Involvement of matrix metalloproteinases in the growth plate response to physiological mechanical load

Journal of Applied Physiology

Volumn 108, Issue 1, 2010, Pages 172-180

  Reich, Adi ^a   Maziel, Stav Simsa ^a   Ashkenazi, Ziv ^a   Ornan, Efrat Monsonego ^a  

^a HEBREW UNIVERSITY OF JERUSALEM   (Israel)

Author keywords

Chondrocyte; Connective tissue growth factor; Extracellular matrix; Matrix metalloproteinase

Indexed keywords

COLLAGENASE 3; CONNECTIVE TISSUE GROWTH FACTOR; GELATINASE A; GELATINASE B; MATRIX METALLOPROTEINASE 16; STROMELYSIN;

ANIMAL CELL; ANIMAL EXPERIMENT; ANIMAL TISSUE; ARTICLE; BIOMECHANICS; CARTILAGE INJURY; CONTROLLED STUDY; DISEASE ASSOCIATION; DOWN REGULATION; GROWTH PLATE; IN VITRO STUDY; LOAD CARRYING CAPACITY; MALE; MECHANICAL STRESS; NONHUMAN; NUCLEOTIDE SEQUENCE; PRIORITY JOURNAL; PROTEIN EXPRESSION; STRETCHING; UPREGULATION;

ANIMALS; ANIMALS, NEWBORN; COMPRESSIVE STRENGTH; GROWTH PLATE; MALE; MATRIX METALLOPROTEINASES; MECHANOTRANSDUCTION, CELLULAR; TIBIA; WEIGHT-BEARING;

EID: 74049099566     PISSN: 87507587     EISSN: 15221601     Source Type: Journal    
DOI: 10.1152/japplphysiol.00821.2009     Document Type: Article

References (62)

1. Armstrong AL, Barrach HJ, Ehrlich MG. Identification of the metalloproteinase stromelysin in the physis. J Orthop Res 20: 289-294, 2002.
2. Asanuma K, Magid R, Johnson C, Nerem RM, Galis ZS. Uniaxial strain upregulates matrix-degrading enzymes produced by human vascular smooth muscle cells. Am J Physiol Heart Circ Physiol 284: H1778-H1784, 2003.
3. Asundi KR, Rempel DM. Cyclic loading inhibits expression of MMP-3 but not MMP-1 in an in vitro rabbit flexor tendon model. Clin Biomech (Bristol, Avon) 23: 117-121, 2008.
4. Bittner K, Vischer P, Bartholmes P, Bruckner P. Role of the subchondral vascular system in endochondral ossification: endothelial cells specifically derepress late differentiation in resting chondrocytes in vitro. Exp Cell Res 238: 491-497, 1998.
5. Boersma B, Wit JM. Catch-up growth. Endocr Rev 18: 646-661, 1997.
6. Cancel M, Grimard G, Thuillard-Crisinel D, Moldovan F, Villemure I. Effects of in vivo static compressive loading on aggrecan and type II and X collagens in the rat growth plate extracellular matrix. Bone 44: 306-315, 2009.
7. Chakraborti S, Mandal M, Das S, Mandal A, Chakraborti T. Regulation of matrix metalloproteinases: an overview. Mol Cell Biochem 253: 269-285, 2003.
8. de Hooge AS, van de Loo FA, Bennink MB, Arntz OJ, Fiselier TJ, Franssen MJ, Joosten LA, Van Lent PL, Richards CD, van den Berg WB. Growth plate damage, a feature of juvenile idiopathic arthritis, can be induced by adenoviral gene transfer of oncostatin M: a comparative study in gene-deficient mice. Arthritis Rheum 48: 1750-1761, 2003.
9. DeLise AM, Fischer L, Tuan RS. Cellular interactions and signaling in cartilage development. Osteoarthritis Cartilage 8: 309-334, 2000.
10. Egeblad M, Werb Z. New functions for the matrix metalloproteinases in cancer progression. Nat Rev Cancer 2: 161-174, 2002.
11. Eguchi T, Kubota S, Kawata K, Mukudai Y, Uehara J, Ohgawara T, Ibaragi S, Sasaki A, Kuboki T, Takigawa M. Novel transcription-factorlike function of human matrix metalloproteinase 3 regulating the CTGF/ CCN2 gene. Mol Cell Biol 28: 2391-2413, 2008.
12. Engsig MT, Chen QJ, Vu TH, Pedersen AC, Therkidsen B, Lund LR, Henriksen K, Lenhard T, Foged NT, Werb Z, Delaisse JM. Matrix metalloproteinase 9 and vascular endothelial growth factor are essential for osteoclast recruitment into developing long bones. J Cell Biol 151: 879-889, 2000.
13. Even-Zohar N, Jacob J, Amariglio N, Rechavi G, Potievsky O, Phillip M, Gat-Yablonski G. Nutrition-induced catch-up growth increases hypoxia inducible factor 1alpha RNA levels in the growth plate. Bone 42: 505-515, 2008.
14. Farnum CE, Lee AO, O'Hara K, Wilsman NJ. Effect of short-term fasting on bone elongation rates: an analysis of catch-up growth in young male rats. Pediatr Res 53: 33-41, 2003.
15. Gelber AC, Hochberg MC, Mead LA, Wang NY, Wigley FM, Klag MJ. Joint injury in young adults and risk for subsequent knee and hip osteoarthritis. Ann Intern Med 133: 321-328, 2000.
16. Gerber HP, Ferrara N. Angiogenesis and bone growth. Trends Cardiovasc Med 10: 223-228, 2000.
17. Gruber G, Greiner RH, Hlushchuk R, Aebersold DM, Altermatt HJ, Berclaz G, Djonov V. Hypoxia-inducible factor 1 alpha in high-risk breast cancer: an independent prognostic parameter? Breast Cancer Res 6: R191-R198, 2004.
18. Guilak F, Fermor B, Keefe FJ, Kraus VB, Olson SA, Pisetsky DS, Setton LA, Weinberg JB. The role of biomechanics and inflammation in cartilage injury and repair. Clin Orthop Relat Res 17-26, 2004.
19. Haeusler G, Walter I, Helmreich M, Egerbacher M. Localization of matrix metalloproteinases (MMPs), their tissue inhibitors, and vascular endothelial growth factor (VEGF) in growth plates of children and adolescents indicates a role for MMPs in human postnatal growth and skeletal maturation. Calcif Tissue Int 76: 326-335, 2005.
20. Hashimoto G, Inoki I, Fujii Y, Aoki T, Ikeda E, Okada Y. Matrix metalloproteinases cleave connective tissue growth factor and reactivate angiogenic activity of vascular endothelial growth factor 165. J Biol Chem 277: 36288-36295, 2002.
21. Inada M, Wang Y, Byrne MH, Rahman MU, Miyaura C, Lopez-Otin C, Krane SM. Critical roles for collagenase-3 (Mmp13) in development of growth plate cartilage and in endochondral ossification. Proc Natl Acad Sci USA 101: 17192-17197, 2004.
22. Inoue K, Masuko-Hongo K, Okamoto M, Nishioka K. Induction of vascular endothelial growth factor and matrix metalloproteinase-3 (stromelysin) by interleukin-1 in human articular chondrocytes and synoviocytes. Rheumatol Int 26: 93-98, 2005.
23. Irie K, Uchiyama E, Iwaso H. Intraarticular inflammatory cytokines in acute anterior cruciate ligament injured knee. Knee 10: 93-96, 2003.
24. Jeffrey JE, Thomson LA, Aspden RM. Matrix loss and synthesis following a single impact load on articular cartilage in vitro. Biochim Biophys Acta 1334: 223-232, 1997.
25. Jung JC, Wang PX, Zhang G, Ezura Y, Fini ME, Birk DE. Collagen fibril growth during chicken tendon development: matrix metalloproteinase-2 and its activation. Cell Tissue Res 336: 79-89, 2009.
26. Kubota S, Takigawa M. Role of CCN2/CTGF/Hcs24 in bone growth. Int Rev Cytol 257: 1-41, 2007.
27. Kume K, Satomura K, Nishisho S, Kitaoka E, Yamanouchi K, Tobiume S, Nagayama M. Potential role of leptin in endochondral ossification. J Histochem Cytochem 50: 159-169, 2002.
28. Lin PM, Chen CT, Torzilli PA. Increased stromelysin-1 (MMP-3), proteoglycan degradation (3B3- and 7D4) and collagen damage in cyclically load-injured articular cartilage. Osteoarthritis Cartilage 12: 485-496, 2004.
29. Maeda A, Nishida T, Aoyama E, Kubota S, Lyons KM, Kuboki T, Takigawa M. CCN family 2/connective tissue growth factor modulates BMP signalling as a signal conductor, which action regulates the proliferation and differentiation of chondrocytes. J Biochem 145: 207-216, 2009.
30. Malemud CJ. Matrix metalloproteinases: role in skeletal development and growth plate disorders. Front Biosci 11: 1702-1715, 2006.
31. Mao JJ, Nah HD. Growth and development: hereditary and mechanical modulations. Am J Orthod Dentofacial Orthop 125: 676-689, 2004.
32. Massova I, Kotra LP, Fridman R, Mobashery S. Matrix metalloproteinases: structures, evolution, diversification. FASEB J 12: 1075-1095, 1998.
33. Molinos I, Santos F, Carbajo-Perez E, Garcia E, Rodriguez J, Garcia-Alvarez O, Gil H, Ordonez FA, Loredo V, Mallada L. Catch-up growth follows an abnormal pattern in experimental renal insufficiency and growth hormone treatment normalizes it. Kidney Int 70: 1955-1961, 2006.
34. Monfort J, Garcia-Giralt N, Lopez-Armada MJ, Monllau JC, Bonilla A, Benito P, Blanco FJ. Decreased metalloproteinase production as a response to mechanical pressure in human cartilage: a mechanism for homeostatic regulation. Arthriris Res Ther 8: R149, 2006.
35. Monsonego E, Halevy O, Gertler A, Volokita M, Schickler M, Hurwitz S, Pines M. Growth hormone receptors in avian epiphyseal growthplate chondrocytes. Gen Comp Endocrinol 92: 179-188, 1993.
36. Mullender M, El Haj AJ, Yang Y, van Duin MA, Burger EH, Klein-Nulend J. Mechanotransduction of bone cells in vitro: mechanobiology of bone tissue. Med Biol Eng Comput 42: 14-21, 2004.
37. Murphy G, Knauper V, Cowell S, Hembry R, Stanton H, Butler G, Freije J, Pendas AM, Lopez-Otin C. Evaluation of some newer matrix metalloproteinases. Ann N Y Acad Sci 878: 25-39, 1999.
38. Nakata E, Nakanishi T, Kawai A, Asaumi K, Yamaai T, Asano M, Nishida T, Mitani S, Inoue H, Takigawa M. Expression of connective tissue growth factor/hypertrophic chondrocyte-specific gene product 24 (CTGF/Hcs24) during fracture healing. Bone 31: 441-447, 2002.
39. Nishida T, Kubota S, Fukunaga T, Kondo S, Yosimichi G, Nakanishi T, Takano-Yamamoto T, Takigawa M. CTGF/Hcs24, hypertrophic chondrocyte-specific gene product, interacts with perlecan in regulating the proliferation and differentiation of chondrocytes. J Cell Physiol 196: 265-275, 2003.
40. Nishida T, Kubota S, Kojima S, Kuboki T, Nakao K, Kushibiki T, Tabata Y, Takigawa M. Regeneration of defects in articular cartilage in rat knee joints by CCN2 (connective tissue growth factor). J Bone Miner Res 19: 1308-1319, 2004.
41. Nishida T, Maeda A, Kubota S, Takigawa M. Role of mechanical-stress inducible protein Hcs24/CTGF/CCN2 in cartilage growth and regeneration: mechanical stress induces expression of Hcs24/CTGF/CCN2 in a human chondrocytic cell line HCS-2/8, rabbit costal chondrocytes and meniscus tissue cells. Biorheology 45: 289-299, 2008.
42. Olsen BR, Reginato AM, Wang W. Bone development. Annu Rev Cell Dev Biol 16: 191-220, 2000.
43. Pepper MS. Role of the matrix metalloproteinase and plasminogen activator-plasmin systems in angiogenesis. Arterioscler Thromb Vasc Biol 21: 1104-1117, 2001.
44. Raif el M. Effect of cyclic tensile load on the regulation of the expression of matrix metalloproteases (MMPs -1, -3) and structural components in synovial cells. J Cell Mol Med 12: 2439-2448, 2008.
45. Reich A, Jaffe N, Tong A, Lavelin I, Genina O, Pines M, Sklan D, Nussinovitch A, Monsonego-Ornan E. Weight loading young chicks inhibits bone elongation and promotes growth plate ossification and vascularization. J Appl Physiol 98: 2381-2389, 2005.
46. Reich A, Sharir A, Zelzer E, Hacker L, Monsonego-Ornan E, Shahar R. The effect of weight loading and subsequent release from loading on the postnatal skeleton. Bone 43: 766-774, 2008.
47. Roth A, Mollenhauer J, Wagner A, Fuhrmann R, Straub A, Venbrocks RA, Petrow P, Brauer R, Schubert H, Ozegowski J, Peschel G, Muller PJ, Kinne RW. Intra-articular injections of high-molecular-weight hyaluronic acid have biphasic effects on joint inflammation and destruction in rat antigen-induced arthritis. Arthriris Res Ther 7: R677-R686, 2005.
48. Rundhaug JE. Matrix metalloproteinases and angiogenesis. J Cell Mol Med 9: 267-285, 2005.
49. Segev O, Samach A, Faerman A, Kalinski H, Beiman M, Gelfand A, Turam H, Boguslavsky S, Moshayov A, Gottlieb H, Kazanov E, Nevo Z, Robinson D, Skaliter R, Einat P, Binderman I, Feinstein E. CMF608-a novel mechanical strain-induced bone-specific protein expressed in early osteochondroprogenitor cells. Bone 34: 246-260, 2004.
50. Simsa S, Genina O, Ornan EM. Matrix metalloproteinase expression and localization in turkey (Meleagris gallopavo) during the endochondral ossification process. J Anim Sci 85: 1393-1401, 2007.
51. Sternlicht MD, Werb Z. How matrix metalloproteinases regulate cell behavior. Annu Rev Cell Dev Biol 17: 463-516, 2001.
52. Stickens D, Behonick DJ, Ortega N, Heyer B, Hartenstein B, Yu Y, Fosang AJ, Schorpp-Kistner M, Angel P, Werb Z. Altered endochondral bone development in matrix metalloproteinase 13-deficient mice. Development 131: 5883-5895, 2004.
53. Surazynski A, Donald SP, Cooper SK, Whiteside MA, Salnikow K, Liu Y, Phang JM. Extracellular matrix and HIF-1 signaling: the role of prolidase. Int J Cancer 122: 1435-1440, 2008.
54. Sylvestre MN, Balcerzak D, Feidt C, Baracos VE, Brun Bellut J. Elevated rate of collagen solubilization and postmortem degradation in muscles of lambs with high growth rates: possible relationship with activity of matrix metalloproteinases. J Anim Sci 80: 1871-1878, 2002.
55. Tchetverikov I, Lohmander LS, Verzijl N, Huizinga TW, TeKoppele JM, Hanemaaijer R, DeGroot J. MMP protein and activity levels in synovial fluid from patients with joint injury, inflammatory arthritis, and osteoarthritis. Ann Rheum Dis 64: 694-698, 2005.
56. Tong A, Reich A, Genin O, Pines M, Monsonego-Ornan E. Expression of chicken 75-kDa gelatinase B-like enzyme in perivascular chondrocytes suggests its role in vascularization of the growth plate. J Bone Miner Res 18: 1443-1452, 2003.
57. Tsumaki N, Yoshikawa H. The role of bone morphogenetic proteins in endochondral bone formation. Cytokine Growth Factor Rev 16: 279-285, 2005.
58. Visse R, Nagase H. Matrix metalloproteinases and tissue inhibitors of metalloproteinases: structure, function, and biochemistry. Circ Res 92: 827-839, 2003.
59. Vu TH. Don't mess with the matrix. Nat Genet 28: 202-203, 2001.
60. Vu TH, Shipley JM, Bergers G, Berger JE, Helms JA, Hanahan D, Shapiro SD, Senior RM, Werb Z. MMP-9/gelatinase B is a key regulator of growth plate angiogenesis and apoptosis of hypertrophic chondrocytes. Cell 93: 411-422, 1998.
61. Weizmann S, Tong A, Reich A, Genina O, Yayon A, Monsonego-Ornan E. FGF upregulates osteopontin in epiphyseal growth plate chondrocytes: implications for endochondral ossification. Matrix Biol 24: 520-529, 2005.
62. Zhou Z, Apte SS, Soininen R, Cao R, Baaklini GY, Rauser RW, Wang J, Cao Y, Tryggvason K. Impaired endochondral ossification and angiogenesis in mice deficient in membrane-type matrix metalloproteinase I. Proc Natl Acad Sci USA 97: 4052-4057, 2000.