Skip to main content

Advertisement

Log in

Light-induced modulation of the mitochondrial respiratory chain activity: possibilities and limitations

  • Original Article
  • Published:
Cellular and Molecular Life Sciences Aims and scope Submit manuscript

Abstract

Biological effects of high fluence low-power (HFLP) lasers have been reported for some time, yet the molecular mechanisms procuring cellular responses remain obscure. A better understanding of the effects of HFLP lasers on living cells will be instrumental for the development of new experimental and therapeutic strategies. Therefore, we investigated sub-cellular mechanisms involved in the laser interaction with human hepatic cell lines. We show that mitochondria serve as sub-cellular “sensor” and “effector” of laser light non-specific interactions with cells. We demonstrated that despite blue and red laser irradiation results in similar apoptotic death, cellular signaling and kinetic of biochemical responses are distinct. Based on our data, we concluded that blue laser irradiation inhibited cytochrome c oxidase activity in electron transport chain of mitochondria. Contrary, red laser triggered cytochrome c oxidase excessive activation. Moreover, we showed that Bcl-2 protein inhibited laser-induced toxicity by stabilizing mitochondria membrane potential. Thus, cells that either overexpress or have elevated levels of Bcl-2 are protected from laser-induced cytotoxicity. Our findings reveal the mechanism how HFLP laser irradiation interfere with cell homeostasis and underscore that such laser irradiation permits remote control of mitochondrial function in the absence of chemical or biological agents.

This is a preview of subscription content, log in via an institution to check access.

Access this article

Price excludes VAT (USA)
Tax calculation will be finalised during checkout.

Instant access to the full article PDF.

Fig. 1
Fig. 2
Fig. 3
Fig. 4
Fig. 5
Fig. 6
Fig. 7
Fig. 8
Fig. 9
Fig. 10

Similar content being viewed by others

Abbreviations

HFLP:

High fluence low-power

ROS:

Reactive oxygen species

COX:

Cytochrome c oxidase

MOMP:

Permeabilization of the mitochondrial outer membrane

PMB:

Photobiomodulation

ETC:

Electron transport chain

IMM:

Inner mitochondrial membrane

SIM:

Structured illumination microscopy

ΔmΦ:

Mitochondrial membrane potential

ER:

Endoplasmic reticulum

mPTP:

Mitochondrial permeability transition pore

LLLT:

Low‐level light therapy

References

  1. Chung H, Dai T, Sharma SK, Huang YY, Carroll JD, Hamblin MR (2012) The nuts and bolts of low-level laser (light) therapy. Ann Biomed Eng 40(2):516–533. https://doi.org/10.1007/s10439-011-0454-7

    Article  PubMed  Google Scholar 

  2. Yun SH, Kwok SJJ (2017) Light in diagnosis, therapy and surgery. Nat Biomed Eng 1:0008. https://doi.org/10.1038/s41551-016-0008

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  3. Hamblin MR (2017) Mechanisms and applications of the anti-inflammatory effects of photobiomodulation. AIMS Biophys 4(3):337–361. https://doi.org/10.3934/biophy.2017.3.337

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  4. Chow RT, Johnson MI, Lopes-Martins RA, Bjordal JM (2009) 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. https://doi.org/10.1016/S0140-6736(09)61522-1

    Article  PubMed  Google Scholar 

  5. Arany PR, Cho A, Hunt TD, Sidhu G, Shin K, Hahm E, Huang GX, Weaver J, Chen AC, Padwa BL, Hamblin MR, Barcellos-Hoff MH, Kulkarni AB, Mooney DJ (2014) Photoactivation of endogenous latent transforming growth factor-beta1 directs dental stem cell differentiation for regeneration. Sci Transl Med 6(238):238ra269. https://doi.org/10.1126/scitranslmed.3008234

    Article  CAS  Google Scholar 

  6. Eells JT, Henry MM, Summerfelt P, Wong-Riley MT, Buchmann EV, Kane M, Whelan NT, Whelan HT (2003) Therapeutic photobiomodulation for methanol-induced retinal toxicity. Proc Natl Acad Sci USA 100(6):3439–3444. https://doi.org/10.1073/pnas.0534746100

    Article  CAS  PubMed  Google Scholar 

  7. de Sousa MVP, Kawakubo M, Ferraresi C, Kaippert B, Yoshimura EM, Hamblin MR (2018) Pain management using photobiomodulation: mechanisms, location, and repeatability quantified by pain threshold and neural biomarkers in mice. J Biophotonics 11(7):e201700370. https://doi.org/10.1002/jbio.201700370(UNSP e201700370)

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  8. Santos L, Olmo-Aguado SD, Valenzuela PL, Winge K, Iglesias-Soler E, Arguelles-Luis J, Alvarez-Valle S, Parcero-Iglesias GJ, Fernandez-Martinez A, Lucia A (2019) Photobiomodulation in Parkinson’s disease: a randomized controlled trial. Brain Stimul 12(3):810–812. https://doi.org/10.1016/j.brs.2019.02.009

    Article  PubMed  Google Scholar 

  9. Lavery LA, Murdoch DP, Williams J, Lavery DC (2008) Does anodyne light therapy improve peripheral neuropathy in diabetes? A double-blind, sham-controlled, randomized trial to evaluate monochromatic infrared photoenergy. Diabetes Care 31(2):316–321. https://doi.org/10.2337/dc07-1794

    Article  PubMed  Google Scholar 

  10. Arnall DA, Nelson AG, Lopez L, Sanz N, Iversen L, Sanz I, Stambaugh L, Arnall SB (2006) The restorative effects of pulsed infrared light therapy on significant loss of peripheral protective sensation in patients with long-term type 1 and type 2 diabetes mellitus. Acta Diabetol 43(1):26–33. https://doi.org/10.1007/s00592-006-0207-5

    Article  CAS  PubMed  Google Scholar 

  11. Brosseau L, Robinson V, Wells G, Debie R, Gam A, Harman K, Morin M, Shea B, Tugwell P (2005) Low level laser therapy (Classes I, II and III) for treating rheumatoid arthritis. Cochrane Database Syst Rev. https://doi.org/10.1002/14651858.cd002049.pub2

    Article  PubMed  Google Scholar 

  12. Huang Z, Ma J, Chen J, Shen B, Pei F, Kraus VB (2015) The effectiveness of low-level laser therapy for nonspecific chronic low back pain: a systematic review and meta-analysis. Arthritis Res Ther 17:360. https://doi.org/10.1186/s13075-015-0882-0

    Article  PubMed  PubMed Central  Google Scholar 

  13. Yousefi-Nooraie R, Schonstein E, Heidari K, Rashidian A, Pennick V, Akbari-Kamrani M, Irani S, Shakiba B, Mortaz Hejri SA, Mortaz Hejri SO, Jonaidi A (2008) Low level laser therapy for nonspecific low-back pain. Cochrane Database Syst Rev. https://doi.org/10.1002/14651858.cd005107.pub4

    Article  PubMed  Google Scholar 

  14. Smolkova B, Uzhytchak M, Lynnyk A, Kubinova S, Dejneka A, Lunov O (2019) A critical review on selected external physical cues and modulation of cell behavior: magnetic nanoparticles, non-thermal plasma and lasers. J Funct Biomater 10(1):2. https://doi.org/10.3390/jfb10010002

    Article  CAS  Google Scholar 

  15. Henderson TA, Morries LD (2015) Near-infrared photonic energy penetration: can infrared phototherapy effectively reach the human brain? Neuropsych Dis Treat 11:2191–2208. https://doi.org/10.2147/Ndt.S78182

    Article  CAS  Google Scholar 

  16. Denton ML, Foltz MS, Estlack LE, Stolarski DJ, Noojin GD, Thomas RJ, Eikum D, Rockwell BA (2006) Damage thresholds for exposure to NIR and blue lasers in an in vitro RPE cell system. Invest Ophthalmol Vis Sci 47(7):3065–3073. https://doi.org/10.1167/iovs.05-1066

    Article  PubMed  Google Scholar 

  17. Yarmolenko PS, Moon EJ, Landon C, Manzoor A, Hochman DW, Viglianti BL, Dewhirst MW (2011) Thresholds for thermal damage to normal tissues: an update. Int J Hyperthermia 27(4):320–343. https://doi.org/10.3109/02656736.2010.534527

    Article  PubMed  PubMed Central  Google Scholar 

  18. Wu S, Xing D, Gao X, Chen WR (2009) High fluence low-power laser irradiation induces mitochondrial permeability transition mediated by reactive oxygen species. J Cell Physiol 218(3):603–611. https://doi.org/10.1002/jcp.21636

    Article  CAS  PubMed  Google Scholar 

  19. Waldchen S, Lehmann J, Klein T, van de Linde S, Sauer M (2015) Light-induced cell damage in live-cell super-resolution microscopy. Sci Rep 5:15348. https://doi.org/10.1038/srep15348

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  20. Golovynska I, Golovynskyi S, Stepanov YV, Garmanchuk LV, Stepanova LI, Qu J, Ohulchanskyy TY (2019) Red and near-infrared light induces intracellular Ca(2+) flux via the activation of glutamate N-methyl-d-aspartate receptors. J Cell Physiol 234:15989–16002. https://doi.org/10.1002/jcp.28257

    Article  CAS  Google Scholar 

  21. Lynnyk A, Lunova M, Jirsa M, Egorova D, Kulikov A, Kubinova S, Lunov O, Dejneka A (2018) Manipulating the mitochondria activity in human hepatic cell line Huh7 by low-power laser irradiation. Biomed Opt Express 9(3):1283–1300. https://doi.org/10.1364/BOE.9.001283

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  22. Zein R, Selting W, Hamblin MR (2018) Review of light parameters and photobiomodulation efficacy: dive into complexity. J Biomed Opt 23(12):1–17. https://doi.org/10.1117/1.JBO.23.12.120901

    Article  PubMed  Google Scholar 

  23. Wu S, Zhou F, Wei Y, Chen WR, Chen Q, Xing D (2014) Cancer phototherapy via selective photoinactivation of respiratory chain oxidase to trigger a fatal superoxide anion burst. Antioxid Redox Signal 20(5):733–746. https://doi.org/10.1089/ars.2013.5229

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  24. Schermelleh L, Ferrand A, Huser T, Eggeling C, Sauer M, Biehlmaier O, Drummen GPC (2019) Super-resolution microscopy demystified. Nat Cell Biol 21(1):72–84. https://doi.org/10.1038/s41556-018-0251-8

    Article  CAS  PubMed  Google Scholar 

  25. Sahl SJ, Hell SW, Jakobs S (2017) Fluorescence nanoscopy in cell biology. Nat Rev Mol Cell Biol 18(11):685–701. https://doi.org/10.1038/nrm.2017.71

    Article  CAS  PubMed  Google Scholar 

  26. Artifacts of light (2013) Nat Methods 10(12):1135. https://doi.org/10.1038/nmeth.2760

    Article  CAS  Google Scholar 

  27. Passarella S, Casamassima E, Molinari S, Pastore D, Quagliariello E, Catalano IM, Cingolani A (1984) Increase of proton electrochemical potential and ATP synthesis in rat liver mitochondria irradiated in vitro by helium-neon laser. FEBS Lett 175(1):95–99

    Article  CAS  Google Scholar 

  28. Karu TI, Pyatibrat LV, Kolyakov SF, Afanasyeva NI (2005) Absorption measurements of a cell monolayer relevant to phototherapy: reduction of cytochrome c oxidase under near IR radiation. J Photochem Photobiol, B 81(2):98–106. https://doi.org/10.1016/j.jphotobiol.2005.07.002

    Article  CAS  Google Scholar 

  29. Lim KS, Harun SW, Arof H, Ahmad H (2012) Fabrication and applications of microfiber. Sel Top Opt Fiber Technol. https://doi.org/10.5772/2429

    Article  Google Scholar 

  30. Papadopoulos NG, Dedoussis GV, Spanakos G, Gritzapis AD, Baxevanis CN, Papamichail M (1994) An improved fluorescence assay for the determination of lymphocyte-mediated cytotoxicity using flow cytometry. J Immunol Methods 177(1–2):101–111. https://doi.org/10.1016/0022-1759(94)90147-3

    Article  CAS  PubMed  Google Scholar 

  31. Smolkova B, Lunova M, Lynnyk A, Uzhytchak M, Churpita O, Jirsa M, Kubinova S, Lunov O, Dejneka A (2019) Non-thermal plasma, as a new physicochemical source, to induce redox imbalance and subsequent cell death in liver cancer cell lines. Cell Physiol Biochem 52(1):119–140. https://doi.org/10.33594/000000009

    Article  CAS  PubMed  Google Scholar 

  32. Lunova M, Prokhorov A, Jirsa M, Hof M, Olzynska A, Jurkiewicz P, Kubinova S, Lunov O, Dejneka A (2017) Nanoparticle core stability and surface functionalization drive the mTOR signaling pathway in hepatocellular cell lines. Sci Rep 7(1):16049. https://doi.org/10.1038/s41598-017-16447-6

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  33. Smiley ST, Reers M, Mottola-Hartshorn C, Lin M, Chen A, Smith TW, Steele GD Jr, Chen LB (1991) Intracellular heterogeneity in mitochondrial membrane potentials revealed by a J-aggregate-forming lipophilic cation JC-1. Proc Natl Acad Sci USA 88(9):3671–3675. https://doi.org/10.1073/pnas.88.9.3671

    Article  CAS  PubMed  Google Scholar 

  34. Zuliani T, Duval R, Jayat C, Schnebert S, Andre P, Dumas M, Ratinaud MH (2003) 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 54(2):100–108. https://doi.org/10.1002/cyto.a.10059

    Article  PubMed  Google Scholar 

  35. Wubbolts R, Fernandez-Borja M, Oomen L, Verwoerd D, Janssen H, Calafat J, Tulp A, Dusseljee S, Neefjes J (1996) Direct vesicular transport of MHC class II molecules from lysosomal structures to the cell surface. J Cell Biol 135(3):611–622. https://doi.org/10.1083/jcb.135.3.611

    Article  CAS  PubMed  Google Scholar 

  36. Beriault DR (1833) Werstuck GH (2013) Detection and quantification of endoplasmic reticulum stress in living cells using the fluorescent compound. Thioflavin T. Bba-Mol Cell Res 10:2293–2301. https://doi.org/10.1016/j.bbamcr.2013.05.020

    Article  CAS  Google Scholar 

  37. Hom JR, Quintanilla RA, Hoffman DL, de Mesy Bentley KL, Molkentin JD, Sheu SS, Porter GA Jr (2011) The permeability transition pore controls cardiac mitochondrial maturation and myocyte differentiation. Dev Cell 21(3):469–478. https://doi.org/10.1016/j.devcel.2011.08.008

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  38. Petronilli V, Miotto G, Canton M, Brini M, Colonna R, Bernardi P, Di Lisa F (1999) Transient and long-lasting openings of the mitochondrial permeability transition pore can be monitored directly in intact cells by changes in mitochondrial calcein fluorescence. Biophys J 76(2):725–734. https://doi.org/10.1016/S0006-3495(99)77239-5

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  39. Bernardi P, Rasola A, Forte M, Lippe G (2015) The mitochondrial permeability transition pore: channel formation by F-ATP synthase, integration in signal transduction, and role in pathophysiology. Physiol Rev 95(4):1111–1155. https://doi.org/10.1152/physrev.00001.2015

    Article  PubMed  PubMed Central  Google Scholar 

  40. Lunov O, Zablotskii V, Churpita O, Lunova M, Jirsa M, Dejneka A, Kubinova S (2017) Chemically different non-thermal plasmas target distinct cell death pathways. Sci Rep 7(1):600. https://doi.org/10.1038/s41598-017-00689-5

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  41. Lunov O, Syrovets T, Rocker C, Tron K, Nienhaus GU, Rasche V, Mailander V, Landfester K, Simmet T (2010) Lysosomal degradation of the carboxydextran shell of coated superparamagnetic iron oxide nanoparticles and the fate of professional phagocytes. Biomaterials 31(34):9015–9022. https://doi.org/10.1016/j.biomaterials.2010.08.003

    Article  CAS  PubMed  Google Scholar 

  42. Wang NS, Unkila MT, Reineks EZ, Distelhorst CW (2001) Transient expression of wild-type or mitochondrially targeted Bcl-2 induces apoptosis, whereas transient expression of endoplasmic reticulum-targeted Bcl-2 is protective against Bax-induced cell death. J Biol Chem 276(47):44117–44128. https://doi.org/10.1074/jbc.M101958200

    Article  CAS  PubMed  Google Scholar 

  43. Hamilton N (2009) Quantification and its applications in fluorescent microscopy imaging. Traffic 10(8):951–961. https://doi.org/10.1111/j.1600-0854.2009.00938.x

    Article  CAS  PubMed  Google Scholar 

  44. Dell RB, Holleran S, Ramakrishnan R (2002) Sample size determination. ILAR J 43(4):207–213. https://doi.org/10.1093/ilar.43.4.207

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  45. Landes T, Martinou JC (2011) Mitochondrial outer membrane permeabilization during apoptosis: the role of mitochondrial fission. Biochim Biophys Acta 1813(4):540–545. https://doi.org/10.1016/j.bbamcr.2011.01.021

    Article  CAS  PubMed  Google Scholar 

  46. Mishra P, Chan DC (2016) Metabolic regulation of mitochondrial dynamics. J Cell Biol 212(4):379–387. https://doi.org/10.1083/jcb.201511036

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  47. Hayashi S (2016) Resolution doubling using confocal microscopy via analogy with structured illumination microscopy. Jpn J Appl Phys 55(8):082501. https://doi.org/10.7567/jjap.55.082501(Artn 082501)

    Article  Google Scholar 

  48. Hayashi S, Okada Y (2015) Ultrafast superresolution fluorescence imaging with spinning disk confocal microscope optics. Mol Biol Cell 26(9):1743–1751. https://doi.org/10.1091/mbc.E14-08-1287

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  49. Martin SJ, Reutelingsperger CPM, Mcgahon AJ, Rader JA, Vanschie RCAA, Laface DM, Green DR (1995) 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. https://doi.org/10.1084/jem.182.5.1545

    Article  CAS  PubMed  Google Scholar 

  50. Hoek JB, Cahill A, Pastorino JG (2002) Alcohol and mitochondria: a dysfunctional relationship. Gastroenterology 122(7):2049–2063. https://doi.org/10.1053/gast.2002.33613

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  51. Kinnally KW, Peixoto PM, Ryu SY, Dejean LM (2011) Is mPTP the gatekeeper for necrosis, apoptosis, or both? Biochim Biophys Acta 1813(4):616–622. https://doi.org/10.1016/j.bbamcr.2010.09.013

    Article  CAS  PubMed  Google Scholar 

  52. Malhotra JD, Kaufman RJ (2011) ER stress and its functional link to mitochondria: role in cell survival and death. Cold Spring Harb Perspect Biol 3(9):a004424. https://doi.org/10.1101/cshperspect.a004424

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  53. Boya P, Cohen I, Zamzami N, Vieira HL, Kroemer G (2002) Endoplasmic reticulum stress-induced cell death requires mitochondrial membrane permeabilization. Cell Death Differ 9(4):465–467. https://doi.org/10.1038/sj/cdd/4401006

    Article  CAS  PubMed  Google Scholar 

  54. Boya P, Andreau K, Poncet D, Zamzami N, Perfettini JL, Metivier D, Ojcius DM, Jaattela M, Kroemer G (2003) Lysosomal membrane permeabilization induces cell death in a mitochondrion-dependent fashion. J Exp Med 197(10):1323–1334. https://doi.org/10.1084/jem.20021952

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  55. Lim CY, Zoncu R (2016) The lysosome as a command-and-control center for cellular metabolism. J Cell Biol 214(6):653–664. https://doi.org/10.1083/jcb.201607005

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  56. Wang M, Kaufman RJ (2016) Protein misfolding in the endoplasmic reticulum as a conduit to human disease. Nature 529(7586):326–335. https://doi.org/10.1038/nature17041

    Article  CAS  PubMed  Google Scholar 

  57. Dikalova AE, Bikineyeva AT, Budzyn K, Nazarewicz RR, McCann L, Lewis W, Harrison DG, Dikalov SI (2010) Therapeutic targeting of mitochondrial superoxide in hypertension. Circ Res 107(1):106–116. https://doi.org/10.1161/CIRCRESAHA.109.214601

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  58. Ni R, Cao T, Xiong S, Ma J, Fan GC, Lacefield JC, Lu Y, Le Tissier S, Peng T (2016) Therapeutic inhibition of mitochondrial reactive oxygen species with mito-TEMPO reduces diabetic cardiomyopathy. Free Radic Biol Med 90:12–23. https://doi.org/10.1016/j.freeradbiomed.2015.11.013

    Article  CAS  PubMed  Google Scholar 

  59. Liang HL, Sedlic F, Bosnjak Z, Nilakantan V (2010) SOD1 and MitoTEMPO partially prevent mitochondrial permeability transition pore opening, necrosis, and mitochondrial apoptosis after ATP depletion recovery. Free Radic Biol Med 49(10):1550–1560. https://doi.org/10.1016/j.freeradbiomed.2010.08.018

    Article  CAS  PubMed  Google Scholar 

  60. Liu M, Liu H, Dudley SC Jr (2010) Reactive oxygen species originating from mitochondria regulate the cardiac sodium channel. Circ Res 107(8):967–974. https://doi.org/10.1161/CIRCRESAHA.110.220673

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  61. Huttemann M, Helling S, Sanderson TH, Sinkler C, Samavati L, Mahapatra G, Varughese A, Lu GR, Liu J, Ramzan R, Vogt S, Grossman LI, Doan JW, Marcus K (1817) Lee I (2012) Regulation of mitochondrial respiration and apoptosis through cell signaling: cytochrome c oxidase and cytochrome c in ischemia/reperfusion injury and inflammation. Biochim Biophys Acta-Bioenerg 4:598–609. https://doi.org/10.1016/j.bbabio.2011.07.001

    Article  CAS  Google Scholar 

  62. Sazanov LA (2015) A giant molecular proton pump: structure and mechanism of respiratory complex I. Nat Rev Mol Cell Biol 16(6):375–388. https://doi.org/10.1038/nrm3997

    Article  CAS  PubMed  Google Scholar 

  63. Pearce LL, Bominaar EL, Hill BC, Peterson J (2003) Reversal of cyanide inhibition of cytochrome c oxidase by the auxiliary substrate nitric oxide: an endogenous antidote to cyanide poisoning? J Biol Chem 278(52):52139–52145. https://doi.org/10.1074/jbc.M310359200

    Article  CAS  PubMed  Google Scholar 

  64. Oliva CR, Markert T, Ross LJ, White EL, Rasmussen L, Zhang W, Everts M, Moellering DR, Bailey SM, Suto MJ, Griguer CE (2016) Identification of small molecule inhibitors of human cytochrome c oxidase that target chemoresistant glioma cells. J Biol Chem 291(46):24188–24199. https://doi.org/10.1074/jbc.M116.749978

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  65. Casarin A, Giorgi G, Pertegato V, Siviero R, Cerqua C, Doimo M, Basso G, Sacconi S, Cassina M, Rizzuto R, Brosel S, Dimauro S, Schon EA, Clementi M, Trevisson E, Salviati L (2012) Copper and bezafibrate cooperate to rescue cytochrome c oxidase deficiency in cells of patients with SCO2 mutations. Orphanet J Rare Dis 7:21. https://doi.org/10.1186/1750-1172-7-21

    Article  PubMed  PubMed Central  Google Scholar 

  66. Yatsuga S, Suomalainen A (2012) Effect of bezafibrate treatment on late-onset mitochondrial myopathy in mice. Hum Mol Genet 21(3):526–535. https://doi.org/10.1093/hmg/ddr482

    Article  CAS  PubMed  Google Scholar 

  67. Bastin J, Aubey F, Rotig A, Munnich A, Djouadi F (2008) Activation of peroxisome proliferator-activated receptor pathway stimulates the mitochondrial respiratory chain and can correct deficiencies in patients’ cells lacking its components. J Clin Endocrinol Metab 93(4):1433–1441. https://doi.org/10.1210/jc.2007-1701

    Article  CAS  PubMed  Google Scholar 

  68. Vaseva AV, Moll UM (2009) The mitochondrial p53 pathway. Biochim Biophys Acta 1787(5):414–420. https://doi.org/10.1016/j.bbabio.2008.10.005

    Article  CAS  PubMed  Google Scholar 

  69. Haupt S, Berger M, Goldberg Z, Haupt Y (2003) Apoptosis - the p53 network. J Cell Sci 116(Pt 20):4077–4085. https://doi.org/10.1242/jcs.00739

    Article  CAS  PubMed  Google Scholar 

  70. Kale J, Osterlund EJ, Andrews DW (2018) BCL-2 family proteins: changing partners in the dance towards death. Cell Death Differ 25(1):65–80. https://doi.org/10.1038/cdd.2017.186

    Article  CAS  PubMed  Google Scholar 

  71. Montero J, Letai A (2018) Why do BCL-2 inhibitors work and where should we use them in the clinic? Cell Death Differ 25(1):56–64. https://doi.org/10.1038/cdd.2017.183

    Article  CAS  PubMed  Google Scholar 

  72. Koczor CA, Torres RA, Fields EJ, Boyd A, Lewis W (2013) Mitochondrial matrix P53 sensitizes cells to oxidative stress. Mitochondrion 13(4):277–281. https://doi.org/10.1016/j.mito.2013.03.001

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  73. Bressac B, Galvin KM, Liang TJ, Isselbacher KJ, Wands JR, Ozturk M (1990) Abnormal structure and expression of p53 gene in human hepatocellular carcinoma. Proc Natl Acad Sci U S A 87(5):1973–1977. https://doi.org/10.1073/pnas.87.5.1973

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  74. Mitchell JK, Midkiff BR, Israelow B, Evans MJ, Lanford RE, Walker CM, Lemon SM, McGivern DR (2017) Hepatitis C virus indirectly disrupts DNA damage-induced p53 responses by activating protein kinase R. MBio 8(2):e00121-00117. https://doi.org/10.1128/mBio.00121-17

    Article  Google Scholar 

  75. Hollville E, Carroll RG, Cullen SP, Martin SJ (2014) Bcl-2 family proteins participate in mitochondrial quality control by regulating Parkin/PINK1-dependent mitophagy. Mol Cell 55(3):451–466. https://doi.org/10.1016/j.molcel.2014.06.001

    Article  CAS  PubMed  Google Scholar 

  76. Shimizu S, Eguchi Y, Kamiike W, Funahashi Y, Mignon A, Lacronique V, Matsuda H, Tsujimoto Y (1998) Bcl-2 prevents apoptotic mitochondrial dysfunction by regulating proton flux. Proc Natl Acad Sci USA 95(4):1455–1459. https://doi.org/10.1073/pnas.95.4.1455

    Article  CAS  PubMed  Google Scholar 

  77. Ni Z, Wang B, Dai X, Ding W, Yang T, Li X, Lewin S, Xu L, Lian J, He F (2014) HCC cells with high levels of Bcl-2 are resistant to ABT-737 via activation of the ROS-JNK-autophagy pathway. Free Radic Biol Med 70:194–203. https://doi.org/10.1016/j.freeradbiomed.2014.02.012

    Article  CAS  PubMed  Google Scholar 

  78. Mirkovic N, Voehringer DW, Story MD, McConkey DJ, McDonnell TJ, Meyn RE (1997) Resistance to radiation-induced apoptosis in Bcl-2-expressing cells is reversed by depleting cellular thiols. Oncogene 15(12):1461–1470. https://doi.org/10.1038/sj.onc.1201310

    Article  CAS  PubMed  Google Scholar 

  79. Kang MH, Reynolds CP (2009) Bcl-2 inhibitors: targeting mitochondrial apoptotic pathways in cancer therapy. Clin Cancer Res 15(4):1126–1132. https://doi.org/10.1158/1078-0432.CCR-08-0144

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  80. Hikita H, Takehara T, Shimizu S, Kodama T, Shigekawa M, Iwase K, Hosui A, Miyagi T, Tatsumi T, Ishida H, Li W, Kanto T, Hiramatsu N, Hayashi N (2010) The Bcl-xL inhibitor, ABT-737, efficiently induces apoptosis and suppresses growth of hepatoma cells in combination with sorafenib. Hepatology 52(4):1310–1321. https://doi.org/10.1002/hep.23836

    Article  CAS  PubMed  Google Scholar 

  81. Wang J, Wei Q, Wang CY, Hill WD, Hess DC, Dong Z (2004) Minocycline up-regulates Bcl-2 and protects against cell death in mitochondria. J Biol Chem 279(19):19948–19954. https://doi.org/10.1074/jbc.M313629200

    Article  CAS  PubMed  Google Scholar 

  82. Susnow N, Zeng LY, Margineantu D, Hockenbery DM (2009) Bcl-2 family proteins as regulators of oxidative stress. Semin Cancer Biol 19(1):42–49. https://doi.org/10.1016/j.semcancer.2008.12.002

    Article  CAS  PubMed  Google Scholar 

  83. Moon J, Yun J, Yoon YD, Park SI, Seo YJ, Park WS, Chu HY, Park KH, Lee MY, Lee CW, Oh SJ, Kwak YS, Jang YP, Kang JS (2017) Blue light effect on retinal pigment epithelial cells by display devices. Integr Biol 9(5):436–443. https://doi.org/10.1039/c7ib00032d

    Article  CAS  Google Scholar 

  84. Marino G, Niso-Santano M, Baehrecke EH, Kroemer G (2014) Self-consumption: the interplay of autophagy and apoptosis. Nat Rev Mol Cell Biol 15(2):81–94. https://doi.org/10.1038/nrm3735

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  85. Ong WK, Chen HF, Tsai CT, Fu YJ, Wong YS, Yen DJ, Chang TH, Huang HD, Lee OK, Chien S, Ho JH (2013) The activation of directional stem cell motility by green light-emitting diode irradiation. Biomaterials 34(8):1911–1920. https://doi.org/10.1016/j.biomaterials.2012.11.065

    Article  CAS  PubMed  Google Scholar 

  86. Wang Y, Huang YY, Wang Y, Lyu P, Hamblin MR (2016) Photobiomodulation (blue and green light) encourages osteoblastic-differentiation of human adipose-derived stem cells: role of intracellular calcium and light-gated ion channels. Sci Rep 6:33719. https://doi.org/10.1038/srep33719

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  87. Mason MG, Nicholls P (1837) Cooper CE (2014) Re-evaluation of the near infrared spectra of mitochondrial cytochrome c oxidase: implications for non invasive in vivo monitoring of tissues. Biochim Biophys Acta 11:1882–1891. https://doi.org/10.1016/j.bbabio.2014.08.005

    Article  CAS  Google Scholar 

  88. Chen E (1993) Inhibition of cytochrome oxidase and blue-light damage in rat retina. Graefes Arch Clin Exp Ophthalmol 231(7):416–423. https://doi.org/10.1007/BF00919652

    Article  CAS  PubMed  Google Scholar 

  89. Chen E, Soderberg PG, Lindstrom B (1992) Cytochrome oxidase activity in rat retina after exposure to 404 nm blue light. Curr Eye Res 11(9):825–831. https://doi.org/10.1111/j.1755-3768.1993.tb08723.x

    Article  CAS  PubMed  Google Scholar 

  90. Godley BF, Shamsi FA, Liang FQ, Jarrett SG, Davies S, Boulton M (2005) Blue light induces mitochondrial DNA damage and free radical production in epithelial cells. J Biol Chem 280(22):21061–21066. https://doi.org/10.1074/jbc.M502194200

    Article  CAS  PubMed  Google Scholar 

  91. King A, Gottlieb E, Brooks DG, Murphy MP, Dunaief JL (2004) Mitochondria-derived reactive oxygen species mediate blue light-induced death of retinal pigment epithelial cells. Photochem Photobiol 79(5):470–475. https://doi.org/10.1111/j.1751-1097.2004.tb00036.x

    Article  CAS  PubMed  Google Scholar 

  92. Hu WP, Wang JJ, Yu CL, Lan CC, Chen GS, Yu HS (2007) Helium-neon laser irradiation stimulates cell proliferation through photostimulatory effects in mitochondria. J Invest Dermatol 127(8):2048–2057. https://doi.org/10.1038/sj.jid.5700826

    Article  CAS  PubMed  Google Scholar 

  93. Karu TI (2010) Multiple roles of cytochrome c oxidase in mammalian cells under action of red and IR-A radiation. IUBMB Life 62(8):607–610. https://doi.org/10.1002/iub.359

    Article  CAS  PubMed  Google Scholar 

  94. Wong-Riley MT, Liang HL, Eells JT, Chance B, Henry MM, Buchmann E, Kane M, Whelan HT (2005) Photobiomodulation directly benefits primary neurons functionally inactivated by toxins: role of cytochrome c oxidase. J Biol Chem 280(6):4761–4771. https://doi.org/10.1074/jbc.M409650200

    Article  CAS  PubMed  Google Scholar 

  95. Gottlieb E, Vander Heiden MG, Thompson CB (2000) Bcl-x(L) prevents the initial decrease in mitochondrial membrane potential and subsequent reactive oxygen species production during tumor necrosis factor alpha-induced apoptosis. Mol Cell Biol 20(15):5680–5689. https://doi.org/10.1128/MCB.20.15.5680-5689.2000

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  96. Crawford MJ, Krishnamoorthy RR, Rudick VL, Collier RJ, Kapin M, Aggarwal BB, Al-Ubaidi MR, Agarwal N (2001) Bcl-2 overexpression protects photooxidative stress-induced apoptosis of photoreceptor cells via NF-kappaB preservation. Biochem Biophys Res Commun 281(5):1304–1312. https://doi.org/10.1006/bbrc.2001.4501

    Article  CAS  PubMed  Google Scholar 

  97. Lum MG, Nagley P (2003) Two phases of signalling between mitochondria during apoptosis leading to early depolarisation and delayed cytochrome c release. J Cell Sci 116(8):1437–1447. https://doi.org/10.1242/jcs.00320

    Article  CAS  PubMed  Google Scholar 

Download references

Acknowledgements

The work is supported by Operational Programme Research, Development and Education financed by European Structural and Investment Funds and the Czech Ministry of Education, Youth and Sports (Project No. SOLID21—CZ.02.1.01/0.0/0.0/16_019/0000760), the Ministry of Science and Higher Education of the Russian Federation, goszadanie no 8.3134.2017/4.6 and MH CZ—DRO Institute for Clinical and Experimental Medicine—IKEM, IN 00023001.

Author information

Authors and Affiliations

Authors

Corresponding author

Correspondence to Oleg Lunov.

Ethics declarations

Conflict of interest

The authors declare no conflicts of interests.

Additional information

Publisher's Note

Springer Nature remains neutral with regard to jurisdictional claims in published maps and institutional affiliations.

Electronic supplementary material

Below is the link to the electronic supplementary material.

Supplementary material 1 (PDF 2169 kb)

Rights and permissions

Reprints and permissions

About this article

Check for updates. Verify currency and authenticity via CrossMark

Cite this article

Lunova, M., Smolková, B., Uzhytchak, M. et al. Light-induced modulation of the mitochondrial respiratory chain activity: possibilities and limitations. Cell. Mol. Life Sci. 77, 2815–2838 (2020). https://doi.org/10.1007/s00018-019-03321-z

Download citation

  • Received:

  • Revised:

  • Accepted:

  • Published:

  • Issue Date:

  • DOI: https://doi.org/10.1007/s00018-019-03321-z

Keywords

Navigation