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Laser photobiomodulation influences the expression of genes related to the inflammatory process and muscle cell differentiation during the process of muscle healing

Einfluss der Laser-Photobiomodulation auf die Genexpression als Reaktion auf Entzündungsprozesse und Muskelzelldifferenzierung während der Muskelheilung
  • Natalia Camargo Rodrigues EMAIL logo , Roberta Brunelli , Heloísa Selistre de Araújo , Nivaldo Antonio Parizotto and Ana Claudia Muniz Renno
Published/Copyright: November 20, 2013
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Abstract

Background and objective: The aim of this study was to evaluate the effects of 780-nm laser therapy on the expression of genes related to muscle healing.

Materials and methods: Sixty-three rats were distributed into three groups: 1) injured control group (CG), 2) injured treatment group at 10 J/cm2 (G10), and 3) injured treatment group at 50 J/cm2 (G50). Histopathological analysis and mRNA genes expression were evaluated after 7, 14 and 21 days post-injury.

Results: At day 7, G10 presented a smaller necrosis area compared to CG and G50. Fourteen days post-surgery, G10 and G50 presented a smaller amount of inflammatory cells and a better tissue organization compared to CG. On day 21, G10 and G50 showed better muscle structure than the control. A significantly decreased COX-2 expression was observed in groups G10 and G50 at day 7 compared to the control animals. No difference was found among the experimental groups after 14 days, but G50 presented statistically higher COX-2 down-regulation at day 21. VEGF expression decreased in the first period analyzed in both treatment groups, increased after 14 days in G10, and increased after 21 days in G50. Both irradiated groups had a higher MyoD expression in all the evaluated periods and myogenin levels increased after 14 days in both treatment groups and in G10 after 21 days.

Conclusion: 780-nm laser therapy had positive effects during muscle regeneration through the gene expression modulation related to the inflammatory process and the new muscle fibers formation, in both fluencies used in the present study, but the fluence of 10 J/cm2 was more efficient.

Zusammenfassung

Hintergrund und Zielsetzung: Das Ziel dieser Studie war es, die Auswirkungen der 780 nm-Laserherapie auf die im Zusammenhang mit der Muskelheilung stehende Genexpression zu bewerten.

Materialien und Methoden: Für die Studie wurden 63 Ratten in drei Gruppen aufgeteilt: 1) verletzte Kontrollgruppe ohne Therapie (CG), 2) verletzte Behandlungsgruppe mit 10 J/cm2 (G10) und 3) verletzte Behandlungsgruppe mit 50 J/cm2 (G50). Die histopathologische Analyse sowie die Bestimmung der Genexpression (mRNA-Expression) erfolgte jeweils 7, 14 und 21 Tage nach der Verletzung.

Ergebnisse: Am Tag 7 wurde in der G10-Gruppe im Vergleich zu den beiden anderen Untersuchungsgruppen CG und G50 ein kleinerer Nekrosebereich festgestellt. Vierzehn Tage nach der Operation zeigten sich in den beiden Behandlungsgruppen G10 und G50 eine kleinere Menge von Entzündungszellen und eine bessere Gewebeorganisation als in der Kontrollgruppe CG. Am Tag 21 erwies sich die Muskelstruktur in den beiden behandelten Gruppen G10 und G50 besser als in der Kontrollgruppe. Nach 7 Tagen wurde im Vergleich zu den Kontrolltieren eine verminderte COX2-Expression in den Gruppen G10 und G50 beobachtet. Es wurde aber kein Unterschied zwischen den experimentellen Gruppen nach 14 Tagen gefunden. Hingegen war die Down-Regulierung der COX2-Expression am Tag 21 in der G50-Gruppe statistisch höher. Die VEGF-Expression sank zunächst in beiden Behandlungsgruppen, erhöhte sich nach 14 Tagen in der G10-Gruppe und nach 21 Tagen in der G50-Gruppe. Beide bestrahlten Gruppen hatten an allen beobachteten Tagen eine höhere MyoD-Expression; der Myogenin-Anteil stieg nach 14 Tagen in beiden behandelten Gruppen an und war nach 21 Tagen in der G10-Gruppe am höchsten.

Fazit: Die 780 nm-Lasertherapie hatte für beide in der Studie untersuchten Bestrahlungsstärken einen positiven Effekt bei der Regeneration der Muskulatur durch die Modulation der Genexpression in Bezug auf die Entzündung und die neue Muskelfaserbildung, allerdings war eine Laserbestrahlung mit 10 J/cm2 effektiver.


Corresponding author: Natalia Camargo Rodrigues, Department of Physiotherapy, Federal University of São Carlos, Rodovia Washington Luís (SP-310), Km 235, Postcode: 13565-905, São Carlos, SP, Brazil, e-mail:

This work was supported by “Coordenação de Aperfeiçoamento de Pessoal de Nível Superior” (CAPES Foundation-20226300).

References

[1] Silveira PC, Silva LA, Fraga DB, Freitas TP, Streck EL, Pinho R. Evaluation of mitochondrial respiratory chain activity in muscle healing by low-level laser therapy. J Photochem Photobiol B 2009;95(2):89–92.10.1016/j.jphotobiol.2009.01.004Search in Google Scholar PubMed

[2] Mesquita-Ferrari RA, Martins MD, Silva JA Jr, da Silva TD, Piovesan RF, Pavesi VC, Bussadori SK, Fernandes KP. Effects of low-level laser therapy on expression of TNF-α and TGF-β in skeletal muscle during the repair process. Lasers Med Sci 2011;26(3):335–40.10.1007/s10103-010-0850-5Search in Google Scholar PubMed

[3] Pereira Lopes FR, Lisboa BC, Frattini F, Almeida FM, Tomaz MA, Matsumoto PK, Langone F, Lora S, Melo PA, Borojevic R, Han SW, Martinez AM. Enhancement of sciatic nerve regeneration after vascular endothelial growth factor (VEGF) gene therapy. Neuropathol Appl Neurobiol 2011;37(6):600–12.10.1111/j.1365-2990.2011.01159.xSearch in Google Scholar PubMed

[4] Chargé SB, Rudnicki MA. Cellular and molecular regulation of muscle regeneration. Physiol Rev 2004;84(1):209–38.10.1152/physrev.00019.2003Search in Google Scholar PubMed

[5] Yahiaoui L, Gvozdic D, Danialou G, Mack M, Petrof BJ. CC family chemokines directly regulate myoblast responses to skeletal muscle injury. J Physiol 2008;586(16):3991–4004.10.1113/jphysiol.2008.152090Search in Google Scholar PubMed PubMed Central

[6] Ehrhardt J, Morgan J. Regenerative capacity of skeletal muscle. Curr Opin Neurol 2005;18(5):548–53.10.1097/01.wco.0000177382.62156.82Search in Google Scholar PubMed

[7] Kuang S, Kuroda K, Le Grand F, Rudnicki MA. Asymmetric self-renewal and commitment of satellite stem cells in muscle. Cell 2007;129(5):999–1010.10.1016/j.cell.2007.03.044Search in Google Scholar PubMed PubMed Central

[8] Warren GL, Summan M, Gao X, Chapman R, Hulderman T, Simeonova PP. Mechanisms of skeletal muscle injury and repair revealed by gene expression studies in mouse models. J Physiol 2007;582(Pt 2):825–41.10.1113/jphysiol.2007.132373Search in Google Scholar PubMed PubMed Central

[9] Järvinen TA, Järvinen TL, Kääriäinen M, Aärimaa V, Vaittinen S, Kalimo H, Järvinen M. Muscle injuries: optimising recovery. Best Pract Res Clin Rheumatol 2007;21(2):317–31.10.1016/j.berh.2006.12.004Search in Google Scholar PubMed

[10] Rennó AC, Toma RL, Feitosa SM, Fernandes K, Bossini PS, de Oliveira P, Parizotto N, Ribeiro DA. Comparative effects of low-intensity pulsed ultrasound and low-level laser therapy on injured skeletal muscle. Photomed Laser Surg 2011;29(1):5–10.10.1089/pho.2009.2715Search in Google Scholar PubMed

[11] Minamoto VB, Bunho SR, Salvini TF. Regenerated rat skeletal muscle after periodic contusions. Braz J Med Biol Res 2001;34(11):1447–52.10.1590/S0100-879X2001001100012Search in Google Scholar PubMed

[12] Baptista J, Martins MD, Pavesi VC, Bussadori SK, Fernandes KP, Pinto Júnior Ddos S, Ferrari RA. Influence of laser photobiomodulation on collagen IV during skeletal muscle tissue remodeling after injury in rats. Photomed Laser Surg 2011;29(1):11–7.10.1089/pho.2009.2737Search in Google Scholar PubMed

[13] Pinheiro AL, Soares LG, Aciole GT, Correia NA, Barbosa AF, Ramalho LM, Dos Santos JN. Light microscopic description of the effects of laser phototherapy on bone defects grafted with mineral trioxide aggregate, bone morphogenetic proteins, and guided bone regeneration in a rodent model. J Biomed Mater Res A 2011;98(2):212–21.10.1002/jbm.a.33107Search in Google Scholar PubMed

[14] Amaral AC, Parizotto NA, Salvini TF. Dose-dependency of low-energy HeNe laser effect in regeneration of skeletal muscle in mice. Lasers Med Sci 2001;16(1):44–51.10.1007/PL00011336Search in Google Scholar

[15] Cressoni MD, Dib Giusti HH, Casarotto RA, Anaruma CA. The effects of a 785-nm AlGaInP laser on the regeneration of rat anterior tibialis muscle after surgically-induced injury. Photomed Laser Surg 2008;26(5):461–6.10.1089/pho.2007.2150Search in Google Scholar PubMed

[16] Stein A, Benayahu D, Maltz L, Oron U. Low-level laser irradiation promotes proliferation and differentiation of human osteoblasts in vitro. Photomed Laser Surg 2005;23(2):161–6.10.1089/pho.2005.23.161Search in Google Scholar PubMed

[17] Miyabara EH, Martin JL, Griffin TM, Moriscot AS, Mestril R. Overexpression of inducible 70-kDa heat shock protein in mouse attenuates skeletal muscle damage induced by cryolesioning. Am J Physiol Cell Physiol 2006;290(4):C1128–38.10.1152/ajpcell.00399.2005Search in Google Scholar PubMed

[18] Rodrigues NC, Brunelli R, de Araújo HS, Parizotto NA, Renno AC. Low-level laser therapy (LLLT) (660nm) alters gene expression during muscle healing in rats. J Photochem Photobiol B 2013;120:29–35.10.1016/j.jphotobiol.2013.01.002Search in Google Scholar PubMed

[19] Brunelli RM, Rodrigues NC, Ribeiro DA, Fernandes K, Magri A, Assis L, Parizotto NA, Cliquet A Jr, Renno AC, Abreu DC. The effects of 780-nm low-level laser therapy on muscle healing process after cryolesion. Lasers Med Sci 2013. doi: 10.1007/s10103-013-1277-6.10.1007/s10103-013-1277-6Search in Google Scholar PubMed

[20] Servetto N, Cremonezzi D, Simes JC, Moya M, Soriano F, Palma JA, Campana VR. Evaluation of inflammatory biomarkers associated with oxidative stress and histological assessment of low-level laser therapy in experimental myopathy. Lasers Surg Med 2010;42(6):577–83.10.1002/lsm.20910Search in Google Scholar PubMed

[21] Rizzi CF, Mauriz JL, Freitas Corrêa DS, Moreira AJ, Zettler CG, Filippin LI, Marroni NP, González-Gallego J. Effects of low-level laser therapy (LLLT) on the nuclear factor (NF)-kappaB signaling pathway in traumatized muscle. Lasers Surg Med 2006;38(7):704–13.10.1002/lsm.20371Search in Google Scholar PubMed

[22] de Souza TO, Mesquita DA, Ferrari RA, Dos Santos Pinto D Jr, Correa L, Bussadori SK, Fernandes KP, Martins MD. Phototherapy with low-level laser affects the remodeling of types I and III collagen in skeletal muscle repair. Lasers Med Sci 2011;26(6):803–14.10.1007/s10103-011-0951-9Search in Google Scholar PubMed

[23] Prisk V, Huard J. Muscle injuries and repair: the role of prostaglandins and inflammation. Histol Histopathol 2003;18(4):1243–56.Search in Google Scholar

[24] Tidball JG. Inflammatory processes in muscle injury and repair. Am J Physiol Regul Integr Comp Physiol 2005;288(2):R345–53.10.1152/ajpregu.00454.2004Search in Google Scholar PubMed

[25] Pires D, Xavier M, Araújo T, Silva JA Jr, Aimbire F, Albertini R. Low-level laser therapy (LLLT; 780 nm) acts differently on mRNA expression of anti- and pro-inflammatory mediators in an experimental model of collagenase-induced tendinitis in rat. Lasers Med Sci 2011;26(1):85–94.10.1007/s10103-010-0811-zSearch in Google Scholar PubMed

[26] de Almeida P, Lopes-Martins RÁ, Tomazoni SS, Silva JA Jr, de Carvalho Pde T, Bjordal JM, Leal Junior EC. Low-level laser therapy improves skeletal muscle performance, decreases skeletal muscle damage and modulates mRNA expression of COX-1 and COX-2 in a dose-dependent manner. Photochem Photobiol 2011;87(5):1159–63.10.1111/j.1751-1097.2011.00968.xSearch in Google Scholar PubMed

[27] Arsic N, Zacchigna S, Zentilin L, Ramirez-Correa G, Pattarini L, Salvi A, Sinagra G, Giacca M. Vascular endothelial growth factor stimulates skeletal muscle regeneration in vivo. Mol Ther 2004;10(5):844–54.10.1016/j.ymthe.2004.08.007Search in Google Scholar PubMed

[28] Ryan NA, Zwetsloot KA, Westerkamp LM, Hickner RC, Pofahl WE, Gavin TP. Lower skeletal muscle capillarization and VEGF expression in aged vs. young men. J Appl Physiol 2006;100(1):178–85.10.1152/japplphysiol.00827.2005Search in Google Scholar PubMed

[29] Boontheekul T, Mooney DJ. Protein-based signaling systems in tissue engineering. Curr Opin Biotechnol 2003;14(5): 559–65.10.1016/j.copbio.2003.08.004Search in Google Scholar PubMed

[30] Bryan BA, Walshe TE, Mitchell DC, Havumaki JS, Saint-Geniez M, Maharaj AS, Maldonado AE, D’Amore PA. Coordinated vascular endothelial growth factor expression and signaling during skeletal myogenic differentiation. Mol Biol Cell 2008;19(3):994–1006.10.1091/mbc.e07-09-0856Search in Google Scholar PubMed PubMed Central

[31] Dias FJ, Issa JP, Barbosa AP, de Vasconcelos PB, Watanabe IS, Mizusakiiyomasa M. Effects of low-level laser irradiation in ultrastructural morphology, and immunoexpression of VEGF and VEGFR-2 of rat masseter muscle. Micron 2012; 43(2–3):237–44.10.1016/j.micron.2011.08.005Search in Google Scholar PubMed

[32] Assis L, Moretti AI, Abrahão TB, de Souza HP, Hamblin MR, Parizotto NA. Low-level laser therapy (808 nm) contributes to muscle regeneration and prevents fibrosis in rat tibialis anterior muscle after cryolesion. Lasers Med Sci 2013;28(3):947–55.10.1007/s10103-012-1183-3Search in Google Scholar PubMed PubMed Central

[33] Liu M, Stevens-Lapsley JE, Jayaraman A, Ye F, Conover C, Walter GA, Bose P, Thompson FJ, Borst SE, Vandenborne K. Impact of treadmill locomotor training on skeletal muscle IGF1 and myogenic regulatory factors in spinal cord injured rats. Eur J Appl Physiol 2010;109(4):709–20.10.1007/s00421-010-1392-zSearch in Google Scholar PubMed

[34] Marsh DR, Criswell DS, Carson JA, Booth FW. Myogenic regulatory factors during regeneration of skeletal muscle in young, adult, and old rats. J Appl Physiol 1997;83(4): 1270–5.10.1152/jappl.1997.83.4.1270Search in Google Scholar PubMed

[35] Degens H. Age-related skeletal muscle dysfunction: causes and mechanisms. J Musculoskelet Neuronal Interact 2007;7(3):246–52.Search in Google Scholar

[36] Vatansever F, Rodrigues NC, Assis LL, Peviani SS, Durigan JL, Moreira FM, Hamblin MR, Parizotto NA. Low intensity laser therapy accelerates muscle regeneration in aged rats. Photonics Lasers Med 2012;1(4):287–97.10.1515/plm-2012-0035Search in Google Scholar PubMed PubMed Central

[37] Friedrichs M, Wirsdöerfer F, Flohé SB, Schneider S, Wuelling M, Vortkamp A. BMP signaling balances proliferation and differentiation of muscle satellite cell descendants. BMC Cell Biol 2011;12:26.10.1186/1471-2121-12-26Search in Google Scholar PubMed PubMed Central

[38] Silva LH, Silva MT, Gutierrez RM, Conte TC, Toledo CA, Aoki MS, Liebano RE, Miyabara EH. GaAs 904-nm laser irradiation improves myofiber mass recovery during regeneration of skeletal muscle previously damaged by crotoxin. Lasers Med Sci 2012;27(5):993–1000.10.1007/s10103-011-1031-xSearch in Google Scholar PubMed

Erhalten: 2013-6-19
Revidiert: 2013-7-22
Angenommen: 2013-10-21
Online erschienen: 2013-11-20
Erschienen im Druck: 2014-2-1

©2014 by Walter de Gruyter Berlin Boston

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