Abstract

Low-power laser irradiation of red light has been recognized as a promising tool across a vast variety of biomedical applications. However, deep understanding of the molecular mechanisms behind laser-induced cellular effects remains a significant challenge. Here, we investigated mechanisms involved in the death process in human hepatic cell line Huh7 at a laser irradiation. We decoupled distinct cell death pathways targeted by laser irradiations of different powers. Our data demonstrate that high dose laser irradiation exhibited the highest levels of total reactive oxygen species production, leading to cyclophilin D-related necrosis via the mitochondrial permeability transition. On the contrary, low dose laser irradiation resulted in the nuclear accumulation of superoxide and apoptosis execution. Our findings offer a novel insight into laser-induced cellular responses, and reveal distinct cell death pathways triggered by laser irradiation. The observed link between mitochondria depolarization and triggering ROS could be a fundamental phenomenon in laser-induced cellular responses.

© 2018 Optical Society of America under the terms of the OSA Open Access Publishing Agreement

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2017 (7)

O. Lunov, V. Zablotskii, O. Churpita, M. Lunova, M. Jirsa, A. Dejneka, and Š. Kubinová, “Chemically different non-thermal plasmas target distinct cell death pathways,” Sci. Rep. 7(1), 600 (2017).
[Crossref] [PubMed]

M. Lunova, A. Prokhorov, M. Jirsa, M. Hof, A. Olżyńska, P. Jurkiewicz, Š. Kubinová, O. Lunov, and A. Dejneka, “Nanoparticle core stability and surface functionalization drive the mtor signaling pathway in hepatocellular cell lines,” Sci. Rep. 7(1), 16049 (2017).
[Crossref] [PubMed]

S. B. Goncalves, J. F. Ribeiro, A. F. Silva, R. M. Costa, and J. H. Correia, “Design and manufacturing challenges of optogenetic neural interfaces: A review,” J. Neural Eng. 14(4), 041001 (2017).
[Crossref] [PubMed]

H. Vakifahmetoglu-Norberg, A. T. Ouchida, and E. Norberg, “The role of mitochondria in metabolism and cell death,” Biochem. Biophys. Res. Commun. 482(3), 426–431 (2017).
[Crossref] [PubMed]

Y. Wang, H. He, S. Wang, Y. Liu, M. Hu, Y. Cao, S. Kong, X. Wei, and C. Wang, “Photostimulation by femtosecond laser triggers restorable fragmentation in single mitochondrion,” J. Biophotonics 10(2), 286–293 (2017).
[Crossref] [PubMed]

Y. Zhu and H. He, “Molecular response of mitochondria to a short-duration femtosecond-laser stimulation,” Biomed. Opt. Express 8(11), 4965–4973 (2017).
[Crossref] [PubMed]

J. Moon, J. Yun, Y. D. Yoon, S. I. Park, Y. J. Seo, W. S. Park, H. Y. Chu, K. H. Park, M. Y. Lee, C. W. Lee, S. J. Oh, Y. S. Kwak, Y. P. Jang, and J. S. Kang, “Blue light effect on retinal pigment epithelial cells by display devices,” Integr. Biol. 9(5), 436–443 (2017).
[Crossref] [PubMed]

2016 (3)

W. P. Roos, A. D. Thomas, and B. Kaina, “DNA damage and the balance between survival and death in cancer biology,” Nat. Rev. Cancer 16(1), 20–33 (2016).
[Crossref] [PubMed]

O. Lunov, V. Zablotskii, O. Churpita, A. Jäger, L. Polívka, E. Syková, A. Dejneka, and Š. Kubinová, “The interplay between biological and physical scenarios of bacterial death induced by non-thermal plasma,” Biomaterials 82, 71–83 (2016).
[Crossref] [PubMed]

D. Yang, W. Yi, E. Wang, and M. Wang, “Effects of light-emitting diode irradiation on the osteogenesis of human umbilical cord mesenchymal stem cells in vitro,” Sci. Rep. 6(1), 37370 (2016).
[Crossref] [PubMed]

2015 (5)

I. Khan, E. Tang, and P. Arany, “Molecular pathway of near-infrared laser phototoxicity involves atf-4 orchestrated er stress,” Sci. Rep. 5(1), 10581 (2015).
[Crossref] [PubMed]

Z. Huang, J. Ma, J. Chen, B. Shen, F. Pei, and V. B. Kraus, “The effectiveness of low-level laser therapy for nonspecific chronic low back pain: A systematic review and meta-analysis,” Arthritis Res. Ther. 17(1), 360 (2015).
[Crossref] [PubMed]

O. Lunov, V. Zablotskii, O. Churpita, E. Chánová, E. Syková, A. Dejneka, and S. Kubinová, “Cell death induced by ozone and various non-thermal plasmas: Therapeutic perspectives and limitations,” Sci. Rep. 4(1), 7129 (2015).
[Crossref] [PubMed]

T. Vanden Berghe, W. J. Kaiser, M. J. M. Bertrand, and P. Vandenabeele, “Molecular crosstalk between apoptosis, necroptosis, and survival signaling,” Mol. Cell. Oncol. 2(4), e975093 (2015).
[Crossref] [PubMed]

T. A. Henderson and L. D. Morries, “Near-infrared photonic energy penetration: Can infrared phototherapy effectively reach the human brain?” Neuropsychiatr. Dis. Treat. 11, 2191–2208 (2015).
[Crossref] [PubMed]

2014 (5)

A. Linkermann and D. R. Green, “Necroptosis,” N. Engl. J. Med. 370(5), 455–465 (2014).
[Crossref] [PubMed]

G. Mariño, M. Niso-Santano, E. H. Baehrecke, and G. Kroemer, “Self-consumption: The interplay of autophagy and apoptosis,” Nat. Rev. Mol. Cell Biol. 15(2), 81–94 (2014).
[Crossref] [PubMed]

G. Mariño, M. Niso-Santano, E. H. Baehrecke, and G. Kroemer, “Self-consumption: The interplay of autophagy and apoptosis,” Nat. Rev. Mol. Cell Biol. 15(2), 81–94 (2014).
[Crossref] [PubMed]

P. R. Arany, A. Cho, T. D. Hunt, G. Sidhu, K. Shin, E. Hahm, G. X. Huang, J. Weaver, A. C. Chen, B. L. Padwa, M. R. Hamblin, M. H. Barcellos-Hoff, A. B. Kulkarni, and D. J Mooney, “Photoactivation of endogenous latent transforming growth factor-β1 directs dental stem cell differentiation for regeneration,” Sci. Transl. Med. 6(238), 238ra69 (2014).
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N. Kaludercic, S. Deshwal, and F. Di Lisa, “Reactive oxygen species and redox compartmentalization,” Front. Physiol. 5, 285 (2014).
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2013 (7)

W. K. Ong, H. F. Chen, C. T. Tsai, Y. J. Fu, Y. S. Wong, D. J. Yen, T. H. Chang, H. D. Huang, O. K. Lee, S. Chien, and J. H. Ho, “The activation of directional stem cell motility by green light-emitting diode irradiation,” Biomaterials 34(8), 1911–1920 (2013).
[Crossref] [PubMed]

R. R. Anderson, “Lasers for dermatology and skin biology,” J. Invest. Dermatol. 133(E1), E21–E23 (2013).
[Crossref] [PubMed]

N. Shirasu, S. O. Nam, and M. Kuroki, “Tumor-targeted photodynamic therapy,” Anticancer Res. 33(7), 2823–2831 (2013).
[PubMed]

V. Nikoletopoulou, M. Markaki, K. Palikaras, and N. Tavernarakis, “Crosstalk between apoptosis, necrosis and autophagy,” Biochim. Biophys. Acta 1833(12), 3448–3459 (2013).
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E. Panieri, V. Gogvadze, E. Norberg, R. Venkatesh, S. Orrenius, and B. Zhivotovsky, “Reactive oxygen species generated in different compartments induce cell death, survival, or senescence,” Free Radic. Biol. Med. 57, 176–187 (2013).
[Crossref] [PubMed]

J. Shen, C. Chui, and X. Tao, “Luminous fabric devices for wearable low-level light therapy,” Biomed. Opt. Express 4(12), 2925–2937 (2013).
[Crossref] [PubMed]

R. Matthes, C. Bender, R. Schlüter, I. Koban, R. Bussiahn, S. Reuter, J. Lademann, K. D. Weltmann, and A. Kramer, “Antimicrobial efficacy of two surface barrier discharges with air plasma against in vitro biofilms,” PLoS One 8(7), e70462 (2013).
[Crossref] [PubMed]

2012 (2)

M. Di Carlo, D. Giacomazza, P. Picone, D. Nuzzo, and P. L. San Biagio, “Are oxidative stress and mitochondrial dysfunction the key players in the neurodegenerative diseases?” Free Radic. Res. 46(11), 1327–1338 (2012).
[Crossref] [PubMed]

H. Chung, T. Dai, S. K. Sharma, Y. Y. Huang, J. D. Carroll, and M. R. Hamblin, “The nuts and bolts of low-level laser (light) therapy,” Ann. Biomed. Eng. 40(2), 516–533 (2012).
[Crossref] [PubMed]

2011 (6)

A. C. Chen, P. R. Arany, Y. Y. Huang, E. M. Tomkinson, S. K. Sharma, G. B. Kharkwal, T. Saleem, D. Mooney, F. E. Yull, T. S. Blackwell, and M. R. Hamblin, “Low-level laser therapy activates nf-kb via generation of reactive oxygen species in mouse embryonic fibroblasts,” PLoS One 6(7), e22453 (2011).
[Crossref] [PubMed]

Y. Y. Huang, S. K. Sharma, J. Carroll, and M. R. Hamblin, “Biphasic dose response in low level light therapy - an update,” Dose Response 9(4), 602–618 (2011).
[Crossref] [PubMed]

P. S. Yarmolenko, E. J. Moon, C. Landon, A. Manzoor, D. W. Hochman, B. L. Viglianti, and M. W. Dewhirst, “Thresholds for thermal damage to normal tissues: An update,” Int. J. Hyperthermia 27(4), 320–343 (2011).
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O. Yizhar, L. E. Fenno, T. J. Davidson, M. Mogri, and K. Deisseroth, “Optogenetics in neural systems,” Neuron 71(1), 9–34 (2011).
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S. Wu, F. Zhou, Z. Zhang, and D. Xing, “Mitochondrial oxidative stress causes mitochondrial fragmentation via differential modulation of mitochondrial fission-fusion proteins,” FEBS J. 278(6), 941–954 (2011).
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K. W. Kinnally, P. M. Peixoto, S. Y. Ryu, and L. M. Dejean, “Is mptp the gatekeeper for necrosis, apoptosis, or both?” Biochim. Biophys. Acta 1813(4), 616–622 (2011).
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2010 (4)

S. W. Tait and D. R. Green, “Mitochondria and cell death: Outer membrane permeabilization and beyond,” Nat. Rev. Mol. Cell Biol. 11(9), 621–632 (2010).
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H. A. Woo, S. H. Yim, D. H. Shin, D. Kang, D. Y. Yu, and S. G. Rhee, “Inactivation of peroxiredoxin i by phosphorylation allows localized h2o2 accumulation for cell signaling,” Cell 140(4), 517–528 (2010).
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O. Gavet and J. Pines, “Progressive activation of cyclinb1-cdk1 coordinates entry to mitosis,” Dev. Cell 18(4), 533–543 (2010).
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S. Y. Ryu, P. M. Peixoto, O. Teijido, L. M. Dejean, and K. W. Kinnally, “Role of mitochondrial ion channels in cell death,” Biofactors 36(4), 255–263 (2010).
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2009 (5)

S. Wu, D. Xing, X. Gao, and W. R. Chen, “High fluence low-power laser irradiation induces mitochondrial permeability transition mediated by reactive oxygen species,” J. Cell. Physiol. 218(3), 603–611 (2009).
[Crossref] [PubMed]

H. K. Soong and J. B. Malta, “Femtosecond lasers in ophthalmology,” Am. J. Ophthalmol. 147(2), 189–197 (2009).
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R. T. Chow, M. I. Johnson, R. A. Lopes-Martins, and J. M. Bjordal, “Efficacy of low-level laser therapy in the management of neck pain: A systematic review and meta-analysis of randomised placebo or active-treatment controlled trials,” Lancet 374(9705), 1897–1908 (2009).
[Crossref] [PubMed]

Y. Y. Huang, A. C. Chen, J. D. Carroll, and M. R. Hamblin, “Biphasic dose response in low level light therapy,” Dose Response 7(4), 358–383 (2009).
[Crossref] [PubMed]

M. P. Murphy, “How mitochondria produce reactive oxygen species,” Biochem. J. 417(1), 1–13 (2009).
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2008 (3)

C. C. Winterbourn, “Reconciling the chemistry and biology of reactive oxygen species,” Nat. Chem. Biol. 4(5), 278–286 (2008).
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R. Yousefi-Nooraie, E. Schonstein, K. Heidari, A. Rashidian, V. Pennick, M. Akbari-Kamrani, S. Irani, B. Shakiba, S. A. Mortaz Hejri, S. O. Mortaz Hejri, and A. Jonaidi, “Low level laser therapy for nonspecific low-back pain,” Cochrane Database Syst. Rev. 2, CD005107 (2008).
[PubMed]

T. I. Karu, L. V. Pyatibrat, S. F. Kolyakov, and N. I. Afanasyeva, “Absorption measurements of cell monolayers relevant to mechanisms of laser phototherapy: Reduction or oxidation of cytochrome c oxidase under laser radiation at 632.8 nm,” Photomed. Laser Surg. 26(6), 593–599 (2008).
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2007 (2)

R. S. Stern, “Psoralen and ultraviolet a light therapy for psoriasis,” N. Engl. J. Med. 357(7), 682–690 (2007).
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S. Wu, D. Xing, F. Wang, T. Chen, and W. R. Chen, “Mechanistic study of apoptosis induced by high-fluence low-power laser irradiation using fluorescence imaging techniques,” J. Biomed. Opt. 12(6), 064015 (2007).
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2006 (2)

M. L. Denton, M. S. Foltz, L. E. Estlack, D. J. Stolarski, G. D. Noojin, R. J. Thomas, D. Eikum, and B. A. Rockwell, “Damage thresholds for exposure to nir and blue lasers in an in vitro rpe cell system,” Invest. Ophthalmol. Vis. Sci. 47(7), 3065–3073 (2006).
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M. T. Lin and M. F. Beal, “Mitochondrial dysfunction and oxidative stress in neurodegenerative diseases,” Nature 443(7113), 787–795 (2006).
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2005 (4)

J. F. Pittet, H. Lee, M. Pespeni, A. O’Mahony, J. Roux, and W. J. Welch, “Stress-induced inhibition of the NF-kappaB signaling pathway results from the insolubilization of the ikappab kinase complex following its dissociation from heat shock protein 90,” J. Immunol. 174(1), 384–394 (2005).
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F. Wang, T. S. Chen, D. Xing, J. J. Wang, and Y. X. Wu, “Measuring dynamics of caspase-3 activity in living cells using FRET technique during apoptosis induced by high fluence low-power laser irradiation,” Lasers Surg. Med. 36(1), 2–7 (2005).
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A. Degterev, Z. Huang, M. Boyce, Y. Li, P. Jagtap, N. Mizushima, G. D. Cuny, T. J. Mitchison, M. A. Moskowitz, and J. Yuan, “Chemical inhibitor of nonapoptotic cell death with therapeutic potential for ischemic brain injury,” Nat. Chem. Biol. 1(2), 112–119 (2005).
[Crossref] [PubMed]

L. Brosseau, V. Robinson, G. Wells, R. Debie, A. Gam, K. Harman, M. Morin, B. Shea, and P. Tugwell, “Low level laser therapy (classes i, ii and iii) for treating rheumatoid arthritis,” Cochrane Database Syst. Rev. 4, CD002049 (2005).
[PubMed]

2004 (2)

A. Valencia and J. Morán, “Reactive oxygen species induce different cell death mechanisms in cultured neurons,” Free Radic. Biol. Med. 36(9), 1112–1125 (2004).
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N. N. Danial and S. J. Korsmeyer, “Cell death: Critical control points,” Cell 116(2), 205–219 (2004).
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2003 (4)

J. D. Ly, D. R. Grubb, and A. Lawen, “The mitochondrial membrane potential (delta psi m) in apoptosis; an update,” Apoptosis 8(2), 115–128 (2003).
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T. Zuliani, R. Duval, C. Jayat, S. Schnébert, P. André, M. Dumas, and M. H. Ratinaud, “Sensitive and reliable jc-1 and toto-3 double staining to assess mitochondrial transmembrane potential and plasma membrane Integrity: interest for cell death investigations,” Cytometry A 54A(2), 100–108 (2003).
[Crossref] [PubMed]

J. T. Eells, M. M. Henry, P. Summerfelt, M. T. Wong-Riley, E. V. Buchmann, M. Kane, N. T. Whelan, and H. T. Whelan, “Therapeutic photobiomodulation for methanol-induced retinal toxicity,” Proc. Natl. Acad. Sci. U.S.A. 100(6), 3439–3444 (2003).
[Crossref] [PubMed]

H. T. Whelan, E. V. Buchmann, A. Dhokalia, M. P. Kane, N. T. Whelan, M. T. Wong-Riley, J. T. Eells, L. J. Gould, R. Hammamieh, R. Das, and M. Jett, “Effect of nasa light-emitting diode irradiation on molecular changes for wound healing in diabetic mice,” J. Clin. Laser Med. Surg. 21(2), 67–74 (2003).
[Crossref] [PubMed]

2002 (1)

J. B. Hoek, A. Cahill, and J. G. Pastorino, “Alcohol and mitochondria: A dysfunctional relationship,” Gastroenterology 122(7), 2049–2063 (2002).
[Crossref] [PubMed]

2001 (1)

M. Greco, R. A. Vacca, L. Moro, E. Perlino, V. A. Petragallo, E. Marra, and S. Passarella, “Helium-neon laser irradiation of hepatocytes can trigger increase of the mitochondrial membrane potential and can stimulate c-fos expression in a Ca2+-dependent manner,” Lasers Surg. Med. 29(5), 433–441 (2001).
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2000 (1)

G. Kroemer and J. C. Reed, “Mitochondrial control of cell death,” Nat. Med. 6(5), 513–519 (2000).
[Crossref] [PubMed]

1999 (2)

W. Fiers, R. Beyaert, W. Declercq, and P. Vandenabeele, “More than one way to die: Apoptosis, necrosis and reactive oxygen damage,” Oncogene 18(54), 7719–7730 (1999).
[Crossref] [PubMed]

H. Wang and J. A. Joseph, “Quantifying cellular oxidative stress by dichlorofluorescein assay using microplate reader,” Free Radic. Biol. Med. 27(5-6), 612–616 (1999).
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1997 (1)

R. A. Vacca, L. Moro, V. A. Petragallo, M. Greco, F. Fontana, and S. Passarella, “The irradiation of hepatocytes with he-ne laser causes an increase of cytosolic free calcium concentration and an increase of cell membrane potential, correlated with it, both increases taking place in an oscillatory manner,” Biochem. Mol. Biol. Int. 43(5), 1005–1014 (1997).
[PubMed]

1996 (1)

M. Weil, M. D. Jacobson, H. S. Coles, T. J. Davies, R. L. Gardner, K. D. Raff, and M. C. Raff, “Constitutive expression of the machinery for programmed cell death,” J. Cell Biol. 133(5), 1053–1059 (1996).
[Crossref] [PubMed]

1995 (1)

S. J. Martin, C. P. Reutelingsperger, A. J. McGahon, J. A. Rader, R. C. van Schie, D. M. LaFace, and D. R. Green, “Early redistribution of plasma membrane phosphatidylserine is a general feature of apoptosis regardless of the initiating stimulus: inhibition by overexpression of bcl-2 and abl,” J. Exp. Med. 182(5), 1545–1556 (1995).
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1994 (1)

N. G. Papadopoulos, G. V. Dedoussis, G. Spanakos, A. D. Gritzapis, C. N. Baxevanis, and M. Papamichail, “An improved fluorescence assay for the determination of lymphocyte-mediated cytotoxicity using flow cytometry,” J. Immunol. Methods 177(1-2), 101–111 (1994).
[Crossref] [PubMed]

1991 (2)

S. T. Smiley, M. Reers, C. Mottola-Hartshorn, M. Lin, A. Chen, T. W. Smith, G. D. Steele, and L. B. Chen, “Intracellular heterogeneity in mitochondrial membrane potentials revealed by a J-aggregate-forming lipophilic cation jc-1,” Proc. Natl. Acad. Sci. U.S.A. 88(9), 3671–3675 (1991).
[Crossref] [PubMed]

S. T. Smiley, M. Reers, C. Mottola-Hartshorn, M. Lin, A. Chen, T. W. Smith, G. D. Steele, and L. B. Chen, “Intracellular heterogeneity in mitochondrial membrane potentials revealed by a j-aggregate-forming lipophilic cation jc-1,” Proc. Natl. Acad. Sci. U.S.A. 88(9), 3671–3675 (1991).
[Crossref] [PubMed]

1989 (1)

T. Karu, “Photobiology of low-power laser effects,” Health Phys. 56(5), 691–704 (1989).
[Crossref] [PubMed]

1985 (1)

H. C. Birnboim and M. Kanabus-Kaminska, “The production of DNA strand breaks in human leukocytes by superoxide anion may involve a metabolic process,” Proc. Natl. Acad. Sci. U.S.A. 82(20), 6820–6824 (1985).
[Crossref] [PubMed]

1982 (1)

K. J. Henle and R. L. Warters, “Heat protection by glycerol in vitro,” Cancer Res. 42(6), 2171–2176 (1982).
[PubMed]

Afanasyeva, N. I.

T. I. Karu, L. V. Pyatibrat, S. F. Kolyakov, and N. I. Afanasyeva, “Absorption measurements of cell monolayers relevant to mechanisms of laser phototherapy: Reduction or oxidation of cytochrome c oxidase under laser radiation at 632.8 nm,” Photomed. Laser Surg. 26(6), 593–599 (2008).
[Crossref] [PubMed]

Akbari-Kamrani, M.

R. Yousefi-Nooraie, E. Schonstein, K. Heidari, A. Rashidian, V. Pennick, M. Akbari-Kamrani, S. Irani, B. Shakiba, S. A. Mortaz Hejri, S. O. Mortaz Hejri, and A. Jonaidi, “Low level laser therapy for nonspecific low-back pain,” Cochrane Database Syst. Rev. 2, CD005107 (2008).
[PubMed]

Anderson, R. R.

R. R. Anderson, “Lasers for dermatology and skin biology,” J. Invest. Dermatol. 133(E1), E21–E23 (2013).
[Crossref] [PubMed]

André, P.

T. Zuliani, R. Duval, C. Jayat, S. Schnébert, P. André, M. Dumas, and M. H. Ratinaud, “Sensitive and reliable jc-1 and toto-3 double staining to assess mitochondrial transmembrane potential and plasma membrane Integrity: interest for cell death investigations,” Cytometry A 54A(2), 100–108 (2003).
[Crossref] [PubMed]

Arany, P.

I. Khan, E. Tang, and P. Arany, “Molecular pathway of near-infrared laser phototoxicity involves atf-4 orchestrated er stress,” Sci. Rep. 5(1), 10581 (2015).
[Crossref] [PubMed]

Arany, P. R.

P. R. Arany, A. Cho, T. D. Hunt, G. Sidhu, K. Shin, E. Hahm, G. X. Huang, J. Weaver, A. C. Chen, B. L. Padwa, M. R. Hamblin, M. H. Barcellos-Hoff, A. B. Kulkarni, and D. J Mooney, “Photoactivation of endogenous latent transforming growth factor-β1 directs dental stem cell differentiation for regeneration,” Sci. Transl. Med. 6(238), 238ra69 (2014).
[Crossref] [PubMed]

A. C. Chen, P. R. Arany, Y. Y. Huang, E. M. Tomkinson, S. K. Sharma, G. B. Kharkwal, T. Saleem, D. Mooney, F. E. Yull, T. S. Blackwell, and M. R. Hamblin, “Low-level laser therapy activates nf-kb via generation of reactive oxygen species in mouse embryonic fibroblasts,” PLoS One 6(7), e22453 (2011).
[Crossref] [PubMed]

Baehrecke, E. H.

G. Mariño, M. Niso-Santano, E. H. Baehrecke, and G. Kroemer, “Self-consumption: The interplay of autophagy and apoptosis,” Nat. Rev. Mol. Cell Biol. 15(2), 81–94 (2014).
[Crossref] [PubMed]

G. Mariño, M. Niso-Santano, E. H. Baehrecke, and G. Kroemer, “Self-consumption: The interplay of autophagy and apoptosis,” Nat. Rev. Mol. Cell Biol. 15(2), 81–94 (2014).
[Crossref] [PubMed]

Barcellos-Hoff, M. H.

P. R. Arany, A. Cho, T. D. Hunt, G. Sidhu, K. Shin, E. Hahm, G. X. Huang, J. Weaver, A. C. Chen, B. L. Padwa, M. R. Hamblin, M. H. Barcellos-Hoff, A. B. Kulkarni, and D. J Mooney, “Photoactivation of endogenous latent transforming growth factor-β1 directs dental stem cell differentiation for regeneration,” Sci. Transl. Med. 6(238), 238ra69 (2014).
[Crossref] [PubMed]

Baxevanis, C. N.

N. G. Papadopoulos, G. V. Dedoussis, G. Spanakos, A. D. Gritzapis, C. N. Baxevanis, and M. Papamichail, “An improved fluorescence assay for the determination of lymphocyte-mediated cytotoxicity using flow cytometry,” J. Immunol. Methods 177(1-2), 101–111 (1994).
[Crossref] [PubMed]

Beal, M. F.

M. T. Lin and M. F. Beal, “Mitochondrial dysfunction and oxidative stress in neurodegenerative diseases,” Nature 443(7113), 787–795 (2006).
[Crossref] [PubMed]

Bender, C.

R. Matthes, C. Bender, R. Schlüter, I. Koban, R. Bussiahn, S. Reuter, J. Lademann, K. D. Weltmann, and A. Kramer, “Antimicrobial efficacy of two surface barrier discharges with air plasma against in vitro biofilms,” PLoS One 8(7), e70462 (2013).
[Crossref] [PubMed]

Bertrand, M. J. M.

T. Vanden Berghe, W. J. Kaiser, M. J. M. Bertrand, and P. Vandenabeele, “Molecular crosstalk between apoptosis, necroptosis, and survival signaling,” Mol. Cell. Oncol. 2(4), e975093 (2015).
[Crossref] [PubMed]

Beyaert, R.

W. Fiers, R. Beyaert, W. Declercq, and P. Vandenabeele, “More than one way to die: Apoptosis, necrosis and reactive oxygen damage,” Oncogene 18(54), 7719–7730 (1999).
[Crossref] [PubMed]

Birnboim, H. C.

H. C. Birnboim and M. Kanabus-Kaminska, “The production of DNA strand breaks in human leukocytes by superoxide anion may involve a metabolic process,” Proc. Natl. Acad. Sci. U.S.A. 82(20), 6820–6824 (1985).
[Crossref] [PubMed]

Bjordal, J. M.

R. T. Chow, M. I. Johnson, R. A. Lopes-Martins, and J. M. Bjordal, “Efficacy of low-level laser therapy in the management of neck pain: A systematic review and meta-analysis of randomised placebo or active-treatment controlled trials,” Lancet 374(9705), 1897–1908 (2009).
[Crossref] [PubMed]

Blackwell, T. S.

A. C. Chen, P. R. Arany, Y. Y. Huang, E. M. Tomkinson, S. K. Sharma, G. B. Kharkwal, T. Saleem, D. Mooney, F. E. Yull, T. S. Blackwell, and M. R. Hamblin, “Low-level laser therapy activates nf-kb via generation of reactive oxygen species in mouse embryonic fibroblasts,” PLoS One 6(7), e22453 (2011).
[Crossref] [PubMed]

Boyce, M.

A. Degterev, Z. Huang, M. Boyce, Y. Li, P. Jagtap, N. Mizushima, G. D. Cuny, T. J. Mitchison, M. A. Moskowitz, and J. Yuan, “Chemical inhibitor of nonapoptotic cell death with therapeutic potential for ischemic brain injury,” Nat. Chem. Biol. 1(2), 112–119 (2005).
[Crossref] [PubMed]

Brosseau, L.

L. Brosseau, V. Robinson, G. Wells, R. Debie, A. Gam, K. Harman, M. Morin, B. Shea, and P. Tugwell, “Low level laser therapy (classes i, ii and iii) for treating rheumatoid arthritis,” Cochrane Database Syst. Rev. 4, CD002049 (2005).
[PubMed]

Buchmann, E. V.

J. T. Eells, M. M. Henry, P. Summerfelt, M. T. Wong-Riley, E. V. Buchmann, M. Kane, N. T. Whelan, and H. T. Whelan, “Therapeutic photobiomodulation for methanol-induced retinal toxicity,” Proc. Natl. Acad. Sci. U.S.A. 100(6), 3439–3444 (2003).
[Crossref] [PubMed]

H. T. Whelan, E. V. Buchmann, A. Dhokalia, M. P. Kane, N. T. Whelan, M. T. Wong-Riley, J. T. Eells, L. J. Gould, R. Hammamieh, R. Das, and M. Jett, “Effect of nasa light-emitting diode irradiation on molecular changes for wound healing in diabetic mice,” J. Clin. Laser Med. Surg. 21(2), 67–74 (2003).
[Crossref] [PubMed]

Bussiahn, R.

R. Matthes, C. Bender, R. Schlüter, I. Koban, R. Bussiahn, S. Reuter, J. Lademann, K. D. Weltmann, and A. Kramer, “Antimicrobial efficacy of two surface barrier discharges with air plasma against in vitro biofilms,” PLoS One 8(7), e70462 (2013).
[Crossref] [PubMed]

Cahill, A.

J. B. Hoek, A. Cahill, and J. G. Pastorino, “Alcohol and mitochondria: A dysfunctional relationship,” Gastroenterology 122(7), 2049–2063 (2002).
[Crossref] [PubMed]

Cao, Y.

Y. Wang, H. He, S. Wang, Y. Liu, M. Hu, Y. Cao, S. Kong, X. Wei, and C. Wang, “Photostimulation by femtosecond laser triggers restorable fragmentation in single mitochondrion,” J. Biophotonics 10(2), 286–293 (2017).
[Crossref] [PubMed]

Carroll, J.

Y. Y. Huang, S. K. Sharma, J. Carroll, and M. R. Hamblin, “Biphasic dose response in low level light therapy - an update,” Dose Response 9(4), 602–618 (2011).
[Crossref] [PubMed]

Carroll, J. D.

H. Chung, T. Dai, S. K. Sharma, Y. Y. Huang, J. D. Carroll, and M. R. Hamblin, “The nuts and bolts of low-level laser (light) therapy,” Ann. Biomed. Eng. 40(2), 516–533 (2012).
[Crossref] [PubMed]

Y. Y. Huang, A. C. Chen, J. D. Carroll, and M. R. Hamblin, “Biphasic dose response in low level light therapy,” Dose Response 7(4), 358–383 (2009).
[Crossref] [PubMed]

Chang, T. H.

W. K. Ong, H. F. Chen, C. T. Tsai, Y. J. Fu, Y. S. Wong, D. J. Yen, T. H. Chang, H. D. Huang, O. K. Lee, S. Chien, and J. H. Ho, “The activation of directional stem cell motility by green light-emitting diode irradiation,” Biomaterials 34(8), 1911–1920 (2013).
[Crossref] [PubMed]

Chánová, E.

O. Lunov, V. Zablotskii, O. Churpita, E. Chánová, E. Syková, A. Dejneka, and S. Kubinová, “Cell death induced by ozone and various non-thermal plasmas: Therapeutic perspectives and limitations,” Sci. Rep. 4(1), 7129 (2015).
[Crossref] [PubMed]

Chen, A.

S. T. Smiley, M. Reers, C. Mottola-Hartshorn, M. Lin, A. Chen, T. W. Smith, G. D. Steele, and L. B. Chen, “Intracellular heterogeneity in mitochondrial membrane potentials revealed by a J-aggregate-forming lipophilic cation jc-1,” Proc. Natl. Acad. Sci. U.S.A. 88(9), 3671–3675 (1991).
[Crossref] [PubMed]

S. T. Smiley, M. Reers, C. Mottola-Hartshorn, M. Lin, A. Chen, T. W. Smith, G. D. Steele, and L. B. Chen, “Intracellular heterogeneity in mitochondrial membrane potentials revealed by a j-aggregate-forming lipophilic cation jc-1,” Proc. Natl. Acad. Sci. U.S.A. 88(9), 3671–3675 (1991).
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Chen, A. C.

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W. K. Ong, H. F. Chen, C. T. Tsai, Y. J. Fu, Y. S. Wong, D. J. Yen, T. H. Chang, H. D. Huang, O. K. Lee, S. Chien, and J. H. Ho, “The activation of directional stem cell motility by green light-emitting diode irradiation,” Biomaterials 34(8), 1911–1920 (2013).
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S. Wu, D. Xing, X. Gao, and W. R. Chen, “High fluence low-power laser irradiation induces mitochondrial permeability transition mediated by reactive oxygen species,” J. Cell. Physiol. 218(3), 603–611 (2009).
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P. R. Arany, A. Cho, T. D. Hunt, G. Sidhu, K. Shin, E. Hahm, G. X. Huang, J. Weaver, A. C. Chen, B. L. Padwa, M. R. Hamblin, M. H. Barcellos-Hoff, A. B. Kulkarni, and D. J Mooney, “Photoactivation of endogenous latent transforming growth factor-β1 directs dental stem cell differentiation for regeneration,” Sci. Transl. Med. 6(238), 238ra69 (2014).
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O. Lunov, V. Zablotskii, O. Churpita, E. Chánová, E. Syková, A. Dejneka, and S. Kubinová, “Cell death induced by ozone and various non-thermal plasmas: Therapeutic perspectives and limitations,” Sci. Rep. 4(1), 7129 (2015).
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O. Yizhar, L. E. Fenno, T. J. Davidson, M. Mogri, and K. Deisseroth, “Optogenetics in neural systems,” Neuron 71(1), 9–34 (2011).
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O. Yizhar, L. E. Fenno, T. J. Davidson, M. Mogri, and K. Deisseroth, “Optogenetics in neural systems,” Neuron 71(1), 9–34 (2011).
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O. Lunov, V. Zablotskii, O. Churpita, A. Jäger, L. Polívka, E. Syková, A. Dejneka, and Š. Kubinová, “The interplay between biological and physical scenarios of bacterial death induced by non-thermal plasma,” Biomaterials 82, 71–83 (2016).
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O. Lunov, V. Zablotskii, O. Churpita, E. Chánová, E. Syková, A. Dejneka, and S. Kubinová, “Cell death induced by ozone and various non-thermal plasmas: Therapeutic perspectives and limitations,” Sci. Rep. 4(1), 7129 (2015).
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M. Di Carlo, D. Giacomazza, P. Picone, D. Nuzzo, and P. L. San Biagio, “Are oxidative stress and mitochondrial dysfunction the key players in the neurodegenerative diseases?” Free Radic. Res. 46(11), 1327–1338 (2012).
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N. Kaludercic, S. Deshwal, and F. Di Lisa, “Reactive oxygen species and redox compartmentalization,” Front. Physiol. 5, 285 (2014).
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Eells, J. T.

H. T. Whelan, E. V. Buchmann, A. Dhokalia, M. P. Kane, N. T. Whelan, M. T. Wong-Riley, J. T. Eells, L. J. Gould, R. Hammamieh, R. Das, and M. Jett, “Effect of nasa light-emitting diode irradiation on molecular changes for wound healing in diabetic mice,” J. Clin. Laser Med. Surg. 21(2), 67–74 (2003).
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J. T. Eells, M. M. Henry, P. Summerfelt, M. T. Wong-Riley, E. V. Buchmann, M. Kane, N. T. Whelan, and H. T. Whelan, “Therapeutic photobiomodulation for methanol-induced retinal toxicity,” Proc. Natl. Acad. Sci. U.S.A. 100(6), 3439–3444 (2003).
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M. L. Denton, M. S. Foltz, L. E. Estlack, D. J. Stolarski, G. D. Noojin, R. J. Thomas, D. Eikum, and B. A. Rockwell, “Damage thresholds for exposure to nir and blue lasers in an in vitro rpe cell system,” Invest. Ophthalmol. Vis. Sci. 47(7), 3065–3073 (2006).
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O. Yizhar, L. E. Fenno, T. J. Davidson, M. Mogri, and K. Deisseroth, “Optogenetics in neural systems,” Neuron 71(1), 9–34 (2011).
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Fiers, W.

W. Fiers, R. Beyaert, W. Declercq, and P. Vandenabeele, “More than one way to die: Apoptosis, necrosis and reactive oxygen damage,” Oncogene 18(54), 7719–7730 (1999).
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Foltz, M. S.

M. L. Denton, M. S. Foltz, L. E. Estlack, D. J. Stolarski, G. D. Noojin, R. J. Thomas, D. Eikum, and B. A. Rockwell, “Damage thresholds for exposure to nir and blue lasers in an in vitro rpe cell system,” Invest. Ophthalmol. Vis. Sci. 47(7), 3065–3073 (2006).
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W. K. Ong, H. F. Chen, C. T. Tsai, Y. J. Fu, Y. S. Wong, D. J. Yen, T. H. Chang, H. D. Huang, O. K. Lee, S. Chien, and J. H. Ho, “The activation of directional stem cell motility by green light-emitting diode irradiation,” Biomaterials 34(8), 1911–1920 (2013).
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L. Brosseau, V. Robinson, G. Wells, R. Debie, A. Gam, K. Harman, M. Morin, B. Shea, and P. Tugwell, “Low level laser therapy (classes i, ii and iii) for treating rheumatoid arthritis,” Cochrane Database Syst. Rev. 4, CD002049 (2005).
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S. Wu, D. Xing, X. Gao, and W. R. Chen, “High fluence low-power laser irradiation induces mitochondrial permeability transition mediated by reactive oxygen species,” J. Cell. Physiol. 218(3), 603–611 (2009).
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M. Weil, M. D. Jacobson, H. S. Coles, T. J. Davies, R. L. Gardner, K. D. Raff, and M. C. Raff, “Constitutive expression of the machinery for programmed cell death,” J. Cell Biol. 133(5), 1053–1059 (1996).
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M. Di Carlo, D. Giacomazza, P. Picone, D. Nuzzo, and P. L. San Biagio, “Are oxidative stress and mitochondrial dysfunction the key players in the neurodegenerative diseases?” Free Radic. Res. 46(11), 1327–1338 (2012).
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S. B. Goncalves, J. F. Ribeiro, A. F. Silva, R. M. Costa, and J. H. Correia, “Design and manufacturing challenges of optogenetic neural interfaces: A review,” J. Neural Eng. 14(4), 041001 (2017).
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H. T. Whelan, E. V. Buchmann, A. Dhokalia, M. P. Kane, N. T. Whelan, M. T. Wong-Riley, J. T. Eells, L. J. Gould, R. Hammamieh, R. Das, and M. Jett, “Effect of nasa light-emitting diode irradiation on molecular changes for wound healing in diabetic mice,” J. Clin. Laser Med. Surg. 21(2), 67–74 (2003).
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N. G. Papadopoulos, G. V. Dedoussis, G. Spanakos, A. D. Gritzapis, C. N. Baxevanis, and M. Papamichail, “An improved fluorescence assay for the determination of lymphocyte-mediated cytotoxicity using flow cytometry,” J. Immunol. Methods 177(1-2), 101–111 (1994).
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J. D. Ly, D. R. Grubb, and A. Lawen, “The mitochondrial membrane potential (delta psi m) in apoptosis; an update,” Apoptosis 8(2), 115–128 (2003).
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P. R. Arany, A. Cho, T. D. Hunt, G. Sidhu, K. Shin, E. Hahm, G. X. Huang, J. Weaver, A. C. Chen, B. L. Padwa, M. R. Hamblin, M. H. Barcellos-Hoff, A. B. Kulkarni, and D. J Mooney, “Photoactivation of endogenous latent transforming growth factor-β1 directs dental stem cell differentiation for regeneration,” Sci. Transl. Med. 6(238), 238ra69 (2014).
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Hamblin, M. R.

P. R. Arany, A. Cho, T. D. Hunt, G. Sidhu, K. Shin, E. Hahm, G. X. Huang, J. Weaver, A. C. Chen, B. L. Padwa, M. R. Hamblin, M. H. Barcellos-Hoff, A. B. Kulkarni, and D. J Mooney, “Photoactivation of endogenous latent transforming growth factor-β1 directs dental stem cell differentiation for regeneration,” Sci. Transl. Med. 6(238), 238ra69 (2014).
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H. Chung, T. Dai, S. K. Sharma, Y. Y. Huang, J. D. Carroll, and M. R. Hamblin, “The nuts and bolts of low-level laser (light) therapy,” Ann. Biomed. Eng. 40(2), 516–533 (2012).
[Crossref] [PubMed]

A. C. Chen, P. R. Arany, Y. Y. Huang, E. M. Tomkinson, S. K. Sharma, G. B. Kharkwal, T. Saleem, D. Mooney, F. E. Yull, T. S. Blackwell, and M. R. Hamblin, “Low-level laser therapy activates nf-kb via generation of reactive oxygen species in mouse embryonic fibroblasts,” PLoS One 6(7), e22453 (2011).
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Y. Y. Huang, S. K. Sharma, J. Carroll, and M. R. Hamblin, “Biphasic dose response in low level light therapy - an update,” Dose Response 9(4), 602–618 (2011).
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Y. Y. Huang, A. C. Chen, J. D. Carroll, and M. R. Hamblin, “Biphasic dose response in low level light therapy,” Dose Response 7(4), 358–383 (2009).
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Hammamieh, R.

H. T. Whelan, E. V. Buchmann, A. Dhokalia, M. P. Kane, N. T. Whelan, M. T. Wong-Riley, J. T. Eells, L. J. Gould, R. Hammamieh, R. Das, and M. Jett, “Effect of nasa light-emitting diode irradiation on molecular changes for wound healing in diabetic mice,” J. Clin. Laser Med. Surg. 21(2), 67–74 (2003).
[Crossref] [PubMed]

Harman, K.

L. Brosseau, V. Robinson, G. Wells, R. Debie, A. Gam, K. Harman, M. Morin, B. Shea, and P. Tugwell, “Low level laser therapy (classes i, ii and iii) for treating rheumatoid arthritis,” Cochrane Database Syst. Rev. 4, CD002049 (2005).
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Y. Wang, H. He, S. Wang, Y. Liu, M. Hu, Y. Cao, S. Kong, X. Wei, and C. Wang, “Photostimulation by femtosecond laser triggers restorable fragmentation in single mitochondrion,” J. Biophotonics 10(2), 286–293 (2017).
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Supplementary Material (3)

NameDescription
» Visualization 1       Control cells. Cell viability was detected by the fluorescent live/dead cell assay kit (Thermo Fisher Scientific). After loading the Huh7 cells with calcein-AM (green) and etidium homodimer (red) images were acquired by confocal microscopy.
» Visualization 2       Laser exposure. Cell viability was detected by the fluorescent live/dead cell assay kit (Thermo Fisher Scientific). After loading the Huh7 cells with calcein-AM (green) and etidium homodimer (red) images were acquired by confocal microscopy.
» Visualization 3       Huh7 exposed to the laser light for indicated time periods with supplementation of 5 mM NAC (1 h pre-treatment with NAC followed by 50 min laser irradiation). Cell viability was detected by the fluorescent live/dead cell assay kit.

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Figures (7)

Fig. 1
Fig. 1 Characterization of the laser system. (A) Experimental setup. (B) Scheme of the laser system. LD - laser diode. (C) Divergence of laser beam.
Fig. 2
Fig. 2 Laser irradiation induces acute cell death of Huh7 cells. (A) Cell viability was detected by the fluorescent live/dead cell assay kit (Thermo Fisher Scientific). After loading with calcein-AM (green) and ethidium homodimer (red) images were acquired by confocal microscopy from Huh7 cells treated with laser (1 mW). Control cells were untreated. ImageJ software (NIH) was used for image processing and quantification. Fluorescence intensity of both dyes was measured at the respective time points and was normalized to total fluorescence. Data are expressed as means ± SEM (n = 3), t = 0 time point served as control, **P< 0.01 ***P< 0.001. (B) Dose-dependent laser-induced cytotoxicity. Cells were irradiated with different laser fluences and analyzed as in (A). Data are expressed as means ± SEM (n = 3), t = 0 time point served as control, **P< 0.01 ***P< 0.001. (C) Non-uniform cellular response due to the non-uniform distribution of the laser intensity from the fiber output. Line intensity profile and surface intensity plot of cells irradiated with laser (1 mW) as in (B). Graphs show non-uniform calcein-AM fluorescence depending on displacement from optical taper. ImageJ software (NIH) was used for image processing and quantification.
Fig. 3
Fig. 3 Dose-dependent ROS induction by laser irradiation. (A) Cells were labeled with the ROS-sensitive fluorescent dyes using the cellular ROS/Superoxide detection kit (Abcam, Cambridge, United Kingdom). Cell membranes were labeled with CellMask. Non-irradiated cells with no chemical treatment served as a negative control (left panel). Non-irradiated cells treated with Pyocyanin (200 μM) were used as a ROS positive control (left panel). Cells irradiated by laser fluences of 1 mW and 46 µW are shown on the right panel. All fluorescence images were acquired by confocal microscopy. (B) Quantitative analysis of relative ROS fluorescence emission intensity from cells treated by laser. ImageJ software (NIH) was used for image processing and quantification. Data are expressed as means ± SEM (n = 3), *P< 0.05 **P< 0.01 ***P< 0.001. (C) Quantitative analysis of relative superoxide fluorescence emission intensity from cells treated by laser. ImageJ software (NIH) was used for image processing and quantification. Data are expressed as means ± SEM (n = 3), *P< 0.05 **P< 0.01 ***P< 0.001. (D) ROS scavenger N-acetyl-L-cysteine (NAC) reduces the cytotoxicity induced by laser. Viability of Huh7 cells exposed to the laser for indicated time periods with supplementation of 5 mM NAC was detected by the Thermo Fisher Scientific fluorescent live/dead cell assay kit. Cells were imaged and analyzed as in Fig. 2. Data are expressed as means ± SEM (n = 3), t = 0 time point served as control, *P< 0.05 **P< 0.01 ***P< 0.001.
Fig. 4
Fig. 4 High dose (1 mW) laser irradiation induces necrotic cell death of Huh7 cells. (A) Cell viability was detected by the Thermo Fisher Scientific fluorescent live/dead cell assay kit. Full growth medium with 1 M glycerol was used as thermoprotective. Cells were imaged and analyzed as in Fig. 2. Data are expressed as means ± SEM (n = 3), **P< 0.01. Cells heated for 1 h at 45 °C were used as a positive control. (B) Cells were treated with laser for 40 min and then labeled with NucRed nuclear stain (blue), annexin V (green) and PI (red). Cells treated with 2 μM staurosporine for 3 h served as a positive control. Labeled cells were imaged with fluorescence microscopy. Representative images out of three independent experiments are shown. Annexin V and PI fluorescence intensities were analyzed with ImageJ. Data are expressed as means ± SEM (n = 3), ***P< 0.001, ###P< 0.001. (C) Cells were irradiated with laser for 40 min. Further, post-treatment cells were incubated with caspase-3 inhibitor VAD-FMK conjugated to FITC (FITC-VAD-FMK). Following the staining, cells were analyzed using a fluorescent microscope. Fluorescence intensities were analyzed with ImageJ. Data are expressed as means ± SEM (n = 3), ***P< 0.001. (D) Cells were irradiated with laser for 40 min, then stained with 2 μM JC-1 for 30 min, and analyzed by confocal microscopy. Red fluorescent images of dye aggregates indicate high- ΔmΦ mitochondria. As a positive control, cells were treated with 10% ethanol for 10 min. (E) Quantitative analysis of ΔmΦ imaged in (D). ImageJ software (NIH) was used for image processing and quantification. Data are expressed as means ± SEM (n = 3), ***P< 0.001.
Fig. 5
Fig. 5 Low dose laser irradiation induces apoptotic cell death of Huh7 cells. (A) Cells were treated with low dose (46 µW) laser irradiation for 40 min and then labeled with NucRed nuclear stain (blue), annexin V (green) and PI (red). Cells treated with 2 μM staurosporine for 3 h served as a positive control. Labeled cells were imaged with fluorescence microscopy. Representative images out of three independent experiments are shown. Annexin V and PI fluorescence intensities were analyzed with ImageJ. Data are expressed as means ± SEM (n = 3), ***P< 0.001, ##P< 0.01. (B) Cells were treated with low dose (46 µW) laser irradiation for 40 min and then incubated with caspase-3 inhibitor VAD-FMK conjugated to FITC (FITC-VAD-FMK). Following the staining, cells were analyzed using a fluorescent microscope. Fluorescence intensities were analyzed with ImageJ. Data are expressed as means ± SEM (n = 3), **P< 0.01 ***P< 0.001. (C) Cells were treated with low dose (46 µW) laser for 40 min then stained with 2 μM JC-1 for 30 min and then analyzed by confocal microscopy. As a positive control, cells were treated with 10% ethanol for 10 min. ImageJ software (NIH) was used for image processing and quantification. Data are expressed as means ± SEM (n = 3), **P< 0.01 ***P< 0.001. (D) Viability of Huh7 cells exposed to the laser light with supplementation of 10 µM Nec-1 (1 h pre-treatment with Nec-1 followed by 40 min laser irradiation) was detected by the Thermo Fisher Scientific fluorescent live/dead cell assay kit. Cells were imaged and analyzed as in Fig. 2. Data are expressed as means ± SEM (n = 3). (E) Viability of cells exposed to the laser light with supplementation of 20 µM CsA (1 h pre-treatment with Cs-A followed by 40 min laser irradiation) was detected as in (D). Cells were imaged and analyzed as in Fig. 2. Data are expressed as means ± SEM (n = 3), ##P< 0.01 ***P< 0.001.
Fig. 6
Fig. 6 Cyclosporin A inhibits depolarization of mitochondrial membrane potential exerted by 1 mW laser irradiation. (A) Cells were irradiated with laser for 40 min, then stained with 2 μM JC-1 for 30 min, and analyzed by confocal microscopy. Red fluorescent images of dye aggregates indicate high- ΔmΦ mitochondria. Cells were preincubated with 0.1, 1, 10 µM CsA before treatment with laser. As a positive control, cells were treated with 10% ethanol for 10 min. Quantitative analysis of ΔmΦ was performed by ImageJ software (NIH). Data are expressed as means ± SEM (n = 5), ***P< 0.001. (B) Cultures were co-loaded with SYTO 13 (green) and MitoTracker red CM-H2XRos (red) and confocal images (1000x) obtained after 1 mW laser irradiation. Cells were preincubated with 10 µM CsA before treatment with laser. Representative images out of three independent experiments are shown. Non-irradiated cells treated with Pyocyanin (200 μM) were used as a ROS positive control. Mito-ROS fluorescence intensities were analyzed with ImageJ. Data are expressed as means ± SEM (n = 3), ***P< 0.001. (C) ROS scavenger N-acetyl-L-cysteine (NAC) reduces the mitochondrial damage induced by laser. Mitochondrial damage of cells exposed to the laser with supplementation of 5 mM NAC was performed using JC-1 assay as in (A). Data are expressed as means ± SEM (n = 3), ***P< 0.001.
Fig. 7
Fig. 7 Low dose laser irradiation induces nuclear accumulation of superoxide. (A) Cells were labeled with the ROS-sensitive fluorescent dyes using the cellular ROS/Superoxide detection kit (Abcam, Cambridge, United Kingdom) and then treated by different laser fluences. The fluorescence images were acquired by confocal microscopy. Non-irradiated cells with no chemical treatment served as control. Pyocyanin (200 μM) treatment was used in the non-irradiated cells representing the ROS + positive control. (B) Quantitative analysis of relative superoxide fluorescence emission intensity from cells treated by laser. ImageJ software (NIH) was used for image processing and quantification. Data are expressed as means ± SEM (n = 3), **P< 0.01 ***P< 0.001. (C) Scheme of district biochemical signaling activation in cells after stimulation with different laser doses. ∆mΦ – mitochondrial membrane potential.

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