Skip to main content

Advertisement

SpringerLink
Log in

Photobiomodulation therapy on expression of HSP70 protein and tissue repair in experimental acute Achilles tendinitis

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

Abstract

The aim of the present study was to investigate the effects of photobiomodulation (PBM) therapy on the expression of heat shock protein 70 (HSP70) and tissue repair in an experimental model of collagenase-induced Achilles tendinitis. Thirty Wistar rats (aged 12 weeks) were randomly distributed among control group (n = 8), tendinitis group (n = 11), and LED group (n = 11). Tendinitis was induced in the tendinitis and LED groups through a peritendinous injection of collagenase (100 μl). The LED group animals received the first irradiation 1 h after injury. A 630 ± 20 nm, 300-mW continuous wave light-emitting diode (LED), spot size 1 cm2, was placed in contact with the skin. One point over the tendon was irradiated for 30 s, delivering 9 J (9 J/cm2). LED irradiation was performed once daily for 7 days, with the total energy delivered being 63 J. The tendons were surgically removed and expression of the HSP70 protein was calculated using semi-quantitative analyses of immunohistochemistry (HSCORE). Number of fibroblasts and amount of collagen were measured using histological and histochemical analyses. An increase in the mean HSCORE for HSP70, in the number of fibroblasts, and in the amount of collagen were found in the LED group compared with those in the tendinitis and control group (P ≤ 0.05). PBM therapy increased the expression of the HSP70, number of fibroblasts, and amount of collagen in the acute Achilles tendinitis in rats.

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

Access this article

Log in via an institution

Subscribe and save

Springer+ Basic
$34.99 /Month
  • Get 10 units per month
  • Download Article/Chapter or eBook
  • 1 Unit = 1 Article or 1 Chapter
  • Cancel anytime
Subscribe now

Buy Now

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
Fig. 5
Fig. 6

Similar content being viewed by others

References

  1. Li HY, Hua YH (2016) Achilles tendinopathy: current concepts about the basic science and clinical treatments. Biomed Res Int:6492597. https://doi.org/10.1155/2016/6492597

  2. Federer AE, Steele JR, Dekker TJ, Liles JL, Adams SB (2017) Tendonitis and tendinopathy. Foot Ankle Clin 22(4):665–676. https://doi.org/10.1016/j.fcl.2017.07.002

    Article  PubMed  Google Scholar 

  3. Sharma P, Maffulli N (2006) Biology of tendon injury: healing, modeling and remodeling. J Musculoskelet Neuronal Interact 6(2):181–190

    CAS  PubMed  Google Scholar 

  4. Marcos RL, Leal-Junior EC, Arnold G et al (2012) Low-level laser therapy in collagenase-induced Achilles tendinitis in rats: analyses of biochemical and biomechanical aspects. J Orthop Res 30:1945–1951. https://doi.org/10.1002/jor.22156

    Article  CAS  PubMed  Google Scholar 

  5. Longo UG, Ronga M, Maffulli N (2018) Achilles tendinopathy. Sports Med Arthrosc 26(1):16–30. https://doi.org/10.1097/jsa.0000000000000185

    Article  PubMed  Google Scholar 

  6. Xu Y, Murrell GAC (2008) The basic science of tendinopathy. Clin Orthop Relat Res 466(7):1528–1538. https://doi.org/10.1007/s11999-008-0286-4

    Article  PubMed  PubMed Central  Google Scholar 

  7. Schlesinger MJ (1990) Heat shock proteins. J Biol Chem 265(21):12111–12114

    Article  CAS  Google Scholar 

  8. Millar NL, Murrell GA (2012) Heat shock proteins in tendinopathy: novel molecular regulators. Mediat Inflamm 436203. https://doi.org/10.1155/2012/436203

  9. Nell EM, Merwe LVD, Cook J et al (2012) The apoptosis pathway and the genetic predisposition to Achilles tendinopathy. J Orthop Res 30(11):1719–1724. https://doi.org/10.1002/jor.22144

    Article  CAS  PubMed  Google Scholar 

  10. Lanneau D, de Thonel A, Maurel S, Didelot C, Garrido C (2007) Apoptosis versus cell differentiation: role of heat shock proteins HSP90, HSP70 and HSP27. Prion 1(1):53–60. https://doi.org/10.4161/pri.1.1.4059

    Article  PubMed  PubMed Central  Google Scholar 

  11. Samali A, Orrenius S (1998) Heat shock proteins: regulators of stress response and apoptosis. Cell Stress Chaperones 3:228–236. https://doi.org/10.1379/1466-1268(1998)003<0228:hspros>2.3.co;2

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  12. Millar NL, Reilly JH, Kerr SC, Campbell AL, Little KJ, Leach WJ (2012) Hypoxia: a critical regulator of early human tendinopathy. Ann Rheum Dis 71(2):302–310. https://doi.org/10.1136/ard.2011.154229

    Article  CAS  PubMed  Google Scholar 

  13. Bellmann K, Jäättelä M, Wissing D, Burkart V, Kolb H (1996) Heat shock protein hsp70 overexpression confers resistance against nitric oxide. FEBS Lett 391(1–2):185–188. https://doi.org/10.1016/0014-5793(96)00730-2

    Article  CAS  PubMed  Google Scholar 

  14. Torres-Silva R, Lopes-Martins RA, Bjordal JM et al (2015) The low level laser therapy (LLLT) operating in 660 nm reduce gene expression of inflammatory mediators in the experimental model of collagenase-induced rat tendinitis. Lasers Med Sci 30(7):1985–1990. https://doi.org/10.1007/s10103-014-1676-3

    Article  PubMed  Google Scholar 

  15. Xavier M, de Souza RA, Pires VA, Santos AP, Aimbire F, Silva JA Jr, Albertini R, Villaverde AB (2014) Low-level light-emitting diode therapy increases mRNA expressions of IL-10 and type I and III collagens on Achilles tendinitis in rats. Lasers Med Sci 29(1):85–90. https://doi.org/10.1007/s10103-013-1280-y

    Article  PubMed  Google Scholar 

  16. Novoselova EG, Glushkova OV, Cherenkov DA, Chudnovsky VM, Fesenko EE (2006) Effects of low-power laser radiation on mice immunity. Photodermatol Photoimmunol Photomed 22(1):33–38. https://doi.org/10.1111/j.1600-0781.2006.00191.x

    Article  CAS  PubMed  Google Scholar 

  17. Du S, Zhang Q, Zhang S, Wang L, Lian J (2012) Heat shock protein 70 expression induced by diode laser irradiation on choroid-retinal endothelial cells in vitro. Mol Vis 18:2380–2387

    CAS  PubMed  PubMed Central  Google Scholar 

  18. Xavier M, David DR, de Souza RA et al (2010) Anti-inflammatory effects of low-level light emitting diode therapy on Achilles tendinitis in rats. Laser Surg Med 42:553–558. https://doi.org/10.1002/lsm.20896

    Article  Google Scholar 

  19. Varghese F, Bukhari AB, Malhotra R, De A (2014) IHC profiler: an open source plugin for the quantitative evaluation and automated scoring of immunohistochemistry images of human tissue samples. PLoS One 9(5):e96801. https://doi.org/10.1371/journal.pone.0096801

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  20. Flanagan MB, Dabbs DJ, Brufsky AM, Beriwal S, Bhargava R (2008) Histopathologic variables predict Oncotype DX recurrence score. Mod Pathol 21(10):1255–1261. https://doi.org/10.1038/modpathol.2008.54

    Article  CAS  PubMed  Google Scholar 

  21. Cardoso CM, Sartorio PV, Machado ASD, Vignardi CP et al (2015) Hsp70 and p53 expressions and behavior of juvenile pompano, Trachinotus carolinus (Perciformes, Carangidae), at controlled temperature increase. J Exp Mar Biol Ecol 470:34–42. https://doi.org/10.1016/j.jembe.2015.04.024

    Article  CAS  Google Scholar 

  22. Pires D, Xavier M, Araújo T, Silva JA Jr, Aimbire F, Albertini R (2011) 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 26:85–94. https://doi.org/10.1007/s10103-010-0811-z

    Article  PubMed  Google Scholar 

  23. de Lima FM, Albertini R, Dantas Y et al (2013) Low level laser therapy restores the oxidative stress balance in acute lung injury induced by gut schemia and reperfusion. Photochem Photobiol 89(1):179–188. https://doi.org/10.1111/j.1751-1097.2012.01214

    Article  PubMed  Google Scholar 

  24. Sun Y, Zhang S, Liao H et al (2015) Pre-exposure to low-power diode laser irradiation promotes cytoprotection in the rat retina. Lasers Med Sci 30(1):127–133. https://doi.org/10.1007/s10103-014-1619-z

    Article  PubMed  Google Scholar 

  25. Casalechi HL, de Farias Marques AC, da Silva EAP et al (2014) Analysis of the effect of phototherapy in model with traumatic Achilles tendon injury in rats. Lasers Med Sci 29:1075. https://doi.org/10.1007/s10103-013-1468-1

    Article  PubMed  Google Scholar 

  26. Marques AC, Albertini R, Serra AJ et al (2016) Photobiomodulation therapy on collagen type I and III, vascular endothelial growth factor, and metalloproteinase in experimentally induced tendinopathy in aged rats. Lasers Med Sci 31:1915. https://doi.org/10.1007/s10103-016-2070-0

    Article  PubMed  Google Scholar 

  27. Naterstad IF, Rossi RP, Marcos RL et al (2018) Comparison of photobiomodulation and anti-inflammatory drugs on tissue repair on collagenase-induced Achilles tendon inflammation in rats. Photomed Laser Surg 36(3):137–145. https://doi.org/10.1089/pho.2017.4364

    Article  CAS  PubMed  Google Scholar 

  28. Lim W, Lee S, Kim I et al (2007) The anti-inflammatory mechanism of 635 nm light-emitting-diode irradiation compared with existing cox inhibitors. Lasers Surg Med 39:614–621. https://doi.org/10.1002/lsm.20533

    Article  PubMed  Google Scholar 

  29. Karu TI, Kolyakov SF (2005) Exact action spectra for cellular responses relevant to phototherapy. Photomed Laser Surg 23(4):355–361. https://doi.org/10.1089/pho.2005.23.355

    Article  CAS  PubMed  Google Scholar 

  30. Enwemeka CS, Parker JC, Dowdy DS et al (2004) The efficacy of low-power lasers in tissue repair and pain control: a meta-analysis study. Photomed Laser Surg 22:323–329. https://doi.org/10.1089/pho.2004.22.323

    Article  PubMed  Google Scholar 

  31. Bastos JLN, Lizarelli RFZ, Parizotto NA (2009) Comparative study of laser and LED systems of low intensity applied to tendon healing. Laser Phys 19(9):1925–1931. https://doi.org/10.1134/s1054660x09170022

    Article  CAS  Google Scholar 

  32. Casalechi HL, Nicolau RA, Casalechi VL, Silveira-Júnior L, Paula AMB, Pacheco MTT (2009) The effects of low level light emitting diode on the repair process of Achilles tendon therapy in rats. Lasers Med Sci 24:659–665. https://doi.org/10.1007/s10103-008-0607-6

    Article  PubMed  Google Scholar 

  33. Moura Júnior MD, Arisawa EA, Martin AA et al (2014) Effects of low-power LED and therapeutic ultrasound in the tissue healing and inflammation in a tendinitis experimental model in rats. Lasers Med Sci 29:301–311. https://doi.org/10.1007/s10103-013-1327-0

    Article  Google Scholar 

  34. Helrigle C, de Carvalho PD, Casalechi HL et al (2016) Effects of low-intensity non-coherent light therapy on the inflammatory process in the calcaneal tendon of ovariectomized rats. Lasers Med Sci 31(1):33–40. https://doi.org/10.1007/s10103-015-1821-7

    Article  PubMed  Google Scholar 

Download references

Funding

This study was supported in part by the Fundação de Amparo à Pesquisa do Estado de Minas Gerais (FAPEMIG) (APQ-01239-14) and the Coordenação de Aperfeiçoamento de Pessoal de Nível Superior (CAPES) (finance code 001).

Author information

Authors and Affiliations

  1. Department of Physical Therapy, Federal University of Jequitinhonha and Mucuri Valleys, UFVJM, Campus JK - MG Rodovia MGT 367 - Km 583, n° 5000 - Alto da Jacuba, Diamantina, 39100-000, Brazil

    André Nobre Evangelista, Flávia Franciele dos Santos, Lorena Pacheco de Oliveira Martins, Thais Peixoto Gaiad, Karine Beatriz Costa, Ana Paula Santos & Murilo Xavier Oliveira

  2. School of Medicine, Federal University of Jequitinhonha and Mucuri Valleys, UFVJM, Campus JK, Diamantina, MG, Brazil

    Alex Sander Dias Machado & Etel Rocha-Vieira

Authors
  1. André Nobre Evangelista
    View author publications

    You can also search for this author in PubMed Google Scholar

  2. Flávia Franciele dos Santos
    View author publications

    You can also search for this author in PubMed Google Scholar

  3. Lorena Pacheco de Oliveira Martins
    View author publications

    You can also search for this author in PubMed Google Scholar

  4. Thais Peixoto Gaiad
    View author publications

    You can also search for this author in PubMed Google Scholar

  5. Alex Sander Dias Machado
    View author publications

    You can also search for this author in PubMed Google Scholar

  6. Etel Rocha-Vieira
    View author publications

    You can also search for this author in PubMed Google Scholar

  7. Karine Beatriz Costa
    View author publications

    You can also search for this author in PubMed Google Scholar

  8. Ana Paula Santos
    View author publications

    You can also search for this author in PubMed Google Scholar

  9. Murilo Xavier Oliveira
    View author publications

    You can also search for this author in PubMed Google Scholar

Contributions

All authors contributed to the study conception and design. Material preparation, data collection, and analysis were performed by André Nobre Evangelista, Lorena Pacheco de Oliveira Martins, Flávia Franciele dos Santos, Karine Beatriz Costa, Etel Rocha-Vieira, and Ana Paula Santos. Funding acquisition and supervision were performed by Murilo Xavier Oliveira, Thais Peixoto Gaiad, and Alex Sander Dias Machado. The first draft of the manuscript was written by André Nobre Evangelista, Lorena Pacheco de Oliveira Martins, and Flávia Franciele dos Santos, and all authors commented on previous versions of the manuscript. All authors read and approved the final manuscript.

Corresponding author

Correspondence to Murilo Xavier Oliveira.

Ethics declarations

Conflict of interest

The authors declare that they have no conflict of interest.

Ethical approval

The study was approved by the Ethics Committee on Animal Use of the Federal University of Jequitinhonha and Mucuri Valleys (certificate number: 007/2014).

Consent to participate

Not applicable.

Consent for publication

Not applicable.

Additional information

Publisher’s note

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

Rights and permissions

Reprints and permissions

About this article

Check for updates. Verify currency and authenticity via CrossMark

Cite this article

Evangelista, A.N., dos Santos, F.F., de Oliveira Martins, L.P. et al. Photobiomodulation therapy on expression of HSP70 protein and tissue repair in experimental acute Achilles tendinitis. Lasers Med Sci 36, 1201–1208 (2021). https://doi.org/10.1007/s10103-020-03155-3

Download citation

  • Received:

  • Accepted:

  • Published:

  • Issue Date:

  • DOI: https://doi.org/10.1007/s10103-020-03155-3

Keywords

Search

Navigation