Skip to main content

Advertisement

SpringerLink
Log in

Comparative effects of low-level laser therapy pre- and post-injury on mRNA expression of MyoD, myogenin, and IL-6 during the skeletal muscle repair

  • Original Article
  • Published:
Lasers in Medical Science Aims and scope Submit manuscript

Abstract

This study analyzed the effect of pre-injury and post-injury irradiation with low-level laser therapy (LLLT) on the mRNA expression of myogenic regulatory factors and interleukin 6 (IL-6) during the skeletal muscle repair. Male rats were divided into six groups: control group, sham group, LLLT group, injury group; pre-injury LLLT group, and post-injury LLLT group. LLLT was performed with a diode laser (wavelength 780 nm; output power 40 mW’ and total energy 3.2 J). Cryoinjury was induced by two applications of a metal probe cooled in liquid nitrogen directly onto the belly of the tibialis anterior (TA) muscle. After euthanasia, the TA muscle was removed for the isolation of total RNA and analysis of MyoD, myogenin, and IL-6 using real-time quantitative PCR. Significant increases were found in the expression of MyoD mRNA at 3 and 7 days as well as the expression of myogenin mRNA at 14 days in the post-injury LLLT group in comparison to injury group. A significant reduction was found in the expression of IL-6 mRNA at 3 and 7 days in the pre-injury LLLT and post-injury LLLT groups. A significant increase in IL-6 mRNA was found at 14 days in the post-injury LLLT group in comparison to the injury group. LLLT administered following muscle injury modulates the mRNA expression of MyoD and myogenin. Moreover, the both forms of LLLT administration were able to modulate the mRNA expression of IL-6 during the muscle repair process.

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

Access this article

Log in via an institution

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

Instant access to the full article PDF.

Institutional subscriptions

Fig 1
Fig 2
Fig 3

Similar content being viewed by others

References

  1. Järvinen TA, Järvinen TL, Kääriäinen M, Kalimo H, Järvinen M (2005) Muscle injuries: biology and treatment. Am J Sports Med 33:745–764

    Article  PubMed  Google Scholar 

  2. Shin EH, Caterson EJ, Jackson WM, Nesti LJ (2014) Quality of healing: defining, quantifying, and enhancing skeletal muscle healing. Wound Repair Regen 22:18–24. doi:10.1111/wrr.12163

    Article  PubMed  Google Scholar 

  3. Huard J, Li Y, Fu FH (2002) Muscle injuries and repair: current trends in research. J Bone Joint Surg Am 84-A:822–832

    PubMed  Google Scholar 

  4. Orchard J, Best TM (2002) The management of muscle strain injuries: an early return versus the risk of recurrence. Clin J Sport Med 12:3–5

    Article  PubMed  Google Scholar 

  5. Alves AN, Fernandes KP, Deana AM, Bussadori SK, Mesquita-Ferrari RA (2014) Effects of low-level laser therapy on skeletal muscle repair: a systematic review. Am J Phys Med Rehabil 93:1073–1085. doi:10.1097/PHM.0000000000000158

    Article  PubMed  Google Scholar 

  6. Tidball JG, Villalta SA (2010) Regulatory interactions between muscle and the immune system during muscle regeneration. Am J Physiol Regul Integr Comp Physiol 298:1173–1187. doi:10.1152/ajpregu.00735.2009

    Article  Google Scholar 

  7. Mann CJ, Perdiguero E, Kharraz Y, Aguilar S, Pessina P, Serrano AL, Muñoz-Cánoves P (2011) Review: aberrant repair and fibrosis development in skeletal muscle. Skelet Muscle 1:21. doi:10.1186/2044-5040-1-21

    Article  PubMed  PubMed Central  Google Scholar 

  8. Hawke TJ, Garry DJ (2001) Myogenic satellite cells: physiology to molecular biology. J Appl Physiol (1985) 91:534–551

    CAS  Google Scholar 

  9. Shi X, Garry DJ (2006) Muscle stem cells in development, regeneration, and disease. Genes Dev 20:1692–1708

    Article  CAS  PubMed  Google Scholar 

  10. Bentzinger CF, Wang YX, Rudnicki MA (2012) Building muscle: molecular regulation of myogenesis. Cold Spring Harb Perspect Biol 4:a008342. doi:10.1101/cshperspect.a008342

    Article  PubMed  PubMed Central  Google Scholar 

  11. Rincon M (2012) Interleukin-6: from an inflammatory marker to a target for inflammatory diseases. Trends Immunol 33:571–577. doi:10.1016/j.it.2012.07.003

    Article  CAS  PubMed  Google Scholar 

  12. Tanaka T, Narazaki M, Kishimoto T (2014) IL-6 in inflammation, immunity, and disease. Cold Spring Harb Perspect Biol 6:a016295. doi:10.1101/cshperspect.a016295

    Article  PubMed  Google Scholar 

  13. Hoene M, Runge H, Häring HU, Schleicher ED, Weigert C (2013) Interleukin-6 promotes myogenic differentiation of mouse skeletal muscle cells: role of the STAT3 pathway. Am J Physiol Cell Physiol 304:128–136. doi:10.1152/ajpcell.00025.2012

    Article  Google Scholar 

  14. Kurosaka M, Machida S (2013) Interleukin-6-induced satellite cell proliferation is regulated by induction of the JAK2/STAT3 signalling pathway through cyclin D1 targeting. Cell Prolif 46:365–373. doi:10.1111/cpr.12045

    Article  CAS  PubMed  Google Scholar 

  15. Leal-Junior EC, Vanin AA, Miranda EF, de Carvalho PD, Dal Corso S, Bjordal JM (2015) Effect of phototherapy (low-level laser therapy and light-emitting diode therapy) on exercise performance and markers of exercise recovery: a systematic review with meta-analysis. Lasers Med Sci 30:925–939. doi:10.1007/s10103-013-1465-4

    Article  PubMed  Google Scholar 

  16. Ribeiro BG, Alves AN, Santos LA, Fernandes KP, Cantero TM, Gomes MT, França CM, Silva DF, Bussadori SK, Mesquita-Ferrari RA (2015) The effect of low-level laser therapy (LLLT) applied prior to muscle injury. Lasers Surg Med. doi:10.1002/lsm.22381

    Google Scholar 

  17. Mesquita-Ferrari RA, Martins MD, Silva JA Jr, da Silva TD, Piovesan RF, Pavesi VC, Bussadori SK, Fernandes KP (2011) Effects of low-level laser therapy on expression of TNF-α and TGF-β in skeletal muscle during the repair process. Lasers Med Sci 26:335–340. doi:10.1007/s10103-010-0850-5

    Article  PubMed  Google Scholar 

  18. Fernandes KP, Alves AN, Nunes FD, Souza NH, Silva JA Jr, Bussadori SK, Ferrari RA (2013) Effect of photobiomodulation on expression of IL-1β in skeletal muscle following acute injury. Lasers Med Sci 28:1043–1046. doi:10.1007/s10103-012-1233-x

    Article  PubMed  Google Scholar 

  19. Alves AN, Fernandes KP, Melo CA, Yamaguchi RY, França CM, Teixeira DF, Bussadori SK, Nunes FD, Mesquita-Ferrari RA (2014) Modulating effect of low-level laser therapy on fibrosis in the repair process of the tibialis anterior muscle in rats. Lasers Med Sci 29:813–821. doi:10.1007/s10103-013-1428-9

    Article  CAS  PubMed  Google Scholar 

  20. Piovesan RF, Fernandes KP, Alves AN, Teixeira VP, Silva Junior JA, Martins MD, Bussadori SK, Albertini R, Mesquita-Ferrari RA (2013) Effect of nandrolone decanoate on skeletal muscle repair. Int J Sports Med 34:87–92. doi:10.1055/s-0032-1311652

    CAS  PubMed  Google Scholar 

  21. Livak KJ, Schmittgen TD (2001) Analysis of relative gene expression data using real-time quantitative PCR and the 2(−delta delta C(T)) method. Methods 25:402–408

    Article  CAS  PubMed  Google Scholar 

  22. Megeney LA, Kablar B, Garrett K, Anderson JE, Rudnicki MA (1996) MyoD is required for myogenic stem cell function in adult skeletal muscle. Genes Dev 10:1173–1183

    Article  CAS  PubMed  Google Scholar 

  23. Mastroyiannopoulos NP, Nicolaou P, Anayasa M, Uney JB, Phylactou LA (2012) Downregulation of myogenin can reverse terminal muscle cell differentiation. PLoS One 7, e29896. doi:10.1371/journal.pone

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  24. Rodrigues NC, Brunelli R, de Araújo HS, Parizotto NA, Renno AC (2013) Low-level laser therapy (LLLT) (660 nm) alters gene expression during muscle healing in rats. J Photochem Photobiol B 120:29–35. doi:10.1016/j.jphotobiol.2013.01.002

    Article  CAS  PubMed  Google Scholar 

  25. Brunelli RM, Rodrigues NC, Ribeiro DA, Fernandes K, Magri A, Assis L, Parizotto NA, Cliquet A Jr, Renno AC, Abreu DC (2014) The effects of 780-nm low-level laser therapy on muscle healing process after cryolesion. Lasers Med Sci 29:91–96. doi:10.1007/s10103-013-1277-6

    Article  PubMed  Google Scholar 

  26. Zhang C, Li Y, Wu Y, Wang L, Wang X, Du J (2013) Interleukin-6/signal transducer and activator of transcription 3 (STAT3) pathway is essential for macrophage infiltration and myoblast proliferation during muscle regeneration. J Biol Chem 288:1489–1499. doi:10.1074/jbc.M112.419788

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  27. Hirano T (1998) Interleukin 6 and its receptor: ten years later. Int Rev Immunol 16:249–284

    Article  CAS  PubMed  Google Scholar 

  28. Muñoz-Cánoves P, Scheele C, Pedersen BK, Serrano AL (2013) Interleukin-6 myokine signaling in skeletal muscle: a double-edged sword? FEBS J 280:4131–4148. doi:10.1111/febs.12338

    Article  PubMed  PubMed Central  Google Scholar 

  29. Haddad F, Zaldivar F, Cooper DM, Adams GR (2005) IL-6-induced skeletal muscle atrophy. J Appl Physiol (1985) 98:911–917

    Article  CAS  Google Scholar 

  30. Lopes-Martins RA, Marcos RL, Leonardo PS, Prianti AC Jr, Muscará MN, Aimbire F, Frigo L, Iversen VV, Bjordal JM (2006) Effect of low-level laser (Ga-Al-As 655 nm) on skeletal muscle fatigue induced by electrical stimulation in rats. J Appl Physiol (1985) 101:283–288

    Article  Google Scholar 

  31. Silveira PC, Silva LA, Fraga DB, Freitas TP, Streck EL, Pinho R (2009) Evaluation of mitochondrial respiratory chain activity in muscle healing by low-level laser therapy. J Photochem Photobiol B 95:89–92. doi:10.1016/j.jphotobiol.2009.01.004

    Article  CAS  PubMed  Google Scholar 

  32. Albuquerque-Pontes GM, Vieira Rde P, Tomazoni SS, Caires CO, Nemeth V, Vanin AA, Santos LA, Pinto HD, Marcos RL, Bjordal JM, de Carvalho Pde T, Leal-Junior EC (2015) Effect of pre-irradiation with different doses, wavelengths, and application intervals of low-level laser therapy on cytochrome c oxidase activity in intact skeletal muscle of rats. Lasers Med Sci 30:59–66. doi:10.1007/s10103-014-1616-2

Download references

Acknowledgments

The authors wish to thank UNINOVE and the Brazilian fostering agencies, Coordination for the Improvement of Higher Education Personnel—CAPES (grants 1182781; 1510536) and São Paulo Research Foundation—FAPESP (grants 2011/04452-8; 2011/17638-2; 2012/11461-6; 2013/21540-3; and 2014/12381-1) for financial support.

Author information

Authors and Affiliations

  1. Postgraduate Program in Rehabilitation Sciences, Universidade Nove de Julho—UNINOVE, Rua Vergueiro, 235/249, Liberdade, CEP 01504-001, São Paulo, SP, Brazil

    Agnelo Neves Alves, Beatriz Guimarães Ribeiro, Nadhia Helena Costa Souza, Sandra Kalil Bussadori & Raquel Agnelli Mesquita-Ferrari

  2. Postgraduate Program in Biophotonics Applied to Health Sciences, Universidade Nove de Julho—UNINOVE, São Paulo, SP, Brazil

    Kristianne Porta Santos Fernandes, Sandra Kalil Bussadori & Raquel Agnelli Mesquita-Ferrari

  3. Departament of Molecular Pathology, School of Dentistry, Universidade de São Paulo—FOUSP, São Paulo, SP, Brazil

    Lília Alves Rocha

  4. Departament of Oral Pathology, School of Dentistry, Universidade de São Paulo—FOUSP, São Paulo, SP, Brazil

    Fabio Daumas Nunes

Authors
  1. Agnelo Neves Alves
    View author publications

    You can also search for this author in PubMed Google Scholar

  2. Beatriz Guimarães Ribeiro
    View author publications

    You can also search for this author in PubMed Google Scholar

  3. Kristianne Porta Santos Fernandes
    View author publications

    You can also search for this author in PubMed Google Scholar

  4. Nadhia Helena Costa Souza
    View author publications

    You can also search for this author in PubMed Google Scholar

  5. Lília Alves Rocha
    View author publications

    You can also search for this author in PubMed Google Scholar

  6. Fabio Daumas Nunes
    View author publications

    You can also search for this author in PubMed Google Scholar

  7. Sandra Kalil Bussadori
    View author publications

    You can also search for this author in PubMed Google Scholar

  8. Raquel Agnelli Mesquita-Ferrari
    View author publications

    You can also search for this author in PubMed Google Scholar

Corresponding author

Correspondence to Raquel Agnelli Mesquita-Ferrari.

Ethics declarations

All procedures were performed in accordance with the guidelines of the Brazilian National Council for the Control of Animal Experimentation. This study received approval from the University Nove de Julho Animal Research Ethics Committee, process numbers AN12/2012 and AN16/2012

Conflict of interest

The authors declare that they have no competing interests.

Rights and permissions

Reprints and permissions

About this article

Check for updates. Verify currency and authenticity via CrossMark

Cite this article

Alves, A.N., Ribeiro, B.G., Fernandes, K.P.S. et al. Comparative effects of low-level laser therapy pre- and post-injury on mRNA expression of MyoD, myogenin, and IL-6 during the skeletal muscle repair. Lasers Med Sci 31, 679–685 (2016). https://doi.org/10.1007/s10103-016-1908-9

Download citation

  • Received:

  • Accepted:

  • Published:

  • Issue Date:

  • DOI: https://doi.org/10.1007/s10103-016-1908-9

Keywords

Search

Navigation