Biological Responses of Stem Cells to Photobiomodulation Therapy

Author(s): Khatereh Khorsandi, Reza Hosseinzadeh, Heidi Abrahamse, Reza Fekrazad*

Journal Name: Current Stem Cell Research & Therapy

Volume 15 , Issue 5 , 2020


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Abstract:

Background: Stem cells have attracted the researchers interest, due to their applications in regenerative medicine. Their self-renewal capacity for multipotent differentiation, and immunomodulatory properties make them unique to significantly contribute to tissue repair and regeneration applications. Recently, stem cells have shown increased proliferation when irradiated with low-level laser therapy or Photobiomodulation Therapy (PBMT), which induces the activation of intracellular and extracellular chromophores and the initiation of cellular signaling. The purpose of this study was to evaluate this phenomenon in the literature.

Methods: The literature investigated the articles written in English in four electronic databases of PubMed, Scopus, Google Scholar and Cochrane up to April 2019. Stem cell was searched by combining the search keyword of "low-level laser therapy" OR "low power laser therapy" OR "low-intensity laser therapy" OR "photobiomodulation therapy" OR "photo biostimulation therapy" OR "LED". In total, 46 articles were eligible for evaluation.

Results: Studies demonstrated that red to near-infrared light is absorbed by the mitochondrial respiratory chain. Mitochondria are significant sources of reactive oxygen species (ROS). Mitochondria play an important role in metabolism, energy generation, and are also involved in mediating the effects induced by PBMT. PBMT may result in the increased production of (ROS), nitric oxide (NO), adenosine triphosphate (ATP), and cyclic adenosine monophosphate (cAMP). These changes, in turn, initiate cell proliferation and induce the signal cascade effect.

Conclusion: The findings of this review suggest that PBMT-based regenerative medicine could be a useful tool for future advances in tissue engineering and cell therapy.

Keywords: Stem cell, low-level laser therapy, regenerative medicine, photobiomodulation, mesenchymal stem cells.

[1]
Berebichez-Fridman R, Montero-Olvera PR. Sources and Clinical Applications of Mesenchymal Stem Cells: State-of-the-art review. Sultan Qaboos Univ Med J 2018; 18(3): e264-77.
[2]
Barry FP, Murphy JM. Mesenchymal stem cells: clinical applications and biological characterization. Int J Biochem Cell Biol 2004; 36(4): 568-84.
[http://dx.doi.org/10.1016/j.biocel.2003.11.001] [PMID: 15010324]
[3]
Chen Y, Shao J-Z, Xiang L-X, Dong X-J, Zhang G-R. Mesenchymal stem cells: a promising candidate in regenerative medicine. Int J Biochem Cell Biol 2008; 40(5): 815-20.
[http://dx.doi.org/10.1016/j.biocel.2008.01.007] [PMID: 18295530]
[4]
Cotler HB, Chow RT, Hamblin MR, Carroll J. The Use of Low Level Laser Therapy (LLLT) For Musculoskeletal Pain. MOJ Orthop Rheumatol 2015; 2(5): 68.
[http://dx.doi.org/10.15406/mojor.2015.02.00068] [PMID: 26858986]
[5]
Chung H, Dai T, Sharma SK, Huang Y-Y, Carroll JD, Hamblin MR. The nuts and bolts of low-level laser (light) therapy. Ann Biomed Eng 2012; 40(2): 516-33.
[http://dx.doi.org/10.1007/s10439-011-0454-7] [PMID: 22045511]
[6]
de Freitas LF, Hamblin MR. Proposed Mechanisms of Photobiomodulation or Low-Level Light Therapy. IEEE J Sel Top Quantum Electron 2016; 22(3): 348-64.
[http://dx.doi.org/10.1109/JSTQE.2016.2561201] [PMID: 28070154]
[7]
Abrahamse H. Regenerative medicine, stem cells, and low-level laser therapy: future directives. Photomed Laser Surg 2012; 30(12): 681-2.
[http://dx.doi.org/10.1089/pho.2012.9881] [PMID: 23140266]
[8]
Stewart MC, Stewart AA. Mesenchymal stem cells: characteristics, sources, and mechanisms of action. Vet Clin North Am Equine Pract 2011; 27(2): 243-61.
[http://dx.doi.org/10.1016/j.cveq.2011.06.004] [PMID: 21872757]
[9]
Ilic D, Ogilvie C. Concise Review: Human Embryonic Stem Cells-What Have We Done? What Are We Doing? Where Are We Going? Stem Cells 2017; 35(1): 17-25.
[http://dx.doi.org/10.1002/stem.2450] [PMID: 27350255]
[10]
Romito A, Cobellis G. Pluripotent Stem Cells: Current Understanding and Future Directions. Stem Cells Int 2016; 20169451492
[http://dx.doi.org/10.1155/2016/9451492] [PMID: 26798367]
[11]
Condic ML. Totipotency: what it is and what it is not. Stem Cells Dev 2014; 23(8): 796-812.
[http://dx.doi.org/10.1089/scd.2013.0364] [PMID: 24368070]
[12]
Zakrzewski W, Dobrzyński M, Szymonowicz M, Rybak Z. Stem cells: past, present, and future. Stem Cell Res Ther 2019; 10(1): 68.
[http://dx.doi.org/10.1186/s13287-019-1165-5] [PMID: 30808416]
[13]
Han Y, Li X, Zhang Y, Han Y, Chang F, Ding J. Mesenchymal Stem Cells for Regenerative Medicine. Cells 2019; 8(8): 886.
[http://dx.doi.org/10.3390/cells8080886] [PMID: 31412678]
[14]
Fahy N, Alini M, Stoddart MJ. Mechanical stimulation of mesenchymal stem cells: Implications for cartilage tissue engineering. J Orthop Res 2017.
[http://dx.doi.org/10.1002/jor.23670] [PMID: 28763118]
[15]
Tamrin SH, Majedi FS, Tondar M, Sanati-Nezhad A, Hasani-Sadrabadi MM. Electromagnetic Fields and Stem Cell Fate: When Physics Meets Biology 2016; 63-97.
[16]
Marycz K, Kornicka K, Röcken M. Static Magnetic Field (SMF) as a Regulator of Stem Cell Fate - New Perspectives in Regenerative Medicine Arising from an Underestimated Tool. Stem Cell Rev Rep 2018; 14(6): 785-92.
[http://dx.doi.org/10.1007/s12015-018-9847-4] [PMID: 30225821]
[17]
Zhang Y, Yan J, Xu H, et al. Extremely low frequency electromagnetic fields promote mesenchymal stem cell migration by increasing intracellular Ca2+ and activating the FAK/Rho GTPases signaling pathways in vitro. Stem Cell Res Ther 2018; 9(1): 143.
[http://dx.doi.org/10.1186/s13287-018-0883-4] [PMID: 29784011]
[18]
Bloise N, Petecchia L, Ceccarelli G, et al. The effect of pulsed electromagnetic field exposure on osteoinduction of human mesenchymal stem cells cultured on nano-TiO2 surfaces. PLoS One 2018; 13(6)e0199046
[http://dx.doi.org/10.1371/journal.pone.0199046] [PMID: 29902240]
[19]
Fekrazad R, Asefi S, Allahdadi M, Kalhori KAM. Effect of Photobiomodulation on Mesenchymal Stem Cells. Photomed Laser Surg 2016; 34(11): 533-42.
[http://dx.doi.org/10.1089/pho.2015.4029] [PMID: 27070113]
[20]
Hiew VV, Simat SFB, Teoh PL. The Advancement of Biomaterials in Regulating Stem Cell Fate. Stem Cell Rev Rep 2018; 14(1): 43-57.
[http://dx.doi.org/10.1007/s12015-017-9764-y] [PMID: 28884292]
[21]
Avci P, Gupta A, Sadasivam M, et al. Low-level laser (light) therapy (LLLT) in skin: stimulating, healing, restoring. Semin Cutan Med Surg 2013; 32(1): 41-52.
[PMID: 24049929]
[22]
Jang D-H, Song D-H, Chang E-J, Jeon JY. Anti-inflammatory and lymphangiogenetic effects of low-level laser therapy on lymphedema in an experimental mouse tail model. Lasers Med Sci 2016; 31(2): 289-96.
[http://dx.doi.org/10.1007/s10103-015-1854-y] [PMID: 26714983]
[23]
Schneede P, Jelkmann W, Schramm U, Fricke H, Steinmetz M, Hofstetter A. Effects of the helium-neon laser on rat kidney epithelial cells in culture. Lasers Med Sci 1988; 3: 249-57.
[http://dx.doi.org/10.1007/BF02593820]
[24]
Song HJ, Seo H-J, Lee Y, Kim SK. Effectiveness of high-intensity laser therapy in the treatment of musculoskeletal disorders: A systematic review and meta-analysis of randomized controlled trials. Medicine (Baltimore) 2018; 97(51)e13126
[http://dx.doi.org/10.1097/MD.0000000000013126] [PMID: 30572425]
[25]
Bouvet-Gerbettaz S, Merigo E, Rocca J-P, Carle GF, Rochet N. Effects of low-level laser therapy on proliferation and differentiation of murine bone marrow cells into osteoblasts and osteoclasts. Lasers Surg Med 2009; 41(4): 291-7.
[http://dx.doi.org/10.1002/lsm.20759] [PMID: 19347941]
[26]
Kushibiki T, Hirasawa T, Okawa S, Ishihara M. Low reactive level laser therapy for mesenchymal stromal cells therapies. Stem Cells Int 2015; 2015974864
[http://dx.doi.org/10.1155/2015/974864] [PMID: 26273309]
[27]
Esmaeelinejad M, Bayat M, Darbandi H, Bayat M, Mosaffa N. The effects of low-level laser irradiation on cellular viability and proliferation of human skin fibroblasts cultured in high glucose mediums. Lasers Med Sci 2014; 29(1): 121-9.
[http://dx.doi.org/10.1007/s10103-013-1289-2] [PMID: 23455657]
[28]
Basso FG, Pansani TN, Turrioni APS, Bagnato VS, Hebling J, de Souza Costa CA. In vitro wound healing improvement by low-level laser therapy application in cultured gingival fibroblasts. Int J Dent 2012; 2012719452
[http://dx.doi.org/10.1155/2012/719452] [PMID: 22844284]
[29]
Góralczyk K, Szymańska J, Szot K, Fisz J, Rość D. Low-level laser irradiation effect on endothelial cells under conditions of hyperglycemia. Lasers Med Sci 2016; 31(5): 825-31.
[http://dx.doi.org/10.1007/s10103-016-1880-4] [PMID: 26861982]
[30]
Mantineo M, Pinheiro JP, Morgado AM. Low-level laser therapy on skeletal muscle inflammation: evaluation of irradiation parameters. J Biomed Opt 2014; 19(9): 98002.
[http://dx.doi.org/10.1117/1.JBO.19.9.098002] [PMID: 25200395]
[31]
Assis L, Yamashita F, Magri AMP, Fernandes KR, Yamauchi L, Renno ACM. Effect of low-level laser therapy (808 nm) on skeletal muscle after endurance exercise training in rats. Braz J Phys Ther 2015; 19(6): 457-65.
[http://dx.doi.org/10.1590/bjpt-rbf.2014.0113] [PMID: 26647747]
[32]
Sperandio FF, Simões A, Corrêa L, et al. Low-level laser irradiation promotes the proliferation and maturation of keratinocytes during epithelial wound repair. J Biophotonics 2015; 8(10): 795-803.
[http://dx.doi.org/10.1002/jbio.201400064] [PMID: 25411997]
[33]
Zhang C-P, Li S-D, Chen Y, Jiang Y-M, Chen P, Wang C-Z, et al. Stimulative Effects of Low Intensity He-Ne Laser Irradiation on the Proliferative Potential and Cell-Cycle Progression of Myoblasts in Culture. Int J Photoenergy 2014; 2014: 1-8.
[http://dx.doi.org/10.1155/2014/205839]
[34]
Chen CH, Tsai JL, Wang YH, Lee CL, Chen JK, Huang MH. Low-level laser irradiation promotes cell proliferation and mRNA expression of type I collagen and decorin in porcine Achilles tendon fibroblasts in vitro. J Orthop Res 2009; 27(5): 646-50.
[http://dx.doi.org/10.1002/jor.20800] [PMID: 18991342]
[35]
Fernandes AP, Junqueira MdeA, Marques NC, et al. Effects of low-level laser therapy on stem cells from human exfoliated deciduous teeth. J Appl Oral Sci 2016; 24(4): 332-7.
[http://dx.doi.org/10.1590/1678-775720150275] [PMID: 27556203]
[36]
Kushibiki T, Ishihara M. Biological Function of Low Reactive Level Laser Therapy (LLLT). Photomed. - Adv. Clin. Pract., InTech 2017.
[http://dx.doi.org/10.5772/65747]
[37]
Coombe AR, Ho C-TG, Darendeliler MA, et al. The effects of low level laser irradiation on osteoblastic cells. Clin Orthod Res 2001; 4(1): 3-14.
[http://dx.doi.org/10.1034/j.1600-0544.2001.040102.x] [PMID: 11553080]
[38]
Hu W-P, Wang J-J, Yu C-L, Lan C-CE, Chen G-S, Yu H-S. Helium-neon laser irradiation stimulates cell proliferation through photostimulatory effects in mitochondria. J Invest Dermatol 2007; 127(8): 2048-57.
[http://dx.doi.org/10.1038/sj.jid.5700826] [PMID: 17446900]
[39]
Hamblin MR, Demidova TN. Mechanisms of low level light therapy. Proc of SPIE 2006 ; Vol. ; 6140614001
[http://dx.doi.org/10.1117/12.646294]
[40]
Karu TI, Pyatibrat LV, Afanasyeva NI. Cellular effects of low power laser therapy can be mediated by nitric oxide. Lasers Surg Med 2005; 36(4): 307-14.
[http://dx.doi.org/10.1002/lsm.20148] [PMID: 15739174]
[41]
Peplow PV, Chung T-Y, Ryan B, Baxter GD. Laser photobiomodulation of gene expression and release of growth factors and cytokines from cells in culture: a review of human and animal studies. Photomed Laser Surg 2011; 29(5): 285-304.
[http://dx.doi.org/10.1089/pho.2010.2846] [PMID: 21309703]
[42]
Lavi R, Shainberg A, Friedmann H, et al. Low energy visible light induces reactive oxygen species generation and stimulates an increase of intracellular calcium concentration in cardiac cells. J Biol Chem 2003; 278(42): 40917-22.
[http://dx.doi.org/10.1074/jbc.M303034200] [PMID: 12851407]
[43]
Kokoska ER, Wolff AB, Smith GS, Miller TA. Epidermal growth factor-induced cytoprotection in human intestinal cells involves intracellular calcium signaling. J Surg Res 2000; 88(2): 97-103.
[http://dx.doi.org/10.1006/jsre.1999.5740] [PMID: 10644473]
[44]
Lou Z, Zhang C, Gong T, Xue C, Scholp A, Jiang JJ. Wound-healing effects of 635-nm low-level laser therapy on primary human vocal fold epithelial cells: an in vitro study. Lasers Med Sci 2019; 34(3): 547-54.
[http://dx.doi.org/10.1007/s10103-018-2628-0] [PMID: 30244401]
[45]
Szezerbaty SKF, de Oliveira RF, Pires-Oliveira DAA, Soares CP, Sartori D, Poli-Frederico RC. The effect of low-level laser therapy (660 nm) on the gene expression involved in tissue repair. Lasers Med Sci 2018; 33(2): 315-21.
[http://dx.doi.org/10.1007/s10103-017-2375-7] [PMID: 29159515]
[46]
Hawkins D, Abrahamse H. Effect of multiple exposures of low-level laser therapy on the cellular responses of wounded human skin fibroblasts. Photomed Laser Surg 2006; 24(6): 705-14.
[http://dx.doi.org/10.1089/pho.2006.24.705] [PMID: 17199470]
[47]
Zhou D, Shao L, Spitz DR. Reactive Oxygen Species in Normal and Tumor Stem Cells 2014; 1-67..
[http://dx.doi.org/10.1016/B978-0-12-420117-0.00001-3]
[48]
Wu Z-H, Zhou Y, Chen J-Y, Zhou L-W. Mitochondrial signaling for histamine releases in laser-irradiated RBL-2H3 mast cells. Lasers Surg Med 2010; 42(6): 503-9.
[http://dx.doi.org/10.1002/lsm.20924] [PMID: 20662027]
[49]
Hamblin MR. Mechanisms and Mitochondrial Redox Signaling in Photobiomodulation. Photochem Photobiol 2018; 94(2): 199-212.
[http://dx.doi.org/10.1111/php.12864] [PMID: 29164625]
[50]
Sommer AP. Revisiting the Photon/Cell Interaction Mechanism in Low-Level Light Therapy. Photobiomodul Photomed Laser Surg 2019; 37(6): 336-41.
[http://dx.doi.org/10.1089/photob.2018.4606] [PMID: 31107170]
[51]
Zhang W, Liu HT. MAPK signal pathways in the regulation of cell proliferation in mammalian cells. Cell Res 2002; 12(1): 9-18.
[http://dx.doi.org/10.1038/sj.cr.7290105] [PMID: 11942415]
[52]
Merighi S, Benini A, Mirandola P, et al. Modulation of the Akt/Ras/Raf/MEK/ERK pathway by A3 adenosine receptor. Purinergic Signal 2006; 2(4): 627-32.
[http://dx.doi.org/10.1007/s11302-006-9020-4] [PMID: 18404465]
[53]
Eblen ST. Extracellular-Regulated Kinases: Signaling From Ras to ERK Substrates to Control Biological Outcomes 2018;; 99-142..
[54]
Rubinfeld H, Seger R. The ERK cascade: a prototype of MAPK signaling. Mol Biotechnol 2005; 31(2): 151-74.
[http://dx.doi.org/10.1385/MB:31:2:151] [PMID: 16170216]
[55]
Kim JE, Woo YJ, Sohn KM, Jeong KH, Kang H. Wnt/β-catenin and ERK pathway activation: A possible mechanism of photobiomodulation therapy with light-emitting diodes that regulate the proliferation of human outer root sheath cells. Lasers Surg Med 2017; 49(10): 940-7.
[http://dx.doi.org/10.1002/lsm.22736] [PMID: 28944964]
[56]
Song S, Zhou F, Chen WR. Low-level laser therapy regulates microglial function through Src-mediated signaling pathways: implications for neurodegenerative diseases. J Neuroinflammation 2012; 9: 219.
[http://dx.doi.org/10.1186/1742-2094-9-219] [PMID: 22989325]
[57]
Zhang J, Xing D, Gao X. Low-power laser irradiation activates Src tyrosine kinase through reactive oxygen species-mediated signaling pathway. J Cell Physiol 2008; 217(2): 518-28.
[http://dx.doi.org/10.1002/jcp.21529] [PMID: 18615581]
[58]
Partovian C, Simons M. Regulation of protein kinase B/Akt activity and Ser473 phosphorylation by protein kinase Calpha in endothelial cells. Cell Signal 2004; 16(8): 951-7.
[http://dx.doi.org/10.1016/j.cellsig.2004.01.008] [PMID: 15157674]
[59]
Kassenbrock CK, Hunter S, Garl P, Johnson GL, Anderson SM. Inhibition of Src family kinases blocks epidermal growth factor (EGF)-induced activation of Akt, phosphorylation of c-Cbl, and ubiquitination of the EGF receptor. J Biol Chem 2002; 277(28): 24967-75.
[http://dx.doi.org/10.1074/jbc.M201026200] [PMID: 11994282]
[60]
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(3): 553-62.
[http://dx.doi.org/10.1002/jcp.21697] [PMID: 19142866]
[61]
Karu T. Primary and secondary mechanisms of action of visible to near-IR radiation on cells. J Photochem Photobiol B 1999; 49(1): 1-17.
[http://dx.doi.org/10.1016/S1011-1344(98)00219-X] [PMID: 10365442]
[62]
Wang X, McCullough KD, Franke TF, Holbrook NJ. Epidermal growth factor receptor-dependent Akt activation by oxidative stress enhances cell survival. J Biol Chem 2000; 275(19): 14624-31.
[http://dx.doi.org/10.1074/jbc.275.19.14624] [PMID: 10799549]
[63]
Huang Y-Y, Chen AC-H, Carroll JD, Hamblin MR. Biphasic dose response in low level light therapy. Dose Response 2009; 7(4): 358-83.
[http://dx.doi.org/10.2203/dose-response.09-027.Hamblin] [PMID: 20011653]
[64]
Gao X, Xing D. Molecular mechanisms of cell proliferation induced by low power laser irradiation. J Biomed Sci 2009; 16: 4.
[http://dx.doi.org/10.1186/1423-0127-16-4] [PMID: 19272168]
[65]
Boulton M, Marshall J. He-Ne laser stimulation of human fibroblast proliferation and attachment in vitro. Lasers Life Sci 1986; 1(2): 125-34.
[66]
Karu TI. Effects of visible radiation on cultured cells. Photochem Photobiol 1990; 52(6): 1089-98.
[http://dx.doi.org/10.1111/j.1751-1097.1990.tb08450.x] [PMID: 2087499]
[67]
Hamblin MR. Shining light on the head: Photobiomodulation for brain disorders. BBA Clin 2016; 6: 113-24.
[http://dx.doi.org/10.1016/j.bbacli.2016.09.002] [PMID: 27752476]
[68]
Ferraresi C, Kaippert B, Avci P, et al. Low-level laser (light) therapy increases mitochondrial membrane potential and ATP synthesis in C2C12 myotubes with a peak response at 3-6 h. Photochem Photobiol 2015; 91(2): 411-6.
[http://dx.doi.org/10.1111/php.12397] [PMID: 25443662]
[69]
Tan S, Wu T, Zhang D, Zhang Z. Cell or cell membrane-based drug delivery systems. Theranostics 2015; 5(8): 863-81.
[http://dx.doi.org/10.7150/thno.11852] [PMID: 26000058]
[70]
Schneckenburger H, Hendinger A, Sailer R, Strauss WSL, Schmitt M. Laser-assisted optoporation of single cells. J Biomed Opt 2002; 7(3): 410-6.
[http://dx.doi.org/10.1117/1.1485758] [PMID: 12175291]
[71]
da Silva JP, da Silva MA, Almeida APF, Lombardi Junior I, Matos AP. Laser therapy in the tissue repair process: a literature review. Photomed Laser Surg 2010; 28(1): 17-21.
[http://dx.doi.org/10.1089/pho.2008.2372] [PMID: 19764898]
[72]
Barboza CAG, Ginani F, Soares DM, Henriques ÁCG, Freitas R de A. Low-level laser irradiation induces in vitro proliferation of mesenchymal stem cells. Einstein (Sao Paulo) 2014; 12(1): 75-81.
[http://dx.doi.org/10.1590/S1679-45082014AO2824] [PMID: 24728250]
[73]
Ginani F, Soares DM, Rocha HAO, Barboza CAG. Low-level laser irradiation promotes proliferation of cryopreserved adipose-derived stem cells. Einstein (Sao Paulo) 2017; 15(3): 334-8.
[http://dx.doi.org/10.1590/s1679-45082017ao3991] [PMID: 29091156]
[74]
Wang Y, Huang Y-Y, Wang Y, Lyu P, Hamblin MR. Red (660 nm) or near-infrared (810 nm) photobiomodulation stimulates, while blue (415 nm), green (540 nm) light inhibits proliferation in human adipose-derived stem cells. Sci Rep 2017; 7(1): 7781.
[http://dx.doi.org/10.1038/s41598-017-07525-w] [PMID: 28798481]
[75]
Emelyanov AN, Kiryanova VV. Photomodulation of proliferation and differentiation of stem cells by the visible and infrared light. Photomed Laser Surg 2015; 33(3): 164-74.
[http://dx.doi.org/10.1089/pho.2014.3830] [PMID: 25692649]
[76]
de Villiers JA, Houreld NN, Abrahamse H. Influence of low intensity laser irradiation on isolated human adipose derived stem cells over 72 hours and their differentiation potential into smooth muscle cells using retinoic acid. Stem Cell Rev Rep 2011; 7(4): 869-82.
[http://dx.doi.org/10.1007/s12015-011-9244-8] [PMID: 21373882]
[77]
Giannelli M, Chellini F, Sassoli C, et al. Photoactivation of bone marrow mesenchymal stromal cells with diode laser: effects and mechanisms of action. J Cell Physiol 2013; 228(1): 172-81.
[http://dx.doi.org/10.1002/jcp.24119] [PMID: 22628164]
[78]
Mvula B, Moore TJ, Abrahamse H. Effect of low-level laser irradiation and epidermal growth factor on adult human adipose-derived stem cells. Lasers Med Sci 2010; 25(1): 33-9.
[http://dx.doi.org/10.1007/s10103-008-0636-1] [PMID: 19172344]
[79]
Amid R, Kadkhodazadeh M, Ahsaie MG, Hakakzadeh A. Effect of low level laser therapy on proliferation and differentiation of the cells contributing in bone regeneration. J Lasers Med Sci 2014; 5(4): 163-70.
[PMID: 25653816]
[80]
Ginani F, Soares DM, Barreto MP e V, Barboza CAG. Effect of low-level laser therapy on mesenchymal stem cell proliferation: a systematic review. Lasers Med Sci 2015; 30(8): 2189-94.
[http://dx.doi.org/10.1007/s10103-015-1730-9] [PMID: 25764448]
[81]
Bloise N, Ceccarelli G, Minzioni P, et al. Investigation of low-level laser therapy potentiality on proliferation and differentiation of human osteoblast-like cells in the absence/presence of osteogenic factors. J Biomed Opt 2013; 18(12)128006
[http://dx.doi.org/10.1117/1.JBO.18.12.128006] [PMID: 24365957]
[82]
Fekrazad R, Eslaminejad MB, Shayan AM, Kalhori KAM, Abbas FM, Taghiyar L, et al. artilage Defects in a Rabbit MoEffects of Photobiomodulation and Mesenchymal Stem Cells on Articular Cdel. Photomed Laser Surg 2016; 34: 543-9.
[http://dx.doi.org/10.1089/pho.2015.4028] [PMID: 27058019]
[83]
Jawad MM, Husein A, Azlina A, Alam MK, Hassan R, Shaari R. Effect of 940 nm low-level laser therapy on osteogenesis in vitro. J Biomed Opt 2013; 18(12)128001
[http://dx.doi.org/10.1117/1.JBO.18.12.128001] [PMID: 24337495]
[84]
Fekrazad R, Asefi S, Baghaban Eslaminejad MB, Taghiar L, Bordbar S, Hamblin MR. Photobiomodulation with single and combination laser wavelengths on bone marrow mesenchymal stem cells: proliferation and differentiation to bone or cartilage. Lasers Med Sci 2019; 34(1): 115-26.
[http://dx.doi.org/10.1007/s10103-018-2620-8] [PMID: 30264177]
[85]
Choi K, Kang B-J, Kim H, et al. Low-level laser therapy promotes the osteogenic potential of adipose-derived mesenchymal stem cells seeded on an acellular dermal matrix. J Biomed Mater Res B Appl Biomater 2013; 101(6): 919-28.
[http://dx.doi.org/10.1002/jbm.b.32897] [PMID: 23529895]
[86]
Soleimani M, Abbasnia E, Fathi M, Sahraei H, Fathi Y, Kaka G. The effects of low-level laser irradiation on differentiation and proliferation of human bone marrow mesenchymal stem cells into neurons and osteoblasts--an in vitro study. Lasers Med Sci 2012; 27(2): 423-30.
[http://dx.doi.org/10.1007/s10103-011-0930-1] [PMID: 21597948]
[87]
Liao X, Li S-H, Xie G-H, et al. Preconditioning With Low-Level Laser Irradiation Enhances the Therapeutic Potential of Human Adipose-derived Stem Cells in a Mouse Model of Photoaged Skin. Photochem Photobiol 2018; 94(4): 780-90.
[http://dx.doi.org/10.1111/php.12912] [PMID: 29457847]
[88]
Wang Y-H, Wu J-Y, Kong SC, et al. Low power laser irradiation and human adipose-derived stem cell treatments promote bone regeneration in critical-sized calvarial defects in rats. PLoS One 2018; 13(4)e0195337
[http://dx.doi.org/10.1371/journal.pone.0195337] [PMID: 29621288]
[89]
Lucke LD, Bortolazzo FO, Theodoro V, et al. Low-level laser and adipose-derived stem cells altered remodelling genes expression and improved collagen reorganization during tendon repair. Cell Prolif 2019; 52(3)e12580
[http://dx.doi.org/10.1111/cpr.12580] [PMID: 30734394]
[90]
Pasternak‐-Mnich K, Ziemba B, Szwed A, Kopacz K, Synder M, Bryszewska M, et als Effect Of Photobiomodulation Therapy On The Increase Of Viability And Proliferation Of Human Mesenchymal Stem Cells. Lasers Surg Med 2019.
[http://dx.doi.org/10.1002/lsm.23107]
[91]
de Lima RDN, Vieira SS, Antonio EL, et al. Low-level laser therapy alleviates the deleterious effect of doxorubicin on rat adipose tissue-derived mesenchymal stem cells. J Photochem Photobiol B 2019; 196111512
[http://dx.doi.org/10.1016/j.jphotobiol.2019.111512] [PMID: 31129505]
[92]
Babaee A, Nematollahi-Mahani SN, Dehghani-Soltani S, Shojaei M, Ezzatabadipour M. Photobiomodulation and gametogenic potential of human Wharton’s jelly-derived mesenchymal cells. Biochem Biophys Res Commun 2019; 514(1): 239-45.
[http://dx.doi.org/10.1016/j.bbrc.2019.04.059] [PMID: 31029424]
[93]
Kim K, Lee J, Jang H, et al. Photobiomodulation Enhances the Angiogenic Effect of Mesenchymal Stem Cells to Mitigate Radiation-Induced Enteropathy. Int J Mol Sci 2019; 20(5): 1131.
[http://dx.doi.org/10.3390/ijms20051131] [PMID: 30841658]
[94]
Han B, Fan J, Liu L, et al. Adipose-derived mesenchymal stem cells treatments for fibroblasts of fibrotic scar via downregulating TGF-β1 and Notch-1 expression enhanced by photobiomodulation therapy. Lasers Med Sci 2019; 34(1): 1-10.
[http://dx.doi.org/10.1007/s10103-018-2567-9] [PMID: 30367294]
[95]
Ferreira LS, Diniz IMA, Maranduba CMS, et al. Short-term evaluation of photobiomodulation therapy on the proliferation and undifferentiated status of dental pulp stem cells. Lasers Med Sci 2019; 34(4): 659-66.
[http://dx.doi.org/10.1007/s10103-018-2637-z] [PMID: 30250986]
[96]
Chen H, Wu H, Yin H, et al. Effect of photobiomodulation on neural differentiation of human umbilical cord mesenchymal stem cells. Lasers Med Sci 2019; 34(4): 667-75.
[http://dx.doi.org/10.1007/s10103-018-2638-y] [PMID: 30232645]
[97]
Tani A, Chellini F, Giannelli M, Nosi D, Zecchi-Orlandini S, Sassoli C. Red (635 nm), Near-Infrared (808 nm) and Violet-Blue (405 nm) Photobiomodulation Potentiality on Human Osteoblasts and Mesenchymal Stromal Cells: A Morphological and Molecular In Vitro Study. Int J Mol Sci 2018; 19(7): 1946.
[http://dx.doi.org/10.3390/ijms19071946] [PMID: 29970828]
[98]
Priglinger E, Maier J, Chaudary S, et al. Photobiomodulation of freshly isolated human adipose tissue-derived stromal vascular fraction cells by pulsed light-emitting diodes for direct clinical application. J Tissue Eng Regen Med 2018; 12(6): 1352-62.
[http://dx.doi.org/10.1002/term.2665] [PMID: 29603903]
[99]
Amaroli A, Agas D, Laus F, et al. The Effects of Photobiomodulation of 808 nm Diode Laser Therapy at Higher Fluence on the in Vitro Osteogenic Differentiation of Bone Marrow Stromal Cells. Front Physiol 2018; 9: 123.
[http://dx.doi.org/10.3389/fphys.2018.00123] [PMID: 29527174]
[100]
Stancker TG, Vieira SS, Serra AJ, et al. Can photobiomodulation associated with implantation of mesenchymal adipose-derived stem cells attenuate the expression of MMPs and decrease degradation of type II collagen in an experimental model of osteoarthritis? Lasers Med Sci 2018; 33(5): 1073-84.
[http://dx.doi.org/10.1007/s10103-018-2466-0] [PMID: 29520686]
[101]
Peat FJ, Colbath AC, Bentsen LM, Goodrich LR, King MR. In Vitro Effects of High-Intensity Laser Photobiomodulation on Equine Bone Marrow-Derived Mesenchymal Stem Cell Viability and Cytokine Expression. Photomed Laser Surg 2018; 36(2): 83-91.
[http://dx.doi.org/10.1089/pho.2017.4344] [PMID: 29131717]
[102]
Farfara D, Tuby H, Trudler D, et al. Low-level laser therapy ameliorates disease progression in a mouse model of Alzheimer’s disease. J Mol Neurosci 2015; 55(2): 430-6.
[http://dx.doi.org/10.1007/s12031-014-0354-z] [PMID: 24994540]
[103]
de Oliveira TS, Serra AJ, Manchini MT, et al. Effects of low level laser therapy on attachment, proliferation, and gene expression of VEGF and VEGF receptor 2 of adipocyte-derived mesenchymal stem cells cultivated under nutritional deficiency. Lasers Med Sci 2015; 30(1): 217-23.
[http://dx.doi.org/10.1007/s10103-014-1646-9] [PMID: 25192841]
[104]
Huertas RM, Luna-Bertos ED, Ramos-Torrecillas J, Leyva FM, Ruiz C, García-Martínez O. Effect and clinical implications of the low-energy diode laser on bone cell proliferation. Biol Res Nurs 2014; 16(2): 191-6.
[http://dx.doi.org/10.1177/1099800413482695] [PMID: 23559459]
[105]
Migliario M, Pittarella P, Fanuli M, Rizzi M, Renò F. Laser-induced osteoblast proliferation is mediated by ROS production. Lasers Med Sci 2014; 29(4): 1463-7.
[http://dx.doi.org/10.1007/s10103-014-1556-x] [PMID: 24595962]
[106]
Wu J-Y, Chen C-H, Yeh L-Y, Yeh M-L, Ting C-C, Wang Y-H. Low-power laser irradiation promotes the proliferation and osteogenic differentiation of human periodontal ligament cells via cyclic adenosine monophosphate. Int J Oral Sci 2013; 5(2): 85-91.
[http://dx.doi.org/10.1038/ijos.2013.38] [PMID: 23788285]
[107]
Pyo S-J, Song W-W, Kim I-R, et al. Low-level laser therapy induces the expressions of BMP-2, osteocalcin, and TGF-β1 in hypoxic-cultured human osteoblasts. Lasers Med Sci 2013; 28(2): 543-50.
[http://dx.doi.org/10.1007/s10103-012-1109-0] [PMID: 22552925]
[108]
Leonida A, Paiusco A, Rossi G, Carini F, Baldoni M, Caccianiga G. Effects of low-level laser irradiation on proliferation and osteoblastic differentiation of human mesenchymal stem cells seeded on a three-dimensional biomatrix: in vitro pilot study. Lasers Med Sci 2013; 28(1): 125-32.
[http://dx.doi.org/10.1007/s10103-012-1067-6] [PMID: 22447402]
[109]
Soares DM, Ginani F, Henriques ÁG, Barboza CAG. Effects of laser therapy on the proliferation of human periodontal ligament stem cells. Lasers Med Sci 2015; 30(3): 1171-4.
[http://dx.doi.org/10.1007/s10103-013-1436-9] [PMID: 24013624]
[110]
Anwer AG, Gosnell ME, Perinchery SM, Inglis DW, Goldys EM. Visible 532 nm laser irradiation of human adipose tissue-derived stem cells: effect on proliferation rates, mitochondria membrane potential and autofluorescence. Lasers Surg Med 2012; 44(9): 769-78.
[http://dx.doi.org/10.1002/lsm.22083] [PMID: 23047589]
[111]
Wu YH, Wang J, Gong DX, Gu HY, Hu SS, Zhang H. Effects of low-level laser irradiation on mesenchymal stem cell proliferation: a microarray analysis. Lasers Med Sci 2012; 27(2): 509-19.
[http://dx.doi.org/10.1007/s10103-011-0995-x] [PMID: 21956279]
[112]
Pereira LO, Longo JPF, Azevedo RB. Laser irradiation did not increase the proliferation or the differentiation of stem cells from normal and inflamed dental pulp. Arch Oral Biol 2012; 57(8): 1079-85.
[http://dx.doi.org/10.1016/j.archoralbio.2012.02.012] [PMID: 22469390]
[113]
Kim H, Choi K, Kweon O-K, Kim WH. Enhanced wound healing effect of canine adipose-derived mesenchymal stem cells with low-level laser therapy in athymic mice. J Dermatol Sci 2012; 68(3): 149-56.
[http://dx.doi.org/10.1016/j.jdermsci.2012.09.013] [PMID: 23084629]
[114]
Wu J-Y, Wang Y-H, Wang G-J, et al. Low-power GaAlAs laser irradiation promotes the proliferation and osteogenic differentiation of stem cells via IGF1 and BMP2. PLoS One 2012; 7(9)e44027
[http://dx.doi.org/10.1371/journal.pone.0044027] [PMID: 22962596]
[115]
Wang J, Huang W, Wu Y, et al. MicroRNA-193 pro-proliferation effects for bone mesenchymal stem cells after low-level laser irradiation treatment through inhibitor of growth family, member 5. Stem Cells Dev 2012; 21(13): 2508-19.
[http://dx.doi.org/10.1089/scd.2011.0695] [PMID: 22384930]
[116]
Peng F, Wu H, Zheng Y, Xu X, Yu J. The effect of noncoherent red light irradiation on proliferation and osteogenic differentiation of bone marrow mesenchymal stem cells. Lasers Med Sci 2012; 27(3): 645-53.
[http://dx.doi.org/10.1007/s10103-011-1005-z] [PMID: 22016038]
[117]
Tuby H, Maltz L, Oron U. Induction of autologous mesenchymal stem cells in the bone marrow by low-level laser therapy has profound beneficial effects on the infarcted rat heart. Lasers Surg Med 2011; 43(5): 401-9.
[http://dx.doi.org/10.1002/lsm.21063] [PMID: 21674545]
[118]
Aleksic V, Aoki A, Iwasaki K, et al. Low-level Er:YAG laser irradiation enhances osteoblast proliferation through activation of MAPK/ERK. Lasers Med Sci 2010; 25(4): 559-69.
[http://dx.doi.org/10.1007/s10103-010-0761-5] [PMID: 20186556]
[119]
Renno ACM, McDonnell PA, Crovace MC, Zanotto ED, Laakso E-L. Effect of 830-nm laser phototherapy on olfactory neuronal ensheathing cells grown in vitro on novel bioscaffolds J Appl Biomater Funct Mater 2015;; 13: 0-0.
[120]
Li W-T, Leu Y-C, Wu J-L. Red-light light-emitting diode irradiation increases the proliferation and osteogenic differentiation of rat bone marrow mesenchymal stem cells. Photomed Laser Surg 2010; 28(Suppl. 1): S157-65.
[http://dx.doi.org/10.1089/pho.2009.2540] [PMID: 20583914]
[121]
Kushibiki T, Awazu K. Blue laser irradiation enhances extracellular calcification of primary mesenchymal stem cells. Photomed Laser Surg 2009; 27(3): 493-8.
[http://dx.doi.org/10.1089/pho.2008.2343] [PMID: 19405859]
[122]
Horvát-Karajz K, Balogh Z, Kovács V, Drrernat AH, Sréter L, Uher F. In vitro effect of carboplatin, cytarabine, paclitaxel, vincristine, and low-power laser irradiation on murine mesenchymal stem cells. Lasers Surg Med 2009; 41(6): 463-9.
[http://dx.doi.org/10.1002/lsm.20791] [PMID: 19588531]
[123]
Kim HK, Kim JH, Abbas AA, et al. Red light of 647 nm enhances osteogenic differentiation in mesenchymal stem cells. Lasers Med Sci 2009; 24(2): 214-22.
[http://dx.doi.org/10.1007/s10103-008-0550-6] [PMID: 18386092]


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VOLUME: 15
ISSUE: 5
Year: 2020
Published on: 21 July, 2020
Page: [400 - 413]
Pages: 14
DOI: 10.2174/1574888X15666200204123722
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