Advertisement

Lasers in Medical Science

, Volume 28, Issue 3, pp 725–734 | Cite as

Effects of low-level laser therapy on ROS homeostasis and expression of IGF-1 and TGF-β1 in skeletal muscle during the repair process

  • Li Luo
  • Zhongwen Sun
  • Lin Zhang
  • Xiaoning Li
  • Yu Dong
  • Timon Cheng-Yi LiuEmail author
Original Article

Abstract

The aim of the present study was to determine the effects of low-level laser therapy (LLLT) on the homeostasis of reactive oxygen species (ROS) and expression of IGF-1 and TGF-β1 in the gastrocnemius muscles of rats following contusion. Muscle regeneration involves cell proliferation, migration, and differentiation and is regulated by growth factors. A growing body of evidence suggests that LLLT promotes skeletal muscle regeneration and accelerates tissue repair. Adult male Sprague-Dawley rats (n = 96) were randomly divided into three groups: control group (no lesion, untreated, n = 6), contusion group (n = 48), and contusion-plus-LLLT group (n = 42). Gallium aluminum arsenide (GaAlAs) laser irradiation (635 nm; beam spot, 0.4 cm2; output power, 7 mW; power density, 17.5 mW/cm2; 20 min) was administered to the gastrocnemius contusion for 20 min daily for 10 days. Muscle remodeling was evaluated at 0 h and 1, 2, 3, 7, 14, 21, and 28 days after injury. Hematoxylin and eosin and Van Gieson staining were used to evaluate regeneration and fibrosis; muscle superoxide dismutase (SOD) and malondialdehyde (MDA) were detected via biochemical methods; expression of transforming growth factor beta-1 (TGF-β1) and insulin-like growth factor-1 (IGF-1) were investigated via immunohistochemistry. The results showed that LLLT markedly promoted the regeneration of muscle and reduced scar formation. LLLT also significantly enhanced muscle SOD activity and significantly decreased muscle MDA levels 1, 2, and 3 days after injury. LLLT increased the expression of IGF-1 2, 3, and 7 days after injury and decreased the expression of IGF-1 21 and 28 days after injury. LLLT decreased the expression of TGF-β1 3 and 28 days after injury but increased expression at 7 and 14 days after injury. Our study showed that LLLT could modulate the homeostasis of ROS and of the growth factors IGF-1 and TGF-β1, which are known to play important roles in the repair process. This may constitute a new preventive approach to muscular fibrosis.

Keywords

IGF-1 TGF-β1 ROS Low-level laser therapy Skeletal muscle 

Notes

Competing interests

The authors have declared that no competing interests exist.

Funding

This work was supported by the National Science Foundation of China (60878061)

Supplementary material

10103_2012_1133_MOESM1_ESM.docx (40 kb)
ESM 1 (DOCX 40 kb)

References

  1. 1.
    Fillipin LI, Mauriz JL, Vedovelli K, Moreira AJ, Zettler CG, Lech O, Marroni NP, Gonzalez-Gallego J (2005) Low-level laser therapy (LLLT) prevents oxidative stress and reduces fibrosis in rat traumatized Achilles tendon. Lasers Surg Med 37(4):293–300. doi: 10.1002/lsm.20225 PubMedCrossRefGoogle Scholar
  2. 2.
    Rizzi CF, Mauriz JL, Freitas Correa DS, Moreira AJ, Zettler CG, Filippin LI, Marroni NP, Gonzalez-Gallego J (2006) Effects of low-level laser therapy (LLLT) on the nuclear factor (NF)-kappaB signaling pathway in traumatized muscle. Lasers Surg Med 38(7):704–713. doi: 10.1002/lsm.20371 PubMedCrossRefGoogle Scholar
  3. 3.
    Nussbaum EL (1999) Low-intensity laser therapy for benign fibrotic lumps in the breast following reduction mammaplasty. Phys Ther 79(7):691–698PubMedGoogle Scholar
  4. 4.
    Katz TM, Glaich AS, Goldberg LH, Friedman PM (2010) 595-nm long pulsed dye laser and 1450-nm diode laser in combination with intralesional triamcinolone/5-fluorouracil for hypertrophic scarring following a phenol peel. J Am Acad Dermatol 62(6):1045–1049. doi: 10.1016/j.jaad.2009.06.054 PubMedCrossRefGoogle Scholar
  5. 5.
    Cassuto DA, Scrimali L, Sirago P (2010) Treatment of hypertrophic scars and keloids with an LBO laser (532 nm) and silicone gel sheeting. J Cosmet Laser Ther 12(1):32–37. doi: 10.3109/14764170903453846 PubMedCrossRefGoogle Scholar
  6. 6.
    Huard J, Li Y, Fu FH (2002) Muscle injuries and repair: current trends in research. J Bone Joint Surg Am 84-A(5):822–832PubMedGoogle Scholar
  7. 7.
    Cuzzocrea S, Thiemermann C, Salvemini D (2004) Potential therapeutic effect of antioxidant therapy in shock and inflammation. Curr Med Chem 11(9):1147–1162PubMedCrossRefGoogle Scholar
  8. 8.
    Luciani A, Villella VR, Esposito S, Brunetti-Pierri N, Medina D, Settembre C, Gavina M, Pulze L, Giardino I, Pettoello-Mantovani M, D'Apolito M, Guido S, Masliah E, Spencer B, Quaratino S, Raia V, Ballabio A, Maiuri L (2010) Defective CFTR induces aggresome formation and lung inflammation in cystic fibrosis through ROS-mediated autophagy inhibition. Nat Cell Biol 12(9):863–875. doi: 10.1038/ncb2090 PubMedCrossRefGoogle Scholar
  9. 9.
    De Minicis S, Seki E, Paik YH, Osterreicher CH, Kodama Y, Kluwe J, Torozzi L, Miyai K, Benedetti A, Schwabe RF, Brenner DA (2010) Role and cellular source of nicotinamide adenine dinucleotide phosphate oxidase in hepatic fibrosis. Hepatology 52(4):1420–1430. doi: 10.1002/hep.23804 PubMedCrossRefGoogle Scholar
  10. 10.
    Sedeek M, Callera G, Montezano A, Gutsol A, Heitz F, Szyndralewiez C, Page P, Kennedy CR, Burns KD, Touyz RM, Hebert RL (2010) Critical role of Nox4-based NADPH oxidase in glucose-induced oxidative stress in the kidney: implications in type 2 diabetic nephropathy. Am J Physiol Renal Physiol 299(6):F1348–F1358. doi: 10.1152/ajprenal.00028.2010 PubMedCrossRefGoogle Scholar
  11. 11.
    Nabeebaccus A, Zhang M, Shah AM (2011) NADPH oxidases and cardiac remodelling. Heart Fail Rev 16(1):5–12. doi: 10.1007/s10741-010-9186-2 PubMedCrossRefGoogle Scholar
  12. 12.
    Chan EC, Jiang F, Peshavariya HM, Dusting GJ (2009) Regulation of cell proliferation by NADPH oxidase-mediated signaling: potential roles in tissue repair, regenerative medicine and tissue engineering. Pharmacol Ther 122(2):97–108. doi: 10.1016/j.pharmthera.2009.02.005 PubMedCrossRefGoogle Scholar
  13. 13.
    Smith C, Kruger MJ, Smith RM, Myburgh KH (2008) The inflammatory response to skeletal muscle injury: illuminating complexities. Sports Med 38(11):947–969. doi: 10.2165/00007256-200838110-000055 PubMedCrossRefGoogle Scholar
  14. 14.
    Urish KL, Vella JB, Okada M, Deasy BM, Tobita K, Keller BB, Cao B, Piganelli JD, Huard J (2009) Antioxidant levels represent a major determinant in the regenerative capacity of muscle stem cells. Mol Biol Cell 20(1):509–520. doi: 10.1091/mbc.E08-03-0274 PubMedCrossRefGoogle Scholar
  15. 15.
    Lubart R, Eichler M, Lavi R, Friedman H, Shainberg A (2005) Low-energy laser irradiation promotes cellular redox activity. Photomed Laser Surg 23(1):3–9. doi: 10.1089/pho.2005.23.3 PubMedCrossRefGoogle Scholar
  16. 16.
    Fujimaki Y, Shimoyama T, Liu Q, Umeda T, Nakaji S, Sugawara K (2003) Low-level laser irradiation attenuates production of reactive oxygen species by human neutrophils. J Clin Laser Med Surg 21(3):165–170. doi: 10.1089/104454703321895635 PubMedCrossRefGoogle Scholar
  17. 17.
    Avni D, Levkovitz S, Maltz L, Oron U (2005) Protection of skeletal muscles from ischemic injury: low-level laser therapy increases antioxidant activity. Photomed Laser Surg 23(3):273–277. doi: 10.1089/pho.2005.23.273 PubMedCrossRefGoogle Scholar
  18. 18.
    Pelosi L, Giacinti C, Nardis C, Borsellino G, Rizzuto E, Nicoletti C, Wannenes F, Battistini L, Rosenthal N, Molinaro M, Musaro A (2007) Local expression of IGF-1 accelerates muscle regeneration by rapidly modulating inflammatory cytokines and chemokines. FASEB J 21(7):1393–1402. doi: 10.1096/fj.06-7690com PubMedCrossRefGoogle Scholar
  19. 19.
    Ten Broek RW, Grefte S, Von den Hoff JW (2010) Regulatory factors and cell populations involved in skeletal muscle regeneration. J Cell Physiol 224(1):7–16. doi: 10.1002/jcp.22127 PubMedGoogle Scholar
  20. 20.
    Li Y, Foster W, Deasy BM, Chan Y, Prisk V, Tang Y, Cummins J, Huard J (2004) Transforming growth factor-beta1 induces the differentiation of myogenic cells into fibrotic cells in injured skeletal muscle: a key event in muscle fibrogenesis. Am J Pathol 164(3):1007–1019PubMedCrossRefGoogle Scholar
  21. 21.
    Cencetti FBC, Nincheri P, Donati C, Bruni P (2010) Transforming growth factor-beta1 induces transdifferentiation of myoblasts into myofibroblasts via up-regulation of sphingosine kinase-1/S1P3 axis. Mol Biol Cell 21(6):1111–1124PubMedCrossRefGoogle Scholar
  22. 22.
    Minamoto VB, Grazziano CR, Salvini TF (1999) Effect of single and periodic contusion on the rat soleus muscle at different stages of regeneration. Anat Rec 254(2):281–287. doi:10.1002/(SICI)1097-0185(19990201)254:2<281::AID-AR14>3.0.CO;2-ZPubMedCrossRefGoogle Scholar
  23. 23.
    Kami K, Masuhara M, Kashiba H, Kawai Y, Noguchi K, Senba E (1993) Changes of vinculin and extracellular matrix components following blunt trauma to rat skeletal muscle. Med Sci Sports Exerc 25(7):832–840PubMedCrossRefGoogle Scholar
  24. 24.
    Crisco JJ, Jokl P, Heinen GT, Connell MD, Panjabi MM (1994) A muscle contusion injury model. Biomechanics, physiology, and histology. Am J Sports Med 22(5):702–710PubMedCrossRefGoogle Scholar
  25. 25.
    Beiner JM, Jokl P, Cholewicki J, Panjabi MM (1999) The effect of anabolic steroids and corticosteroids on healing of muscle contusion injury. Am J Sports Med 27(1):2–9PubMedGoogle Scholar
  26. 26.
    McBrier NM, Neuberger T, Okita N, Webb A, Sharkey N (2009) Reliability and validity of a novel muscle contusion device. J Athl Train 44(3):275–278. doi: 10.4085/1062-6050-44.3.275 PubMedCrossRefGoogle Scholar
  27. 27.
    Chan YS, Li Y, Foster W, Horaguchi T, Somogyi G, Fu FH, Huard J (2003) Antifibrotic effects of suramin in injured skeletal muscle after laceration. J Appl Physiol 95(2):771–780. doi: 10.1152/japplphysiol.00915.2002 PubMedGoogle Scholar
  28. 28.
    Hurme T, Kalimo H (1992) Activation of myogenic precursor cells after muscle injury. Med Sci Sports Exerc 24(2):197–205PubMedGoogle Scholar
  29. 29.
    Rao VP, Branzoli SE, Ricci D, Miyagi N, O'Brien T, Tazelaar HD, Russell SJ, McGregor CG (2007) Recombinant adenoviral gene transfer does not affect cardiac allograft vasculopathy. J Heart Lung Transplant 26(12):1281–1285. doi: 10.1016/j.healun.2007.09.018 PubMedCrossRefGoogle Scholar
  30. 30.
    Patel S, Chung SH, White G, Bao S, Celermajer DS (2010) The "atheroprotective" mediators apolipoprotein A-I and Foxp3 are over-abundant in unstable carotid plaques. Int J Cardiol 145(2):183–187. doi: 10.1016/j.ijcard.2009.05.024 PubMedCrossRefGoogle Scholar
  31. 31.
    Grounds MD (1999) Muscle regeneration: molecular aspects and therapeutic implications. Curr Opin Neurol 12(5):535–543PubMedCrossRefGoogle Scholar
  32. 32.
    Shi X, Garry DJ (2006) Muscle stem cells in development, regeneration, and disease. Genes Dev 20(13):1692–1708. doi: 10.1101/gad.1419406 PubMedCrossRefGoogle Scholar
  33. 33.
    Karu T (1998) The science of low-power laser therapy. Gordon and Breach Science Publishers, AmsterdamGoogle Scholar
  34. 34.
    Choi JE, Lee SS, Sunde DA, Huizar I, Haugk KL, Thannickal VJ, Vittal R, Plymate SR, Schnapp LM (2009) Insulin-like growth factor-I receptor blockade improves outcome in mouse model of lung injury. Am J Respir Crit Care Med 179(3):212–219. doi: 10.1164/rccm.200802-228OC PubMedCrossRefGoogle Scholar
  35. 35.
    Feghali-Bostwick CA (2005) IGF-I: mediator of fibrosis or carcinogenesis? Am J Physiol Lung Cell Mol Physiol 288(5):L803–L804. doi: 10.1152/ajplung.00012.2005 PubMedCrossRefGoogle Scholar
  36. 36.
    Shen WLY, Zhu J, Schwendener R, Huard J (2008) Interaction between macrophages, TGF-beta1, and the COX-2 pathway during the inflammatory phase of skeletal muscle healing after injury. J Cell Physiol 214(2):405–412PubMedCrossRefGoogle Scholar
  37. 37.
    Tidball JG (2005) Inflammatory processes in muscle injury and repair. Am J Physiol Regul Integr Comp Physiol 288(2):R345–R353. doi: 10.1152/ajpregu.00454.2004 PubMedCrossRefGoogle Scholar
  38. 38.
    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-alpha and TGF-beta in skeletal muscle during the repair process. Lasers Med Sci 26(3):335–340. doi: 10.1007/s10103-010-0850-5 PubMedCrossRefGoogle Scholar

Copyright information

© Springer-Verlag London Ltd 2012

Authors and Affiliations

  • Li Luo
    • 1
    • 2
  • Zhongwen Sun
    • 3
  • Lin Zhang
    • 1
  • Xiaoning Li
    • 4
  • Yu Dong
    • 5
  • Timon Cheng-Yi Liu
    • 6
    • 7
    Email author
  1. 1.School of Physical Education and Sports ScienceSoochow UniversitySuzhouChina
  2. 2.School of MedicineSoochow UniversitySuzhouChina
  3. 3.Department of Microbiology and ImmunologySuzhou Health College of Vocational TechnologySuzhouChina
  4. 4.Department of PathologySuzhou Health College of Vocational TechnologySuzhouChina
  5. 5.Department of Orthopaedics and Sports MedicineHuashan Hospital, Fudan UniversityShanghaiChina
  6. 6.College of Sports Science and Research Center of Nationalistic Constitution and HealthSouth China Normal UniversityGuangzhouChina
  7. 7.Laboratory of Laser Sports MedicineSouth China Normal UniversityGuangzhouChina

Personalised recommendations