Top

Published in:

01-01-2015 | Original Article

Second messengers mediating the proliferation and collagen synthesis of tenocytes induced by low-level laser irradiation

Authors: Mei-Hsiu Chen, Yun-Chien Huang, Jui-Sheng Sun, Yuan-Hung Chao, Ming-Hong Chen

Published in: Lasers in Medical Science | Issue 1/2015

Abstract

For decades, low-level laser therapy (LLLT) has widespread applications in tendon-related injuries. Although the therapeutic effect of LLLT could be explained by photostimulation of target tissue and cells, how tenocytes sense photonic energy and convert them into cascades of cellular and molecular events is still not well understood. This study was designed to elucidate the effects of LLLT on cell proliferation and collagen synthesis by examining the associated second messengers including ATP, Ca²⁺, and nitric oxide using rat Achilles tenocytes. Moreover, proliferating cell nuclear antigen (PCNA) and transforming growth factor-β1 (TGF-β1) related to cell proliferation and matrix metabolism were also studied. The results showed that 904 nm GaAs laser of 1 J/cm² could significantly increase the MTT activity and collagen synthesis of tenocytes. Second messengers including ATP and intracellular Ca2+ were increased after laser treatment. Quantitative PCR analysis of tenocytes treated with laser revealed up-regulated expression of PCNA, type I collagen, and TGF-β1. Besides, laser-induced TGF-β1 expression was significantly inhibited by extracellular signal-regulated kinase (ERK) specific inhibitor (PD98059). The findings suggested that LLLT stimulated ATP production and increased intracellular calcium concentration. Directly or indirectly via production of TGF-β1, these second messengers mediated the proliferation of tenocytes and synthesis of collagen.

Hawkins D, Abrahamse H (2006) Effect of multiple exposures of low-level laser therapy on the cellular responses of wounded human skin fibroblasts. Photomed Laser Surg 24:705–714. doi:10.1089/pho.2006.24.705 PubMedCrossRef

Bjordal JM, Lopes-Martins RA, Joensen J et al (2008) A systematic review with procedural assessments and meta-analysis of low level laser therapy in lateral elbow tendinopathy (tennis elbow). BMC Musculoskelet Disord 9:75. doi:10.1186/1471-2474-9-75 PubMedCentralPubMedCrossRef

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 29:1075–1081. doi:10.1007/s10103-013-1468-1 PubMedCrossRef

Oliveira FS, Pinfildi CE, Parizoto NA et al (2009) Effect of low level laser therapy (830 nm) with different therapy regimes on the process of tissue repair in partial lesion calcaneous tendon. Lasers Surg Med 41:271–276. doi:10.1002/lsm.20760 PubMedCrossRef

Fillipin LI, Mauriz JL, Vedovelli K et al (2005) Low-level laser therapy (LLLT) prevents oxidative stress and reduces fibrosis in rat traumatized Achilles tendon. Lasers Surg Med 37:293–300. doi:10.1002/lsm.20225 PubMedCrossRef

Guerra FDR, Vieira CP, Almeida MS et al (2013) LLLT improves tendon healing through increase of MMP activity and collagen synthesis. Lasers Med Sci 28:1281–1288. doi:10.1007/s10103-012-1236-7 CrossRef

Evans DH, Abrahamse H (2009) A review of laboratory-based methods to investigate second messengers in low-level laser therapy (LLLT). Med Laser Appl 24:201–215. doi:10.1016/j.mla.2009.05.003 CrossRef

Fujita T, Shiba H, Sakata M et al (2002) Effects of transforming growth factor-beta 1 and fibronectin on SPARC expression in cultures of human periodontal ligament cells. Cell Biol Int 26:1065–1072PubMedCrossRef

Chao Y-H, Tsuang Y-H, Sun J-S et al (2008) Effects of shock waves on tenocyte proliferation and extracellular matrix metabolism. Ultrasound Med Biol 34:841–852. doi:10.1016/j.ultrasmedbio.2007.11.002 PubMedCrossRef

10.

Kjaer M (2004) Role of extracellular matrix in adaptation of tendon and skeletal muscle to mechanical loading. Physiol Rev 84:649–698. doi:10.1152/physrev.00031.2003 PubMedCrossRef

11.

Cowan KJ, Storey KB (2003) Mitogen-activated protein kinases: new signaling pathways functioning in cellular responses to environmental stress. J Exp Biol 206:1107–1115PubMedCrossRef

12.

Chao Y-H, Tsuang Y-H, Sun J-S et al (2011) The cross-talk between transforming growth factor-beta1 and ultrasound stimulation during mechanotransduction of rat tenocytes. Connect Tissue Res 52:313–321. doi:10.3109/03008207.2010.525673 PubMedCrossRef

13.

Prelich G, Stillman B (1988) Coordinated leading and lagging strand synthesis during SV40 DNA replication in vitro requires PCNA. Cell 53:117–126PubMedCrossRef

14.

Tsai W-C, Cheng J-W, Chen J-L et al (2014) Low-level laser irradiation stimulates tenocyte proliferation in association with increased NO synthesis and upregulation of PCNA and cyclins. Lasers Med Sci 29:1377–1384. doi:10.1007/s10103-014-1528-1 PubMedCrossRef

15.

AlGhamdi KM, Kumar A, Moussa NA (2012) Low-level laser therapy: a useful technique for enhancing the proliferation of various cultured cells. Lasers Med Sci 27:237–249. doi:10.1007/s10103-011-0885-2 PubMedCrossRef

16.

Stork PJS, Schmitt JM (2002) Crosstalk between cAMP and MAP kinase signaling in the regulation of cell proliferation. Trends Cell Biol 12:258–266PubMedCrossRef

17.

Vacca RA, Moro L, Petragallo VA et al (1997) The irradiation of hepatocytes with He-Ne laser causes an increase of cytosolic free calcium concentration and an increase of cell membrane potential, correlated with it, both increases taking place in an oscillatory manner. Biochem Mol Biol Int 43:1005–1014PubMed

18.

Coombe AR, Ho CT, Darendeliler MA et al (2001) The effects of low level laser irradiation on osteoblastic cells. Clin Orthod Res 4:3–14PubMedCrossRef

19.

Chuderland D, Marmor G, Shainskaya A, Seger R (2008) Calcium-mediated interactions regulate the subcellular localization of extracellular signal-regulated kinases. J Biol Chem 283:11176–11188. doi:10.1074/jbc.M709030200 PubMedCrossRef

20.

Cohen N, Lubart R, Rubinstein S, Breitbart H (1998) Light irradiation of mouse spermatozoa: stimulation of in vitro fertilization and calcium signals. Photochem Photobiol 68:407–413PubMedCrossRef

21.

Murrell GA, Szabo C, Hannafin JA et al (1997) Modulation of tendon healing by nitric oxide. Inflamm Res Off J Eur Histamine Res Soc Al 46:19–27

22.

Sharma P, Maffulli N (2005) Tendon injury and tendinopathy: healing and repair. J Bone Joint Surg Am 87:187–202. doi:10.2106/JBJS.D.01850 PubMedCrossRef

23.

Abrahamsson SO (1991) Matrix metabolism and healing in the flexor tendon. Experimental studies on rabbit tendon. Scand J Plast Reconstr Surg Hand Surg Suppl 23:1–51PubMed

24.

Chen C-H, Tsai J-L, Wang Y-H et al (2009) Low-level laser irradiation promotes cell proliferation and mRNA expression of type I collagen and decorin in porcine Achilles tendon fibroblasts in vitro. J Orthop Res Off Publ Orthop Res Soc 27:646–650. doi:10.1002/jor.20800 CrossRef

25.

Wood VT, Pinfildi CE, Neves MAI et al (2010) Collagen changes and realignment induced by low-level laser therapy and low-intensity ultrasound in the calcaneal tendon. Lasers Surg Med 42:559–565. doi:10.1002/lsm.20932 PubMedCrossRef

26.

Neves MAI, Pinfildi CE, Wood VT et al (2011) Different power settings of LLLT on the repair of the calcaneal tendon. Photomed Laser Surg 29:663–668. doi:10.1089/pho.2010.2919 PubMedCrossRef

27.

Lijnen PJ, Petrov VV, Fagard RH (2000) Induction of cardiac fibrosis by transforming growth factor-beta(1). Mol Genet Metab 71:418–435. doi:10.1006/mgme.2000.3032 PubMedCrossRef

28.

Aliodoust M, Bayat M, Jalili MR et al (2014) Evaluating the effect of low-level laser therapy on healing of tentomized Achilles tendon in streptozotocin-induced diabetic rats by light microscopical and gene expression examinations. Lasers Med Sci 29:1495–1503. doi:10.1007/s10103-014-1561-0 PubMedCrossRef

29.

Molloy T, Wang Y, Murrell G (2003) The roles of growth factors in tendon and ligament healing. Sports Med Auckl NZ 33:381–394CrossRef

30.

Shefer G, Oron U, Irintchev A et al (2001) Skeletal muscle cell activation by low-energy laser irradiation: a role for the MAPK/ERK pathway. J Cell Physiol 187:73–80. doi:10.1002/1097-4652(2001)9999:9999<::AID-JCP1053>3.0.CO;2-9 PubMedCrossRef

31.

Miyata H, Genma T, Ohshima M et al (2006) Mitogen-activated protein kinase/extracellular signal-regulated protein kinase activation of cultured human dental pulp cells by low-power gallium-aluminium-arsenic laser irradiation. Int Endod J 39:238–244. doi:10.1111/j.1365-2591.2006.01080.x PubMedCrossRef

Title: Second messengers mediating the proliferation and collagen synthesis of tenocytes induced by low-level laser irradiation
Authors: Mei-Hsiu Chen
Yun-Chien Huang
Jui-Sheng Sun
Yuan-Hung Chao
Ming-Hong Chen
Publication date: 01-01-2015
Publisher: Springer London
Published in: Lasers in Medical Science / Issue 1/2015
Print ISSN: 0268-8921
Electronic ISSN: 1435-604X
DOI: https://doi.org/10.1007/s10103-014-1658-5

Keynote webinar | Spotlight on medication adherence

Springer Medicine

Second messengers mediating the proliferation and collagen synthesis of tenocytes induced by low-level laser irradiation

Abstract

Keynote webinar | Spotlight on medication adherence

Springer Medicine

Abstract

Please log in to get access to this content

Other articles of this Issue 1/2015

Laser irradiation of ferrous particles for hyperthermia as cancer therapy, a theoretical study

Combination of a novel photosensitizer DTPP with 650 nm laser results in efficient apoptosis, arresting cell cycle and cytoskeleton protein changes in lung cancer A549 cells

Low power laser stimulation of the bone consolidation in tibial fractures of rats: a radiologic and histopathological analysis

Expression of mPGES-1 and IP mRNA is reduced by LLLT in both subplantar and brain tissues in the model of peripheral inflammation induced by carrageenan

The effect of dosage on the efficiency of LLLT in new bone formation at the expanded suture in rats

Antimicrobial action from a novel porphyrin derivative in photodynamic antimicrobial chemotherapy in vitro