Cellular Signalling and Photobiomodulation in Chronic Wound Repair

Thobekile S Leyane, Sandy W Jere, Nicolette N Houreld, Thobekile S Leyane, Sandy W Jere, Nicolette N Houreld

Abstract

Photobiomodulation (PBM) imparts therapeutically significant benefits in the healing of chronic wounds. Chronic wounds develop when the stages of wound healing fail to progress in a timely and orderly frame, and without an established functional and structural outcome. Therapeutic benefits associated with PBM include augmenting tissue regeneration and repair, mitigating inflammation, relieving pain, and reducing oxidative stress. PBM stimulates the mitochondria, resulting in an increase in adenosine triphosphate (ATP) production and the downstream release of growth factors. The binding of growth factors to cell surface receptors induces signalling pathways that transmit signals to the nucleus for the transcription of genes for increased cellular proliferation, viability, and migration in numerous cell types, including stem cells and fibroblasts. Over the past few years, significant advances have been made in understanding how PBM regulates numerous signalling pathways implicated in chronic wound repair. This review highlights the significant role of PBM in the activation of several cell signalling pathways involved in wound healing.

Keywords: JAK/STAT; MAPKs; calcium; cellular signalling pathway; photobiomodulation; wound healing.

Conflict of interest statement

The authors declare no conflict of interest. The funders had no role in the writing of the manuscript, or in the decision to publish.

Figures

Figure 1
Figure 1
Simplified overview of the MAPK signalling pathway.
Figure 2
Figure 2
Schematic representation of the intracellular signalling pathways activated by PBM. The intracellular signalling pathways activated by PBM include the MAPK, PI3K/Akt/mTOR, JAK/STAT, BMP/Smad, and TFG-β/Smad pathway. Intracellular signalling pathways are activated in response to a wide array of extracellular signals and are frequently activated in parallel. They are integrated by positive and negative feedback and generate numerous biological signals that depend on the stimulus and on the activated cell type.

References

    1. Findlay M.W., Gurtner G.C. Engineering niches for skin and wound healing. In: Vishwakarma A., Karp J., editors. Biology and Engineering of Stem Cell Niches. 1st ed. Academic Press; San Diego, CA, USA: 2017. pp. 559–579.
    1. Dubhashi S.P., Sindwani R.D. A comparative study of honey and phenytoin dressings for chronic wounds. Indian J. Surg. 2015;77((Suppl. S3)):S1209–S1213. doi: 10.1007/s12262-015-1251-6.
    1. Ahmed O.M., Mohamed T., Moustafa H., Hamdy H., Ahmed R.R., Aboud E. Quercetin and low level laser therapy promote wound healing process in diabetic rats via structural reorganization and modulatory effects on inflammation and oxidative stress. Biomed. Pharm. 2018;101:58–73. doi: 10.1016/j.biopha.2018.02.040.
    1. Demidova-Rice T.N., Hamblin M.R., Herman I.R. Acute and impaired wound healing: Pathophysiology and current methods for drug delivery, part 1: Normal and chronic wounds: Biology, causes, and approaches to care. Adv. Ski. Wound Care. 2012;25:304–314. doi: 10.1097/01.ASW.0000416006.55218.d0.
    1. Graves N., Zheng H. Modelling the direct health care costs of chronic wounds in Australia. Wound Pract. Res. 2014;22:20–32.
    1. Järbrink K., Ni G., Sönnergren H., Schimidtchen A., Pang C., Bajpai R., Car J. The humanistic and economic burden of chronic wounds: A protocol for a systematic review. Syst. Rev. 2017;6:15. doi: 10.1186/s13643-016-0400-8.
    1. Avci P., Gupta A., Sadasivam M., Vecchio D., Pam Z., Pam N., Hamblin M.R. Low-level laser (light) therapy (LLLT) in skin: Stimulating, healing, restoring. Semin. Cutan. Med. Surg. 2013;32:41–52.
    1. Ponnusamy S., Mosca R., Desai K., Arany P. Photobiomodulation therapy in diabetic wound healing. In: Bagchi D., Das A., Roy S., editors. Wound Healing, Tissue Repair, and Regeneration in Diabetes. Academic Press; San Diego, CA, USA: 2020. pp. 305–321.
    1. Huang Y.Y., Chenet A.C., Carroll J.D., Hamblin R.M. Biphasic dose response in low level light therapy. Dose Response. 2009;7:358–383. doi: 10.2203/dose-response.09-027.Hamblin.
    1. Li W., Hu X., Lu X., Liu J., Chen Z., Zhou X., Liu M., Liu S. RNA-Seq analysis revealed the molecular mechanisms of photobiomodulation effect on human fibroblasts. Photodermatol. Photoimmunol. Photomed. 2020;36:299–307. doi: 10.1111/phpp.12554.
    1. Bagheri M., Mostafavinia A., Abdollahifar M., Amini A., Ghoreishi S.K., Chien S., Hamblin M.R., Bayat S., Bayat M. Combined effects of metformin and photobiomodulation improve the proliferation phase of wound healing in type 2 diabetic rats. Biomed. Pharm. 2020;123:109776. doi: 10.1016/j.biopha.2019.109776.
    1. Keshri G.K., Kumar G., Sharma M., Bora K., Kumar B., Gupta A. Photobiomodulation effects of pulsed-NIR laser (810 nm) and LED (808 ± 3 nm) with identical treatment regimen on burn wound healing: A quantitative label-free global proteomic approach. J. Photochem. Photobiol. 2021;6:100024. doi: 10.1016/j.jpap.2021.100024.
    1. Hamdan S., Pastar I., Drakulich S., Dikici E., Tomic-Canic M., Deo S., Daunert S. Nanotechnology-driven therapeutic interventions in wound healing: Potential uses and applications. ACS Cent. Sci. 2017;3:163–175. doi: 10.1021/acscentsci.6b00371.
    1. Ghilardi S.J., O’Reilly B.M., Sgro A.E. Intracellular signaling dynamics and their role in coordinating tissue repair. WIREs Syst. Biol. Med. 2019;12:e1479. doi: 10.1002/wsbm.1479.
    1. Lee S., Kim M.S., Jung S.J., Kim D., Park H.J., Cho D. ERK activating peptide, AES16-2M promotes wound healing through accelerating migration of keratinocytes. Sci. Rep. 2018;8:14398. doi: 10.1038/s41598-018-32851-y.
    1. Chu Y.H., Chen S.Y., Hsieh Y.L., Teng Y.H., Cheng Y.J. Low-level laser therapy prevents endothelial cells from TNF-α/cycloheximide-induced apoptosis. Lasers Med. Sci. 2018;33:279–286. doi: 10.1007/s10103-017-2364-x.
    1. Arnold K.M., Opdenaker L.M., Flynn D., Sims-Mourtada J. Wound healing and cancer stem cells: Inflammation as a driver of treatment resistance in breast cancer. Cancer Growth Metastasis. 2015;8:1–13. doi: 10.4137/CGM.S11286.
    1. De Freitas L.F., Hamblin M.R. Proposed mechanisms of photobiomodulation or low-level light therapy. IEEE J. Sel. Top Quantum Electron. 2016;22:7000417. doi: 10.1109/JSTQE.2016.2561201.
    1. Zhao Y., Ming L., Wei Z., Bin W., Yudong Z., Haiwen S., Ren X., Hao Q. Changes in the expression of Wnt/β-catenin signaling pathway in diabetic ulcers. Chin. J. Pathophysiol. 2015;17:2033–2038.
    1. Whyte J.L., Smith A.A., Helms J.A. Wnt signaling and injury repair. Cold Spring Harb. Perspect. Biol. 2012;4:a008078. doi: 10.1101/cshperspect.a008078.
    1. Jere S.W., Houreld N.N., Abrahamse H. Photobiomodulation at 660 nm stimulates proliferation and migration of diabetic wounded cells via the expression of epidermal growth factor and the JAK/STAT pathway. J. Photochem. Photobiol. B. 2018;179:74–83. doi: 10.1016/j.jphotobiol.2017.12.026.
    1. Feng Y., Sanders A.J., Ruge F., Morris C.-A., Harding K.G., Jiang W.G. Expression of the SOCS family in human chronic wound tissues: Potential implications for SOCS in chronic wound healing. Int. J. Mol. Med. 2016;38:1349–1358. doi: 10.3892/ijmm.2016.2733.
    1. Squarize C.H., Castilho R.M., Bugge T.H., Gutkind J.S. Accelerated wound healing by mTOR activation in genetically defined mouse models. PLoS ONE. 2010;13:e10643. doi: 10.1371/journal.pone.0010643.
    1. Huang H., Cui W., Qiu W., Zhu M., Zhao R., Zeng D., Dong C., Wang X., Guo W., Xing W., et al. Impaired wound healing results from the dysfunction of the Akt/mTOR pathway in diabetic rats. J. Dermatol. Sci. 2015;79:241–251. doi: 10.1016/j.jdermsci.2015.06.002.
    1. Finnson K.W., Arany P.R., Philip A. Transforming growth factor beta signaling in cutaneous wound healing: Lessons learned from animal studies. Adv. Wound Care. 2013;2:225–237. doi: 10.1089/wound.2012.0419.
    1. Chigurupati S., Arumugam T.V., Son T.G., Lathia J.D., Jameel S., Mughal M.R., Tang S.-C., Jo D.-G., Camandola S., Giunta M., et al. Involvement of notch signaling in wound healing. PLoS ONE. 2007;2:e1167. doi: 10.1371/journal.pone.0001167.
    1. Chang S.Y., Carpena N.T., Kang B.J., Lee M.Y. Effects of photobiomodulation on stem cells important for regenerative medicine. Med Lasers Eng. Basic Res. Clin. Appl. 2020;9:134–141.
    1. Shao H., Li Y., Pastar I., Xiao M., Prokupets R., Liu S., Yu K., Vazquez-Padron R.I., Tomic-Canic M., Velazquez O.C., et al. Notch1 signaling determines the plasticity and function of fibroblasts in diabetic wounds. Life Sci. Alliance. 2020;3:e202000769. doi: 10.26508/lsa.202000769.
    1. Deng M., Chen W.-L., Takatori A., Peng Z., Zhang L., Mongan M., Parthasarathy R., Sartor M., Miller M., Yang J., et al. A role for the mitogen-activated protein kinase kinase kinase 1 in epithelial wound healing. Mol. Biol. Cell. 2006;17:3446–3455. doi: 10.1091/mbc.e06-02-0102.
    1. Liang C., Wang S., Qin C., Bao M., Cheng G., Liu B., Shao P., Lv Q., Song N., Hua L., et al. TRIM36, a novel androgen-responsive gene, enhances anti-androgen efficacy against prostate cancer by inhibiting MAPK/ERK signaling pathways. Cell Death Dis. 2018;9:1–13. doi: 10.1038/s41419-017-0197-y.
    1. Thouverey C., Caverzasio J. Focus on the p38 MAPK signaling pathway in bone development and maintenance. BoneKEy Rep. 2015;4:711. doi: 10.1038/bonekey.2015.80.
    1. Kovalska M., Kovalska L., Pavlikova M., Janickova M., Mikuskova K., Adamkov M., Kaplan P., Tatarkova Z., Lehotsky J. Intracellular signaling MAPK pathway after cerebral ischemia–reperfusion injury. Neurochem. Res. 2012;37:1568–1577. doi: 10.1007/s11064-012-0752-y.
    1. Edelmayer R.M., Brederson J.D., Jarvis M.F., Bitner R.S. Biochemical and pharmacological assessment of MAP-kinase signaling along pain pathways in experimental rodent models: A potential tool for the discovery of novel antinociceptive therapeutics. Biochem. Pharm. 2014;87:390–398. doi: 10.1016/j.bcp.2013.11.019.
    1. Tripodi N., Corcoran D., Antonello P., Balic N., Knight A., Meehan C., Sidiroglou F., Fraser S., Kiatos D., Husaric M., et al. The effects of photobiomodulation on human dermal fibroblasts in vitro: A systematic review. J. Photochem. Photobiol. B. 2021;214:112100. doi: 10.1016/j.jphotobiol.2020.112100.
    1. Gonzalez A.C.D.O., Costa T.F., Andrade Z.D.A., Medrado A.R.A.P. Wound healing—A literature review. An. Bras. Derm. 2016;91:614–620. doi: 10.1590/abd1806-4841.20164741.
    1. Piva J.A.A.C., Abreu E.M.C., Silva V.S., Nicolau R.A. Effect of low-level laser therapty on the initial stages of tissue repair: Basic principles. An. Bras. Derm. 2011;86:947–954. doi: 10.1590/S0365-05962011000500013.
    1. Shaw T.J., Martin P. Wound repair at a glance. J. Cell Sci. 2009;122:3209–3213. doi: 10.1242/jcs.031187.
    1. Monsuur H.N., Boink M.A., Weijers E.M., Roffel S., Breetveld M., Gefen A., van der Broek L.J., Gibbs S. Methods to study differences in cell mobility during skin wound healing in vitro. J. Biomech. 2016;49:1381–1387. doi: 10.1016/j.jbiomech.2016.01.040.
    1. Layegh E.R., Fathabadi F.F., Lotfinia M., Zare F., Tofigh A.M., Abrishami S., Piryaei A. Photobiomodulation therapy improves the growth factor and cytokine secretory profile in human type 2 diabetic fibroblasts. J. Photochem. Photobiol. B. 2020;210:111962. doi: 10.1016/j.jphotobiol.2020.111962.
    1. Medrado A., Costa T., Prado T., Reis S., Andrade Z. Phenotype characterization of pericytes during tissue repair following low-level laser therapy. Photodermatol. Photoimmunol. Photomed. 2010;26:192–197. doi: 10.1111/j.1600-0781.2010.00521.x.
    1. Menke N.B., Ward K.R., Witten T.M., Bonchev D.G., Diegelmann R.F. Impaired wound healing. Clin. Derm. 2007;25:19–25. doi: 10.1016/j.clindermatol.2006.12.005.
    1. Darby I.A., Laverdet B., Bonté F., Desmoulière A. Fibroblasts and myofibroblasts in wound healing. Clin. Cosmet. Investig. Derm. 2014;7:301–311.
    1. Schultz G.S., Chin G.A., Moldawer L., Diegelmann R.F. Principles of wound healing. In: Fitridge R., Thompson M., editors. Mechanisms of Vascular Disease: A Reference Book for Vascular Specialists. University of Adelaide Press; Adelaide, Australia: 2011. pp. 329–345.
    1. Handly L.N., Wollman R. Wound-induced Ca2+ wave propagates through a simple release and diffusion mechanism. Mol. Biol. Cell. 2017;28:1457–1466. doi: 10.1091/mbc.e16-10-0695.
    1. Handly L.N., Pilko A., Wollman R. Paracrine communication maximizes cellular response fidelity in wound signaling. eLife. 2015;4:e09652. doi: 10.7554/eLife.09652.
    1. Rodrigues M., Kosaric N., Bonham C.A., Gurtner G.C. Wound healing: A cellular perspective. Physiol. Rev. 2019;99:665–706. doi: 10.1152/physrev.00067.2017.
    1. Antunes M., Pereira T., Cordeiro J.V., Almeida L., Jacinto A. Coordinated waves of actomyosin flow and apical cell constriction immediately after wounding. J. Cell Biol. 2013;202:365–379. doi: 10.1083/jcb.201211039.
    1. Lee S.E., Lee S.H. Skin barrier and calcium. Ann. Derm. 2018;30:265–275. doi: 10.5021/ad.2018.30.3.265.
    1. Subramaniam T., Fauzi M.B., Lokanathan Y., Law J.X. The role of calcium in wound healing. Int. J. Mol. Sci. 2021;22:6486. doi: 10.3390/ijms22126486.
    1. Yoo S.K., Freisinger C.M., LeBert D.C., Huttenlocher A. Early redox, Src family kinase, and calcium signaling integrate wound responses and tissue regeneration in zebrafish. J. Cell Biol. 2012;199:225–234. doi: 10.1083/jcb.201203154.
    1. Klepeis V.E., Cornell-Bell A., Trinkaus-Randall V. Growth factors but not gap junctions play a role in injury-induced Ca2+ waves in epithelial cells. J. Cell Sci. 2001;114:4185–4195. doi: 10.1242/jcs.114.23.4185.
    1. Shabir S., Southgate J. Calcium signalling in wound-responsive normal human urothelial cell monolayers. Cell Calcium. 2008;44:453–464. doi: 10.1016/j.ceca.2008.02.008.
    1. Chifflet S., Justet C., Hernández J.A., Nin V., Escande C., Benech J.C. Early and late calcium waves during wound healing in corneal endothelial cells. Wound Repair Regen. 2012;20:28–37. doi: 10.1111/j.1524-475X.2011.00749.x.
    1. Berra-Romani R., Raqeeb A., Torres-Jácome J., Guzman-Silva A., Guerra G., Tanzi F., Moccia F. The mechanism of injury-induced intracellular calcium concentration oscillations in the endothelium of excised rat aorta. J. Vasc. Res. 2012;49:65–76. doi: 10.1159/000329618.
    1. Togo T. Cell membrane disruption stimulates cAMP and Ca2+ signaling to potentiate cell membrane resealing in neighboring cells. Biol. Open. 2017;6:1814–1819. doi: 10.1242/bio.028977.
    1. Bagur R., Hajnóczky G. Intracellular Ca2+ sensing: Role in calcium homeostasis and signaling. Mol. Cell. 2017;66:780–788. doi: 10.1016/j.molcel.2017.05.028.
    1. Sun J., Nan G. The mitogen-activated protein kinase (MAPK) signaling pathway as a discovery target in stroke. J. Mol. Neurosci. 2016;59:90–98. doi: 10.1007/s12031-016-0717-8.
    1. Du W., Hu H., Zhang J., Bao G., Chen R., Quan R. The mechanism of MAPK signal transduction pathway involved with electroacupuncture treatment for different diseases. Evid. Based Complement. Altern. Med. 2019;2019:8138017. doi: 10.1155/2019/8138017.
    1. Xia D., Tian S., Chen Z., Qin W., Liu Q. MiR302a inhibits the proliferation of esophageal cancer cells through the MAPK and PI3K/Akt signaling pathways. Oncol. Lett. 2018;15:3937–3943. doi: 10.3892/ol.2018.7782.
    1. Xu D., Zhu J., Jeong S., Li D., Hua X., Huang L., Zhang J., Luo Y., Xia Q. Rictor deficiency aggregates hepatic ischemia/reperfusion injury in mice by suppressing autography and regulating MAPK signaling. Cell. Physiol. Biochem. 2018;45:2199–2212. doi: 10.1159/000488165.
    1. Bianchi E.N., Ferrari S.L. β-arrestin2 regulates parathyroid hormone effects on a p38 MAPK and NFκB gene expression network in osteoblasts. Bone. 2009;45:716–725. doi: 10.1016/j.bone.2009.06.020.
    1. Petersen H.O., Höger S.K., Looso M., Lengfeld T., Kuhn A., Warnken U., Nishimiya-Fujisawa C., Schnölzer M., Krüger M., Özbek S., et al. A comprehensive transcriptomic and proteomic analysis of hydra head regeneration. Mol. Biol. Evol. 2015;32:1928–1947. doi: 10.1093/molbev/msv079.
    1. Thuraisingam T., Xu Y.Z., Eadie K., Heravi M., Guiot M.-C., Greemberg R., Gaestel M., Radzioch D. MAPKAPK-2 signaling is critical for cutaneous wound healing. J. Investig. Derm. 2010;130:278–286. doi: 10.1038/jid.2009.209.
    1. Arthur J.S.C., Ley S.C. Mitogen-activated protein kinases in innate immunity. Nat. Rev. Immunol. 2013;13:679–692. doi: 10.1038/nri3495.
    1. Cassidy H., Radford R., Slyne J., O’Connell S., Slattery C., Ryan M.P., McMorrow T. The role of MAPK in drug-induced kidney injury. J. Signal Transduct. 2012;2012:463617. doi: 10.1155/2012/463617.
    1. Kong T., Liu M., Ji B., Bai B., Cheng B., Wang C. Role of the Extracellular signal-regulated kinase 1/2 signaling pathway in ischemia-reperfusion injury. Front. Physiol. 2019;10:1038. doi: 10.3389/fphys.2019.01038.
    1. Lee C.H., Yoo K.Y., Park O.K., Choi J.H., Kang I.J., Bae E., Kim S.K., Hwang I.K., Won M.H. Phosphorylated extracellular signal regulated kinase 1/2 immunoreactivity and its protein levels in the gerbil hippocampus during normal aging. Mol. Cells. 2010;29:373–378. doi: 10.1007/s10059-010-0046-7.
    1. Aoki K., Kondo Y., Naoki H., Hiratsuka T., Itoh R.E., Matsuda M. Propagating wave of ERK activation orients collective cell migration. Dev. Cell. 2017;43:305–317.e5. doi: 10.1016/j.devcel.2017.10.016.
    1. Singh B., Carpenter G., Coffey R.J. EGF receptor ligands: Recent advances. F1000Research. 2016;5:2270. doi: 10.12688/f1000research.9025.1.
    1. Wortzel I., Seger R. The ERK cascade. Genes Cancer. 2011;2:195–209. doi: 10.1177/1947601911407328.
    1. Bas D.B., Abdelmoaty S., Sandor K., Codeluppi S., Fitzsimmons B., Steinauer J., Hua X.Y., Yaksh T.L., Svensson C.I. Spinal release of tumour necrosis factor activates c-Jun N-terminal kinase and mediates inflammation-induced hypersensitivity. Eur. J. Pain. 2015;19:260–270. doi: 10.1002/ejp.544.
    1. Ramet M., Lanot R., Zachary D., Manfruelli P. JNK signaling pathway is required for efficient wound healing in Drosophila. Dev. Biol. 2002;241:145–156. doi: 10.1006/dbio.2001.0502.
    1. Bosch M., Serras F., Martin-Blanco E., Baguna J. JNK signaling pathway required for wound healing in regenerating Drosophila wing imaginal discs. Dev. Biol. 2005;280:73–86. doi: 10.1016/j.ydbio.2005.01.002.
    1. Yang Y., Kim S.C., Yu T., Yi T.Y., Rhee M.H., Sung G.H., Yoo B.C., Cho J.Y. Functional roles of p38 mitogen-activated protein kinase in macrophage-mediated inflammatory responses. Mediat. Inflamm. 2014;2014:352371. doi: 10.1155/2014/352371.
    1. Harrison D.A. The JAK/STAT pathway. Cold Spring Harb. Perspect. Biol. 2012;4:a011205. doi: 10.1101/cshperspect.a011205.
    1. Tapia V.S., Larrain J. Role of JAK-STAT signalling on motor function recovery after spinal cord injury. In: Fuller H., Gates M., editors. Recovery of Motor Function Following Spinal Cord Injury. IntechOpen; London, UK: 2016.
    1. Kiu H., Nicholson S.E. Biology and significance of the JAK/STAT signalling pathways. Growth Factors. 2012;30:88–106. doi: 10.3109/08977194.2012.660936.
    1. Seif F., Khoshmirsafa M., Aazami H., Mohsenzadegan M., Sedighi G., Mohammadali B. The role of JAK-STAT signaling pathway and its regulators in the fate of T helper cells. Cell Commun. Signal. 2017;15:23. doi: 10.1186/s12964-017-0177-y.
    1. Thomas S.J., Snowden J.A., Danson S.J. The role of JAK/STAT signalling in the pathogenesis, prognosis and treatment of solid tumours. Br. J. Cancer. 2015;113:365–371. doi: 10.1038/bjc.2015.233.
    1. Brooks A.J., Dai W., O’Mara M.L., Abankwa D., Chhabra Y., Pelekanos R.A., Gardon O., Tunny K.A., Blucher K.M., Morton C.J., et al. Mechanism of activation of protein kinase JAK2 by the growth hormone receptor. Science. 2014;344:1249783. doi: 10.1126/science.1249783.
    1. Linke A., Goren I., Bösl M.R., Pfeilschifter J., Frank S. The suppressor of cytokine signaling (SOCS)-3 determines keratinocyte proliferative and migratory potential during skin repair. J. Investig. Derm. 2010;130:876–885. doi: 10.1038/jid.2009.344.
    1. Mester E., Szende B., Gartnerne T. Influence of laser beams on the growth of hair in mice. Kiserl Orv. 1967;19:628–631.
    1. Karu T.I. Molecular mechanism of the therapeutic effect of low-intensity laser irradiation. Dokl. Akad. Nauk SSSR. 1986;291:1245–1249.
    1. Beckmann K.H., Meyer-Hamme G., Schröder S. Low level laser therapy for the treatment of diabetic foot ulcers: A clinical survey. eCAM. 2014;2014:626127. doi: 10.1155/2014/626127.
    1. Mosca R.C., Ong A.A., Albasha O., Bass K., Arany P. Photobiomodulation therapy for wound care: A potent, noninvasive, photoceutical approach. Adv. Ski. Wound Care. 2019;32:157–167. doi: 10.1097/01.ASW.0000553600.97572.d2.
    1. Cotler H.B., Chow R.T., Hamblin M.R., Carroll J. The use of low level laser therapy (LLLT) for musculoskeletal pain. MOJ Orthoped. Rheumatol. 2015;2:188–194. doi: 10.15406/mojor.2015.02.00068.
    1. Taradaj J., Shay B., Dymarek R., Sopel M., Walewicz K., Beeckman D., Schoonhoven L., Gefen A., Rosinczuk J. Effect of laser therapy on expression of angio- and fibrogenic factors, and cytokine concentrations during the healing process of huma pressure ulcers. Int. J. Med. Sci. 2018;15:1105. doi: 10.7150/ijms.25651.
    1. Rathnakar B., Rao B.S.S., Pravu V., Chandra S., Rai S., Rao A.C.K., Sharma M., Gupta P.K., Mahato K.K. Photo-biomodulatory response of low-power laser irradiation on burn tissue repair in mice. Lasers Med. Sci. 2016;31:1741–1750. doi: 10.1007/s10103-016-2044-2.
    1. Almeida-Lopes L., Rigau J., Zângaro R.A., Guidugli-Neto J., Jaeger M.M. Comparison of the low level laser therapy effects on cultured human gingival fibroblasts proliferation using different irradiance and same fluence. Lasers Surg. Med. 2001;29:179–184. doi: 10.1002/lsm.1107.
    1. Little A.G., Lau G., Mathers K.E., Leary S.C., Moyes C.D. Comparative biochemistry of cytochrome c oxidase in animals. Comp. Biochem. Physiol. B Biochem. Mol. Biol. 2018;224:170–184. doi: 10.1016/j.cbpb.2017.11.005.
    1. George S., Hamblin M.R., Abrahamse H. Effect of red light and near infrared laser on the generation of reactive oxygen species in primary dermal fibroblasts. J. Photochem. Photobiol. B. 2018;188:60–68. doi: 10.1016/j.jphotobiol.2018.09.004.
    1. Karu T.I., Pyatibrat L.V., Kolyakov S.F., Afanasyeva N.I. Absorption measurements of a cell monolayer relevant to phototherapy: Reduction of cytochrome c oxidase under near IR radiation. J. Photochem. Photobiol. B. 2005;81:98–106. doi: 10.1016/j.jphotobiol.2005.07.002.
    1. Austin E., Geisler A.N., Nguyen J., Kohli I., Hamzavi I., Lim H.W., Jagdeo J. Visible light. Part I: Properties and cutaneous effects of visible light. J. Am. Acad. Derm. 2021;84:1219–1231. doi: 10.1016/j.jaad.2021.02.048.
    1. Houreld N.N. Influence of 660 and 830 Nm Laser irradiation on genetic profile of extracellular matrix proteins in diabetic wounded human skin fibroblast cells; Proceedings of the International Conference on Biomedical and Biological Engineering; Shanghai, China. 15–17 July 2016.
    1. Hamblin M.R. Mechanisms and mitochondrial redox signaling in photobiomodulation. Photochem. Photobiol. 2018;94:199–212. doi: 10.1111/php.12864.
    1. Calles C., Schneider M., Macaluso F., Benesova T., Krutmann J., Schroeder P. Infrared A radiation influences the skin fibroblast transcriptome: Mechanisms and consequences. J. Investig. Derm. 2010;130:1524–1536. doi: 10.1038/jid.2010.9.
    1. Golovynska I., Golovynskyi S., Stepanov Y.V., Stepanova L.I., Qu J., Ohulchanskyy T.Y. Red and near-infrared light evokes Ca2+ influx, endoplasmic reticulum release and membrane depolarization in neurons and cancer cells. J. Photochem. Photobiol. B Biol. 2021;214:112088. doi: 10.1016/j.jphotobiol.2020.112088.
    1. Huang Y.-Y., Nagata K., Tedford C.E., Hamblin M.R. Low-level laser therapy (810-nm) protects primary cortical neurons against excitotoxicity in vitro. J. Biophotonics. 2014;7:656–664. doi: 10.1002/jbio.201300125.
    1. Sharma S.K., Kharkwal G.B., Sajo M., Huang Y.-Y., De Taboada L., McCarthy T., Hamblin M.R. Dose response effects of 810 nm laser light on mouse primary cortical neurons. Lasers Surg. Med. 2011;43:851–859. doi: 10.1002/lsm.21100.
    1. Shingyochi Y., Kanazawa S., Tajima S., Tanaka R., Mizuno H., Tobita M. A low-level carbon dioxide laser promotes fibroblast proliferation and migration through activation of Akt, ERK, and JNK. PLoS ONE. 2017;12:e0168937. doi: 10.1371/journal.pone.0168937.
    1. Kawano Y., Utsunomiya-Kai Y., Kai K., Miyakawa I., Ohshiro T., Narahara H. The production of VEGF involving MAP kinase activation by low level laser therapy in human granulosa cells. Laser Ther. 2012;21:269–274. doi: 10.5978/islsm.12-OR-15.
    1. El-Makakey A.M., El-Sharaby R.M., Hassan M.H., Balbaa A. Comparative study of the efficacy of pulsed electromagnetic field and low level laser therapy on mitogen-activated protein kinases. Biochem. Biophys. Rep. 2017;9:316–321. doi: 10.1016/j.bbrep.2017.01.008.
    1. Dang Y., Liu B., Liu L., Ye X., Bi X., Zhang Y., Gu J. The 800-nm diode laser irradiation induces skin collagen synthesis by stimulating TGF-β/Smad signaling pathway. Lasers Med. Sci. 2011;26:837–884. doi: 10.1007/s10103-011-0985-z.
    1. Mokoena D.R., Houreld N.N., Dhilip Kumar S.S., Abrahamse H. Photobiomodulation at 660 nm stimulates fibroblast differentiation. Lasers Surg. Med. 2020;52:671–681. doi: 10.1002/lsm.23204.
    1. Hirata S., Kitamura C., Fukushima H., Nakamichi I., Abiko Y., Terashita M., Jimi E. Low-level laser irradiation enhances BMP-induced osteoblast differentiation by stimulating the BMP/Smad signaling pathway. J. Cell. Biochem. 2010;111:1445–1452. doi: 10.1002/jcb.22872.
    1. Zhang L., Xing D., Gao X., Wu S. Low-power laser irradiation promotes cell proliferation by activating PI3K/Akt pathway. J. Cell. Physiol. 2009;219:553–562. doi: 10.1002/jcp.21697.
    1. Agas D., Hanna R., Benedicenti S., De Angelis N., Sabbieti M.G., Amaroli A. Photobiomodulation by near-infrared 980-nm wavelengths regulates pre-osteoblast proliferation and viability through the PI3K/Akt/Bcl-2 pathway. Int. J. Mol. Sci. 2021;22:7586. doi: 10.3390/ijms22147586.
    1. Rajendran N.K., Houreld N.N., Abrahamse H. Photobiomodulation reduces oxidative stress in diabetic wounded fibroblast cells by inhibiting the FOXO1 signaling pathway. J. Cell Commun. Signal. 2021;15:195–206. doi: 10.1007/s12079-020-00588-x.
    1. Brenner D.R., Ruan Y., Adams S.C., Courneya K.S., Friedenreich C.M. The impact of exercise on growth factors (VEGF and FGF2): Results from a 12-month randomized intervention trial. Eur. Rev. Aging Phys. Act. 2019;16:8. doi: 10.1186/s11556-019-0215-4.
    1. Jere S.W., Houreld N.N., Abrahamse H. Photobiomodulation and the expression of genes related to the JAK/STAT signalling pathway in wounded and diabetic wounded cells. J. Photochem. Photobiol. B Biol. 2020;204:111791. doi: 10.1016/j.jphotobiol.2020.111791.
    1. Midgley A.C., Morris G., Phillips A.O., Steadman R. 17β-estradiol ameliorates age-associated loss of fibroblast function by attenuating IFN-γ/STAT1-dependent miR-7 upregulation. Aging Cell. 2016;15:531–541. doi: 10.1111/acel.12462.
    1. Morikawa M., Derynck R., Miyazono K. TGF-β and the TGF-β family: Context-dependent roles in cell and tissue physiology. Cold Spring Harb. Perspect. Biol. 2016;8:a021873. doi: 10.1101/cshperspect.a021873.
    1. Walton K.L., Johnson K.E., Harrison C.A. Targeting TGF-β mediated Smad signaling for the prevention of fibrosis. Front. Pharm. 2017;8:461. doi: 10.3389/fphar.2017.00461.
    1. Blank U., Karlsson S. The role of Smad signaling in hematopoiesis and translational hematology. Leukemia. 2011;25:1379–1388. doi: 10.1038/leu.2011.95.
    1. Shi Y., Massague J. Mechanisms of TGF-beta signaling from cell membrane to nucleus. Cell. 2003;113:685–700. doi: 10.1016/S0092-8674(03)00432-X.
    1. Shi X., Wang J., Lei Y., Cong C., Tan D., Zhou X. Research progress on the PI3K/AKT signaling pathway in gynecological cancer (Review) Mol. Med. Rep. 2019;19:4529–4535. doi: 10.3892/mmr.2019.10121.
    1. Farivar S., Malekshahabi T., Shiari R. Biological effects of low level laser therapy. J. Lasers Med. Sci. 2014;5:58–62.

Source: PubMed

Sponsorer och medarbetare

Medicinska tillstånd

Läkemedelsinterventioner

3
Prenumerera