VEGF, VEGFR-1, and CTGF cell densities in tendon are increased with cyclical loading: An in vivo tendinopathy model

Journal of Orthopaedic Research

Volumn 24, Issue 3, 2006, Pages 393-400

  Nakama, Leena H ^a   King, Karen B ^a,b   Abrahamsson, Sven ^c   Rempel, David M ^a,b  

^a UNIVERSITY OF CALIFORNIA   (United States)

^b UNIVERSITY OF CALIFORNIA   (United States)

^c LUND UNIVERSITY HOSPITAL   (Sweden)

Author keywords

CTGF; In vivo loaded tendon; VEGF

Indexed keywords

CONNECTIVE TISSUE GROWTH FACTOR; VASCULOTROPIN; VASCULOTROPIN RECEPTOR 1; IMMEDIATE EARLY PROTEIN; SIGNAL PEPTIDE; VASCULOTROPIN A;

ANIMAL EXPERIMENT; ANIMAL MODEL; ANIMAL TISSUE; ARTICLE; CELL DENSITY; CONTROLLED STUDY; DISEASE COURSE; DISEASE MODEL; ELECTROSTIMULATION; FEMALE; HISTOPATHOLOGY; IMMUNOHISTOCHEMISTRY; IN VIVO STUDY; LOADING TEST; MUSCLE CONTRACTION; NONHUMAN; PATHOGENESIS; PRIORITY JOURNAL; PROTEIN FUNCTION; RABBIT; TENDON DISEASE; ANIMAL; CELL COUNT; ENZYME IMMUNOASSAY; MECHANICAL STRESS; MECHANOTRANSDUCTION; METABOLISM; PATHOLOGY; TENDINITIS; TENDON; TENDON INJURY; WEIGHT BEARING;

ANIMALS; CELL COUNT; DISEASE MODELS, ANIMAL; FEMALE; IMMEDIATE-EARLY PROTEINS; IMMUNOENZYME TECHNIQUES; INTERCELLULAR SIGNALING PEPTIDES AND PROTEINS; MECHANOTRANSDUCTION, CELLULAR; RABBITS; STRESS, MECHANICAL; TENDINOPATHY; TENDON INJURIES; TENDONS; VASCULAR ENDOTHELIAL GROWTH FACTOR A; VASCULAR ENDOTHELIAL GROWTH FACTOR RECEPTOR-1; WEIGHT-BEARING;

EID: 33645733750     PISSN: 07360266     EISSN: None     Source Type: Journal    
DOI: 10.1002/jor.20053     Document Type: Article

References (55)

1. Jozsa L, Kannus P. 1997. Histopathological findings in spontaneous tendon ruptures. Scand J Med Sci Sports 7:113-118.
2. Kannus P. 1997. Tendons - a source of major concern in competitive and recreational athletes. Scand J Med Sci Sports 7:53-54.
3. United States Bureau of Labor Statistics. 1995. Occupational injuries and illnesses - counts, rates, and characteristics. Washington, DC: The Bureau: For sale by the U.S. G.P.O. Supt. of Docs, p v.
4. Allander E. 1974. Prevalence, incidence, and remission rates of some common rheumatic diseases or syndromes. Scand J Rheumatol 3:145-153.
5. Chard MD, Hazleman BL. 1989. Tennis elbow - a reappraisal. Br J Rheumatol 28:186-190.
6. Wetzel BJ, Nindl G, Swez JA, et al. 2002. Quantitative characterization of rat tendinitis to evaluate the efficacy of therapeutic interventions. Biomed Sci Instrum 38:157-162.
7. Chard MD, Cawston TE, Riley GP, et al. 1994. Rotator cuff degeneration and lateral epicondylitis: a comparative histological study. Ann Rheum Dis 53:30-34.
8. Kraushaar BS, Nirschl RP. 1999. Tendinosis of the elbow (tennis elbow). Clinical features and findings of histological, immunohistochemical, and electron microscopy studies. J Bone Joint Surg Am 81:259-278.
9. Pfahler M, Jessel C, Steinborn M, et al. 1998. Magnetic resonance imaging in lateral epicondylitis of the elbow. Arch Orthop Trauma Surg 118: 121-125.
10. Potter HG, Hannafin JA, Morwessel RM, et al. 1995. Lateral epicondylitis: correlation of MR imaging, surgical, and histopathologic findings. Radiology 196:43-46.
11. Regan W, Wold LE, Coonrad R, et al. 1992. Microscopic histopathology of chronic refractory lateral epicondylitis. Am J Sports Med 20:746-749.
12. Steinborn M, Heuck A, Jessel C, et al. 1999. Magnetic resonance imaging of lateral epicondylitis of the elbow with a 0.2-T dedicated system. Eur Radiol 9:1376-1380.
13. Maffulli N, Khan KM, Puddu G. 1998. Overuse tendon conditions: time to change a confusing terminology. Arthroscopy 14:840-843.
14. Soslowsky LJ, Thomopoulos S, Esmail A, et al. 2002. Rotator cuff tendinosis in an animal model: role of extrinsic and overuse factors. Ann Biomed Eng 30:1057-1063.
15. Alfredson H, Lorentzon M, Backman S, et al. 2003. cDNA-arrays and real-time quantitative PCR techniques in the investigation of chronic Achilles tendinosis. J Orthop Res 21:970-975.
16. Petersen W, Pufe T, Zantop T, et al. 2004. Expression of VEGFR-1 and VIEGFR-2 in degenerative Achilles tendons. Clin Orthop 420:286-291.
17. Pufe T, Petersen W, Tillmann B, et al. 2001. The angiogenic peptide vascular endothelial growth factor is expressed in foetal and ruptured tendons. Virchows Arch 439:579-585.
18. Petersen W, Varoga D, Zantop T, et al. 2004. Cyclic strain influences the expression of the vascular endothelial growth factor (VEGF) and the hypoxia inducible factor 1 alpha (HIF-1alpha) in tendon fibroblasts. J Orthop Res 22:847-853.
19. Dvorak HF, Brown LF, Detmar M, et al. 1995. Vascular permeability factor/ vascular endothelial growth factor, microvascular hyperpermeability, and angiogenesis. Am J Pathol 146:1029-1039.
20. Shalaby F, Rossant J, Yamaguchi TP, et al. 1995. Failure of blood-island formation and vasculogenesis in Flk-1-deficient mice. Nature 376:62-66.
21. Petersen W, Pufe T, Zantop T, et al. 2003. Hypoxia and PDGF have a synergistic effect that increases the expression of the angiogenetic peptide vascular endothelial growth factor in Achilles tendon fibroblasts. Arch Orthop Trauma Surg 123:485-488.
22. Brigstock DR. 2002. Regulation of angiogenesis and endothelial cell function by connective tissue growth factor (CTGF) and cysteine-rich 61 (CYR61). Angiogenesis 5:153-165.
23. Deroanne CF, Hajitou A, Calberg-Bacq CM, et al. 1997. Angiogenesis by fibroblast growth factor 4 is mediated through an autocrine up-regulation of vascular endothelial growth factor expression. Cancer Res 57:5590-5997.
24. Boyer MI, Watson JT, Lou J, et al. 2001. Quantitative variation in vascular endothelial growth factor mRNA expression during early flexor tendon healing: an investigation in a canine model. J Orthop Res 19:869-872.
25. de Vries C, Escobedo JA, Ueno H, et al. 1992. The fms-like tyrosine kinase, a receptor for vascular endothelial growth factor. Science 255:989-991.
26. Terman BI, Dougher-Vermazen M, Carrion ME, et al. 1992. Identification of the KDR tyrosine kinase as a receptor for vascular endothelial cell growth factor. Biochem Biophys Res Commun 187:1579-1586.
27. Gerber HP, Condorelli F, Park J, et al. 1997. Differential transcriptional regulation of the two vascular endothelial growth factor receptor genes. Flt-1, but not Flk-1/KDR, is up-regulated by hypoxia. J Biol Chem 272:23659-23667.
28. Barr AE, Barbe MF. 2004. Inflammation reduces physiological tissue tolerance in the development of work-related musculoskeletal disorders. J Electromyogr Kinesiol 14:77-85.
29. Bradham DM, Igarashi A, Potter RL, et al. 1991. Connective tissue growth factor: a cysteine-rich mitogen secreted by human vascular endothelial cells is related to the SRC-induced immediate early gene product CEF-10. J Cell Biol 114:1285-1294.
30. Frazier K, Williams S, Kothapalli D, et al. 1996. Stimulation of fibroblast cell growth, matrix production, and granulation tissue formation by connective tissue growth factor. J Invest Dermatol 107: 404-411.
31. Yang GP, Lau LF. 1991. Cyr61, product of a growth factor-inducible immediate early gene, is associated with the extracellular matrix and the cell surface. Cell Growth Differ 2:351-357.
32. Nishida T, Nakanishi T, Asano M, et al. 2000. Effects of CTGF/Hcs24, a hypertrophic chondrocyte-specific gene product, on the proliferation and differentiation of osteoblastic cells in vitro. J Cell Physiol 184:197-206.
33. Blalock TD, Yuan R, Lewin AS, et al. 2004. Hammerhead ribozyme targeting connective tissue growth factor mRNA blocks transforming growth factor-beta mediated cell proliferation. Exp Eye Res 78:1127-1136.
34. Leask A, Abraham DJ. 2003. The role of connective tissue growth factor, a multifunctional matricellular protein, in fibroblast biology. Biochem Cell Biol 81:355-363.
35. Leask A, Abraham DJ. 2004. TGF-beta signaling and the fibrotic response. FASEB J 18:816-827.
36. Babic AM, Chen CC, Lau LF. 1999. Fisp12/mouse connective tissue growth factor mediates endothelial cell adhesion and migration through integrin alphavbeta3, promotes endothelial cell survival, and induces angiogenesis in vivo. Mol Cell Biol 19:2958-2966.
37. Lau LF, Lam SC. 1999. The CCN family of angiogenic regulators: the integrin connection. Exp Cell Res 248:44-57.
38. Schild C, Trueb B. 2002. Mechanical stress is required for high-level expression of connective tissue growth factor. Exp Cell Res 274:83-91.
39. Schild C, Trueb B. 2004. Three members of the connective tissue growth factor family CCN are differentially regulated by mechanical stress. Biochim Biophys Acta 1691:33-40.
40. Nakama L, King K, Abrahamsson S, et al. Evidence of tendon microtears due to cyclical loading in an in vivo tendinopathy model. J Orthop Res (in press).
41. Bidder M, Towler DA, Gelberman RH, et al. 2000. Expression of mRNA for vascular endothelial growth factor at the repair site of healing canine flexor tendon. J Orthop Res 18:247-252.
42. Tsubone T, Moran SL, Amadio PC, et al. 2004. Expression of growth factors in canine flexor tendon after laceration in vivo. Ann Plast Surg 53:393-397.
43. Wakabayashi I, Itoi E, Sano H, et al. 2003. Mechanical environment of the supraspinatus tendon: a two-dimensional finite element model analysis. J Shoulder Elbow Surg 12:612-617.
44. Petersen W, Pufe T, Kurz B, et al. 2002. Angiogenesis in fetal tendon development: spatial and temporal expression of the angiogenic peptide vascular endothelial cell growth factor. Anat Embryol (Berl) 205:263-270.
45. Backman C, Boquist L, Friden J, et al. 1990. Chronic achilles paratenonitis with tendinosis: an experimental model in the rabbit. J Orthop Res 8: 541-547.
46. Archambault JM, Hart DA, Herzog W. 2001. Response of rabbit Achilles tendon to chronic repetitive loading. Connect Tissue Res 42:13-23.
47. Perry SM, McIlhenny SE, Hoffman MC, et al. 2005. Inflammatory and angiogenic mRNA levels are altered in a supraspinatus tendon overuse animal model. J Shoulder Elbow Surg 14:79S-83S.
48. Soslowsky LJ, Thomopoulos S, Tun S, et al. 2000. Neer Award 1999. Overuse activity injures the supraspinatus tendon in an animal model: a histologic and biomechanical study. J Shoulder Elbow Surg 9:79-84.
49. Barbe MF, Barr AE, Gorzelany I, et al. 2003. Chronic repetitive reaching and grasping results in decreased motor performance and widespread tissue responses in a rat model of MSD. J Orthop Res 21:167-176.
50. Unemori EN, Ferrara N, Bauer EA, et al. 1992. Vascular endothelial growth factor induces interstitial collagenase expression in human endothelial cells. J Cell Physiol 153:557-562.
51. Petersen W, Pufe T, Unterhauser F, et al. 2003. The splice variants 120 and 164 of the angiogenic peptide vascular endothelial cell growth factor (VEGF) are expressed during Achilles tendon healing. Arch Orthop Trauma Surg 123:475-480.
52. Messner K, Wei Y, Andersson B, et al. 1999. Rat model of Achilles tendon disorder. A pilot study. Cells Tissues Organs 165:30-39.
53. National Research Council (U.S.). 2001. Panel on Musculoskeletal Disorders and the Workplace, Institute of Medicine (U.S.): Musculoskeletal disorders and the workplace: low back and upper extremities. Washington, DC: National Academy Press, p xv, 492.
54. Kjaer M. 2004. Role of extracellular matrix in adaptation of tendon and skeletal muscle to mechanical loading. Physiol Rev 84:649-698.
55. See EK, Ng GY, Ng CO, et al. 2004. Running exercises improve the strength of a partially ruptured Achilles tendon. Br J Sports Med 38:597-600.