaging to quantify cellular changes. We obtain a poration efficiency of 80%, viability of 90%, and a pore radius of 20 nm. We quantified area changes in the plasma membrane attached to the substrate (10% decrease), nucleus (5 – 10% decrease), and cytoplasm (5 – 10% decrease) over 1 h after laser treatment. Cytoskeleton fibers show a change of 50% in the alignment, or coherency, of fibers, which stabilizes after 10 mins. We investigate structural and morphological changes due to the poration process to enable the safe development of this technique for therapeutic applications.

© 2017 Optical Society of America

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2017 (1)

N. Saklayen, M. Huber, M. Madrid, V. Nuzzo, D. I. Vulis, W. Shen, J. Nelson, A. A. McClelland, A. Heisterkamp, and E. Mazur, “Intracellular Delivery Using Nanosecond-Laser Excitation of Large-Area Plasmonic Substrate,” ACS Nano 11, 3671 (2017).

2016 (3)

S. Park, S. O. Choi, S. J. Paik, S. Choi, M. Allen, and M. Prausnitz, “Intracellular delivery of molecules using microfabricated nanoneedle arrays,” Biomed. Microdevices 18(1), 10 (2016).
[Crossref] [PubMed]

E. Y. Lukianova-Hleb, Y.-S. Kim, I. Belatsarkouski, A. M. Gillenwater, B. E. O’Neill, and D. O. Lapotko, “Intraoperative diagnostics and elimination of residual microtumours with plasmonic nanobubbles,” Nat. Nano. 11, 25–28 (2016).

Z. Lyu, F. Zhou, Q. Liu, H. Xue, Q. Yu, and H. Chen, “Photoporation: A Universal Platform for Macromolecular Deliveryinto Cells Using Gold Nanoparticle Layers via the Photoporation Effect (Adv. Funct. Mater. 32/2016),” Adv. Funct. Mater. 26(32), 5770 (2016).
[Crossref]

2015 (9)

S. Feng, Z. Li, G. Chen, D. Lin, S. Huang, Z. Huang, Y. Li, J. Lin, R. Chen, and H. Zeng, “Ultrasound-mediated method for rapid delivery of nano-particles into cells for intracellular surface-enhanced Raman spectroscopy and cancer cell screening,” Nanotechnology 26(6), 065101 (2015).
[Crossref] [PubMed]

G. C. Messina, M. Dipalo, R. La Rocca, P. Zilio, V. Caprettini, R. Proietti Zaccaria, A. Toma, F. Tantussi, L. Berdondini, and F. De Angelis, “Spatially, Temporally, and Quantitatively Controlled Delivery of Broad Range of Molecules into Selected Cells through Plasmonic Nanotubes,” Adv. Mater. 27, 7145 (2015).

D. Matsumoto, R. Rao Sathuluri, Y. Kato, Y. R. Silberberg, R. Kawamura, F. Iwata, T. Kobayashi, and C. Nakamura, “Oscillating high-aspect-ratio monolithic silicon nanoneedle array enables efficient delivery of functional bio-macromolecules into living cells,” Sci. Rep. 5(1), 15325 (2015).
[Crossref] [PubMed]

S. Kalies, G. C. Antonopoulos, M. S. Rakoski, D. Heinemann, M. Schomaker, T. Ripken, and H. Meyer, “Investigation of biophysical mechanisms in gold nanoparticle mediated laser manipulation of cells using a multimodal holographic and fluorescence imaging setup,” PLoS One 10(4), e0124052 (2015).
[Crossref] [PubMed]

S. Kalies, S. Keil, S. Sender, S. C. Hammer, G. C. Antonopoulos, M. Schomaker, T. Ripken, H. Murua Escobar, H. Meyer, and D. Heinemann, “Characterization of the cellular response triggered by gold nanoparticle-mediated laser manipulation,” J. Biomed. Opt. 20(11), 115005 (2015).
[Crossref] [PubMed]

I. Fratoddi, I. Venditti, C. Cametti, and M. V. Russo, “How toxic are gold nanoparticles? The state-of-the-art,” Nano Res. 8(6), 1771–1799 (2015).
[Crossref]

S. Courvoisier, N. Saklayen, M. Huber, J. Chen, E. D. Diebold, L. Bonacina, J. P. Wolf, and E. Mazur, “Plasmonic Tipless Pyramid Arrays for Cell Poration,” Nano Lett. 15(7), 4461–4466 (2015).
[Crossref] [PubMed]

Y.-C. Wu, T.-H. Wu, D. L. Clemens, B.-Y. Lee, X. Wen, M. A. Horwitz, M. A. Teitell, and P.-Y. Chiou, “Massively parallel delivery of large cargo into mammalian cells with light pulses,” Nat. Methods 12(5), 439–444 (2015).
[Crossref] [PubMed]

E. Bergeron, C. Boutopoulos, R. Martel, A. Torres, C. Rodriguez, J. Niskanen, J.-J. Lebrun, F. M. Winnik, P. Sapieha, and M. Meunier, “Cell-specific optoporation with near-infrared ultrafast laser and functionalized gold nanoparticles,” Nanoscale 42, 17836–17847 (2015).

2014 (4)

S. Kalies, T. Birr, D. Heinemann, M. Schomaker, T. Ripken, A. Heisterkamp, and H. Meyer, “Enhancement of extracellular molecule uptake in plasmonic laser perforation,” J. Biophotonics 7(7), 474–482 (2014).
[Crossref] [PubMed]

S. Kalies, D. Heinemann, M. Schomaker, H. Murua Escobar, A. Heisterkamp, T. Ripken, and H. Meyer, “Plasmonic laser treatment for Morpholino oligomer delivery in antisense applications,” J. Biophotonics 7(10), 825–833 (2014).
[Crossref] [PubMed]

J. M. Meacham, K. Durvasula, F. L. Degertekin, and A. G. Fedorov, “Physical methods for intracellular delivery: practical aspects from laboratory use to industrial-scale processing,” J. Lab. Autom. 19(1), 1–18 (2014).
[Crossref] [PubMed]

R. Xiong, K. Raemdonck, K. Peynshaert, I. Lentacker, I. De Cock, J. Demeester, S. C. De Smedt, A. G. Skirtach, and K. Braeckmans, “Comparison of gold nanoparticle mediated photoporation: vapor nanobubbles outperform direct heating for delivering macromolecules in live cells,” ACS Nano 8(6), 6288–6296 (2014).
[Crossref] [PubMed]

2013 (3)

D. Heinemann, M. Schomaker, S. Kalies, M. Schieck, R. Carlson, H. Murua Escobar, T. Ripken, H. Meyer, and A. Heisterkamp, “Gold nanoparticle mediated laser transfection for efficient siRNA mediated gene knock down,” PLoS One 8(3), e58604 (2013).
[Crossref] [PubMed]

A. Sharei, J. Zoldan, A. Adamo, W. Y. Sim, N. Cho, E. Jackson, S. Mao, S. Schneider, M.-J. Han, A. Lytton-Jean, P. A. Basto, S. Jhunjhunwala, J. Lee, D. A. Heller, J. W. Kang, G. C. Hartoularos, K.-S. Kim, D. G. Anderson, R. Langer, and K. F. Jensen, “A vector-free microfluidic platform for intracellular delivery,” Proc. Natl. Acad. Sci. U.S.A. 110(6), 2082–2087 (2013).
[Crossref] [PubMed]

A. A. Davis, M. J. Farrar, N. Nishimura, M. M. Jin, and C. B. Schaffer, “Optoporation and Genetic Manipulation of Cells Using Femtosecond Laser Pulses,” Biophys. J. 105(4), 862–871 (2013).
[Crossref] [PubMed]

2012 (7)

Z. Fan, H. Liu, M. Mayer, and C. X. Deng, “Spatiotemporally controlled single cell sonoporation,” Proc. Natl. Acad. Sci. U.S.A. 109(41), 16486–16491 (2012).
[Crossref] [PubMed]

E. Y. Lukianova-Hleb, X. Ren, J. A. Zasadzinski, X. Wu, and D. O. Lapotko, “Plasmonic Nanobubbles Enhance Efficacy and Selectivity of Chemotherapy Against Drug-Resistant Cancer Cells,” Adv. Mater. 24(28), 3831–3837 (2012).
[Crossref] [PubMed]

S. Hashimoto, D. Werner, and T. Uwada, “Studies on the interaction of pulsed lasers with plasmonic gold nanoparticles toward light manipulation, heat management, and nanofabrication,” J. Photochem. Photobiol. C Photochem. Rev. 13, 28–54 (2012).

E. Boulais, R. Lachaine, and M. Meunier, “Plasma mediated off-resonance plasmonic enhanced ultrafast laser-induced nanocavitation,” Nano Lett. 12(9), 4763–4769 (2012).
[Crossref] [PubMed]

Z. Qin and J. C. Bischof, “Thermophysical and biological responses of gold nanoparticle laser heating,” Chem. Soc. Rev. 41(3), 1191–1217 (2012).
[Crossref] [PubMed]

C. A. Schneider, W. S. Rasband, and K. W. Eliceiri, “NIH Image to ImageJ: 25 years of image analysis,” Nat. Methods 9(7), 671–675 (2012).
[Crossref] [PubMed]

R. Rezakhaniha, A. Agianniotis, J. T. C. T. C. Schrauwen, A. Griffa, D. Sage, C. V. C. V. C. Bouten, F. N. N. van de Vosse, M. Unser, and N. Stergiopulos, “Experimental Investigation of Collagen Waviness and Orientation in the Arterial Adventitia Using Confocal Laser Scanning Microscopy,” Biomech. Model. Mechanobiol. 11(3-4), 461–473 (2012).
[Crossref] [PubMed]

2010 (3)

T. Mironava, M. Hadjiargyrou, M. Simon, V. Jurukovski, and M. H. Rafailovich, “Gold nanoparticles cellular toxicity and recovery: effect of size, concentration and exposure time,” Nanotoxicology 4(1), 120–137 (2010).
[Crossref] [PubMed]

A. K. Shalek, J. T. Robinson, E. S. Karp, J. S. Lee, D.-R. Ahn, M.-H. Yoon, A. Sutton, M. Jorgolli, R. S. Gertner, T. S. Gujral, G. MacBeath, E. G. Yang, and H. Park, “Vertical silicon nanowires as a universal platform for delivering biomolecules into living cells,” Proc. Natl. Acad. Sci. U.S.A. 107(5), 1870–1875 (2010).
[Crossref] [PubMed]

E. Y. Lukianova-Hleb, E. Y. Hanna, J. H. Hafner, and D. O. Lapotko, “Tunable plasmonic nanobubbles for cell theranostics,” Nanotechnology 21(8), 085102 (2010).
[Crossref] [PubMed]

2009 (3)

G. Baffou, R. Quidant, and C. Girard, “Heat generation in plasmonic nanostructures: Influence of morphology,” Appl. Phys. Lett. 94(15), 153109 (2009).
[Crossref]

D. Lapotko, “Optical excitation and detection of vapor bubbles around plasmonic nanoparticles,” Opt. Express 17(4), 2538–2556 (2009).
[Crossref] [PubMed]

E. Fonck, G. G. Feigl, J. Fasel, D. Sage, M. Unser, D. A. Rüfenacht, and N. Stergiopulos, “Effect of Aging on Elastin Functionality in Human Cerebral Arteries,” Stroke 40(7), 2552–2556 (2009).
[Crossref] [PubMed]

2008 (2)

V. Zarnitsyn, C. A. Rostad, and M. R. Prausnitz, “Modeling Transmembrane Transport through Cell Membrane Wounds Created by Acoustic Cavitation,” Biophys. J. 95(9), 4124–4138 (2008).
[Crossref] [PubMed]

O. Ekici, R. K. Harrison, N. J. Durr, D. S. Eversole, M. Lee, and A. Ben-Yakar, “Thermal analysis of gold nanorods heated with femtosecond laser pulses,” J. Phys. D Appl. Phys. 41(18), 185501 (2008).
[Crossref] [PubMed]

2006 (1)

P. Mancheño-Corvo and P. Martín-Duque, “Viral gene therapy,” Clin. Transl. Oncol. 8(12), 858–867 (2006).
[Crossref] [PubMed]

2005 (2)

K. K. Ewert, A. Ahmad, H. M. Evans, and C. R. Safinya, “Cationic lipid-DNA complexes for non-viral gene therapy: Relating supramolecular structures to cellular pathways,” Expert Opin. Biol. Ther. 5(1), 33–53 (2005).
[Crossref] [PubMed]

C. Yao, R. Rahmanzadeh, E. Endl, Z. Zhang, J. Gerdes, and G. Huttmann, “Elevation of plasma membrane permeability by laser irradiation of selectively bound nanoparticles,” J. Biomed. Opt. 10(6), 064012 (2005).
[Crossref] [PubMed]

2004 (1)

2003 (2)

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).
[Crossref] [PubMed]

C. E. Thomas, A. Ehrhardt, and M. A. Kay, “Progress and problems with the use of viral vectors for gene therapy,” Nat. Rev. Genet. 4(5), 346–358 (2003).
[Crossref] [PubMed]

2001 (2)

P. J. Canatella, J. F. Karr, J. A. Petros, and M. R. Prausnitz, “Quantitative study of electroporation-mediated molecular uptake and cell viability,” Biophys. J. 80(2), 755–764 (2001).
[Crossref] [PubMed]

P. L. McNeil and M. Terasaki, “Coping with the inevitable: how cells repair a torn surface membrane,” Nat. Cell Biol. 3(5), E124–E129 (2001).
[Crossref] [PubMed]

2000 (1)

B. R. Davis, J. Yannariello-Brown, N. L. Prokopishyn, Z. Luo, M. R. Smith, J. Wang, N. D. Carsrud, and D. B. Brown, “Glass needle-mediated microinjection of macromolecules and transgenes into primary human blood stem/progenitor cells,” Blood 95(2), 437–444 (2000).
[PubMed]

1985 (1)

K. H. Jones and J. A. Senft, “An improved method to determine cell viability by simultaneous staining with fluorescein diacetate-propidium iodide,” J. Histochem. Cytochem. 33(1), 77–79 (1985).
[Crossref] [PubMed]

Adamo, A.

A. Sharei, J. Zoldan, A. Adamo, W. Y. Sim, N. Cho, E. Jackson, S. Mao, S. Schneider, M.-J. Han, A. Lytton-Jean, P. A. Basto, S. Jhunjhunwala, J. Lee, D. A. Heller, J. W. Kang, G. C. Hartoularos, K.-S. Kim, D. G. Anderson, R. Langer, and K. F. Jensen, “A vector-free microfluidic platform for intracellular delivery,” Proc. Natl. Acad. Sci. U.S.A. 110(6), 2082–2087 (2013).
[Crossref] [PubMed]

Agianniotis, A.

R. Rezakhaniha, A. Agianniotis, J. T. C. T. C. Schrauwen, A. Griffa, D. Sage, C. V. C. V. C. Bouten, F. N. N. van de Vosse, M. Unser, and N. Stergiopulos, “Experimental Investigation of Collagen Waviness and Orientation in the Arterial Adventitia Using Confocal Laser Scanning Microscopy,” Biomech. Model. Mechanobiol. 11(3-4), 461–473 (2012).
[Crossref] [PubMed]

Ahmad, A.

K. K. Ewert, A. Ahmad, H. M. Evans, and C. R. Safinya, “Cationic lipid-DNA complexes for non-viral gene therapy: Relating supramolecular structures to cellular pathways,” Expert Opin. Biol. Ther. 5(1), 33–53 (2005).
[Crossref] [PubMed]

Ahn, D.-R.

A. K. Shalek, J. T. Robinson, E. S. Karp, J. S. Lee, D.-R. Ahn, M.-H. Yoon, A. Sutton, M. Jorgolli, R. S. Gertner, T. S. Gujral, G. MacBeath, E. G. Yang, and H. Park, “Vertical silicon nanowires as a universal platform for delivering biomolecules into living cells,” Proc. Natl. Acad. Sci. U.S.A. 107(5), 1870–1875 (2010).
[Crossref] [PubMed]

Allen, M.

S. Park, S. O. Choi, S. J. Paik, S. Choi, M. Allen, and M. Prausnitz, “Intracellular delivery of molecules using microfabricated nanoneedle arrays,” Biomed. Microdevices 18(1), 10 (2016).
[Crossref] [PubMed]

Anderson, D. G.

A. Sharei, J. Zoldan, A. Adamo, W. Y. Sim, N. Cho, E. Jackson, S. Mao, S. Schneider, M.-J. Han, A. Lytton-Jean, P. A. Basto, S. Jhunjhunwala, J. Lee, D. A. Heller, J. W. Kang, G. C. Hartoularos, K.-S. Kim, D. G. Anderson, R. Langer, and K. F. Jensen, “A vector-free microfluidic platform for intracellular delivery,” Proc. Natl. Acad. Sci. U.S.A. 110(6), 2082–2087 (2013).
[Crossref] [PubMed]

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).
[Crossref] [PubMed]

Antonopoulos, G. C.

S. Kalies, G. C. Antonopoulos, M. S. Rakoski, D. Heinemann, M. Schomaker, T. Ripken, and H. Meyer, “Investigation of biophysical mechanisms in gold nanoparticle mediated laser manipulation of cells using a multimodal holographic and fluorescence imaging setup,” PLoS One 10(4), e0124052 (2015).
[Crossref] [PubMed]

S. Kalies, S. Keil, S. Sender, S. C. Hammer, G. C. Antonopoulos, M. Schomaker, T. Ripken, H. Murua Escobar, H. Meyer, and D. Heinemann, “Characterization of the cellular response triggered by gold nanoparticle-mediated laser manipulation,” J. Biomed. Opt. 20(11), 115005 (2015).
[Crossref] [PubMed]

Ashida, H.

Baffou, G.

G. Baffou, R. Quidant, and C. Girard, “Heat generation in plasmonic nanostructures: Influence of morphology,” Appl. Phys. Lett. 94(15), 153109 (2009).
[Crossref]

Basto, P. A.

A. Sharei, J. Zoldan, A. Adamo, W. Y. Sim, N. Cho, E. Jackson, S. Mao, S. Schneider, M.-J. Han, A. Lytton-Jean, P. A. Basto, S. Jhunjhunwala, J. Lee, D. A. Heller, J. W. Kang, G. C. Hartoularos, K.-S. Kim, D. G. Anderson, R. Langer, and K. F. Jensen, “A vector-free microfluidic platform for intracellular delivery,” Proc. Natl. Acad. Sci. U.S.A. 110(6), 2082–2087 (2013).
[Crossref] [PubMed]

Belatsarkouski, I.

E. Y. Lukianova-Hleb, Y.-S. Kim, I. Belatsarkouski, A. M. Gillenwater, B. E. O’Neill, and D. O. Lapotko, “Intraoperative diagnostics and elimination of residual microtumours with plasmonic nanobubbles,” Nat. Nano. 11, 25–28 (2016).

Ben-Yakar, A.

O. Ekici, R. K. Harrison, N. J. Durr, D. S. Eversole, M. Lee, and A. Ben-Yakar, “Thermal analysis of gold nanorods heated with femtosecond laser pulses,” J. Phys. D Appl. Phys. 41(18), 185501 (2008).
[Crossref] [PubMed]

Berdondini, L.

G. C. Messina, M. Dipalo, R. La Rocca, P. Zilio, V. Caprettini, R. Proietti Zaccaria, A. Toma, F. Tantussi, L. Berdondini, and F. De Angelis, “Spatially, Temporally, and Quantitatively Controlled Delivery of Broad Range of Molecules into Selected Cells through Plasmonic Nanotubes,” Adv. Mater. 27, 7145 (2015).

Bergeron, E.

E. Bergeron, C. Boutopoulos, R. Martel, A. Torres, C. Rodriguez, J. Niskanen, J.-J. Lebrun, F. M. Winnik, P. Sapieha, and M. Meunier, “Cell-specific optoporation with near-infrared ultrafast laser and functionalized gold nanoparticles,” Nanoscale 42, 17836–17847 (2015).

Birr, T.

S. Kalies, T. Birr, D. Heinemann, M. Schomaker, T. Ripken, A. Heisterkamp, and H. Meyer, “Enhancement of extracellular molecule uptake in plasmonic laser perforation,” J. Biophotonics 7(7), 474–482 (2014).
[Crossref] [PubMed]

Bischof, J. C.

Z. Qin and J. C. Bischof, “Thermophysical and biological responses of gold nanoparticle laser heating,” Chem. Soc. Rev. 41(3), 1191–1217 (2012).
[Crossref] [PubMed]

Bonacina, L.

S. Courvoisier, N. Saklayen, M. Huber, J. Chen, E. D. Diebold, L. Bonacina, J. P. Wolf, and E. Mazur, “Plasmonic Tipless Pyramid Arrays for Cell Poration,” Nano Lett. 15(7), 4461–4466 (2015).
[Crossref] [PubMed]

Boulais, E.

E. Boulais, R. Lachaine, and M. Meunier, “Plasma mediated off-resonance plasmonic enhanced ultrafast laser-induced nanocavitation,” Nano Lett. 12(9), 4763–4769 (2012).
[Crossref] [PubMed]

Bouten, C. V. C. V. C.

R. Rezakhaniha, A. Agianniotis, J. T. C. T. C. Schrauwen, A. Griffa, D. Sage, C. V. C. V. C. Bouten, F. N. N. van de Vosse, M. Unser, and N. Stergiopulos, “Experimental Investigation of Collagen Waviness and Orientation in the Arterial Adventitia Using Confocal Laser Scanning Microscopy,” Biomech. Model. Mechanobiol. 11(3-4), 461–473 (2012).
[Crossref] [PubMed]

Boutopoulos, C.

E. Bergeron, C. Boutopoulos, R. Martel, A. Torres, C. Rodriguez, J. Niskanen, J.-J. Lebrun, F. M. Winnik, P. Sapieha, and M. Meunier, “Cell-specific optoporation with near-infrared ultrafast laser and functionalized gold nanoparticles,” Nanoscale 42, 17836–17847 (2015).

Braeckmans, K.

R. Xiong, K. Raemdonck, K. Peynshaert, I. Lentacker, I. De Cock, J. Demeester, S. C. De Smedt, A. G. Skirtach, and K. Braeckmans, “Comparison of gold nanoparticle mediated photoporation: vapor nanobubbles outperform direct heating for delivering macromolecules in live cells,” ACS Nano 8(6), 6288–6296 (2014).
[Crossref] [PubMed]

Brown, D. B.

B. R. Davis, J. Yannariello-Brown, N. L. Prokopishyn, Z. Luo, M. R. Smith, J. Wang, N. D. Carsrud, and D. B. Brown, “Glass needle-mediated microinjection of macromolecules and transgenes into primary human blood stem/progenitor cells,” Blood 95(2), 437–444 (2000).
[PubMed]

Cametti, C.

I. Fratoddi, I. Venditti, C. Cametti, and M. V. Russo, “How toxic are gold nanoparticles? The state-of-the-art,” Nano Res. 8(6), 1771–1799 (2015).
[Crossref]

Canatella, P. J.

P. J. Canatella, J. F. Karr, J. A. Petros, and M. R. Prausnitz, “Quantitative study of electroporation-mediated molecular uptake and cell viability,” Biophys. J. 80(2), 755–764 (2001).
[Crossref] [PubMed]

Caprettini, V.

G. C. Messina, M. Dipalo, R. La Rocca, P. Zilio, V. Caprettini, R. Proietti Zaccaria, A. Toma, F. Tantussi, L. Berdondini, and F. De Angelis, “Spatially, Temporally, and Quantitatively Controlled Delivery of Broad Range of Molecules into Selected Cells through Plasmonic Nanotubes,” Adv. Mater. 27, 7145 (2015).

Carlson, R.

D. Heinemann, M. Schomaker, S. Kalies, M. Schieck, R. Carlson, H. Murua Escobar, T. Ripken, H. Meyer, and A. Heisterkamp, “Gold nanoparticle mediated laser transfection for efficient siRNA mediated gene knock down,” PLoS One 8(3), e58604 (2013).
[Crossref] [PubMed]

Carsrud, N. D.

B. R. Davis, J. Yannariello-Brown, N. L. Prokopishyn, Z. Luo, M. R. Smith, J. Wang, N. D. Carsrud, and D. B. Brown, “Glass needle-mediated microinjection of macromolecules and transgenes into primary human blood stem/progenitor cells,” Blood 95(2), 437–444 (2000).
[PubMed]

Chen, G.

S. Feng, Z. Li, G. Chen, D. Lin, S. Huang, Z. Huang, Y. Li, J. Lin, R. Chen, and H. Zeng, “Ultrasound-mediated method for rapid delivery of nano-particles into cells for intracellular surface-enhanced Raman spectroscopy and cancer cell screening,” Nanotechnology 26(6), 065101 (2015).
[Crossref] [PubMed]

Chen, H.

Z. Lyu, F. Zhou, Q. Liu, H. Xue, Q. Yu, and H. Chen, “Photoporation: A Universal Platform for Macromolecular Deliveryinto Cells Using Gold Nanoparticle Layers via the Photoporation Effect (Adv. Funct. Mater. 32/2016),” Adv. Funct. Mater. 26(32), 5770 (2016).
[Crossref]

Chen, J.

S. Courvoisier, N. Saklayen, M. Huber, J. Chen, E. D. Diebold, L. Bonacina, J. P. Wolf, and E. Mazur, “Plasmonic Tipless Pyramid Arrays for Cell Poration,” Nano Lett. 15(7), 4461–4466 (2015).
[Crossref] [PubMed]

Chen, R.

S. Feng, Z. Li, G. Chen, D. Lin, S. Huang, Z. Huang, Y. Li, J. Lin, R. Chen, and H. Zeng, “Ultrasound-mediated method for rapid delivery of nano-particles into cells for intracellular surface-enhanced Raman spectroscopy and cancer cell screening,” Nanotechnology 26(6), 065101 (2015).
[Crossref] [PubMed]

Chiou, P.-Y.

Y.-C. Wu, T.-H. Wu, D. L. Clemens, B.-Y. Lee, X. Wen, M. A. Horwitz, M. A. Teitell, and P.-Y. Chiou, “Massively parallel delivery of large cargo into mammalian cells with light pulses,” Nat. Methods 12(5), 439–444 (2015).
[Crossref] [PubMed]

Cho, N.

A. Sharei, J. Zoldan, A. Adamo, W. Y. Sim, N. Cho, E. Jackson, S. Mao, S. Schneider, M.-J. Han, A. Lytton-Jean, P. A. Basto, S. Jhunjhunwala, J. Lee, D. A. Heller, J. W. Kang, G. C. Hartoularos, K.-S. Kim, D. G. Anderson, R. Langer, and K. F. Jensen, “A vector-free microfluidic platform for intracellular delivery,” Proc. Natl. Acad. Sci. U.S.A. 110(6), 2082–2087 (2013).
[Crossref] [PubMed]

Choi, S.

S. Park, S. O. Choi, S. J. Paik, S. Choi, M. Allen, and M. Prausnitz, “Intracellular delivery of molecules using microfabricated nanoneedle arrays,” Biomed. Microdevices 18(1), 10 (2016).
[Crossref] [PubMed]

Choi, S. O.

S. Park, S. O. Choi, S. J. Paik, S. Choi, M. Allen, and M. Prausnitz, “Intracellular delivery of molecules using microfabricated nanoneedle arrays,” Biomed. Microdevices 18(1), 10 (2016).
[Crossref] [PubMed]

Clemens, D. L.

Y.-C. Wu, T.-H. Wu, D. L. Clemens, B.-Y. Lee, X. Wen, M. A. Horwitz, M. A. Teitell, and P.-Y. Chiou, “Massively parallel delivery of large cargo into mammalian cells with light pulses,” Nat. Methods 12(5), 439–444 (2015).
[Crossref] [PubMed]

Courvoisier, S.

S. Courvoisier, N. Saklayen, M. Huber, J. Chen, E. D. Diebold, L. Bonacina, J. P. Wolf, and E. Mazur, “Plasmonic Tipless Pyramid Arrays for Cell Poration,” Nano Lett. 15(7), 4461–4466 (2015).
[Crossref] [PubMed]

Davis, A. A.

A. A. Davis, M. J. Farrar, N. Nishimura, M. M. Jin, and C. B. Schaffer, “Optoporation and Genetic Manipulation of Cells Using Femtosecond Laser Pulses,” Biophys. J. 105(4), 862–871 (2013).
[Crossref] [PubMed]

Davis, B. R.

B. R. Davis, J. Yannariello-Brown, N. L. Prokopishyn, Z. Luo, M. R. Smith, J. Wang, N. D. Carsrud, and D. B. Brown, “Glass needle-mediated microinjection of macromolecules and transgenes into primary human blood stem/progenitor cells,” Blood 95(2), 437–444 (2000).
[PubMed]

De Angelis, F.

G. C. Messina, M. Dipalo, R. La Rocca, P. Zilio, V. Caprettini, R. Proietti Zaccaria, A. Toma, F. Tantussi, L. Berdondini, and F. De Angelis, “Spatially, Temporally, and Quantitatively Controlled Delivery of Broad Range of Molecules into Selected Cells through Plasmonic Nanotubes,” Adv. Mater. 27, 7145 (2015).

De Cock, I.

R. Xiong, K. Raemdonck, K. Peynshaert, I. Lentacker, I. De Cock, J. Demeester, S. C. De Smedt, A. G. Skirtach, and K. Braeckmans, “Comparison of gold nanoparticle mediated photoporation: vapor nanobubbles outperform direct heating for delivering macromolecules in live cells,” ACS Nano 8(6), 6288–6296 (2014).
[Crossref] [PubMed]

De Smedt, S. C.

R. Xiong, K. Raemdonck, K. Peynshaert, I. Lentacker, I. De Cock, J. Demeester, S. C. De Smedt, A. G. Skirtach, and K. Braeckmans, “Comparison of gold nanoparticle mediated photoporation: vapor nanobubbles outperform direct heating for delivering macromolecules in live cells,” ACS Nano 8(6), 6288–6296 (2014).
[Crossref] [PubMed]

Degertekin, F. L.

J. M. Meacham, K. Durvasula, F. L. Degertekin, and A. G. Fedorov, “Physical methods for intracellular delivery: practical aspects from laboratory use to industrial-scale processing,” J. Lab. Autom. 19(1), 1–18 (2014).
[Crossref] [PubMed]

Demeester, J.

R. Xiong, K. Raemdonck, K. Peynshaert, I. Lentacker, I. De Cock, J. Demeester, S. C. De Smedt, A. G. Skirtach, and K. Braeckmans, “Comparison of gold nanoparticle mediated photoporation: vapor nanobubbles outperform direct heating for delivering macromolecules in live cells,” ACS Nano 8(6), 6288–6296 (2014).
[Crossref] [PubMed]

Deng, C. X.

Z. Fan, H. Liu, M. Mayer, and C. X. Deng, “Spatiotemporally controlled single cell sonoporation,” Proc. Natl. Acad. Sci. U.S.A. 109(41), 16486–16491 (2012).
[Crossref] [PubMed]

Diebold, E. D.

S. Courvoisier, N. Saklayen, M. Huber, J. Chen, E. D. Diebold, L. Bonacina, J. P. Wolf, and E. Mazur, “Plasmonic Tipless Pyramid Arrays for Cell Poration,” Nano Lett. 15(7), 4461–4466 (2015).
[Crossref] [PubMed]

Dipalo, M.

G. C. Messina, M. Dipalo, R. La Rocca, P. Zilio, V. Caprettini, R. Proietti Zaccaria, A. Toma, F. Tantussi, L. Berdondini, and F. De Angelis, “Spatially, Temporally, and Quantitatively Controlled Delivery of Broad Range of Molecules into Selected Cells through Plasmonic Nanotubes,” Adv. Mater. 27, 7145 (2015).

Durr, N. J.

O. Ekici, R. K. Harrison, N. J. Durr, D. S. Eversole, M. Lee, and A. Ben-Yakar, “Thermal analysis of gold nanorods heated with femtosecond laser pulses,” J. Phys. D Appl. Phys. 41(18), 185501 (2008).
[Crossref] [PubMed]

Durvasula, K.

J. M. Meacham, K. Durvasula, F. L. Degertekin, and A. G. Fedorov, “Physical methods for intracellular delivery: practical aspects from laboratory use to industrial-scale processing,” J. Lab. Autom. 19(1), 1–18 (2014).
[Crossref] [PubMed]

Ehrhardt, A.

C. E. Thomas, A. Ehrhardt, and M. A. Kay, “Progress and problems with the use of viral vectors for gene therapy,” Nat. Rev. Genet. 4(5), 346–358 (2003).
[Crossref] [PubMed]

Ekici, O.

O. Ekici, R. K. Harrison, N. J. Durr, D. S. Eversole, M. Lee, and A. Ben-Yakar, “Thermal analysis of gold nanorods heated with femtosecond laser pulses,” J. Phys. D Appl. Phys. 41(18), 185501 (2008).
[Crossref] [PubMed]

Eliceiri, K. W.

C. A. Schneider, W. S. Rasband, and K. W. Eliceiri, “NIH Image to ImageJ: 25 years of image analysis,” Nat. Methods 9(7), 671–675 (2012).
[Crossref] [PubMed]

Endl, E.

C. Yao, R. Rahmanzadeh, E. Endl, Z. Zhang, J. Gerdes, and G. Huttmann, “Elevation of plasma membrane permeability by laser irradiation of selectively bound nanoparticles,” J. Biomed. Opt. 10(6), 064012 (2005).
[Crossref] [PubMed]

Evans, H. M.

K. K. Ewert, A. Ahmad, H. M. Evans, and C. R. Safinya, “Cationic lipid-DNA complexes for non-viral gene therapy: Relating supramolecular structures to cellular pathways,” Expert Opin. Biol. Ther. 5(1), 33–53 (2005).
[Crossref] [PubMed]

Eversole, D. S.

O. Ekici, R. K. Harrison, N. J. Durr, D. S. Eversole, M. Lee, and A. Ben-Yakar, “Thermal analysis of gold nanorods heated with femtosecond laser pulses,” J. Phys. D Appl. Phys. 41(18), 185501 (2008).
[Crossref] [PubMed]

Ewert, K. K.

K. K. Ewert, A. Ahmad, H. M. Evans, and C. R. Safinya, “Cationic lipid-DNA complexes for non-viral gene therapy: Relating supramolecular structures to cellular pathways,” Expert Opin. Biol. Ther. 5(1), 33–53 (2005).
[Crossref] [PubMed]

Fan, Z.

Z. Fan, H. Liu, M. Mayer, and C. X. Deng, “Spatiotemporally controlled single cell sonoporation,” Proc. Natl. Acad. Sci. U.S.A. 109(41), 16486–16491 (2012).
[Crossref] [PubMed]

Farrar, M. J.

A. A. Davis, M. J. Farrar, N. Nishimura, M. M. Jin, and C. B. Schaffer, “Optoporation and Genetic Manipulation of Cells Using Femtosecond Laser Pulses,” Biophys. J. 105(4), 862–871 (2013).
[Crossref] [PubMed]

Fasel, J.

E. Fonck, G. G. Feigl, J. Fasel, D. Sage, M. Unser, D. A. Rüfenacht, and N. Stergiopulos, “Effect of Aging on Elastin Functionality in Human Cerebral Arteries,” Stroke 40(7), 2552–2556 (2009).
[Crossref] [PubMed]

Fedorov, A. G.

J. M. Meacham, K. Durvasula, F. L. Degertekin, and A. G. Fedorov, “Physical methods for intracellular delivery: practical aspects from laboratory use to industrial-scale processing,” J. Lab. Autom. 19(1), 1–18 (2014).
[Crossref] [PubMed]

Feigl, G. G.

E. Fonck, G. G. Feigl, J. Fasel, D. Sage, M. Unser, D. A. Rüfenacht, and N. Stergiopulos, “Effect of Aging on Elastin Functionality in Human Cerebral Arteries,” Stroke 40(7), 2552–2556 (2009).
[Crossref] [PubMed]

Feng, S.

S. Feng, Z. Li, G. Chen, D. Lin, S. Huang, Z. Huang, Y. Li, J. Lin, R. Chen, and H. Zeng, “Ultrasound-mediated method for rapid delivery of nano-particles into cells for intracellular surface-enhanced Raman spectroscopy and cancer cell screening,” Nanotechnology 26(6), 065101 (2015).
[Crossref] [PubMed]

Fonck, E.

E. Fonck, G. G. Feigl, J. Fasel, D. Sage, M. Unser, D. A. Rüfenacht, and N. Stergiopulos, “Effect of Aging on Elastin Functionality in Human Cerebral Arteries,” Stroke 40(7), 2552–2556 (2009).
[Crossref] [PubMed]

Fratoddi, I.

I. Fratoddi, I. Venditti, C. Cametti, and M. V. Russo, “How toxic are gold nanoparticles? The state-of-the-art,” Nano Res. 8(6), 1771–1799 (2015).
[Crossref]

Gerdes, J.

C. Yao, R. Rahmanzadeh, E. Endl, Z. Zhang, J. Gerdes, and G. Huttmann, “Elevation of plasma membrane permeability by laser irradiation of selectively bound nanoparticles,” J. Biomed. Opt. 10(6), 064012 (2005).
[Crossref] [PubMed]

Gertner, R. S.

A. K. Shalek, J. T. Robinson, E. S. Karp, J. S. Lee, D.-R. Ahn, M.-H. Yoon, A. Sutton, M. Jorgolli, R. S. Gertner, T. S. Gujral, G. MacBeath, E. G. Yang, and H. Park, “Vertical silicon nanowires as a universal platform for delivering biomolecules into living cells,” Proc. Natl. Acad. Sci. U.S.A. 107(5), 1870–1875 (2010).
[Crossref] [PubMed]

Gillenwater, A. M.

E. Y. Lukianova-Hleb, Y.-S. Kim, I. Belatsarkouski, A. M. Gillenwater, B. E. O’Neill, and D. O. Lapotko, “Intraoperative diagnostics and elimination of residual microtumours with plasmonic nanobubbles,” Nat. Nano. 11, 25–28 (2016).

Girard, C.

G. Baffou, R. Quidant, and C. Girard, “Heat generation in plasmonic nanostructures: Influence of morphology,” Appl. Phys. Lett. 94(15), 153109 (2009).
[Crossref]

Griffa, A.

R. Rezakhaniha, A. Agianniotis, J. T. C. T. C. Schrauwen, A. Griffa, D. Sage, C. V. C. V. C. Bouten, F. N. N. van de Vosse, M. Unser, and N. Stergiopulos, “Experimental Investigation of Collagen Waviness and Orientation in the Arterial Adventitia Using Confocal Laser Scanning Microscopy,” Biomech. Model. Mechanobiol. 11(3-4), 461–473 (2012).
[Crossref] [PubMed]

Gujral, T. S.

A. K. Shalek, J. T. Robinson, E. S. Karp, J. S. Lee, D.-R. Ahn, M.-H. Yoon, A. Sutton, M. Jorgolli, R. S. Gertner, T. S. Gujral, G. MacBeath, E. G. Yang, and H. Park, “Vertical silicon nanowires as a universal platform for delivering biomolecules into living cells,” Proc. Natl. Acad. Sci. U.S.A. 107(5), 1870–1875 (2010).
[Crossref] [PubMed]

Hadjiargyrou, M.

T. Mironava, M. Hadjiargyrou, M. Simon, V. Jurukovski, and M. H. Rafailovich, “Gold nanoparticles cellular toxicity and recovery: effect of size, concentration and exposure time,” Nanotoxicology 4(1), 120–137 (2010).
[Crossref] [PubMed]

Hafner, J. H.

E. Y. Lukianova-Hleb, E. Y. Hanna, J. H. Hafner, and D. O. Lapotko, “Tunable plasmonic nanobubbles for cell theranostics,” Nanotechnology 21(8), 085102 (2010).
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Hammer, S. C.

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V. Zarnitsyn, C. A. Rostad, and M. R. Prausnitz, “Modeling Transmembrane Transport through Cell Membrane Wounds Created by Acoustic Cavitation,” Biophys. J. 95(9), 4124–4138 (2008).
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N. Saklayen, M. Huber, M. Madrid, V. Nuzzo, D. I. Vulis, W. Shen, J. Nelson, A. A. McClelland, A. Heisterkamp, and E. Mazur, “Intracellular Delivery Using Nanosecond-Laser Excitation of Large-Area Plasmonic Substrate,” ACS Nano 11, 3671 (2017).

S. Courvoisier, N. Saklayen, M. Huber, J. Chen, E. D. Diebold, L. Bonacina, J. P. Wolf, and E. Mazur, “Plasmonic Tipless Pyramid Arrays for Cell Poration,” Nano Lett. 15(7), 4461–4466 (2015).
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E. Bergeron, C. Boutopoulos, R. Martel, A. Torres, C. Rodriguez, J. Niskanen, J.-J. Lebrun, F. M. Winnik, P. Sapieha, and M. Meunier, “Cell-specific optoporation with near-infrared ultrafast laser and functionalized gold nanoparticles,” Nanoscale 42, 17836–17847 (2015).

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A. A. Davis, M. J. Farrar, N. Nishimura, M. M. Jin, and C. B. Schaffer, “Optoporation and Genetic Manipulation of Cells Using Femtosecond Laser Pulses,” Biophys. J. 105(4), 862–871 (2013).
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[Crossref] [PubMed]

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[Crossref] [PubMed]

S. Kalies, T. Birr, D. Heinemann, M. Schomaker, T. Ripken, A. Heisterkamp, and H. Meyer, “Enhancement of extracellular molecule uptake in plasmonic laser perforation,” J. Biophotonics 7(7), 474–482 (2014).
[Crossref] [PubMed]

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[Crossref] [PubMed]

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[Crossref] [PubMed]

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N. Saklayen, M. Huber, M. Madrid, V. Nuzzo, D. I. Vulis, W. Shen, J. Nelson, A. A. McClelland, A. Heisterkamp, and E. Mazur, “Intracellular Delivery Using Nanosecond-Laser Excitation of Large-Area Plasmonic Substrate,” ACS Nano 11, 3671 (2017).

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D. Matsumoto, R. Rao Sathuluri, Y. Kato, Y. R. Silberberg, R. Kawamura, F. Iwata, T. Kobayashi, and C. Nakamura, “Oscillating high-aspect-ratio monolithic silicon nanoneedle array enables efficient delivery of functional bio-macromolecules into living cells,” Sci. Rep. 5(1), 15325 (2015).
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A. Sharei, J. Zoldan, A. Adamo, W. Y. Sim, N. Cho, E. Jackson, S. Mao, S. Schneider, M.-J. Han, A. Lytton-Jean, P. A. Basto, S. Jhunjhunwala, J. Lee, D. A. Heller, J. W. Kang, G. C. Hartoularos, K.-S. Kim, D. G. Anderson, R. Langer, and K. F. Jensen, “A vector-free microfluidic platform for intracellular delivery,” Proc. Natl. Acad. Sci. U.S.A. 110(6), 2082–2087 (2013).
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T. Mironava, M. Hadjiargyrou, M. Simon, V. Jurukovski, and M. H. Rafailovich, “Gold nanoparticles cellular toxicity and recovery: effect of size, concentration and exposure time,” Nanotoxicology 4(1), 120–137 (2010).
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R. Xiong, K. Raemdonck, K. Peynshaert, I. Lentacker, I. De Cock, J. Demeester, S. C. De Smedt, A. G. Skirtach, and K. Braeckmans, “Comparison of gold nanoparticle mediated photoporation: vapor nanobubbles outperform direct heating for delivering macromolecules in live cells,” ACS Nano 8(6), 6288–6296 (2014).
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B. R. Davis, J. Yannariello-Brown, N. L. Prokopishyn, Z. Luo, M. R. Smith, J. Wang, N. D. Carsrud, and D. B. Brown, “Glass needle-mediated microinjection of macromolecules and transgenes into primary human blood stem/progenitor cells,” Blood 95(2), 437–444 (2000).
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G. C. Messina, M. Dipalo, R. La Rocca, P. Zilio, V. Caprettini, R. Proietti Zaccaria, A. Toma, F. Tantussi, L. Berdondini, and F. De Angelis, “Spatially, Temporally, and Quantitatively Controlled Delivery of Broad Range of Molecules into Selected Cells through Plasmonic Nanotubes,” Adv. Mater. 27, 7145 (2015).

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Y.-C. Wu, T.-H. Wu, D. L. Clemens, B.-Y. Lee, X. Wen, M. A. Horwitz, M. A. Teitell, and P.-Y. Chiou, “Massively parallel delivery of large cargo into mammalian cells with light pulses,” Nat. Methods 12(5), 439–444 (2015).
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R. Rezakhaniha, A. Agianniotis, J. T. C. T. C. Schrauwen, A. Griffa, D. Sage, C. V. C. V. C. Bouten, F. N. N. van de Vosse, M. Unser, and N. Stergiopulos, “Experimental Investigation of Collagen Waviness and Orientation in the Arterial Adventitia Using Confocal Laser Scanning Microscopy,” Biomech. Model. Mechanobiol. 11(3-4), 461–473 (2012).
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R. Rezakhaniha, A. Agianniotis, J. T. C. T. C. Schrauwen, A. Griffa, D. Sage, C. V. C. V. C. Bouten, F. N. N. van de Vosse, M. Unser, and N. Stergiopulos, “Experimental Investigation of Collagen Waviness and Orientation in the Arterial Adventitia Using Confocal Laser Scanning Microscopy,” Biomech. Model. Mechanobiol. 11(3-4), 461–473 (2012).
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Wang, J.

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E. Y. Lukianova-Hleb, X. Ren, J. A. Zasadzinski, X. Wu, and D. O. Lapotko, “Plasmonic Nanobubbles Enhance Efficacy and Selectivity of Chemotherapy Against Drug-Resistant Cancer Cells,” Adv. Mater. 24(28), 3831–3837 (2012).
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C. Yao, R. Rahmanzadeh, E. Endl, Z. Zhang, J. Gerdes, and G. Huttmann, “Elevation of plasma membrane permeability by laser irradiation of selectively bound nanoparticles,” J. Biomed. Opt. 10(6), 064012 (2005).
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Z. Lyu, F. Zhou, Q. Liu, H. Xue, Q. Yu, and H. Chen, “Photoporation: A Universal Platform for Macromolecular Deliveryinto Cells Using Gold Nanoparticle Layers via the Photoporation Effect (Adv. Funct. Mater. 32/2016),” Adv. Funct. Mater. 26(32), 5770 (2016).
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G. C. Messina, M. Dipalo, R. La Rocca, P. Zilio, V. Caprettini, R. Proietti Zaccaria, A. Toma, F. Tantussi, L. Berdondini, and F. De Angelis, “Spatially, Temporally, and Quantitatively Controlled Delivery of Broad Range of Molecules into Selected Cells through Plasmonic Nanotubes,” Adv. Mater. 27, 7145 (2015).

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A. Sharei, J. Zoldan, A. Adamo, W. Y. Sim, N. Cho, E. Jackson, S. Mao, S. Schneider, M.-J. Han, A. Lytton-Jean, P. A. Basto, S. Jhunjhunwala, J. Lee, D. A. Heller, J. W. Kang, G. C. Hartoularos, K.-S. Kim, D. G. Anderson, R. Langer, and K. F. Jensen, “A vector-free microfluidic platform for intracellular delivery,” Proc. Natl. Acad. Sci. U.S.A. 110(6), 2082–2087 (2013).
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R. Xiong, K. Raemdonck, K. Peynshaert, I. Lentacker, I. De Cock, J. Demeester, S. C. De Smedt, A. G. Skirtach, and K. Braeckmans, “Comparison of gold nanoparticle mediated photoporation: vapor nanobubbles outperform direct heating for delivering macromolecules in live cells,” ACS Nano 8(6), 6288–6296 (2014).
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Z. Lyu, F. Zhou, Q. Liu, H. Xue, Q. Yu, and H. Chen, “Photoporation: A Universal Platform for Macromolecular Deliveryinto Cells Using Gold Nanoparticle Layers via the Photoporation Effect (Adv. Funct. Mater. 32/2016),” Adv. Funct. Mater. 26(32), 5770 (2016).
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E. Y. Lukianova-Hleb, X. Ren, J. A. Zasadzinski, X. Wu, and D. O. Lapotko, “Plasmonic Nanobubbles Enhance Efficacy and Selectivity of Chemotherapy Against Drug-Resistant Cancer Cells,” Adv. Mater. 24(28), 3831–3837 (2012).
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E. Bergeron, C. Boutopoulos, R. Martel, A. Torres, C. Rodriguez, J. Niskanen, J.-J. Lebrun, F. M. Winnik, P. Sapieha, and M. Meunier, “Cell-specific optoporation with near-infrared ultrafast laser and functionalized gold nanoparticles,” Nanoscale 42, 17836–17847 (2015).

Nanotechnology (2)

S. Feng, Z. Li, G. Chen, D. Lin, S. Huang, Z. Huang, Y. Li, J. Lin, R. Chen, and H. Zeng, “Ultrasound-mediated method for rapid delivery of nano-particles into cells for intracellular surface-enhanced Raman spectroscopy and cancer cell screening,” Nanotechnology 26(6), 065101 (2015).
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Figures (6)

Fig. 1
Fig. 1 Using plasmonic substrates to investigate plasma membrane poration of differentiating myoblasts with fluorescent imaging. (A) The experimental setup consists of an 850-ps laser source illuminating a plasmonic pyramidal substrate consisting of uniform base lengths (2.4 μm), heights (1.4 μm), and base to base spacings (1.2 μm) with adherent C2C12 cells. The substrate-cell composite is placed upside down on a glass coverslip with 200 µL of phosphate-buffered saline containing propidium iodide. The assembly is placed on an objective for fluorescence imaging. The inset shows laser-induced poration, enabling the exchange of intra- and extracellular molecules. (B) Shows bright-field images of the pyramidal substrate exposed at different laser fluences and exposure times to determine the optical damage threshold of the plasmonic substrate. At the bottom are single laser shot simulation results of the temperature of the gold pyramids and surrounding water. (C) Cells pre-stained with Calcein AM confirm plasma membrane poration. A decrease in calcein signal after laser exposure indicates outflow of intracellular molecules, while an increase in propidium iodide signal indicates inflow of extracellular molecules. The poration efficiency of C2C12 as a function of fluence for different laser exposures: (D)10 ms, (E) 20 ms, and (F) 40 ms. Data show standard error of the mean for three independent measurements with around 3-6 cells in each spot.
Fig. 2
Fig. 2 Determining the pore size using time-lapse imaging. (A) Calcein outflow and propidium iodide inflow. (B) Time-lapse imaging of C2C12 cells to determine the decrease in fluorescence over time at 10 frames per second (fps) for 60 s. Outlines of cells show the region in which fluorescence signal is measured. (C) Relative fluorescence of calcein and propidium iodide over time. The data is fitted to Eq. (2). (D) Data showing in/outflow exponential constants τ and a pore radius rs of 18.4 ± 2.9 nm with calcein and 9.7 ± 3.4 nm with Propidium Iodide. Numbers obtained from three independent experiments, using five cells for each experiment.
Fig. 3
Fig. 3 Cell morphology: changes in plasma membrane area, cytoplasmic area, and nuclear area. (A) Schematic representation showing different regions of the cell that are fluorescently labeled. Cells were imaged at 30 s, 10 min, 30 min, and 60 min after laser exposure. (B) The plasma membrane area attached to the pyramidal surface decreases due to laser exposure but stabilizes after 30 min. Boxes represent the 25% and 75% quantile and whiskers represent the 5% and 95% quantile. The straight line across the box represents median and small square box represents mean. Crosses represent minimum and maximum in each data set. (C) Laser-induced decrease in cytoplasmic area due to laser exposure (statistically significant until 60 min.). (D) Laser-induced decrease in nuclear area (not statistically significant after 30 min.). (E) Ratio of nuclear to cytoplasmic area (three independent experiments, with 10 cells each). * = p < 0.05; ** = p < 0.01; *** = p < 0.001.
Fig. 4
Fig. 4 Cellular displacement and repositioning. (A) Position properties measured: center of mass position, long axis, and short axis. (B) Time-dependence of relative center of mass. (C) Change in short-axis length over time. (D) Change in long-axis length over time. Boxes represent the 25% and 75% quantile and whiskers represent the 5% and 95% quantile. The straight line across the box represents median and small square box represents mean. Crosses represent minimum and maximum in each data set. Data obtained from three independent experiments, with 10 cells each. * = p < 0.05; ** = p < 0.01; *** = p < 0.001.
Fig. 5
Fig. 5 Cytoskeleton orientation. (A) Fluorescent imaging of the cytoskeleton before and after laser exposure and calculated fiber orientation of fibers in the cytoskeleton. (B) Change in fiber orientation over time. Boxes represent the 25% and 75% quantile and whiskers represent the 5% and 95% quantile. The straight line across the box represents median and small square box represents mean. Crosses represent minimum and maximum in each data set. Data obtained from three independent experiments, with 10 cells each; p-values all greater than 0.05.
Fig. 6
Fig. 6 Membrane permeabilization of differentiated myotubes. (A) Differentiation of C2C12 myoblasts on the substrate to make longer C2C12 myotube cells. (B) Poration due to laser exposure. Propidium iodide delivery is limited to the laser-exposed area. (C) Fluence-dependence of the membrane poration efficiency for different laser exposures. Data obtained from three independent experiments, with three cells each.

Equations (3)

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Φ( t )=Φ( 0 )exp( t τ ) ,
dΦ( t ) dt = π r 2 D ( Z+ 2πr 4 )V  Φ( t ) ,
τ= (Z+ 2πr 4 )V π r 2 D .

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