Abstract

Can photothermal gold nanoparticle mediated laser manipulation be applied to induce cardiac contraction? Based on our previous work, we present a novel concept of cell stimulation. A 532 nm picosecond laser was employed to heat gold nanoparticles on cardiomyocytes. This leads to calcium oscillations in the HL-1 cardiomyocyte cell line. As calcium is connected to the contractility, we aimed to alter the contraction rate of native and stem cell derived cardiomyocytes. A contraction rate increase was particularly observed in calcium containing buffer with neonatal rat cardiomyocytes. Consequently, the study provides conceptual ideas for a light based, nanoparticle mediated stimulation system.

© 2016 Optical Society of America

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    [Crossref]
  46. G. M. Dittami, S. M. Rajguru, R. A. Lasher, R. W. Hitchcock, and R. D. Rabbitt, “Intracellular calcium transients evoked by pulsed infrared radiation in neonatal cardiomyocytes,” J. Physiol. 589(6), 1295–1306 (2011).
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2016 (2)

J. Krawinkel, U. Richter, M. L. Torres-Mapa, M. Westermann, L. Gamrad, C. Rehbock, S. Barcikowski, and A. Heisterkamp, “Optical and electron microscopy study of laser-based intracellular molecule delivery using peptide-conjugated photodispersible gold nanoparticle agglomerates,” J. Nanobiotechnology 14(1), 2 (2016).
[Crossref] [PubMed]

H. Kempf, B. Andree, and R. Zweigerdt, “Large-scale production of human pluripotent stem cell derived cardiomyocytes,” Adv. Drug Deliv. Rev. 96, 18–30 (2016).
[Crossref] [PubMed]

2015 (4)

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]

H. Kempf, C. Kropp, R. Olmer, U. Martin, and R. Zweigerdt, “Cardiac differentiation of human pluripotent stem cells in scalable suspension culture,” Nat. Protoc. 10(9), 1345–1361 (2015).
[Crossref] [PubMed]

M. Schomaker, D. Killian, S. Willenbrock, D. Heinemann, S. Kalies, A. Ngezahayo, I. Nolte, T. Ripken, C. Junghanß, H. Meyer, H. Murua Escobar, and A. Heisterkamp, “Biophysical effects in off-resonant gold nanoparticle mediated (GNOME) laser transfection of cell lines, primary- and stem cells using fs laser pulses,” J. Biophotonics 8(8), 646–658 (2015).
[Crossref] [PubMed]

J. L. Carvalho-de-Souza, J. S. Treger, B. Dang, S. B. H. Kent, D. R. Pepperberg, and F. Bezanilla, “Photosensitivity of neurons enabled by cell-targeted gold nanoparticles,” Neuron 86(1), 207–217 (2015).
[Crossref] [PubMed]

2014 (6)

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. Yong, K. Needham, W. G. A. Brown, B. A. Nayagam, S. L. McArthur, A. Yu, and P. R. Stoddart, “Gold-nanorod-assisted near-infrared stimulation of primary auditory neurons,” Adv. Healthc. Mater. 3(11), 1862–1868 (2014).
[Crossref] [PubMed]

C. Paviolo, A. C. Thompson, J. Yong, W. G. A. Brown, and P. R. Stoddart, “Nanoparticle-enhanced infrared neural stimulation,” J. Neural Eng. 11(6), 065002 (2014).
[Crossref] [PubMed]

A. Klimas and E. Entcheva, “Toward microendoscopy-inspired cardiac optogenetics in vivo: technical overview and perspective,” J. Biomed. Opt. 19(8), 080701 (2014).
[Crossref] [PubMed]

H. Kempf, R. Olmer, C. Kropp, M. Rückert, M. Jara-Avaca, D. Robles-Diaz, A. Franke, D. A. Elliott, D. Wojciechowski, M. Fischer, A. Roa Lara, G. Kensah, I. Gruh, A. Haverich, U. Martin, and R. Zweigerdt, “Controlling expansion and cardiomyogenic differentiation of human pluripotent stem cells in scalable suspension culture,” Stem Cell Rep. 3(6), 1132–1146 (2014).
[Crossref] [PubMed]

K. Schwanke, S. Merkert, H. Kempf, S. Hartung, M. Jara-Avaca, C. Templin, G. Göhring, A. Haverich, U. Martin, and R. Zweigerdt, “Fast and efficient multitransgenic modification of human pluripotent stem cells,” Hum. Gene Ther. Methods 25(2), 136–153 (2014).
[Crossref] [PubMed]

2013 (4)

Z. Vukadinovic-Nikolic, B. Andrée, S. E. Dorfman, M. Pflaum, T. Horvath, M. Lux, L. Venturini, A. Bär, G. Kensah, A. R. Lara, I. Tudorache, S. Cebotari, D. Hilfiker-Kleiner, A. Haverich, and A. Hilfiker, “Generation of Bioartificial Heart Tissue by Combining a Three-Dimensional Gel-Based Cardiac Construct with Decellularized Small Intestinal Submucosa,” Tissue Eng. Part A 20(3-4), 799–809 (2013).
[Crossref] [PubMed]

E. Boulais, R. Lachaine, A. Hatef, and M. Meunier, “Plasmonics for pulsed-laser cell nanosurgery: Fundamentals and applications,” J. Photochem Photobiol. 17, 26–49 (2013).

C. Robertson, D. D. Tran, and S. C. George, “Concise review: maturation phases of human pluripotent stem cell-derived cardiomyocytes,” Stem Cells 31(5), 829–837 (2013).
[Crossref] [PubMed]

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]

2012 (5)

L. Leybaert and M. J. Sanderson, “Intercellular Ca(2+) waves: mechanisms and function,” Physiol. Rev. 92(3), 1359–1392 (2012).
[Crossref] [PubMed]

H. Jans and Q. Huo, “Gold nanoparticle-enabled biological and chemical detection and analysis,” Chem. Soc. Rev. 41(7), 2849–2866 (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]

G. Bisker and D. Yelin, “Noble-metal nanoparticles and short pulses for nanomanipulations: theoretical analysis,” J. Opt. Soc. Am. B 29(6), 1383 (2012).
[Crossref]

2011 (3)

Z. Jia, V. Valiunas, Z. Lu, H. Bien, H. Liu, H. Z. Wang, B. Rosati, P. R. Brink, I. S. Cohen, and E. Entcheva, “Stimulating cardiac muscle by light: cardiac optogenetics by cell delivery,” Circ Arrhythm Electrophysiol 4(5), 753–760 (2011).
[Crossref] [PubMed]

G. M. Dittami, S. M. Rajguru, R. A. Lasher, R. W. Hitchcock, and R. D. Rabbitt, “Intracellular calcium transients evoked by pulsed infrared radiation in neonatal cardiomyocytes,” J. Physiol. 589(6), 1295–1306 (2011).
[Crossref] [PubMed]

N. Khlebtsov and L. Dykman, “Biodistribution and toxicity of engineered gold nanoparticles: a review of in vitro and in vivo studies,” Chem. Soc. Rev. 40(3), 1647–1671 (2011).
[Crossref] [PubMed]

2010 (6)

M. W. Jenkins, A. R. Duke, S. Gu, H. J. Chiel, H. Fujioka, M. Watanabe, E. D. Jansen, and A. M. Rollins, “Optical pacing of the embryonic heart,” Nat. Photonics 4(9), 623–626 (2010).
[Crossref] [PubMed]

E. Lukianova-Hleb, Y. Hu, L. Latterini, L. Tarpani, S. Lee, R. A. Drezek, J. H. Hafner, and D. O. Lapotko, “Plasmonic nanobubbles as transient vapor nanobubbles generated around plasmonic nanoparticles,” ACS Nano 4(4), 2109–2123 (2010).
[Crossref] [PubMed]

J.-C. Kim, M.-J. Son, K. P. Subedi, D. H. Kim, and S.-H. Woo, “IP3-induced cytosolic and nuclear Ca2+ signals in HL-1 atrial myocytes: possible role of IP3 receptor subtypes,” Mol. Cells 29(4), 387–395 (2010).
[Crossref] [PubMed]

J.-C. Kim, M.-J. Son, K. P. Subedi, Y. Li, J. R. Ahn, and S.-H. Woo, “Atrial local Ca2+ signaling and inositol 1,4,5-trisphosphate receptors,” Prog. Biophys. Mol. Biol. 103(1), 59–70 (2010).
[Crossref] [PubMed]

T. Bruegmann, D. Malan, M. Hesse, T. Beiert, C. J. Fuegemann, B. K. Fleischmann, and P. Sasse, “Optogenetic control of heart muscle in vitro and in vivo,” Nat. Methods 7(11), 897–900 (2010).
[Crossref] [PubMed]

C. Hrelescu, J. Stehr, M. Ringler, R. A. Sperling, W. J. Parak, T. A. Klar, and J. Feldmann, “DNA Melting in Gold Nanostove Clusters,” J. Phys. Chem. C 114(16), 7401–7411 (2010).
[Crossref]

2009 (1)

V. Tseeb, M. Suzuki, K. Oyama, K. Iwai, and S. Ishiwata, “Highly thermosensitive Ca dynamics in a HeLa cell through IP(3) receptors,” HFSP J. 3(2), 117–123 (2009).
[Crossref] [PubMed]

2008 (3)

X. Huang, P. K. Jain, I. H. El-Sayed, and M. A. El-Sayed, “Plasmonic photothermal therapy (PPTT) using gold nanoparticles,” Lasers Med. Sci. 23(3), 217–228 (2008).
[Crossref] [PubMed]

D. Luo, D. Yang, X. Lan, K. Li, X. Li, J. Chen, Y. Zhang, R.-P. Xiao, Q. Han, and H. Cheng, “Nuclear Ca2+ sparks and waves mediated by inositol 1,4,5-trisphosphate receptors in neonatal rat cardiomyocytes,” Cell Calcium 43(2), 165–174 (2008).
[Crossref] [PubMed]

N. I. Smith, Y. Kumamoto, S. Iwanaga, J. Ando, K. Fujita, and S. Kawata, “A femtosecond laser pacemaker for heart muscle cells,” Opt. Express 16(12), 8604–8616 (2008).
[Crossref] [PubMed]

2007 (1)

X. Huang, P. K. Jain, I. H. El-Sayed, and M. A. El-Sayed, “Gold nanoparticles: interesting optical properties and recent applications in cancer diagnostics and therapy,” Nanomedicine (Lond.) 2(5), 681–693 (2007).
[Crossref] [PubMed]

2006 (2)

N. I. Smith, S. Iwanaga, T. Beppu, K. Fujita, O. Nakamura, and S. Kawata, “Photostimulation of two types of Ca 2+ waves in rat pheochromocytoma PC12 cells by ultrashort pulsed near-infrared laser irradiation,” Laser Phys. Lett. 3(3), 154–161 (2006).
[Crossref]

K. Dolnikov, M. Shilkrut, N. Zeevi-Levin, S. Gerecht-Nir, M. Amit, A. Danon, J. Itskovitz-Eldor, and O. Binah, “Functional properties of human embryonic stem cell-derived cardiomyocytes: intracellular Ca2+ handling and the role of sarcoplasmic reticulum in the contraction,” Stem Cells 24(2), 236–245 (2006).
[Crossref] [PubMed]

2003 (3)

G. Nagel, T. Szellas, W. Huhn, S. Kateriya, N. Adeishvili, P. Berthold, D. Ollig, P. Hegemann, and E. Bamberg, “Channelrhodopsin-2, a directly light-gated cation-selective membrane channel,” Proc. Natl. Acad. Sci. U.S.A. 100(24), 13940–13945 (2003).
[Crossref] [PubMed]

S. Orrenius, B. Zhivotovsky, and P. Nicotera, “Regulation of cell death: the calcium-apoptosis link,” Nat. Rev. Mol. Cell Biol. 4(7), 552–565 (2003).
[Crossref] [PubMed]

P. Kohl, “Heterogeneous cell coupling in the heart: an electrophysiological role for fibroblasts,” Circ. Res. 93(5), 381–383 (2003).
[Crossref] [PubMed]

2001 (1)

N. I. Smith, K. Fujita, T. Kaneko, K. Katoh, O. Nakamura, S. Kawata, and T. Takamatsu, “Generation of calcium waves in living cells by pulsed-laser-induced photodisruption,” Appl. Phys. Lett. 79(8), 1208 (2001).
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2000 (3)

P. Lipp, M. Laine, S. C. Tovey, K. M. Burrell, M. J. Berridge, W. Li, and M. D. Bootman, “Functional InsP3 receptors that may modulate excitation-contraction coupling in the heart,” Curr. Biol. 10(15), 939–942 (2000).
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K. R. Gee, K. A. Brown, W. N. Chen, J. Bishop-Stewart, D. Gray, and I. Johnson, “Chemical and physiological characterization of fluo-4 Ca(2+)-indicator dyes,” Cell Calcium 27(2), 97–106 (2000).
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D. M. Bers, “Calcium Fluxes Involved in Control of Cardiac Myocyte Contraction,” Circ. Res. 87(4), 275–281 (2000).
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1998 (1)

W. C. Claycomb, N. A. Lanson, B. S. Stallworth, D. B. Egeland, J. B. Delcarpio, A. Bahinski, and N. J. Izzo., “HL-1 cells: a cardiac muscle cell line that contracts and retains phenotypic characteristics of the adult cardiomyocyte,” Proc. Natl. Acad. Sci. U.S.A. 95(6), 2979–2984 (1998).
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1989 (1)

J. C. Sáez, J. A. Connor, D. C. Spray, and M. V. Bennett, “Hepatocyte gap junctions are permeable to the second messenger, inositol 1,4,5-trisphosphate, and to calcium ions,” Proc. Natl. Acad. Sci. U.S.A. 86(8), 2708–2712 (1989).
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1979 (1)

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Ahn, J. R.

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Amit, M.

K. Dolnikov, M. Shilkrut, N. Zeevi-Levin, S. Gerecht-Nir, M. Amit, A. Danon, J. Itskovitz-Eldor, and O. Binah, “Functional properties of human embryonic stem cell-derived cardiomyocytes: intracellular Ca2+ handling and the role of sarcoplasmic reticulum in the contraction,” Stem Cells 24(2), 236–245 (2006).
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Ando, J.

Andree, B.

H. Kempf, B. Andree, and R. Zweigerdt, “Large-scale production of human pluripotent stem cell derived cardiomyocytes,” Adv. Drug Deliv. Rev. 96, 18–30 (2016).
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Z. Vukadinovic-Nikolic, B. Andrée, S. E. Dorfman, M. Pflaum, T. Horvath, M. Lux, L. Venturini, A. Bär, G. Kensah, A. R. Lara, I. Tudorache, S. Cebotari, D. Hilfiker-Kleiner, A. Haverich, and A. Hilfiker, “Generation of Bioartificial Heart Tissue by Combining a Three-Dimensional Gel-Based Cardiac Construct with Decellularized Small Intestinal Submucosa,” Tissue Eng. Part A 20(3-4), 799–809 (2013).
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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).
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Bahinski, A.

W. C. Claycomb, N. A. Lanson, B. S. Stallworth, D. B. Egeland, J. B. Delcarpio, A. Bahinski, and N. J. Izzo., “HL-1 cells: a cardiac muscle cell line that contracts and retains phenotypic characteristics of the adult cardiomyocyte,” Proc. Natl. Acad. Sci. U.S.A. 95(6), 2979–2984 (1998).
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Bamberg, E.

G. Nagel, T. Szellas, W. Huhn, S. Kateriya, N. Adeishvili, P. Berthold, D. Ollig, P. Hegemann, and E. Bamberg, “Channelrhodopsin-2, a directly light-gated cation-selective membrane channel,” Proc. Natl. Acad. Sci. U.S.A. 100(24), 13940–13945 (2003).
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Z. Vukadinovic-Nikolic, B. Andrée, S. E. Dorfman, M. Pflaum, T. Horvath, M. Lux, L. Venturini, A. Bär, G. Kensah, A. R. Lara, I. Tudorache, S. Cebotari, D. Hilfiker-Kleiner, A. Haverich, and A. Hilfiker, “Generation of Bioartificial Heart Tissue by Combining a Three-Dimensional Gel-Based Cardiac Construct with Decellularized Small Intestinal Submucosa,” Tissue Eng. Part A 20(3-4), 799–809 (2013).
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J. Krawinkel, U. Richter, M. L. Torres-Mapa, M. Westermann, L. Gamrad, C. Rehbock, S. Barcikowski, and A. Heisterkamp, “Optical and electron microscopy study of laser-based intracellular molecule delivery using peptide-conjugated photodispersible gold nanoparticle agglomerates,” J. Nanobiotechnology 14(1), 2 (2016).
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T. Bruegmann, D. Malan, M. Hesse, T. Beiert, C. J. Fuegemann, B. K. Fleischmann, and P. Sasse, “Optogenetic control of heart muscle in vitro and in vivo,” Nat. Methods 7(11), 897–900 (2010).
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J. C. Sáez, J. A. Connor, D. C. Spray, and M. V. Bennett, “Hepatocyte gap junctions are permeable to the second messenger, inositol 1,4,5-trisphosphate, and to calcium ions,” Proc. Natl. Acad. Sci. U.S.A. 86(8), 2708–2712 (1989).
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N. I. Smith, S. Iwanaga, T. Beppu, K. Fujita, O. Nakamura, and S. Kawata, “Photostimulation of two types of Ca 2+ waves in rat pheochromocytoma PC12 cells by ultrashort pulsed near-infrared laser irradiation,” Laser Phys. Lett. 3(3), 154–161 (2006).
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Berridge, M. J.

P. Lipp, M. Laine, S. C. Tovey, K. M. Burrell, M. J. Berridge, W. Li, and M. D. Bootman, “Functional InsP3 receptors that may modulate excitation-contraction coupling in the heart,” Curr. Biol. 10(15), 939–942 (2000).
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Bers, D. M.

D. M. Bers, “Calcium Fluxes Involved in Control of Cardiac Myocyte Contraction,” Circ. Res. 87(4), 275–281 (2000).
[Crossref] [PubMed]

Berthold, P.

G. Nagel, T. Szellas, W. Huhn, S. Kateriya, N. Adeishvili, P. Berthold, D. Ollig, P. Hegemann, and E. Bamberg, “Channelrhodopsin-2, a directly light-gated cation-selective membrane channel,” Proc. Natl. Acad. Sci. U.S.A. 100(24), 13940–13945 (2003).
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J. L. Carvalho-de-Souza, J. S. Treger, B. Dang, S. B. H. Kent, D. R. Pepperberg, and F. Bezanilla, “Photosensitivity of neurons enabled by cell-targeted gold nanoparticles,” Neuron 86(1), 207–217 (2015).
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Z. Jia, V. Valiunas, Z. Lu, H. Bien, H. Liu, H. Z. Wang, B. Rosati, P. R. Brink, I. S. Cohen, and E. Entcheva, “Stimulating cardiac muscle by light: cardiac optogenetics by cell delivery,” Circ Arrhythm Electrophysiol 4(5), 753–760 (2011).
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Binah, O.

K. Dolnikov, M. Shilkrut, N. Zeevi-Levin, S. Gerecht-Nir, M. Amit, A. Danon, J. Itskovitz-Eldor, and O. Binah, “Functional properties of human embryonic stem cell-derived cardiomyocytes: intracellular Ca2+ handling and the role of sarcoplasmic reticulum in the contraction,” Stem Cells 24(2), 236–245 (2006).
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Z. Qin and J. C. Bischof, “Thermophysical and biological responses of gold nanoparticle laser heating,” Chem. Soc. Rev. 41(3), 1191–1217 (2012).
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Bishop-Stewart, J.

K. R. Gee, K. A. Brown, W. N. Chen, J. Bishop-Stewart, D. Gray, and I. Johnson, “Chemical and physiological characterization of fluo-4 Ca(2+)-indicator dyes,” Cell Calcium 27(2), 97–106 (2000).
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Bisker, G.

Bootman, M. D.

P. Lipp, M. Laine, S. C. Tovey, K. M. Burrell, M. J. Berridge, W. Li, and M. D. Bootman, “Functional InsP3 receptors that may modulate excitation-contraction coupling in the heart,” Curr. Biol. 10(15), 939–942 (2000).
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Boulais, E.

E. Boulais, R. Lachaine, A. Hatef, and M. Meunier, “Plasmonics for pulsed-laser cell nanosurgery: Fundamentals and applications,” J. Photochem Photobiol. 17, 26–49 (2013).

Brink, P. R.

Z. Jia, V. Valiunas, Z. Lu, H. Bien, H. Liu, H. Z. Wang, B. Rosati, P. R. Brink, I. S. Cohen, and E. Entcheva, “Stimulating cardiac muscle by light: cardiac optogenetics by cell delivery,” Circ Arrhythm Electrophysiol 4(5), 753–760 (2011).
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Brown, K. A.

K. R. Gee, K. A. Brown, W. N. Chen, J. Bishop-Stewart, D. Gray, and I. Johnson, “Chemical and physiological characterization of fluo-4 Ca(2+)-indicator dyes,” Cell Calcium 27(2), 97–106 (2000).
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Brown, W. G. A.

C. Paviolo, A. C. Thompson, J. Yong, W. G. A. Brown, and P. R. Stoddart, “Nanoparticle-enhanced infrared neural stimulation,” J. Neural Eng. 11(6), 065002 (2014).
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J. Yong, K. Needham, W. G. A. Brown, B. A. Nayagam, S. L. McArthur, A. Yu, and P. R. Stoddart, “Gold-nanorod-assisted near-infrared stimulation of primary auditory neurons,” Adv. Healthc. Mater. 3(11), 1862–1868 (2014).
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Bruegmann, T.

T. Bruegmann, D. Malan, M. Hesse, T. Beiert, C. J. Fuegemann, B. K. Fleischmann, and P. Sasse, “Optogenetic control of heart muscle in vitro and in vivo,” Nat. Methods 7(11), 897–900 (2010).
[Crossref] [PubMed]

Burrell, K. M.

P. Lipp, M. Laine, S. C. Tovey, K. M. Burrell, M. J. Berridge, W. Li, and M. D. Bootman, “Functional InsP3 receptors that may modulate excitation-contraction coupling in the heart,” Curr. Biol. 10(15), 939–942 (2000).
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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).
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Carvalho-de-Souza, J. L.

J. L. Carvalho-de-Souza, J. S. Treger, B. Dang, S. B. H. Kent, D. R. Pepperberg, and F. Bezanilla, “Photosensitivity of neurons enabled by cell-targeted gold nanoparticles,” Neuron 86(1), 207–217 (2015).
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Cebotari, S.

Z. Vukadinovic-Nikolic, B. Andrée, S. E. Dorfman, M. Pflaum, T. Horvath, M. Lux, L. Venturini, A. Bär, G. Kensah, A. R. Lara, I. Tudorache, S. Cebotari, D. Hilfiker-Kleiner, A. Haverich, and A. Hilfiker, “Generation of Bioartificial Heart Tissue by Combining a Three-Dimensional Gel-Based Cardiac Construct with Decellularized Small Intestinal Submucosa,” Tissue Eng. Part A 20(3-4), 799–809 (2013).
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Chen, J.

D. Luo, D. Yang, X. Lan, K. Li, X. Li, J. Chen, Y. Zhang, R.-P. Xiao, Q. Han, and H. Cheng, “Nuclear Ca2+ sparks and waves mediated by inositol 1,4,5-trisphosphate receptors in neonatal rat cardiomyocytes,” Cell Calcium 43(2), 165–174 (2008).
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Chen, W. N.

K. R. Gee, K. A. Brown, W. N. Chen, J. Bishop-Stewart, D. Gray, and I. Johnson, “Chemical and physiological characterization of fluo-4 Ca(2+)-indicator dyes,” Cell Calcium 27(2), 97–106 (2000).
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Cheng, H.

D. Luo, D. Yang, X. Lan, K. Li, X. Li, J. Chen, Y. Zhang, R.-P. Xiao, Q. Han, and H. Cheng, “Nuclear Ca2+ sparks and waves mediated by inositol 1,4,5-trisphosphate receptors in neonatal rat cardiomyocytes,” Cell Calcium 43(2), 165–174 (2008).
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Chiel, H. J.

M. W. Jenkins, A. R. Duke, S. Gu, H. J. Chiel, H. Fujioka, M. Watanabe, E. D. Jansen, and A. M. Rollins, “Optical pacing of the embryonic heart,” Nat. Photonics 4(9), 623–626 (2010).
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Claycomb, W. C.

W. C. Claycomb, N. A. Lanson, B. S. Stallworth, D. B. Egeland, J. B. Delcarpio, A. Bahinski, and N. J. Izzo., “HL-1 cells: a cardiac muscle cell line that contracts and retains phenotypic characteristics of the adult cardiomyocyte,” Proc. Natl. Acad. Sci. U.S.A. 95(6), 2979–2984 (1998).
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Cohen, I. S.

Z. Jia, V. Valiunas, Z. Lu, H. Bien, H. Liu, H. Z. Wang, B. Rosati, P. R. Brink, I. S. Cohen, and E. Entcheva, “Stimulating cardiac muscle by light: cardiac optogenetics by cell delivery,” Circ Arrhythm Electrophysiol 4(5), 753–760 (2011).
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Connor, J. A.

J. C. Sáez, J. A. Connor, D. C. Spray, and M. V. Bennett, “Hepatocyte gap junctions are permeable to the second messenger, inositol 1,4,5-trisphosphate, and to calcium ions,” Proc. Natl. Acad. Sci. U.S.A. 86(8), 2708–2712 (1989).
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Dang, B.

J. L. Carvalho-de-Souza, J. S. Treger, B. Dang, S. B. H. Kent, D. R. Pepperberg, and F. Bezanilla, “Photosensitivity of neurons enabled by cell-targeted gold nanoparticles,” Neuron 86(1), 207–217 (2015).
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K. Dolnikov, M. Shilkrut, N. Zeevi-Levin, S. Gerecht-Nir, M. Amit, A. Danon, J. Itskovitz-Eldor, and O. Binah, “Functional properties of human embryonic stem cell-derived cardiomyocytes: intracellular Ca2+ handling and the role of sarcoplasmic reticulum in the contraction,” Stem Cells 24(2), 236–245 (2006).
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W. C. Claycomb, N. A. Lanson, B. S. Stallworth, D. B. Egeland, J. B. Delcarpio, A. Bahinski, and N. J. Izzo., “HL-1 cells: a cardiac muscle cell line that contracts and retains phenotypic characteristics of the adult cardiomyocyte,” Proc. Natl. Acad. Sci. U.S.A. 95(6), 2979–2984 (1998).
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Z. Vukadinovic-Nikolic, B. Andrée, S. E. Dorfman, M. Pflaum, T. Horvath, M. Lux, L. Venturini, A. Bär, G. Kensah, A. R. Lara, I. Tudorache, S. Cebotari, D. Hilfiker-Kleiner, A. Haverich, and A. Hilfiker, “Generation of Bioartificial Heart Tissue by Combining a Three-Dimensional Gel-Based Cardiac Construct with Decellularized Small Intestinal Submucosa,” Tissue Eng. Part A 20(3-4), 799–809 (2013).
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Duke, A. R.

M. W. Jenkins, A. R. Duke, S. Gu, H. J. Chiel, H. Fujioka, M. Watanabe, E. D. Jansen, and A. M. Rollins, “Optical pacing of the embryonic heart,” Nat. Photonics 4(9), 623–626 (2010).
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N. Khlebtsov and L. Dykman, “Biodistribution and toxicity of engineered gold nanoparticles: a review of in vitro and in vivo studies,” Chem. Soc. Rev. 40(3), 1647–1671 (2011).
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Egeland, D. B.

W. C. Claycomb, N. A. Lanson, B. S. Stallworth, D. B. Egeland, J. B. Delcarpio, A. Bahinski, and N. J. Izzo., “HL-1 cells: a cardiac muscle cell line that contracts and retains phenotypic characteristics of the adult cardiomyocyte,” Proc. Natl. Acad. Sci. U.S.A. 95(6), 2979–2984 (1998).
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H. Kempf, R. Olmer, C. Kropp, M. Rückert, M. Jara-Avaca, D. Robles-Diaz, A. Franke, D. A. Elliott, D. Wojciechowski, M. Fischer, A. Roa Lara, G. Kensah, I. Gruh, A. Haverich, U. Martin, and R. Zweigerdt, “Controlling expansion and cardiomyogenic differentiation of human pluripotent stem cells in scalable suspension culture,” Stem Cell Rep. 3(6), 1132–1146 (2014).
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El-Sayed, I. H.

X. Huang, P. K. Jain, I. H. El-Sayed, and M. A. El-Sayed, “Plasmonic photothermal therapy (PPTT) using gold nanoparticles,” Lasers Med. Sci. 23(3), 217–228 (2008).
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X. Huang, P. K. Jain, I. H. El-Sayed, and M. A. El-Sayed, “Gold nanoparticles: interesting optical properties and recent applications in cancer diagnostics and therapy,” Nanomedicine (Lond.) 2(5), 681–693 (2007).
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El-Sayed, M. A.

X. Huang, P. K. Jain, I. H. El-Sayed, and M. A. El-Sayed, “Plasmonic photothermal therapy (PPTT) using gold nanoparticles,” Lasers Med. Sci. 23(3), 217–228 (2008).
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X. Huang, P. K. Jain, I. H. El-Sayed, and M. A. El-Sayed, “Gold nanoparticles: interesting optical properties and recent applications in cancer diagnostics and therapy,” Nanomedicine (Lond.) 2(5), 681–693 (2007).
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A. Klimas and E. Entcheva, “Toward microendoscopy-inspired cardiac optogenetics in vivo: technical overview and perspective,” J. Biomed. Opt. 19(8), 080701 (2014).
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Z. Jia, V. Valiunas, Z. Lu, H. Bien, H. Liu, H. Z. Wang, B. Rosati, P. R. Brink, I. S. Cohen, and E. Entcheva, “Stimulating cardiac muscle by light: cardiac optogenetics by cell delivery,” Circ Arrhythm Electrophysiol 4(5), 753–760 (2011).
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Feldmann, J.

C. Hrelescu, J. Stehr, M. Ringler, R. A. Sperling, W. J. Parak, T. A. Klar, and J. Feldmann, “DNA Melting in Gold Nanostove Clusters,” J. Phys. Chem. C 114(16), 7401–7411 (2010).
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Fischer, M.

H. Kempf, R. Olmer, C. Kropp, M. Rückert, M. Jara-Avaca, D. Robles-Diaz, A. Franke, D. A. Elliott, D. Wojciechowski, M. Fischer, A. Roa Lara, G. Kensah, I. Gruh, A. Haverich, U. Martin, and R. Zweigerdt, “Controlling expansion and cardiomyogenic differentiation of human pluripotent stem cells in scalable suspension culture,” Stem Cell Rep. 3(6), 1132–1146 (2014).
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Fleischmann, B. K.

T. Bruegmann, D. Malan, M. Hesse, T. Beiert, C. J. Fuegemann, B. K. Fleischmann, and P. Sasse, “Optogenetic control of heart muscle in vitro and in vivo,” Nat. Methods 7(11), 897–900 (2010).
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Franke, A.

H. Kempf, R. Olmer, C. Kropp, M. Rückert, M. Jara-Avaca, D. Robles-Diaz, A. Franke, D. A. Elliott, D. Wojciechowski, M. Fischer, A. Roa Lara, G. Kensah, I. Gruh, A. Haverich, U. Martin, and R. Zweigerdt, “Controlling expansion and cardiomyogenic differentiation of human pluripotent stem cells in scalable suspension culture,” Stem Cell Rep. 3(6), 1132–1146 (2014).
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Fuegemann, C. J.

T. Bruegmann, D. Malan, M. Hesse, T. Beiert, C. J. Fuegemann, B. K. Fleischmann, and P. Sasse, “Optogenetic control of heart muscle in vitro and in vivo,” Nat. Methods 7(11), 897–900 (2010).
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Fujioka, H.

M. W. Jenkins, A. R. Duke, S. Gu, H. J. Chiel, H. Fujioka, M. Watanabe, E. D. Jansen, and A. M. Rollins, “Optical pacing of the embryonic heart,” Nat. Photonics 4(9), 623–626 (2010).
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N. I. Smith, K. Fujita, T. Kaneko, K. Katoh, O. Nakamura, S. Kawata, and T. Takamatsu, “Generation of calcium waves in living cells by pulsed-laser-induced photodisruption,” Appl. Phys. Lett. 79(8), 1208 (2001).
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Gamrad, L.

J. Krawinkel, U. Richter, M. L. Torres-Mapa, M. Westermann, L. Gamrad, C. Rehbock, S. Barcikowski, and A. Heisterkamp, “Optical and electron microscopy study of laser-based intracellular molecule delivery using peptide-conjugated photodispersible gold nanoparticle agglomerates,” J. Nanobiotechnology 14(1), 2 (2016).
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Gee, K. R.

K. R. Gee, K. A. Brown, W. N. Chen, J. Bishop-Stewart, D. Gray, and I. Johnson, “Chemical and physiological characterization of fluo-4 Ca(2+)-indicator dyes,” Cell Calcium 27(2), 97–106 (2000).
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C. Robertson, D. D. Tran, and S. C. George, “Concise review: maturation phases of human pluripotent stem cell-derived cardiomyocytes,” Stem Cells 31(5), 829–837 (2013).
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K. Dolnikov, M. Shilkrut, N. Zeevi-Levin, S. Gerecht-Nir, M. Amit, A. Danon, J. Itskovitz-Eldor, and O. Binah, “Functional properties of human embryonic stem cell-derived cardiomyocytes: intracellular Ca2+ handling and the role of sarcoplasmic reticulum in the contraction,” Stem Cells 24(2), 236–245 (2006).
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K. Schwanke, S. Merkert, H. Kempf, S. Hartung, M. Jara-Avaca, C. Templin, G. Göhring, A. Haverich, U. Martin, and R. Zweigerdt, “Fast and efficient multitransgenic modification of human pluripotent stem cells,” Hum. Gene Ther. Methods 25(2), 136–153 (2014).
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Gray, D.

K. R. Gee, K. A. Brown, W. N. Chen, J. Bishop-Stewart, D. Gray, and I. Johnson, “Chemical and physiological characterization of fluo-4 Ca(2+)-indicator dyes,” Cell Calcium 27(2), 97–106 (2000).
[Crossref] [PubMed]

Gruh, I.

H. Kempf, R. Olmer, C. Kropp, M. Rückert, M. Jara-Avaca, D. Robles-Diaz, A. Franke, D. A. Elliott, D. Wojciechowski, M. Fischer, A. Roa Lara, G. Kensah, I. Gruh, A. Haverich, U. Martin, and R. Zweigerdt, “Controlling expansion and cardiomyogenic differentiation of human pluripotent stem cells in scalable suspension culture,” Stem Cell Rep. 3(6), 1132–1146 (2014).
[Crossref] [PubMed]

Gu, S.

M. W. Jenkins, A. R. Duke, S. Gu, H. J. Chiel, H. Fujioka, M. Watanabe, E. D. Jansen, and A. M. Rollins, “Optical pacing of the embryonic heart,” Nat. Photonics 4(9), 623–626 (2010).
[Crossref] [PubMed]

Hafner, J. H.

E. Lukianova-Hleb, Y. Hu, L. Latterini, L. Tarpani, S. Lee, R. A. Drezek, J. H. Hafner, and D. O. Lapotko, “Plasmonic nanobubbles as transient vapor nanobubbles generated around plasmonic nanoparticles,” ACS Nano 4(4), 2109–2123 (2010).
[Crossref] [PubMed]

Han, Q.

D. Luo, D. Yang, X. Lan, K. Li, X. Li, J. Chen, Y. Zhang, R.-P. Xiao, Q. Han, and H. Cheng, “Nuclear Ca2+ sparks and waves mediated by inositol 1,4,5-trisphosphate receptors in neonatal rat cardiomyocytes,” Cell Calcium 43(2), 165–174 (2008).
[Crossref] [PubMed]

Hartung, S.

K. Schwanke, S. Merkert, H. Kempf, S. Hartung, M. Jara-Avaca, C. Templin, G. Göhring, A. Haverich, U. Martin, and R. Zweigerdt, “Fast and efficient multitransgenic modification of human pluripotent stem cells,” Hum. Gene Ther. Methods 25(2), 136–153 (2014).
[Crossref] [PubMed]

Hatef, A.

E. Boulais, R. Lachaine, A. Hatef, and M. Meunier, “Plasmonics for pulsed-laser cell nanosurgery: Fundamentals and applications,” J. Photochem Photobiol. 17, 26–49 (2013).

Haverich, A.

K. Schwanke, S. Merkert, H. Kempf, S. Hartung, M. Jara-Avaca, C. Templin, G. Göhring, A. Haverich, U. Martin, and R. Zweigerdt, “Fast and efficient multitransgenic modification of human pluripotent stem cells,” Hum. Gene Ther. Methods 25(2), 136–153 (2014).
[Crossref] [PubMed]

H. Kempf, R. Olmer, C. Kropp, M. Rückert, M. Jara-Avaca, D. Robles-Diaz, A. Franke, D. A. Elliott, D. Wojciechowski, M. Fischer, A. Roa Lara, G. Kensah, I. Gruh, A. Haverich, U. Martin, and R. Zweigerdt, “Controlling expansion and cardiomyogenic differentiation of human pluripotent stem cells in scalable suspension culture,” Stem Cell Rep. 3(6), 1132–1146 (2014).
[Crossref] [PubMed]

Z. Vukadinovic-Nikolic, B. Andrée, S. E. Dorfman, M. Pflaum, T. Horvath, M. Lux, L. Venturini, A. Bär, G. Kensah, A. R. Lara, I. Tudorache, S. Cebotari, D. Hilfiker-Kleiner, A. Haverich, and A. Hilfiker, “Generation of Bioartificial Heart Tissue by Combining a Three-Dimensional Gel-Based Cardiac Construct with Decellularized Small Intestinal Submucosa,” Tissue Eng. Part A 20(3-4), 799–809 (2013).
[Crossref] [PubMed]

Hegemann, P.

G. Nagel, T. Szellas, W. Huhn, S. Kateriya, N. Adeishvili, P. Berthold, D. Ollig, P. Hegemann, and E. Bamberg, “Channelrhodopsin-2, a directly light-gated cation-selective membrane channel,” Proc. Natl. Acad. Sci. U.S.A. 100(24), 13940–13945 (2003).
[Crossref] [PubMed]

Heinemann, D.

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]

M. Schomaker, D. Killian, S. Willenbrock, D. Heinemann, S. Kalies, A. Ngezahayo, I. Nolte, T. Ripken, C. Junghanß, H. Meyer, H. Murua Escobar, and A. Heisterkamp, “Biophysical effects in off-resonant gold nanoparticle mediated (GNOME) laser transfection of cell lines, primary- and stem cells using fs laser pulses,” J. Biophotonics 8(8), 646–658 (2015).
[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]

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]

Heisterkamp, A.

J. Krawinkel, U. Richter, M. L. Torres-Mapa, M. Westermann, L. Gamrad, C. Rehbock, S. Barcikowski, and A. Heisterkamp, “Optical and electron microscopy study of laser-based intracellular molecule delivery using peptide-conjugated photodispersible gold nanoparticle agglomerates,” J. Nanobiotechnology 14(1), 2 (2016).
[Crossref] [PubMed]

M. Schomaker, D. Killian, S. Willenbrock, D. Heinemann, S. Kalies, A. Ngezahayo, I. Nolte, T. Ripken, C. Junghanß, H. Meyer, H. Murua Escobar, and A. Heisterkamp, “Biophysical effects in off-resonant gold nanoparticle mediated (GNOME) laser transfection of cell lines, primary- and stem cells using fs laser pulses,” J. Biophotonics 8(8), 646–658 (2015).
[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]

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).
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Hesse, M.

T. Bruegmann, D. Malan, M. Hesse, T. Beiert, C. J. Fuegemann, B. K. Fleischmann, and P. Sasse, “Optogenetic control of heart muscle in vitro and in vivo,” Nat. Methods 7(11), 897–900 (2010).
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Hilfiker, A.

Z. Vukadinovic-Nikolic, B. Andrée, S. E. Dorfman, M. Pflaum, T. Horvath, M. Lux, L. Venturini, A. Bär, G. Kensah, A. R. Lara, I. Tudorache, S. Cebotari, D. Hilfiker-Kleiner, A. Haverich, and A. Hilfiker, “Generation of Bioartificial Heart Tissue by Combining a Three-Dimensional Gel-Based Cardiac Construct with Decellularized Small Intestinal Submucosa,” Tissue Eng. Part A 20(3-4), 799–809 (2013).
[Crossref] [PubMed]

Hilfiker-Kleiner, D.

Z. Vukadinovic-Nikolic, B. Andrée, S. E. Dorfman, M. Pflaum, T. Horvath, M. Lux, L. Venturini, A. Bär, G. Kensah, A. R. Lara, I. Tudorache, S. Cebotari, D. Hilfiker-Kleiner, A. Haverich, and A. Hilfiker, “Generation of Bioartificial Heart Tissue by Combining a Three-Dimensional Gel-Based Cardiac Construct with Decellularized Small Intestinal Submucosa,” Tissue Eng. Part A 20(3-4), 799–809 (2013).
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Hitchcock, R. W.

G. M. Dittami, S. M. Rajguru, R. A. Lasher, R. W. Hitchcock, and R. D. Rabbitt, “Intracellular calcium transients evoked by pulsed infrared radiation in neonatal cardiomyocytes,” J. Physiol. 589(6), 1295–1306 (2011).
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Horvath, T.

Z. Vukadinovic-Nikolic, B. Andrée, S. E. Dorfman, M. Pflaum, T. Horvath, M. Lux, L. Venturini, A. Bär, G. Kensah, A. R. Lara, I. Tudorache, S. Cebotari, D. Hilfiker-Kleiner, A. Haverich, and A. Hilfiker, “Generation of Bioartificial Heart Tissue by Combining a Three-Dimensional Gel-Based Cardiac Construct with Decellularized Small Intestinal Submucosa,” Tissue Eng. Part A 20(3-4), 799–809 (2013).
[Crossref] [PubMed]

Hrelescu, C.

C. Hrelescu, J. Stehr, M. Ringler, R. A. Sperling, W. J. Parak, T. A. Klar, and J. Feldmann, “DNA Melting in Gold Nanostove Clusters,” J. Phys. Chem. C 114(16), 7401–7411 (2010).
[Crossref]

Hu, Y.

E. Lukianova-Hleb, Y. Hu, L. Latterini, L. Tarpani, S. Lee, R. A. Drezek, J. H. Hafner, and D. O. Lapotko, “Plasmonic nanobubbles as transient vapor nanobubbles generated around plasmonic nanoparticles,” ACS Nano 4(4), 2109–2123 (2010).
[Crossref] [PubMed]

Huang, X.

X. Huang, P. K. Jain, I. H. El-Sayed, and M. A. El-Sayed, “Plasmonic photothermal therapy (PPTT) using gold nanoparticles,” Lasers Med. Sci. 23(3), 217–228 (2008).
[Crossref] [PubMed]

X. Huang, P. K. Jain, I. H. El-Sayed, and M. A. El-Sayed, “Gold nanoparticles: interesting optical properties and recent applications in cancer diagnostics and therapy,” Nanomedicine (Lond.) 2(5), 681–693 (2007).
[Crossref] [PubMed]

Huhn, W.

G. Nagel, T. Szellas, W. Huhn, S. Kateriya, N. Adeishvili, P. Berthold, D. Ollig, P. Hegemann, and E. Bamberg, “Channelrhodopsin-2, a directly light-gated cation-selective membrane channel,” Proc. Natl. Acad. Sci. U.S.A. 100(24), 13940–13945 (2003).
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Huo, Q.

H. Jans and Q. Huo, “Gold nanoparticle-enabled biological and chemical detection and analysis,” Chem. Soc. Rev. 41(7), 2849–2866 (2012).
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Ishiwata, S.

V. Tseeb, M. Suzuki, K. Oyama, K. Iwai, and S. Ishiwata, “Highly thermosensitive Ca dynamics in a HeLa cell through IP(3) receptors,” HFSP J. 3(2), 117–123 (2009).
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K. Dolnikov, M. Shilkrut, N. Zeevi-Levin, S. Gerecht-Nir, M. Amit, A. Danon, J. Itskovitz-Eldor, and O. Binah, “Functional properties of human embryonic stem cell-derived cardiomyocytes: intracellular Ca2+ handling and the role of sarcoplasmic reticulum in the contraction,” Stem Cells 24(2), 236–245 (2006).
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Iwai, K.

V. Tseeb, M. Suzuki, K. Oyama, K. Iwai, and S. Ishiwata, “Highly thermosensitive Ca dynamics in a HeLa cell through IP(3) receptors,” HFSP J. 3(2), 117–123 (2009).
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Iwanaga, S.

N. I. Smith, Y. Kumamoto, S. Iwanaga, J. Ando, K. Fujita, and S. Kawata, “A femtosecond laser pacemaker for heart muscle cells,” Opt. Express 16(12), 8604–8616 (2008).
[Crossref] [PubMed]

N. I. Smith, S. Iwanaga, T. Beppu, K. Fujita, O. Nakamura, and S. Kawata, “Photostimulation of two types of Ca 2+ waves in rat pheochromocytoma PC12 cells by ultrashort pulsed near-infrared laser irradiation,” Laser Phys. Lett. 3(3), 154–161 (2006).
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Izzo, N. J.

W. C. Claycomb, N. A. Lanson, B. S. Stallworth, D. B. Egeland, J. B. Delcarpio, A. Bahinski, and N. J. Izzo., “HL-1 cells: a cardiac muscle cell line that contracts and retains phenotypic characteristics of the adult cardiomyocyte,” Proc. Natl. Acad. Sci. U.S.A. 95(6), 2979–2984 (1998).
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Jain, P. K.

X. Huang, P. K. Jain, I. H. El-Sayed, and M. A. El-Sayed, “Plasmonic photothermal therapy (PPTT) using gold nanoparticles,” Lasers Med. Sci. 23(3), 217–228 (2008).
[Crossref] [PubMed]

X. Huang, P. K. Jain, I. H. El-Sayed, and M. A. El-Sayed, “Gold nanoparticles: interesting optical properties and recent applications in cancer diagnostics and therapy,” Nanomedicine (Lond.) 2(5), 681–693 (2007).
[Crossref] [PubMed]

Jans, H.

H. Jans and Q. Huo, “Gold nanoparticle-enabled biological and chemical detection and analysis,” Chem. Soc. Rev. 41(7), 2849–2866 (2012).
[Crossref] [PubMed]

Jansen, E. D.

M. W. Jenkins, A. R. Duke, S. Gu, H. J. Chiel, H. Fujioka, M. Watanabe, E. D. Jansen, and A. M. Rollins, “Optical pacing of the embryonic heart,” Nat. Photonics 4(9), 623–626 (2010).
[Crossref] [PubMed]

Jara-Avaca, M.

H. Kempf, R. Olmer, C. Kropp, M. Rückert, M. Jara-Avaca, D. Robles-Diaz, A. Franke, D. A. Elliott, D. Wojciechowski, M. Fischer, A. Roa Lara, G. Kensah, I. Gruh, A. Haverich, U. Martin, and R. Zweigerdt, “Controlling expansion and cardiomyogenic differentiation of human pluripotent stem cells in scalable suspension culture,” Stem Cell Rep. 3(6), 1132–1146 (2014).
[Crossref] [PubMed]

K. Schwanke, S. Merkert, H. Kempf, S. Hartung, M. Jara-Avaca, C. Templin, G. Göhring, A. Haverich, U. Martin, and R. Zweigerdt, “Fast and efficient multitransgenic modification of human pluripotent stem cells,” Hum. Gene Ther. Methods 25(2), 136–153 (2014).
[Crossref] [PubMed]

Jenkins, M. W.

M. W. Jenkins, A. R. Duke, S. Gu, H. J. Chiel, H. Fujioka, M. Watanabe, E. D. Jansen, and A. M. Rollins, “Optical pacing of the embryonic heart,” Nat. Photonics 4(9), 623–626 (2010).
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Jia, Z.

Z. Jia, V. Valiunas, Z. Lu, H. Bien, H. Liu, H. Z. Wang, B. Rosati, P. R. Brink, I. S. Cohen, and E. Entcheva, “Stimulating cardiac muscle by light: cardiac optogenetics by cell delivery,” Circ Arrhythm Electrophysiol 4(5), 753–760 (2011).
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Johnson, I.

K. R. Gee, K. A. Brown, W. N. Chen, J. Bishop-Stewart, D. Gray, and I. Johnson, “Chemical and physiological characterization of fluo-4 Ca(2+)-indicator dyes,” Cell Calcium 27(2), 97–106 (2000).
[Crossref] [PubMed]

Junghanß, C.

M. Schomaker, D. Killian, S. Willenbrock, D. Heinemann, S. Kalies, A. Ngezahayo, I. Nolte, T. Ripken, C. Junghanß, H. Meyer, H. Murua Escobar, and A. Heisterkamp, “Biophysical effects in off-resonant gold nanoparticle mediated (GNOME) laser transfection of cell lines, primary- and stem cells using fs laser pulses,” J. Biophotonics 8(8), 646–658 (2015).
[Crossref] [PubMed]

Kalies, S.

M. Schomaker, D. Killian, S. Willenbrock, D. Heinemann, S. Kalies, A. Ngezahayo, I. Nolte, T. Ripken, C. Junghanß, H. Meyer, H. Murua Escobar, and A. Heisterkamp, “Biophysical effects in off-resonant gold nanoparticle mediated (GNOME) laser transfection of cell lines, primary- and stem cells using fs laser pulses,” J. Biophotonics 8(8), 646–658 (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, 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]

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]

Kaneko, T.

N. I. Smith, K. Fujita, T. Kaneko, K. Katoh, O. Nakamura, S. Kawata, and T. Takamatsu, “Generation of calcium waves in living cells by pulsed-laser-induced photodisruption,” Appl. Phys. Lett. 79(8), 1208 (2001).
[Crossref]

Kateriya, S.

G. Nagel, T. Szellas, W. Huhn, S. Kateriya, N. Adeishvili, P. Berthold, D. Ollig, P. Hegemann, and E. Bamberg, “Channelrhodopsin-2, a directly light-gated cation-selective membrane channel,” Proc. Natl. Acad. Sci. U.S.A. 100(24), 13940–13945 (2003).
[Crossref] [PubMed]

Katoh, K.

N. I. Smith, K. Fujita, T. Kaneko, K. Katoh, O. Nakamura, S. Kawata, and T. Takamatsu, “Generation of calcium waves in living cells by pulsed-laser-induced photodisruption,” Appl. Phys. Lett. 79(8), 1208 (2001).
[Crossref]

Kawata, S.

N. I. Smith, Y. Kumamoto, S. Iwanaga, J. Ando, K. Fujita, and S. Kawata, “A femtosecond laser pacemaker for heart muscle cells,” Opt. Express 16(12), 8604–8616 (2008).
[Crossref] [PubMed]

N. I. Smith, S. Iwanaga, T. Beppu, K. Fujita, O. Nakamura, and S. Kawata, “Photostimulation of two types of Ca 2+ waves in rat pheochromocytoma PC12 cells by ultrashort pulsed near-infrared laser irradiation,” Laser Phys. Lett. 3(3), 154–161 (2006).
[Crossref]

N. I. Smith, K. Fujita, T. Kaneko, K. Katoh, O. Nakamura, S. Kawata, and T. Takamatsu, “Generation of calcium waves in living cells by pulsed-laser-induced photodisruption,” Appl. Phys. Lett. 79(8), 1208 (2001).
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Kempf, H.

H. Kempf, B. Andree, and R. Zweigerdt, “Large-scale production of human pluripotent stem cell derived cardiomyocytes,” Adv. Drug Deliv. Rev. 96, 18–30 (2016).
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H. Kempf, C. Kropp, R. Olmer, U. Martin, and R. Zweigerdt, “Cardiac differentiation of human pluripotent stem cells in scalable suspension culture,” Nat. Protoc. 10(9), 1345–1361 (2015).
[Crossref] [PubMed]

K. Schwanke, S. Merkert, H. Kempf, S. Hartung, M. Jara-Avaca, C. Templin, G. Göhring, A. Haverich, U. Martin, and R. Zweigerdt, “Fast and efficient multitransgenic modification of human pluripotent stem cells,” Hum. Gene Ther. Methods 25(2), 136–153 (2014).
[Crossref] [PubMed]

H. Kempf, R. Olmer, C. Kropp, M. Rückert, M. Jara-Avaca, D. Robles-Diaz, A. Franke, D. A. Elliott, D. Wojciechowski, M. Fischer, A. Roa Lara, G. Kensah, I. Gruh, A. Haverich, U. Martin, and R. Zweigerdt, “Controlling expansion and cardiomyogenic differentiation of human pluripotent stem cells in scalable suspension culture,” Stem Cell Rep. 3(6), 1132–1146 (2014).
[Crossref] [PubMed]

Kensah, G.

H. Kempf, R. Olmer, C. Kropp, M. Rückert, M. Jara-Avaca, D. Robles-Diaz, A. Franke, D. A. Elliott, D. Wojciechowski, M. Fischer, A. Roa Lara, G. Kensah, I. Gruh, A. Haverich, U. Martin, and R. Zweigerdt, “Controlling expansion and cardiomyogenic differentiation of human pluripotent stem cells in scalable suspension culture,” Stem Cell Rep. 3(6), 1132–1146 (2014).
[Crossref] [PubMed]

Z. Vukadinovic-Nikolic, B. Andrée, S. E. Dorfman, M. Pflaum, T. Horvath, M. Lux, L. Venturini, A. Bär, G. Kensah, A. R. Lara, I. Tudorache, S. Cebotari, D. Hilfiker-Kleiner, A. Haverich, and A. Hilfiker, “Generation of Bioartificial Heart Tissue by Combining a Three-Dimensional Gel-Based Cardiac Construct with Decellularized Small Intestinal Submucosa,” Tissue Eng. Part A 20(3-4), 799–809 (2013).
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Kent, S. B. H.

J. L. Carvalho-de-Souza, J. S. Treger, B. Dang, S. B. H. Kent, D. R. Pepperberg, and F. Bezanilla, “Photosensitivity of neurons enabled by cell-targeted gold nanoparticles,” Neuron 86(1), 207–217 (2015).
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Khlebtsov, N.

N. Khlebtsov and L. Dykman, “Biodistribution and toxicity of engineered gold nanoparticles: a review of in vitro and in vivo studies,” Chem. Soc. Rev. 40(3), 1647–1671 (2011).
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Killian, D.

M. Schomaker, D. Killian, S. Willenbrock, D. Heinemann, S. Kalies, A. Ngezahayo, I. Nolte, T. Ripken, C. Junghanß, H. Meyer, H. Murua Escobar, and A. Heisterkamp, “Biophysical effects in off-resonant gold nanoparticle mediated (GNOME) laser transfection of cell lines, primary- and stem cells using fs laser pulses,” J. Biophotonics 8(8), 646–658 (2015).
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Kim, D. H.

J.-C. Kim, M.-J. Son, K. P. Subedi, D. H. Kim, and S.-H. Woo, “IP3-induced cytosolic and nuclear Ca2+ signals in HL-1 atrial myocytes: possible role of IP3 receptor subtypes,” Mol. Cells 29(4), 387–395 (2010).
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Kim, J.-C.

J.-C. Kim, M.-J. Son, K. P. Subedi, Y. Li, J. R. Ahn, and S.-H. Woo, “Atrial local Ca2+ signaling and inositol 1,4,5-trisphosphate receptors,” Prog. Biophys. Mol. Biol. 103(1), 59–70 (2010).
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J.-C. Kim, M.-J. Son, K. P. Subedi, D. H. Kim, and S.-H. Woo, “IP3-induced cytosolic and nuclear Ca2+ signals in HL-1 atrial myocytes: possible role of IP3 receptor subtypes,” Mol. Cells 29(4), 387–395 (2010).
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Klar, T. A.

C. Hrelescu, J. Stehr, M. Ringler, R. A. Sperling, W. J. Parak, T. A. Klar, and J. Feldmann, “DNA Melting in Gold Nanostove Clusters,” J. Phys. Chem. C 114(16), 7401–7411 (2010).
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Klimas, A.

A. Klimas and E. Entcheva, “Toward microendoscopy-inspired cardiac optogenetics in vivo: technical overview and perspective,” J. Biomed. Opt. 19(8), 080701 (2014).
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P. Kohl, “Heterogeneous cell coupling in the heart: an electrophysiological role for fibroblasts,” Circ. Res. 93(5), 381–383 (2003).
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Krawinkel, J.

J. Krawinkel, U. Richter, M. L. Torres-Mapa, M. Westermann, L. Gamrad, C. Rehbock, S. Barcikowski, and A. Heisterkamp, “Optical and electron microscopy study of laser-based intracellular molecule delivery using peptide-conjugated photodispersible gold nanoparticle agglomerates,” J. Nanobiotechnology 14(1), 2 (2016).
[Crossref] [PubMed]

Kropp, C.

H. Kempf, C. Kropp, R. Olmer, U. Martin, and R. Zweigerdt, “Cardiac differentiation of human pluripotent stem cells in scalable suspension culture,” Nat. Protoc. 10(9), 1345–1361 (2015).
[Crossref] [PubMed]

H. Kempf, R. Olmer, C. Kropp, M. Rückert, M. Jara-Avaca, D. Robles-Diaz, A. Franke, D. A. Elliott, D. Wojciechowski, M. Fischer, A. Roa Lara, G. Kensah, I. Gruh, A. Haverich, U. Martin, and R. Zweigerdt, “Controlling expansion and cardiomyogenic differentiation of human pluripotent stem cells in scalable suspension culture,” Stem Cell Rep. 3(6), 1132–1146 (2014).
[Crossref] [PubMed]

Kumamoto, Y.

Lachaine, R.

E. Boulais, R. Lachaine, A. Hatef, and M. Meunier, “Plasmonics for pulsed-laser cell nanosurgery: Fundamentals and applications,” J. Photochem Photobiol. 17, 26–49 (2013).

Laine, M.

P. Lipp, M. Laine, S. C. Tovey, K. M. Burrell, M. J. Berridge, W. Li, and M. D. Bootman, “Functional InsP3 receptors that may modulate excitation-contraction coupling in the heart,” Curr. Biol. 10(15), 939–942 (2000).
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D. Luo, D. Yang, X. Lan, K. Li, X. Li, J. Chen, Y. Zhang, R.-P. Xiao, Q. Han, and H. Cheng, “Nuclear Ca2+ sparks and waves mediated by inositol 1,4,5-trisphosphate receptors in neonatal rat cardiomyocytes,” Cell Calcium 43(2), 165–174 (2008).
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Supplementary Material (6)

NameDescription
» Visualization 1: MP4 (7456 KB)      . Exemplary video of laser induced calcium responses of HL-1 cells in HBSS+Ca2+. Scale bar 50 µm.
» Visualization 2: MP4 (13972 KB)      Exemplary video of the contractile behavior of a single neonatal rat cardiomyocyte in HBSS+Ca2+ pre and post laser stimulation. Scale bar 50 µm.
» Visualization 3: MP4 (13963 KB)      Exemplary video of the contractile behavior of a single neonatal rat cardiomyocyte in HBSS+hCa2+ pre and post laser stimulation. Scale bar 50 µm.
» Visualization 4: MP4 (14526 KB)      : Exemplary video of calcium signaling in hESC-derived cardiomyocytes in HBSS+Ca2+ pre and post laser stimulation. Scale bar 50 µm.
» Visualization 5: MP4 (14667 KB)      Exemplary video of calcium signaling in hESC-derived cardiomyocytes in HBSS+Ca2+ pre and post laser stimulation over a long spatial distance. Scale bar 200 µm.
» Visualization 6: MP4 (14000 KB)      . Exemplary video of contractile behavior of a set of hESC-derived cardiomyocytes in HBSS+hCa2+ pre and post laser stimulation. Scale bar 50 µm.

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Figures (8)

Fig. 1
Fig. 1 Calcium responses of HL-1 cells in HBSS + Ca2+ after laser stimulation with different radiant exposures and irradiation times for the three considered regions. (a): Distribution of cells within the laser spot (red selection), at the periphery of the laser spot (orange selection) and outside of the laser spot (yellow selection) with the laser spot being marked green. Scale bar: 40 µm. (b): Relative frequency of occurrence of the three different calcium responses shown in HL-1 cells in HBSS + Ca2+ buffer after laser stimulation of cells within the laser spot (top), at the periphery of the laser spot (middle) and outside of the laser spot (bottom). Accumulated over all three areas, calcium oscillations occurred most frequently with a radiant exposure of 15 mJ/cm2 and 20 ms irradiation time. Data represents the mean + SEM of at least n = 10 irradiated cells.
Fig. 2
Fig. 2 Laser induced calcium responses of HL-1 cells in HBSS + Ca2+ after laser stimulation. An orthogonal projection (time plotted along the green lines) of Visualization 1 shows different effects of the laser stimulation on calcium signaling with a radiant exposure of 27 mJ/cm2 in HL-1 cells (a). In both projections, a calcium shock can be observed over time for the cell, which is in the laser treated area after laser application. Calcium oscillations are visible at the periphery or outside of the laser spot. Scale bar 50 µm. Panels b) and c) show the quantified response of a single representative cell. Laser irradiation occurred at 0 s (arrow pointing to asterisk) with the laser spot being located within the marked area. Cells within the laser spot mostly responded with a calcium shock, while cells not directly irradiated often exhibited calcium oscillations after laser treatment. Please refer to Visualization 1 for a time series of subfigures a) to c).
Fig. 3
Fig. 3 Calcium responses of HL-1 cells in Ca2+ containing and Ca2+ free buffer after laser stimulation. Relative frequency of occurrence of the three different calcium responses in HL-1 cells in HBSS + Ca2+ and HBSS-Ca2 after laser stimulation of cells within the laser spot (a), at the periphery of the laser spot (b) and outside of the laser spot (c) for an irradiation time of 20 ms and radiant exposures of 15 mJ/cm2 and 27 mJ/cm2. Data represents the mean + SEM of at least n = 10 irradiated cells.
Fig. 4
Fig. 4 Contractions of neonatal rat cardiomyocytes pre and post laser stimulation with a radiant exposure of 8 mJ/cm2 and an irradiation time of 10 ms. While the laser stimulation did not affect the contractile behavior of the examined cardiomyocyte in HBSS-Ca2+ (a), it induced significant increases of the contraction frequency in cardiomyocytes in HBSS + Ca2+ (b) (referring to Visualization 2). Cardiomyocytes in HBSS + hCa2+ exhibited higher contraction frequencies after laser treatment as well (c) (referring to Visualization 3). Laser irradiation occurred every 15.6 s (red arrows), every peak represents one contraction of the examined cardiomyocyte. Data shown represents the exemplary contractile behavior of one single out of at least n = 7 examined cells or set of cells in HBSS-Ca2+, HBSS + Ca2+ and HBSS + hCa2+, respectively. Narrow peaks are laser light detected by the camera if it was coincident with the frame acquisition.
Fig. 5
Fig. 5 Cell viability of hESC-derived cardiomyocytes in HBSS-Ca2+, HBSS + Ca2+ and HBSS + hCa2+, respectively, one hour after multiple laser irradiations with a radiant exposure of 15 mJ/cm2 and an irradiation time of 10 ms. In all three buffers, cell viability is >80%. Data presents the mean + SEM of at least n = 20 irradiated cells.
Fig. 6
Fig. 6 Calcium signaling in hESC-derived cardiomyocytes in HBSS + Ca2+ pre and post laser stimulation with a radiant exposure of 15 mJ/cm2 and an irradiation time of 10 ms. An orthogonal projection of Visualization 4 indicates the effects of laser stimulation on calcium signaling in hESC-derived cardiomyocytes (a). Scale bar 50 µm. Laser irradiation occurred at 0 s with the laser spot being located within the marked area. The relative fluorescence intensity of cardiomyocytes located outside of the laser spot (marked by arrows) shows the occurrence of a calcium oscillation immediately after laser treatment (arrow and asterisk) (b). Considering a larger field of view using the 10x objective, all hESC-derived cardiomyocytes outside of the laser spot exhibited an additional, simultaneously occurring calcium oscillation immediately after laser treatment (c). Graph (c) refers to Visualization 5. Data shown refers to a single irradiated hESC-derived cardiomyocyte for all graphs out of n = 15 (63x objective) and n = 10 (10x objective) irradiated cells.
Fig. 7
Fig. 7 Contractions of hESC-derived cardiomyocytes pre and post laser stimulation with a radiant exposure of 15 mJ/cm2 and an irradiation time of 10 ms. The laser treatment stopped contractions of the examined cardiomyocyte in HBSS-Ca2+ (a) and did not affect the contractile behavior of hESC-derived cardiomyocytes in HBSS + Ca2+ (b). In hESC-derived cardiomyocytes in HBSS + hCa2+, some contractions occurred immediately after laser stimulation (c) (referring to Visualization 6). Laser irradiation occurred every 7.8 s (red arrows), every peak represents one contraction of the examined cardiomyocyte. Data shown represents the exemplary contractile behavior of one examined cell in HBSS-Ca2+, HBSS + Ca2+ and HBSS + hCa2+, respectively. Narrow peaks are laser light detected by the camera if it was coincident with the frame acquisition.
Fig. 8
Fig. 8 Effects of laser irradiation on HL-1 cells, neonatal rat cardiomyocytes and hESC-derived cardiomyocytes not treated with gold nanoparticles. (a): Relative frequency of occurrence of the three different calcium responses shown in nanoparticle free HL-1 cells in HBSS + Ca2+ after laser stimulation with different radiant exposures and irradiation times. While the calcium level of most cells did not change after irradiation, single calcium spikes, which can occur spontaneously in HL-1 cells, were observed in a small number of cells. No steady intercellular calcium oscillations were observed. Data represents the mean + SEM of at least n = 8 irradiated cells. (b): Contractions of a nanoparticle free neonatal rat cardiomyocyte in HBSS + Ca2+ pre and post laser treatment with a radiant exposure of 8 mJ/cm2 and an irradiation time of 10 ms. Laser irradiation occurred every 15.6 s (red arrows), every peak represents one contraction of the examined cardiomyocyte. No effects of laser irradiation on the cells’ contractile behavior were observed. Data shown represents the exemplary contractile behavior of one single out of n = 10 examined cells or set of cells. (c): Calcium signaling in nanoparticle free hESC-derived cardiomyocytes in HBSS + Ca2+ pre and post laser stimulation with a radiant exposure of 15 mJ/cm2 and an irradiation time of 10 ms. The laser irradiation (arrow and asterisk) did not affect the frequency of calcium oscillations or the overall calcium level represented by the relative fluorescence intensity. Data shown represents the calcium signaling of one single out of n = 8 irradiated cells. (d): Contractions of a nanoparticle free hESC-derived cardiomyocyte in HBSS + hCa2+ pre and post laser treatment with a radiant exposure of 15 mJ/cm2 and an irradiation time of 10 ms. Laser irradiation occurred every 7.8 s (red arrows), every peak represents one contraction of the examined cardiomyocyte. No effects of laser irradiation on the cells’ contractile behavior were observed. Data shown represents the exemplary contractile behavior of one single out of n = 10 examined cells or set of cells. Narrow peaks in (b), (c) and (d) are laser light detected by the camera if it was coincident with the frame acquisition.

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