DOI QR코드

DOI QR Code

Proposed Mechanisms of Photobiomodulation (PBM) Mediated via the Stimulation of Mitochondrial Activity in Peripheral Nerve Injuries

  • Choi, Ji Eun (Department of Otorhinolaryngology-Head and Neck Surgery, Dankook University Hospital)
  • 투고 : 2021.08.02
  • 심사 : 2021.09.24
  • 발행 : 2021.12.31

초록

Evidence shows that nerve injury triggers mitochondrial dysfunction during axonal degeneration. Mitochondria play a pivotal role in axonal regeneration. Therefore, normalizing mitochondrial energy metabolism may represent an elective therapeutic strategy contributing to nerve recovery after damage. Photobiomodulation (PBM) induces a photobiological effect by stimulating mitochondrial activity. An increasing body of evidence demonstrates that PBM improves ATP generation and modulates many of the secondary mediators [reactive oxygen species (ROS), nitric oxide (NO), cyclic adenosine monophosphate (cAMP), and calcium ions (Ca2+)], which in turn activate multiple pathways involved in axonal regeneration.

키워드

과제정보

This work was supported by a National Research Foundation of Korea (NRF) grant funded by the Korean government (MSIT) (no. NRF-2020R1C1C1009849).

참고문헌

  1. Han SM, Baig HS, Hammarlund M. Mitochondria localize to injured axons to support regeneration. Neuron 2016;92:1308-23. https://doi.org/10.1016/j.neuron.2016.11.025
  2. Cheng XT, Sheng ZH. Developmental regulation of microtubule-based trafficking and anchoring of axonal mitochondria in health and diseases. Dev Neurobiol 2021;81:284-99. https://doi.org/10.1002/dneu.22748
  3. Morris RL, Hollenbeck PJ. The regulation of bidirectional mitochondrial transport is coordinated with axonal outgrowth. J Cell Sci 1993;104(Pt 3):917-27. https://doi.org/10.1242/jcs.104.3.917
  4. Tao K, Matsuki N, Koyama R. AMP-activated protein kinase mediates activity-dependent axon branching by recruiting mitochondria to axon. Dev Neurobiol 2014;74:557-73. https://doi.org/10.1002/dneu.22149
  5. Ravera S, Colombo E, Pasquale C, Benedicenti S, Solimei L, Signore A, et al. Mitochondrial bioenergetic, photobiomodulation and trigeminal branches nerve damage, what's the connection? A review. Int J Mol Sci 2021;22:4347. https://doi.org/10.3390/ijms22094347
  6. Bathini M, Raghushaker CR, Mahato KK. The molecular mechanisms of action of photobiomodulation against neurodegenerative diseases: a systematic review. Cell Mol Neurobiol. In press 2020.
  7. Neukomm LJ, Burdett TC, Seeds AM, Hampel S, Coutinho-Budd JC, Farley JE, et al. Axon death pathways converge on Axundead to promote functional and structural axon disassembly. Neuron 2017;95:78-91.e5. https://doi.org/10.1016/j.neuron.2017.06.031
  8. Court FA, Coleman MP. Mitochondria as a central sensor for axonal degenerative stimuli. Trends Neurosci 2012;35:364-72. https://doi.org/10.1016/j.tins.2012.04.001
  9. Sheng ZH, Cai Q. Mitochondrial transport in neurons: impact on synaptic homeostasis and neurodegeneration. Nat Rev Neurosci 2012;13:77-93. https://doi.org/10.1038/nrn3156
  10. Geden MJ, Deshmukh M. Axon degeneration: context defines distinct pathways. Curr Opin Neurobiol 2016;39:108-15. https://doi.org/10.1016/j.conb.2016.05.002
  11. Lin MT, Beal MF. Mitochondrial dysfunction and oxidative stress in neurodegenerative diseases. Nature 2006;443:787-95. https://doi.org/10.1038/nature05292
  12. Baloh RH, Schmidt RE, Pestronk A, Milbrandt J. Altered axonal mitochondrial transport in the pathogenesis of Charcot-Marie-Tooth disease from mitofusin 2 mutations. J Neurosci 2007;27:422-30. https://doi.org/10.1523/JNEUROSCI.4798-06.2007
  13. Lenaz G, Genova ML. Structure and organization of mitochondrial respiratory complexes: a new understanding of an old subject. Antioxid Redox Signal 2010;12:961-1008. https://doi.org/10.1089/ars.2009.2704
  14. Pirahanchi Y, Jessu R, Aeddula NR. Physiology, sodium potassium pump. Treasure Island: StatPearls Publishing; 2021.
  15. Lim TK, Rone MB, Lee S, Antel JP, Zhang J. Mitochondrial and bioenergetic dysfunction in trauma-induced painful peripheral neuropathy. Mol Pain 2015;11:58. https://doi.org/10.1186/s12990-015-0057-7
  16. Demine S, Renard P, Arnould T. Mitochondrial uncoupling: a key controller of biological processes in physiology and diseases. Cells 2019;8:795. https://doi.org/10.3390/cells8080795
  17. Lippe G, Coluccino G, Zancani M, Baratta W, Crusiz P. Mitochondrial F-ATP synthase and its transition into an energy-dissipating molecular machine. Oxid Med Cell Longev 2019;2019:8743257. https://doi.org/10.1155/2019/8743257
  18. Murphy MP. How mitochondria produce reactive oxygen species. Biochem J 2009;417:1-13. https://doi.org/10.1042/BJ20081386
  19. Giorgio M, Trinei M, Migliaccio E, Pelicci PG. Hydrogen peroxide: a metabolic by-product or a common mediator of ageing signals? Nat Rev Mol Cell Biol 2007;8:722-8. https://doi.org/10.1038/nrm2240
  20. Venditti P, Di Stefano L, Di Meo S. Mitochondrial metabolism of reactive oxygen species. Mitochondrion 2013;13:71-82. https://doi.org/10.1016/j.mito.2013.01.008
  21. Murphy MP. Mitochondrial dysfunction indirectly elevates ROS production by the endoplasmic reticulum. Cell Metab 2013;18:145-6. https://doi.org/10.1016/j.cmet.2013.07.006
  22. Solleiro-Villavicencio H, Rivas-Arancibia S. Effect of chronic oxidative stress on neuroinflammatory response mediated by CD4+T cells in neurodegenerative diseases. Front Cell Neurosci 2018;12:114. https://doi.org/10.3389/fncel.2018.00114
  23. Tiwari BS, Belenghi B, Levine A. Oxidative stress increased respiration and generation of reactive oxygen species, resulting in ATP depletion, opening of mitochondrial permeability transition, and programmed cell death. Plant Physiol 2002;128:1271-81. https://doi.org/10.1104/pp.010999
  24. Liemburg-Apers DC, Willems PH, Koopman WJ, Grefte S. Interactions between mitochondrial reactive oxygen species and cellular glucose metabolism. Arch Toxicol 2015;89:1209-26. https://doi.org/10.1007/s00204-015-1520-y
  25. Rizzuto R, De Stefani D, Raffaello A, Mammucari C. Mitochondria as sensors and regulators of calcium signalling. Nat Rev Mol Cell Biol 2012;13:566-78. https://doi.org/10.1038/nrm3412
  26. Lee S, Min KT. The interface between ER and mitochondria: molecular compositions and functions. Mol Cells 2018;41:1000-7. https://doi.org/10.14348/molcells.2018.0438
  27. O'Donnell KC, Vargas ME, Sagasti A. WldS and PGC-1α regulate mitochondrial transport and oxidation state after axonal injury. J Neurosci 2013;33:14778-90. https://doi.org/10.1523/JNEUROSCI.1331-13.2013
  28. Wang Y, Zhao D, Pan B, Song Z, Shah SZA, Yin X, et al. Death receptor 6 and caspase-6 regulate prion peptide-induced axonal degeneration in rat spinal neurons. J Mol Neurosci 2015;56:966-76. https://doi.org/10.1007/s12031-015-0562-1
  29. Conforti L, Tarlton A, Mack TG, Mi W, Buckmaster EA, Wagner D, et al. A Ufd2/D4Cole1e chimeric protein and overexpression of Rbp7 in the slow Wallerian degeneration (WldS) mouse. Proc Natl Acad Sci U S A 2000;97:11377-82. https://doi.org/10.1073/pnas.97.21.11377
  30. Press C, Milbrandt J. Nmnat delays axonal degeneration caused by mitochondrial and oxidative stress. J Neurosci 2008;28:4861-71. https://doi.org/10.1523/JNEUROSCI.0525-08.2008
  31. Yahata N, Yuasa S, Araki T. Nicotinamide mononucleotide adenylyltransferase expression in mitochondrial matrix delays Wallerian degeneration. J Neurosci 2009;29:6276-84. https://doi.org/10.1523/JNEUROSCI.4304-08.2009
  32. Avery MA, Rooney TM, Pandya JD, Wishart TM, Gillingwater TH, Geddes JW, et al. WldS prevents axon degeneration through increased mitochondrial flux and enhanced mitochondrial Ca2+ buffering. Curr Biol 2012;22:596-600. https://doi.org/10.1016/j.cub.2012.02.043
  33. Fang Y, Soares L, Teng X, Geary M, Bonini NM. A novel Drosophila model of nerve injury reveals an essential role of Nmnat in maintaining axonal integrity. Curr Biol 2012;22:590-5. https://doi.org/10.1016/j.cub.2012.01.065
  34. Adalbert R, Morreale G, Paizs M, Conforti L, Walker SA, Roderick HL, et al. Intra-axonal calcium changes after axotomy in wild-type and slow Wallerian degeneration axons. Neuroscience 2012;225:44-54. https://doi.org/10.1016/j.neuroscience.2012.08.056
  35. Ma M, Ferguson TA, Schoch KM, Li J, Qian Y, Shofer FS, et al. Calpains mediate axonal cytoskeleton disintegration during Wallerian degeneration. Neurobiol Dis 2013;56:34-46. https://doi.org/10.1016/j.nbd.2013.03.009
  36. Yang J, Wu Z, Renier N, Simon DJ, Uryu K, Park DS, et al. Pathological axonal death through a MAPK cascade that triggers a local energy deficit. Cell 2015;160:161-76. https://doi.org/10.1016/j.cell.2014.11.053
  37. Gerdts J, Summers DW, Milbrandt J, DiAntonio A. Axon self-destruction: new links among SARM1, MAPKs, and NAD+ metabolism. Neuron 2016;89:449-60. https://doi.org/10.1016/j.neuron.2015.12.023
  38. Osterloh JM, Yang J, Rooney TM, Fox AN, Adalbert R, Powell EH, et al. dSarm/Sarm1 is required for activation of an injury-induced axon death pathway. Science 2012;337:481-4. https://doi.org/10.1126/science.1223899
  39. Gerdts J, Brace EJ, Sasaki Y, DiAntonio A, Milbrandt J. SARM1 activation triggers axon degeneration locally via NAD+ destruction. Science 2015;348:453-7. https://doi.org/10.1126/science.1258366
  40. Wang J, Zhai Q, Chen Y, Lin E, Gu W, McBurney MW, et al. A local mechanism mediates NAD-dependent protection of axon degeneration. J Cell Biol 2005;170:349-55. https://doi.org/10.1083/jcb.200504028
  41. Cavalli V, Kujala P, Klumperman J, Goldstein LS. Sunday Driver links axonal transport to damage signaling. J Cell Biol 2005;168:775-87. https://doi.org/10.1083/jcb.200410136
  42. Xiong T, Tang J, Zhao J, Chen H, Zhao F, Li J, et al. Involvement of the Akt/GSK-3β/CRMP-2 pathway in axonal injury after hypoxic-ischemic brain damage in neonatal rat. Neuroscience 2012;216:123-32. https://doi.org/10.1016/j.neuroscience.2012.04.052
  43. Loreto A, Di Stefano M, Gering M, Conforti L. Wallerian degeneration is executed by an NMN-SARM1-dependent late Ca2+ influx but only modestly influenced by mitochondria. Cell Rep 2015;13:2539-52. https://doi.org/10.1016/j.celrep.2015.11.032
  44. Kuo CC, Su HL, Chang TL, Chiang CY, Sheu ML, Cheng FC, et al. Prevention of axonal degeneration by perineurium injection of mitochondria in a sciatic nerve crush injury model. Neurosurgery 2017;80:475-88. https://doi.org/10.1093/neuros/nyw090
  45. Zhou B, Yu P, Lin MY, Sun T, Chen Y, Sheng ZH. Facilitation of axon regeneration by enhancing mitochondrial transport and rescuing energy deficits. J Cell Biol 2016;214:103-19. https://doi.org/10.1083/jcb.201605101
  46. Kiryu-Seo S, Tamada H, Kato Y, Yasuda K, Ishihara N, Nomura M, et al. Mitochondrial fission is an acute and adaptive response in injured motor neurons. Sci Rep 2016;6:28331. https://doi.org/10.1038/srep28331
  47. Prior R, Van Helleputte L, Benoy V, Van Den Bosch L. Defective axonal transport: a common pathological mechanism in inherited and acquired peripheral neuropathies. Neurobiol Dis 2017;105:300-20. https://doi.org/10.1016/j.nbd.2017.02.009
  48. Mahar M, Cavalli V. Intrinsic mechanisms of neuronal axon regeneration. Nat Rev Neurosci 2018;19:323-37. https://doi.org/10.1038/s41583-018-0001-8
  49. Hwang J, Namgung U. Phosphorylation of STAT3 by axonal Cdk5 promotes axonal regeneration by modulating mitochondrial activity. Exp Neurol 2021;335:113511. https://doi.org/10.1016/j.expneurol.2020.113511
  50. Szczepanek K, Chen Q, Derecka M, Salloum FN, Zhang Q, Szelag M, et al. Mitochondrial-targeted Signal transducer and activator of transcription 3 (STAT3) protects against ischemia-induced changes in the electron transport chain and the generation of reactive oxygen species. J Biol Chem 2011;286:29610-20. https://doi.org/10.1074/jbc.M111.226209
  51. Hamblin MR. Mechanisms and mitochondrial redox signaling in photobiomodulation. Photochem Photobiol 2018;94:199-212. https://doi.org/10.1111/php.12864
  52. Hamblin MR. Shining light on the head: photobiomodulation for brain disorders. BBA Clin 2016;6:113-24. https://doi.org/10.1016/j.bbacli.2016.09.002
  53. Wong-Riley MT, Liang HL, Eells JT, Chance B, Henry MM, Buchmann E, et al. Photobiomodulation directly benefits primary neurons functionally inactivated by toxins: role of cytochrome c oxidase. J Biol Chem 2005;280:4761-71. https://doi.org/10.1074/jbc.M409650200
  54. Lee JH, Carpena NT, Kim S, Lee MY, Jung JY, Choi JE. Photobiomodulation at a wavelength of 633nm leads to faster functional recovery than 804nm after facial nerve injury. J Biophotonics. In press 2021.
  55. Wei L, Mousawi F, Li D, Roger S, Li J, Yang X, et al. Adenosine triphosphate release and P2 receptor signaling in Piezo1 channel-dependent mechanoregulation. Front Pharmacol 2019;10:1304. https://doi.org/10.3389/fphar.2019.01304
  56. Zhang Z, Shen Q, Wu X, Zhang D, Xing D. Activation of PKA/SIRT1 signaling pathway by photobiomodulation therapy reduces Aβ levels in Alzheimer's disease models. Aging Cell 2020;19:e13054. https://doi.org/10.1111/acel.13054
  57. Hu WP, Wang JJ, Yu CL, Lan CC, Chen GS, Yu HS. Heliumneon laser irradiation stimulates cell proliferation through photostimulatory effects in mitochondria. J Invest Dermatol 2007;127:2048-57. https://doi.org/10.1038/sj.jid.5700826
  58. Heo JC, Park JA, Kim DK, Lee JH. Photobiomodulation (660nm) therapy reduces oxidative stress and induces BDNF expression in the hippocampus. Sci Rep 2019;9:10114. https://doi.org/10.1038/s41598-019-46490-4
  59. Li B, Wang X. Photobiomodulation enhances facial nerve regeneration via activation of PI3K/Akt signaling pathway-mediated antioxidant response. Lasers Med Sci. In press 2021.
  60. Moccia F, Negri S, Shekha M, Faris P, Guerra G. Endothelial Ca2+ signaling, angiogenesis and vasculogenesis: just what it takes to make a blood vessel. Int J Mol Sci 2019;20:3962. https://doi.org/10.3390/ijms20163962
  61. Goldsmith ZG, Dhanasekaran DN. G protein regulation of MAPK networks. Oncogene 2007;26:3122-42. https://doi.org/10.1038/sj.onc.1210407
  62. Zhang J, Wang X, Vikash V, Ye Q, Wu D, Liu Y, et al. ROS and ROS-mediated cellular signaling. Oxid Med Cell Longev 2016;2016:4350965. https://doi.org/10.1155/2016/4350965
  63. Klimaschewski L, Hausott B, Angelov DN. The pros and cons of growth factors and cytokines in peripheral axon regeneration. Int Rev Neurobiol 2013;108:137-71. https://doi.org/10.1016/B978-0-12-410499-0.00006-X
  64. Huang HT, Sun ZG, Liu HW, Ma JT, Hu M. ERK/MAPK and PI3K/AKT signal channels simultaneously activated in nerve cell and axon after facial nerve injury. Saudi J Biol Sci 2017;24:1853-8. https://doi.org/10.1016/j.sjbs.2017.11.027
  65. Schmid RS, Pruitt WM, Maness PF. A MAP kinase-signaling pathway mediates neurite outgrowth on L1 and requires Src-dependent endocytosis. J Neurosci 2000;20:4177-88. https://doi.org/10.1523/jneurosci.20-11-04177.2000
  66. Ghosh-Roy A, Wu Z, Goncharov A, Jin Y, Chisholm AD. Calcium and cyclic AMP promote axonal regeneration in Caenorhabditis elegans and require DLK-1 kinase. J Neurosci 2010;30:3175-83. https://doi.org/10.1523/JNEUROSCI.5464-09.2010
  67. Rhee YH, Moon JH, Jung JY, Oh C, Ahn JC, Chung PS. Effect of photobiomodulation therapy on neuronal injuries by ouabain: the regulation of Na, K-ATPase; Src; and mitogen-activated protein kinase signaling pathway. BMC Neurosci 2019;20:19. https://doi.org/10.1186/s12868-019-0499-3