Alpha-2 adrenergic stimulation triggers Achilles tenocyte hypercellularity: Comparison between two model systems

Scandinavian Journal of Medicine and Science in Sports

Volumn 23, Issue 6, 2013, Pages 687-696

  Backman, L J ^a   Andersson, G ^a   Fong, G ^a,b,c   Alfredson, H ^a   Scott, A ^b,c   Danielson, P ^a  

^a UMEÅ UNIVERSITY   (Sweden)

^b UNIVERSITY OF BRITISH COLUMBIA   (Canada)

^c VANCOUVER COASTAL HEALTH   (Canada)

Author keywords

2A adrenoreceptor; Achilles tendon; Tendinopathy; Tendinosis

Indexed keywords

2 (1 METHYL 2 ISOINDOLINYLMETHYL) 2 IMIDAZOLINE; ALPHA 2 ADRENERGIC RECEPTOR; ALPHA 2 ADRENERGIC RECEPTOR BLOCKING AGENT; ALPHA 2 ADRENERGIC RECEPTOR STIMULATING AGENT; CLONIDINE; IMIDAZOLE DERIVATIVE; ISOINDOLE DERIVATIVE; TYROSINE 3 MONOOXYGENASE;

ACHILLES TENDON; ANIMAL; ARTICLE; CELL CULTURE; CELL PROLIFERATION; CUMULATIVE TRAUMA DISORDER; CYTOLOGY; DISEASE MODEL; DRUG EFFECT; FEMALE; HUMAN; IN VITRO STUDY; METABOLISM; RABBIT; TENDINITIS; Α2A ADRENORECEPTOR;

ACHILLES TENDON; TENDINOPATHY; TENDINOSIS; Α2A ADRENORECEPTOR;

ACHILLES TENDON; ADRENERGIC ALPHA-2 RECEPTOR AGONISTS; ADRENERGIC ALPHA-2 RECEPTOR ANTAGONISTS; ANIMALS; CELL PROLIFERATION; CELLS, CULTURED; CLONIDINE; CUMULATIVE TRAUMA DISORDERS; DISEASE MODELS, ANIMAL; FEMALE; HUMANS; IMIDAZOLES; ISOINDOLES; RABBITS; RECEPTORS, ADRENERGIC, ALPHA-2; TENDINOPATHY; TYROSINE 3-MONOOXYGENASE;

EID: 84888127887     PISSN: 09057188     EISSN: 16000838     Source Type: Journal    
DOI: 10.1111/j.1600-0838.2011.01442.x     Document Type: Article

References (42)

1. Alfredson H. Ultrasound and Doppler-guided mini-surgery to treat midportion Achilles tendinosis: results of a large material and a randomised study comparing two scraping techniques. Br J Sports Med 2011: 45: 407-410.
2. Alfredson H, Lorentzon R. Chronic Achilles tendinosis: recommendations for treatment and prevention. Sports Med 2000: 29: 135-146.
3. Alfredson H, Ohberg L, Zeisig E, Lorentzon R. Treatment of midportion Achilles tendinosis: similar clinical results with US and CD-guided surgery outside the tendon and sclerosing polidocanol injections. Knee Surg Sports Traumatol Arthrosc 2007: 15: 1504-1509.
4. Andersson G, Backman LJ, Scott A, Lorentzon R, Forsgren S, Danielson P. Substance P accelerates hypercellularity and angiogenesis in tendon tissue and enhances paratendinitis in response to Achilles tendon overuse in a tendinopathy model. Br J Sports Med 2011a: 45: 1017-1022.
5. Andersson G, Danielson P, Alfredson H, Forsgren S. Nerve-related characteristics of ventral paratendinous tissue in chronic Achilles tendinosis. Knee Surg Sports Traumatol Arthrosc 2007: 15: 1272-1279.
6. Andersson G, Danielson P, Alfredson H, Forsgren S. Presence of substance P and the neurokinin-1 receptor in tenocytes of the human Achilles tendon. Regul Pept 2008: 150: 81-87.
7. Andersson G, Forsgren S, Scott A, Gaida JE, Stjernfeldt JE, Lorentzon R, Alfredson H, Backman C, Danielson P. Tenocyte hypercellularity and vascular proliferation in a rabbit model of tendinopathy: contralateral effects suggest the involvement of central neuronal mechanisms. Br J Sports Med 2011b: 45: 399-406.
8. Astrom M, Westlin N. Blood flow in chronic Achilles tendinopathy. Clin Orthop Relat Res 1994: 308: 166-172.
9. Backman C, Boquist L, Friden J, Lorentzon R, Toolanen G. Chronic Achilles paratenonitis with tendinosis: an experimental model in the rabbit. J Orthop Res 1990: 8: 541-547.
10. Backman C, Friden J, Widmark A. Blood flow in chronic Achilles tendinosis. Radioactive microsphere study in rabbits. Acta Orthop Scand 1991: 62: 386-387.
11. Backman LJ, Fong G, Andersson G, Scott A, Danielson P. Substance P is a mechanoresponsive, autocrine regulator of human tenocyte proliferation. PLoS ONE 2011: 6: e27209. doi:10.1371/journal.pone.0027209.
12. Baron R. Peripheral neuropathic pain: from mechanisms to symptoms. Clin J Pain 2000: 16: S12-S20.
13. Baron R, Levine JD, Fields HL. Causalgia and reflex sympathetic dystrophy: does the sympathetic nervous system contribute to the generation of pain? Muscle Nerve 1999: 22: 678-695.
14. Bjur D, Alfredson H, Forsgren S. The innervation pattern of the human Achilles tendon: studies of the normal and tendinosis tendon with markers for general and sensory innervation. Cell Tissue Res 2005: 320: 201-206.
15. Bjur D, Danielson P, Alfredson H, Forsgren S. Immunohistochemical and in situ hybridization observations favor a local catecholamine production in the human Achilles tendon. Histol Histopathol 2008: 23: 197-208.
16. Bouloumie A, Planat V, Devedjian JC, Valet P, Saulnier-Blache JS, Record M, Lafontan M. Alpha 2-adrenergic stimulation promotes preadipocyte proliferation. Involvement of mitogen-activated protein kinases. J Biol Chem 1994: 269: 30254-30259.
17. Cook JL, Feller JA, Bonar SF, Khan KM. Abnormal tenocyte morphology is more prevalent than collagen disruption in asymptomatic athletes' patellar tendons. J Orthop Res 2004: 22: 334-338.
18. Danielson P, Alfredson H, Forsgren S. In situ hybridization studies confirming recent findings of the existence of a local nonneuronal catecholamine production in human patellar tendinosis. Microsc Res Tech 2007a: 70: 908-911.
19. Danielson P, Alfredson H, Forsgren S. Studies on the importance of sympathetic innervation, adrenergic receptors, and a possible local catecholamine production in the development of patellar tendinopathy (tendinosis) in man. Microsc Res Tech 2007b: 70: 310-324.
20. Danielson P, Andersson G, Alfredson H, Forsgren S. Marked sympathetic component in the perivascular innervation of the dorsal paratendinous tissue of the patellar tendon in arthroscopically treated tendinosis patients. Knee Surg Sports Traumatol Arthrosc 2008: 16: 621-626.
21. Fan TP, Hu DE, Guard S, Gresham GA, Watling KJ. Stimulation of angiogenesis by substance P and interleukin-1 in the rat and its inhibition by NK1 or interleukin-1 receptor antagonists. Br J Pharmacol 1993: 110: 43-49.
22. Humphrey J, Chan O, Crisp T, Padhiar N, Morrissey D, Twycross-Lewis R, King J, Maffulli N. The short-term effects of high volume image guided injections in resistant non-insertional Achilles tendinopathy. J Sci Med Sport 2010: 13: 295-298.
23. Khan KM, Cook JL, Bonar F, Harcourt P, Astrom M. Histopathology of common tendinopathies. Update and implications for clinical management. Sports Med 1999: 27: 393-408.
24. Kim HJ, Na HS, Sung B, Nam HJ, Chung YJ, Hong SK. Is sympathetic sprouting in the dorsal root ganglia responsible for the production of neuropathic pain in a rat model? Neurosci Lett 1999: 269: 103-106.
25. Kim LR, Whelpdale K, Zurowski M, Pomeranz B. Sympathetic denervation impairs epidermal healing in cutaneous wounds. Wound Repair Regen 1998: 6: 194-201.
26. Kim MO, Na SI, Lee MY, Heo JS, Han HJ. Epinephrine increases DNA synthesis via ERK1/2s through cAMP, Ca(2+)/PKC, and PI3K/Akt signaling pathways in mouse embryonic stem cells. J Cell Biochem 2008: 104: 1407-1420.
27. Koon HW, Zhao D, Na X, Moyer MP, Pothoulakis C. Metalloproteinases and transforming growth factor-alpha mediate substance P-induced mitogen-activated protein kinase activation and proliferation in human colonocytes. J Biol Chem 2004: 279: 45519-45527.
28. Lind B, Ohberg L, Alfredson H. Sclerosing polidocanol injections in mid-portion Achilles tendinosis: remaining good clinical results and decreased tendon thickness at 2-year follow-up. Knee Surg Sports Traumatol Arthrosc 2006: 14: 1327-1332.
29. New DC, Wong YH. Molecular mechanisms mediating the G protein-coupled receptor regulation of cell cycle progression. J Mol Signal 2007: 2: 2.
30. Oben JA, Diehl AM. Sympathetic nervous system regulation of liver repair. Anat Rec A Discov Mol Cell Evol Biol 2004: 280: 874-883.
31. Oben JA, Yang S, Lin H, Ono M, Diehl AM. Norepinephrine and neuropeptide Y promote proliferation and collagen gene expression of hepatic myofibroblastic stellate cells. Biochem Biophys Res Commun 2003: 302: 685-690.
32. Ohberg L, Lorentzon R, Alfredson H. Neovascularisation in Achilles tendons with painful tendinosis but not in normal tendons: an ultrasonographic investigation. Knee Surg Sports Traumatol Arthrosc 2001: 9: 233-238.
33. Panoskaltsis-Mortari A, Bucy RP. In situ hybridization with digoxigenin-labeled RNA probes: facts and artifacts. Biotechniques 1995: 18: 300-307.
34. Schaak S, Cussac D, Cayla C, Devedjian JC, Guyot R, Paris H, Denis C. Alpha(2) adrenoceptors regulate proliferation of human intestinal epithelial cells. Gut 2000: 47: 242-250.
35. Schubert TE, Weidler C, Lerch K, Hofstadter F, Straub RH. Achilles tendinosis is associated with sprouting of substance P positive nerve fibres. Ann Rheum Dis 2005: 64: 1083-1086.
36. Seuwen K, Magnaldo I, Kobilka BK, Caron MG, Regan JW, Lefkowitz RJ, Pouyssegur J. Alpha 2-adrenergic agonists stimulate DNA synthesis in Chinese hamster lung fibroblasts transfected with a human alpha 2-adrenergic receptor gene. Cell Regul 1990: 1: 445-451.
37. Souza BR, Cardoso JF, Amadeu TP, Desmouliere A, Costa AM. Sympathetic denervation accelerates wound contraction but delays reepithelialization in rats. Wound Repair Regen 2005: 13: 498-505.
38. Vazquez SM, Mladovan AG, Perez C, Bruzzone A, Baldi A, Luthy IA. Human breast cell lines exhibit functional alpha2-adrenoceptors. Cancer Chemother Pharmacol 2006: 58: 50-61.
39. Wall ME, Faber JE, Yang X, Tsuzaki M, Banes AJ. Norepinephrine-induced calcium signaling and expression of adrenoceptors in avian tendon cells. Am J Physiol Cell Physiol 2004: 287: C912-C918.
40. Watanabe K, Zhang XY, Kitagawa K, Yunoki T, Hayashi A. The effect of clonidine on VEGF expression in human retinal pigment epithelial cells (ARPE-19). Graefes Arch Clin Exp Ophthalmol 2009: 247: 207-213.
41. Yamaguchi K, Richardson MD, Bigner DD, Kwatra MM. Signal transduction through substance P receptor in human glioblastoma cells: roles for Src and PKCdelta. Cancer Chemother Pharmacol 2005: 56: 585-593.
42. Zeisig E, Fahlstrom M, Ohberg L, Alfredson H. Pain relief after intratendinous injections in patients with tennis elbow: results of a randomised study. Br J Sports Med 2008: 42: 267-271.