Electroacupuncture Increases the Concentration and Organization of Collagen in a Tendon Healing Model in Rats

References

• Kaptchuk, T.J. (2002). Acupuncture: Theory, efficacy, and practice. Ann. Inter. Med. 136:374–383.
   PubMed Web of Science ®Google Scholar
• Zijlstra, F.J., Van Den Berg-De Lange, I., Huygen, F.J., and Klein, J. (2003). Anti-inflammatory actions of acupuncture. Mediat. Inflamm. 12:59–69.
   PubMed Web of Science ®Google Scholar
• Kavoussi, B., and Ross, B.E. (2007). The neuroimmune basis of anti-inflammatory acupuncture. Integr. Cancer Ther. 6:251–257.
   PubMed Web of Science ®Google Scholar
• Wang, J., Zhao, H., Mao-Yinq, Q.L., Cao, X.D., Wang, Y.Q., and Wu, G.C. (2009). Electroacupuncture downregulates TLR2/4 and pro-inflammatory cytokine expression after surgical trauma stress without adrenal glands involvement. Brain Res. Bull. 80:89–94.
   PubMed Web of Science ®Google Scholar
• Lee, J.H., Jang, K.J., Lee, Y.T., Choi, Y.H., and Choi, B.T. (2006). Electroacupuncture inhibits inflammatory edema and hyperalgesia through regulation of cyclooxygenase synthesis in both peripheral and central nociceptive sites. Am. J. Chin. Med. 34:981–988.
   PubMed Web of Science ®Google Scholar
• Kim, H.W., Roh, D.H., Yoon, S.Y., Kang, S.Y., Kwon, Y.B., Han, H.J., Lee, H.J., Choi, S.M., Ryu, Y.H., Beitz, A.J., and Lee, J.H. (2006). The anti-inflammatory effects of low- and high-frequency electroacupuncture are mediated by peripheral opioids in a mouse air pouch inflammation model. J. Altern. Complement. Med. 12:39–44.
   PubMed Web of Science ®Google Scholar
• Kim, H.W., Kang, S.Y., Yoon, S.Y., Roh, D.H., Kwon, Y.B., Han, H.J., Lee, H.J., Beitz, A.J., and Lee, J.H. (2007). Low-frequency electroacupuncture suppresses zymosan-induced peripheral inflammation via activation of sympathetic post-ganglionic neurons. Brain Res. 1148:69–75.
   PubMed Web of Science ®Google Scholar
• Kim, H.W., Uh, D.K., Yoon, S.Y., Roh, D.H., Kwon, Y.B., Han, H.J., Lee, H.J., Beitz, A.J., and Lee, J.H. (2008). Low-frequency electroacupuncture suppresses carrageenan-induced paw inflammation in mice via sympathetic post-ganglionic neurons, while high-frequency EA suppression is mediated by the sympathoadrenal medullary axis. Brain Res. Bull. 75:698–705.
   PubMed Web of Science ®Google Scholar
• Lau, W.K., Chan, W.K., Zhang, J.L., Yunq, K.K., and Zhanq, H.Q. (2008). Electroacupuncture inhibits cyclooxygenase-2 up-regulation in rat spinal cord after spinal nerve ligation. Neuroscience 155:463–468.
   PubMed Web of Science ®Google Scholar
• Zhanq, S.P., Zhanq, J.S., Yunq, K.K., and Zhanq, H.Q. (2004). Non-opioid-dependent anti-inflammatory effects of low frequency electroacupuncture. Brain Res. Bull. 62:327–334.
   PubMed Web of Science ®Google Scholar
• Tian, L., Huanq, Y.X., Tian, M., Tian, L., Huanq, Y.X., Tian, M., Gao, W., and Chang, Q. (2003). Downregulation of electroacupuncture at ST36 on TNF-alpha in rats with ulcerative colitis. World J. Gastroenterol. 9:1028–1033.
   PubMed Web of Science ®Google Scholar
• Yim, Y.K., Lee, H., Honq, K.E., Kim, Y., Lee, B.R., Son, C.G., and Kim, J.E. (2007). Electro-acupuncture at acupoint ST36 reduces inflammation and regulates immune activity in collagen-induced arthritic mice. Evid. Based Complement. Alternat. Med. 4:51–57.
   PubMed Web of Science ®Google Scholar
• Langevin, H.M., Churchill, D.L., and Cipolla, M.J. (2001). Mechanical signaling through connective tissue: A mechanism for the therapeutic effect of acupuncture. FASEB J. 15:2275–2282.
   PubMed Web of Science ®Google Scholar
• Langevin, H.M., Bouffard, N.A., Badger, G.J., Churchill, D.L., and Howe, A.K. (2006). Subcutaneous tissue fibroblast cytoskeletal remodeling induced by acupuncture: Evidence for a mechanotransduction-based mechanism. J. Cell. Physiol. 207:767–774.
   PubMed Web of Science ®Google Scholar
• Langevin, H.M., Bouffard, N.A., Churchill, D.L., and Badger, G.J. (2007). Connective tissue fibroblast response to acupuncture: Dose-dependent effect of bidirectional needle rotation. J. Altern. Complement. Med. 13:355–360.
   PubMed Web of Science ®Google Scholar
• Wang, J.H. (2006). Mechanobiology of tendon. J. Biomech. 39: 1563–1582.
   PubMed Web of Science ®Google Scholar
• Järvinen, T.A., Kannus, P., Maffulli, N., and Khan, K.M. (2005). Achilles tendon disorders: Etiology and epidemiology. Foot Ankle Clin. 10:255–266.
   PubMedGoogle Scholar
• Järvinen, T.A., Kannus, P., Paavola, M., Järvinen, T.L., Józsa, L., and Järvinen, M. (2001). Achilles tendon injuries. Curr. Opin. Rheumatol. 13:150–155.
   PubMed Web of Science ®Google Scholar
• Kannus, P., and Natri, A. (1997). Etiology and pathophysiology of tendon ruptures in sports. Scand. J. Med. Sci. Sports 7:107–112.
   PubMed Web of Science ®Google Scholar
• Mazzone, M.F., and McCue, T. (2002). Common conditions of the Achilles tendon. Am. Fam. Physician 65:1805–1810.
   PubMed Web of Science ®Google Scholar
• Riley, G. (2008). Tendinopathy: From basic science to treatment. Nat. Clin. Pract. Rheumatol. 4:82–89.
   PubMedGoogle Scholar
• Abate, M., Silbernagel, K.G., Siljeholm, C., Di Lorio, A., De Amicis, D., Salini, V., Werner, S., and Paganelli, R. (2009). Pathogenesis of tendinopathies: Inflammation or degeneration? Arthritis Res. Ther. 11:235.
   PubMed Web of Science ®Google Scholar
• Sharma, P., and Maffulli, N. (2005). Tendon injury and tendinopathy: Healing and repair. J. Bone Joint Surg. Am. 87:187–202.
   PubMed Web of Science ®Google Scholar
• Yamamura, Y. (2001). Traditional Acupuncture: The Art of Insert [Acupuntura Tradicional: A Arte De Inserir]. São Paulo: ROCA.
   Google Scholar
• Carrinho, P.M., Renno, A.C., Koeke, P., Salate, A.C., Parizotto, N.A., and Vidal, B.C. (2006). Comparative study using 685-nm and 830-nm lasers in the tissue repair of tenotomized tendons in the mouse. Photomed. Laser Surg. 24:754–758.
   PubMed Web of Science ®Google Scholar
• Medeiros, M.A., Canteras, N.S., Suchecki, D., and Mello, L.E. (2003). c-Fos expression induced by electroacupuncture at the Zusanli point in rats submitted to repeated immobilization. Braz. J. Med. Biol. Res. 36:1673–1684.
   PubMed Web of Science ®Google Scholar
• Heinegard, D., and Sommarin, Y. (1987). Isolation and characterization of proteoglycans. Methods Enzymol. 144:319–372.
   PubMed Web of Science ®Google Scholar
• Bradford, M.M. (1976). A rapid and sensitive method for the quantitation of microgram quantities of protein utilizing the principle of protein-dye binding. Anal. Biochem. 72:248–254.
   PubMed Web of Science ®Google Scholar
• Farndale, R.W., Buttle, D.J., and Barret, A.J. (1986). Improved quantitation and discrimination of sulphated glycosaminoglycans by use of dimethylmethylene blue. Biochim. Biophys. Acta 883:173–177.
   PubMed Web of Science ®Google Scholar
• Stegemann, H., and Stalder, K. (1967). Determination of hydroxyproline. Clin. Chim. Acta 18:267–273.
   PubMed Web of Science ®Google Scholar
• Silva, J.A., Lorencini, M., Peroni, L.A., De La Hoz, C.L., Carvalho, H.F., and Stach-Machado, D.R. (2008). The influence of type I diabetes mellitus on the expression and activity of gelatinases (matrix metalloproteinases-2 and -9) in induced periodontal disease. J. Periodontal Res. 43:48–54.
   PubMed Web of Science ®Google Scholar
• Marqueti, R.C., Parizotto, N.A., Chriguer, R.S., Perez, S.E., and Selistre de Araujo, H.S. (2006). Androgenic-anabolic steroids associated with mechanical loading inhibit matrix metallopeptidase activity and affect the remodeling of the Achilles tendon in rats. Am. J. Sports Med. 34:1274–1280.
   PubMed Web of Science ®Google Scholar
• Kiernan, J.A. (1981). Histological and Histochemical Methods in Theory and Practice. Oxford: Pergamon Press.
   Google Scholar
• Mello, M.L., and Vidal, B.C. (2003). Experimental tendon repair: Glycosaminoglycan arrangement in newly synthesized collagen fibers. Cell Mol. Biol. 49:579–585.
   PubMed Web of Science ®Google Scholar
• Vidal, B.C. (1986). Evaluation of the carbohydrate role in the molecular order of collagen bundles: Microphotometric measurements of textual birefringence. Cell Mol. Biol. 32:527–535.
   PubMed Web of Science ®Google Scholar
• Vidal, B.C. (2010). Form birefringence as applied to biopolymer and inorganic material supraorganization. Biotech. Histochem. 85:365–378.
   PubMed Web of Science ®Google Scholar
• Vidal, B.C., and Mello, M.L. (2010). Optical anisotropy of collagen fibers of rat calcaneal tendons: An approach to spatially resolved supramolecular organization. Acta Histochem. 112:53–61.
   PubMed Web of Science ®Google Scholar
• Evanko, S.P., and Vogel, K.G. (1990). Ultrastructure and proteoglycan composition in the developing fibrocartilaginous region of bovine tendon. Matrix 10:420–436.
   PubMedGoogle Scholar
• Aro, A.A., Vidal, B.C., and Pimentel, E.R. (2012). Biochemical and anisotropical properties of tendons. Micron 43:205–214.
   PubMed Web of Science ®Google Scholar
• Scott, J.E. (1995). Extracellular matrix, supramolecular organization and shape. J. Anat. 187:259–269.
   PubMed Web of Science ®Google Scholar
• Scott, J.E. (1998). Proteoglycan-fibrillar collagen interactions. Biochem. J. 252:313–323.
   Google Scholar
• Scott, P.G., Nakano, T., and Dodd, C.M. (1997). Isolation and characterization of small proteoglycans from different zones of the porcine knee meniscus. Biochim. Biophys. Acta 1336:254–262.
   PubMed Web of Science ®Google Scholar
• Iozzo, R.V., and Murdoch, A.D. (1996). Proteoglycans of the extracellular environment: Clues from the gene and protein side offer novel perspectives in molecular diversity and function. FASEB J. 10:598–614.
   PubMed Web of Science ®Google Scholar
• Douglas, T., Heinemann, S., Bierbaum, S., Scharnweber, D., and Worch, H. (2006). Fibrillogenesis of collagen types I, II, and III with small leucine-rich proteoglycans decorin and biglycan. Biomacromolecules 7:2388–2393.
   PubMed Web of Science ®Google Scholar
• Clutterbuck, A.L., Harris, P., Allaway, D., and Mobasheri, A. (2010). Matrix metalloproteinases in inflammatory pathologies of the horse. Vet. J. 183:27–38.
   PubMed Web of Science ®Google Scholar
• Cilli, F., Khan, M., Fu, F., and Wang, J.H. (2004). Prostaglandin E2 affects proliferation and collagen synthesis by human patellar tendon fibroblasts. Clin. J. Sport Med. 14:232–236.
   PubMed Web of Science ®Google Scholar
• Riquet, F.B., Lai, W.F., Birkhead, J.R., Suen, L.F., Karsenty, G., and Goldring, M.B. (2000). Suppression of type I collagen gene expression by prostaglandins in fibroblasts is mediated at the transcriptional level. Mol. Med. 6:705–719.
   PubMed Web of Science ®Google Scholar
• Gosain, A., Jones, S.B., Shankar, R., Gamelli, R.L., and Di Pietro, L.A. (2006). Norepinephrine modulates the inflammatory and proliferative phases of wound healing. J. Trauma. 60:736–744.
   PubMed Web of Science ®Google Scholar
• Casalechi, H.L., Nicolau, R.A., Casalechi, V.L., Silveira, L.Jr., De Paula, A.M., and Pacheco, M.T. (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.
   PubMed Web of Science ®Google Scholar
• Vidal, B.C. (2003). Image analysis of tendon helical superstructure using interference and polarized light microscopy. Micron 34:423–432.
   PubMed Web of Science ®Google Scholar
• Kjaer, M., Langberg, H., Heinemeier, K., Bayer, M.L., Hansen, M., Holm, L., Doessing, S., Kongsgaard, M., Krogsgaard, M.R., and Magnusson, S.P. (2009). From mechanical loading to collagen synthesis, structural changes and function in human tendon. Scand. J. Med. Sci. Sports 19:500–510.
   PubMed Web of Science ®Google Scholar
• Chicurel, M.E., Chen, C.S., and Ingber, D.E. (1998). Cellular control lies in the balance of forces. Curr. Opin. Cell Biol. 10:232–239.
   PubMed Web of Science ®Google Scholar
• Giancotti, F.G., and Ruoslahti, E. (1999). Integrin signaling. Science 285:1028–1032.
   PubMed Web of Science ®Google Scholar
• Burridge, K., Fath, K., Kelly, T., Nuckolls, G., and Turner, C. (1988). Focal adhesions: Trans membrane junctions between the extracellular matrix and the cytoskeleton. Annu. Rev. Cell Biol. 4:487–525.
   PubMedGoogle Scholar
• Banes, A.J., Tsuzaki, M., Yamamoto, J., Fischer, T., Brigman, B., Brown, T., and Miller, L. (1995). Mechanoreception at the cellular level: The detection, interpretation and diversity of responses to mechanical signals. Biochem. Cell Biol. 73:349–365.
   PubMed Web of Science ®Google Scholar
• Dartsch, P.C., and Hammerle, H. (1986). Orientation response of arterial smooth muscle cells to mechanical stimulation. Eur. J. Cell Biol. 41:339–346.
   PubMed Web of Science ®Google Scholar
• Sumpio, B.E., Banes, A.J., Buckley, M., and Johnson, G. (1988). Alterations in aortic endothelial cell morphology and cytoskeletal protein synthesis during cyclic tensional deformation. J. Vasc. Surg. 7:130–138.
   PubMed Web of Science ®Google Scholar