Skip to main content

Advertisement

SpringerLink
Log in

A transient protective effect of low-level laser irradiation against disuse-induced atrophy of rats

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

Abstract

Satellite cells, a population of skeletal muscular stem cells, are generally recognized as the main and, possibly, the sole source of postnatal muscle regeneration. Previous studies have revealed the potential of low-level laser (LLL) irradiation in promoting satellite cell proliferation, which, thereby, boosts the recovery of skeletal muscle from atrophy. The purpose of this study is to investigate the beneficial effect of LLL on disuse-induced atrophy. The optimal irradiation condition of LLL (808 nm) enhancing the proliferation of Pax7+ve cells, isolated from tibialis anterior (TA) muscle, was examined and applied on TA muscle of disuse-induced atrophy model of the rats accordingly. Healthy rats were used as the control. On one hand, transiently, LLL was able to postpone the progression of atrophy for 1 week through a reduction of apoptosis in Pax7−veMyoD+ve (myocyte) population. Simultaneously, a significant enhancement was observed in Pax7+veMyoD+ve population; however, most of the increased cells underwent apoptosis since the second week, which suggested an impaired maturation of the population. On the other hand, in normal control rats with LLL irradiation, a significant increase in Pax7+veMyoD+ve cells and a significant decrease of apoptosis were observed. As a result, a strengthened muscle contraction was observed. Our data showed the capability of LLL in postponing the progression of disuse-induced atrophy for the first time. Furthermore, the result of normal rats with LLL irradiation showed the effectiveness of LLL to strengthen muscle contraction in healthy control.

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
Fig. 4

Similar content being viewed by others

References

  1. Brook MS, Wilkinson DJ, Phillips BE, Perez-Schindler J, Philp A, Smith K, Atherton PJ (2016) Skeletal muscle homeostasis and plasticity in youth and ageing: impact of nutrition and exercise. Acta Physiol (Oxf) 216(1):15–41. https://doi.org/10.1111/apha.12532

    Article  CAS  Google Scholar 

  2. Janssen I, Heymsfield SB, Wang ZM, Ross R (2000) Skeletal muscle mass and distribution in 468 men and women aged 18-88 yr. J Appl Physiol (Bethesda, MD: 1985) 89(1):81–88. https://doi.org/10.1152/jappl.2000.89.1.81

    Article  CAS  Google Scholar 

  3. Ferrans CE, Lipscomb J, Gotay CC, Snyder C (2004) Outcome assessment in cancer, definitions and conceptual models of quality of life. Cambridge University Press

  4. Cezar CA, Mooney DJ (2015) Biomaterial-based delivery for skeletal muscle repair. Adv Drug Deliv Rev 84:188–197. https://doi.org/10.1016/j.addr.2014.09.008

    Article  CAS  PubMed  Google Scholar 

  5. Mauro A (1961) Satellite cell of skeletal muscle fibers. J Biophys Biochem Cytol 9:493–495

    Article  CAS  Google Scholar 

  6. Seale P, Sabourin LA, Girgis-Gabardo A, Mansouri A, Gruss P, Rudnicki MA (2000) Pax7 is required for the specification of myogenic satellite cells. Cell 102(6):777–786

    Article  CAS  Google Scholar 

  7. Rudnicki MA, Schnegelsberg PN, Stead RH, Braun T, Arnold HH, Jaenisch R (1993) MyoD or Myf-5 is required for the formation of skeletal muscle. Cell 75(7):1351–1359

    Article  CAS  Google Scholar 

  8. Kuang S, Kuroda K, Le Grand F, Rudnicki MA (2007) Asymmetric self-renewal and commitment of satellite stem cells in muscle. Cell 129(5):999–1010. https://doi.org/10.1016/j.cell.2007.03.044

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  9. Rudnicki MA, Le Grand F, McKinnell I, Kuang S (2008) The molecular regulation of muscle stem cell function. Cold Spring Harb Symp Quant Biol 73:323–331. https://doi.org/10.1101/sqb.2008.73.064

    Article  CAS  PubMed  Google Scholar 

  10. McCullagh KJ, Perlingeiro RC (2015) Coaxing stem cells for skeletal muscle repair. Adv Drug Deliv Rev 84:198–207. https://doi.org/10.1016/j.addr.2014.07.007

    Article  CAS  PubMed  Google Scholar 

  11. Seale P, Rudnicki MA (2000) A new look at the origin, function, and “stem-cell” status of muscle satellite cells. Dev Biol 218(2):115–124. https://doi.org/10.1006/dbio.1999.9565

    Article  CAS  PubMed  Google Scholar 

  12. Zammit PS, Heslop L, Hudon V, Rosenblatt JD, Tajbakhsh S, Buckingham ME, Beauchamp JR, Partridge TA (2002) Kinetics of myoblast proliferation show that resident satellite cells are competent to fully regenerate skeletal muscle fibers. Exp Cell Res 281(1):39–49

    Article  CAS  Google Scholar 

  13. Benedini-Elias PC, Morgan MC, Gomes AR, Mattiello-Sverzut AC (2009) Changes in postnatal skeletal muscle development induced by alternative immobilization model in female rat. Anat Sci Int 84(3):218–225. https://doi.org/10.1007/s12565-009-0016-3

    Article  PubMed  Google Scholar 

  14. Marimuthu K, Murton AJ, Greenhaff PL (2011) Mechanisms regulating muscle mass during disuse atrophy and rehabilitation in humans. J Appl Physiol (Bethesda, MD: 1985) 110(2):555–560. https://doi.org/10.1152/japplphysiol.00962.2010

    Article  Google Scholar 

  15. Lecker SH, Jagoe RT, Gilbert A, Gomes M, Baracos V, Bailey J, Price SR, Mitch WE, Goldberg AL (2004) Multiple types of skeletal muscle atrophy involve a common program of changes in gene expression. FASEB J 18(1):39–51. https://doi.org/10.1096/fj.03-0610com

    Article  CAS  PubMed  Google Scholar 

  16. Nawrotzki R, Blake DJ, Davies KE (1996) The genetic basis of neuromuscular disorders. Trends Genet 12(8):294–298

    Article  CAS  Google Scholar 

  17. Deitrick JE (1948) The effect of immobilization on metabolic and physiological functions of normal men. Bull N Y Acad Med 24(6):364–375

    CAS  PubMed  PubMed Central  Google Scholar 

  18. Tomanek RJ, Lund DD (1973) Degeneration of different types of skeletal muscle fibres. I Denervation. J Anat 116(Pt 3):395–407

    CAS  PubMed  PubMed Central  Google Scholar 

  19. Zeman RJ, Zhao J, Zhang Y, Zhao W, Wen X, Wu Y, Pan J, Bauman WA, Cardozo C (2009) Differential skeletal muscle gene expression after upper or lower motor neuron transection. Pflugers Archiv Eur J Physiol 458(3):525–535. https://doi.org/10.1007/s00424-009-0643-5

    Article  CAS  Google Scholar 

  20. Bruusgaard JC, Gundersen K (2008) In vivo time-lapse microscopy reveals no loss of murine myonuclei during weeks of muscle atrophy. J Clin Invest 118(4):1450–1457. https://doi.org/10.1172/jci34022

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  21. Wan Q, Yeung SS, Cheung KK, Au SW, Lam WW, Li YH, Dai ZQ, Yeung EW (2016) Optimizing electrical stimulation for promoting satellite cell proliferation in muscle disuse atrophy. Am J Physical Med Rehabil 95(1):28–38. https://doi.org/10.1097/phm.0000000000000307

    Article  Google Scholar 

  22. Passarella S, Casamassima E, Molinari S, Pastore D, Quagliariello E, Catalano IM, Cingolani A (1984) Increase of proton electrochemical potential and ATP synthesis in rat liver mitochondria irradiated in vitro by helium-neon laser. FEBS Lett 175(1):95–99

    Article  CAS  Google Scholar 

  23. Alves AN, Fernandes KP, Melo CA, Yamaguchi RY, Franca 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(2):813–821. https://doi.org/10.1007/s10103-013-1428-9

    Article  CAS  PubMed  Google Scholar 

  24. Iyomasa DM, Garavelo I, Iyomasa MM, Watanabe IS, Issa JP (2009) Ultrastructural analysis of the low level laser therapy effects on the lesioned anterior tibial muscle in the gerbil. Micron 40(4):413–418. https://doi.org/10.1016/j.micron.2009.02.002

    Article  CAS  PubMed  Google Scholar 

  25. Conlan MJ, Rapley JW, Cobb CM (1996) Biostimulation of wound healing by low-energy laser irradiation. A review. J Clin Periodontol 23(5):492–496

    Article  CAS  Google Scholar 

  26. Yaakobi T, Maltz L, Oron U (1996) Promotion of bone repair in the cortical bone of the tibia in rats by low energy laser (He-Ne) irradiation. Calcif Tissue Int 59(4):297–300

    Article  CAS  Google Scholar 

  27. Rochkind S, Geuna S, Shainberg A (2009) Chapter 25: phototherapy in peripheral nerve injury: effects on muscle preservation and nerve regeneration. Int Rev Neurobiol 87:445–464. https://doi.org/10.1016/s0074-7742(09)87025-6

    Article  PubMed  Google Scholar 

  28. Bibikova A, Belkin V, Oron U (1994) Enhancement of angiogenesis in regenerating gastrocnemius muscle of the toad (Bufo viridis) by low-energy laser irradiation. Anat Embryol 190(6):597–602

    Article  CAS  Google Scholar 

  29. Amaral AC, Parizotto NA, Salvini TF (2001) Dose-dependency of low-energy HeNe laser effect in regeneration of skeletal muscle in mice. Lasers Med Sci 16(1):44–51

    Article  CAS  Google Scholar 

  30. Wollman Y, Rochkind S (1993) Muscle fiber formation in vitro is delayed by low power laser irradiation. J Photochem Photobiol B 17(3):287–290

    Article  CAS  Google Scholar 

  31. Rochkind S, Shainberg A (2013) Protective effect of laser phototherapy on acetylcholine receptors and creatine kinase activity in denervated muscle. Photomed Laser Surg 31(10):499–504. https://doi.org/10.1089/pho.2013.3537

    Article  CAS  PubMed  Google Scholar 

  32. Ben-Dov N, Shefer G, Irintchev A, Wernig A, Oron U, Halevy O (1999) Low-energy laser irradiation affects satellite cell proliferation and differentiation in vitro. Biochim Biophys Acta 1448(3):372–380

    Article  CAS  Google Scholar 

  33. Shefer G, Oron U, Irintchev A, Wernig A, Halevy O (2001) Skeletal muscle cell activation by low-energy laser irradiation: a role for the MAPK/ERK pathway. J Cell Physiol 187(1):73–80. https://doi.org/10.1002/1097-4652(2001)9999:9999<::aid-jcp1053>3.0.co;2-9

    Article  CAS  PubMed  Google Scholar 

  34. Shefer G, Partridge TA, Heslop L, Gross JG, Oron U, Halevy O (2002) Low-energy laser irradiation promotes the survival and cell cycle entry of skeletal muscle satellite cells. J Cell Sci 115(Pt 7):1461–1469

    CAS  PubMed  Google Scholar 

  35. Nakano J, Kataoka H, Sakamoto J, Origuchi T, Okita M, Yoshimura T (2009) Low-level laser irradiation promotes the recovery of atrophied gastrocnemius skeletal muscle in rats. Exp Physiol 94(9):1005–1015. https://doi.org/10.1113/expphysiol.2009.047738

    Article  CAS  PubMed  Google Scholar 

  36. Chang H, Yoshimoto M, Umeda K, Iwasa T, Mizuno Y, Fukada S, Yamamoto H, Motohashi N, Miyagoe-Suzuki Y, Takeda S, Heike T, Nakahata T (2009) Generation of transplantable, functional satellite-like cells from mouse embryonic stem cells. FASEB J 23(6):1907–1919. https://doi.org/10.1096/fj.08-123661

    Article  CAS  PubMed  Google Scholar 

  37. Ramos J, Chamberlain JS (2015) Gene therapy for Duchenne muscular dystrophy. Expert Opin Orphan Drugs 3(11):1255–1266. https://doi.org/10.1517/21678707.2015.1088780

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  38. Mizuno Y, Chang H, Umeda K, Niwa A, Iwasa T, Awaya T, Fukada S, Yamamoto H, Yamanaka S, Nakahata T, Heike T (2010) Generation of skeletal muscle stem/progenitor cells from murine induced pluripotent stem cells. FASEB J 24(7):2245–2253. https://doi.org/10.1096/fj.09-137174

    Article  CAS  PubMed  Google Scholar 

  39. Nobrega C, da Silva EM, de Macedo CR (2013) Low-level laser therapy for treatment of pain associated with orthodontic elastomeric separator placement: a placebo-controlled randomized double-blind clinical trial. Photomed Laser Surg 31(1):10–16. https://doi.org/10.1089/pho.2012.3338

    Article  CAS  PubMed  Google Scholar 

  40. Rochkind S, Shainberg A (2017) Muscle response to complete peripheral nerve injury: changes of acetylcholine receptor and creatine kinase activity over time. J Reconstr Microsurg 33(5):352–357. https://doi.org/10.1055/s-0037-1598619

    Article  PubMed  Google Scholar 

Download references

Acknowledgments

We thank our colleague, Yu-Shan Lin, who has contributed to the concepts and experiments in this manuscript.

Funding

This study was supported by the Grant-in-Aid for Scientific Research TMU100-AE1-B10, 101TMU-TMUH-11 from the Taipei Medical University, and the Taipei Medical University Hospital and Grant-in-Aid for Scientific Research 101-2314-B-038-017-MY3 from the Ministry of Science and Technology, R.O.C., Taiwan.

Author information

Authors and Affiliations

  1. Department of Pediatrics, Shung Ho Hospital, Taipei Medical University, Taipei, Taiwan

    Yung-Ting Kou

  2. Department of Pediatrics, School of Medicine, College of Medicine, Taipei Medical University, Taipei, Taiwan

    Yung-Ting Kou & Hsi Chang

  3. Graduate Institute of Medical Sciences, College of Medicine, Taipei Medical University, Taipei, Taiwan

    Hui-Tien Liu & Chung-Min Tsai

  4. Department of Family Medicine, Taipei City Hospital, Taipei, Taiwan

    Chun-Yin Hou

  5. Department of Clinical Application, Center for iPS Cell Research and Application (CiRA), Kyoto University, Kyoto, Japan

    Chuang-Yu Lin

  6. Department of Pediatrics, Taipei Medical University Hospital, Taipei, Taiwan

    Hsi Chang

Authors
  1. Yung-Ting Kou
    View author publications

    You can also search for this author in PubMed Google Scholar

  2. Hui-Tien Liu
    View author publications

    You can also search for this author in PubMed Google Scholar

  3. Chun-Yin Hou
    View author publications

    You can also search for this author in PubMed Google Scholar

  4. Chuang-Yu Lin
    View author publications

    You can also search for this author in PubMed Google Scholar

  5. Chung-Min Tsai
    View author publications

    You can also search for this author in PubMed Google Scholar

  6. Hsi Chang
    View author publications

    You can also search for this author in PubMed Google Scholar

Corresponding author

Correspondence to Hsi Chang.

Ethics declarations

Conflict of interests

The authors declare that they have no competing or financial interests. The authors also certify that they have no affiliations with or involvement in any organization or entity with any financial interest or non-financial interest in the subject matter or materials discussed in this manuscript.

Additional information

Publisher’s note

Springer Nature remains neutral with regard to jurisdictional claims in published maps and institutional affiliations.

Yung-Ting Kou and Hui-Tien Liu contribute equally.

Electronic supplementary material

Supplementary Figure 1

Experiments in time line. (PPTX 123 kb)

Supplementary Figure 2

Disused animal model. (PPTX 435 kb)

Supplementary Figure 3

Toe lift test. (PPTX 1763 kb)

Rights and permissions

Reprints and permissions

About this article

Check for updates. Verify currency and authenticity via CrossMark

Cite this article

Kou, YT., Liu, HT., Hou, CY. et al. A transient protective effect of low-level laser irradiation against disuse-induced atrophy of rats. Lasers Med Sci 34, 1829–1839 (2019). https://doi.org/10.1007/s10103-019-02778-5

Download citation

  • Received:

  • Accepted:

  • Published:

  • Issue Date:

  • DOI: https://doi.org/10.1007/s10103-019-02778-5

Keywords

Search

Navigation