Chondrocyte-intrinsic Smad3 represses Runx2-inducible matrix metalloproteinase 13 expression to maintain articular cartilage and prevent osteoarthritis

Arthritis and Rheumatism

Volumn 64, Issue 10, 2012, Pages 3278-3289

  Chen, Carol G ^a   Thuillier, Daniel ^a   Chin, Emily N ^a   Alliston, Tamara ^a  

^a UNIVERSITY OF CALIFORNIA   (United States)

Author keywords

[No Author keywords available]

Indexed keywords

COLLAGEN TYPE 2; COLLAGENASE 3; MESSENGER RNA; SMAD3 PROTEIN; SYNAPTOPHYSIN; TRANSCRIPTION FACTOR RUNX2; TRANSFORMING GROWTH FACTOR BETA;

ANIMAL CELL; ANIMAL EXPERIMENT; ANIMAL MODEL; ANIMAL TISSUE; ARTICLE; CARTILAGE CELL; CARTILAGE DEGENERATION; CONTROLLED STUDY; GENE EXPRESSION; HISTOPATHOLOGY; IN VITRO STUDY; IN VIVO STUDY; MOUSE; NONHUMAN; OSTEOARTHRITIS; PERICHONDRIUM; PRIORITY JOURNAL; PROTEIN EXPRESSION; PROTEIN FUNCTION; PROTEIN SYNTHESIS REGULATION; SIGNAL TRANSDUCTION;

ANIMALS; CARTILAGE, ARTICULAR; CHONDROCYTES; CORE BINDING FACTOR ALPHA 1 SUBUNIT; MATRIX METALLOPROTEINASE 13; MICE; OSTEOARTHRITIS; SMAD3 PROTEIN;

EID: 84869050198     PISSN: 00043591     EISSN: 15290131     Source Type: Journal    
DOI: 10.1002/art.34566     Document Type: Article

References (50)

1. Goldring MB, Marcu KB. Cartilage homeostasis in health and rheumatic diseases. Arthritis Res Ther 2009;11:224.
2. Aigner T, Vornehm SI, Zeiler G, Dudhia J, von der Mark K, Bayliss MT. Suppression of cartilage matrix gene expression in upper zone chondrocytes of osteoarthritic cartilage. Arthritis Rheum 1997; 40: 562-9. (Pubitemid 27123673)
3. Shlopov BV, Lie WR, Mainardi CL, Cole AA, Chubinskaya S, Hasty KA. Osteoarthritic lesions: involvement of three different collagenases. Arthritis Rheum 1997; 40: 2065-74. (Pubitemid 27494668)
4. Mitchell PG, Magna HA, Reeves LM, Lopresti-Morrow LL, Yocum SA, Rosner PJ, et al. Cloning, expression, and type II collagenolytic activity of matrix metalloproteinase-13 from human osteoarthritic cartilage. J Clin Invest 1996; 97: 761-8. (Pubitemid 26060542)
5. Blaney Davidson EN, Van Der Kraan PM, Van Den Berg WB. TGF-and osteoarthritis. Osteoarthritis Cartilage 2007; 15: 597-604.
6. Yang X, Chen L, Xu X, Li C, Huang C, Deng CX. TGF-/Smad3 signals repress chondrocyte hypertrophic differentiation and are required for maintaining articular cartilage. J Cell Biol 2001;153: 35-46.
7. Wu Q, Kim KO, Sampson ER, Chen D, Awad H, O'Brien T, et al. Induction of an osteoarthritis-like phenotype and degradation of phosphorylated Smad3 by Smurf2 in transgenic mice. Arthritis Rheum 2008; 58: 3132-44.
8. Valdes AM, Spector TD, Tamm A, Kisand K, Doherty SA, Dennison EM, et al. Genetic variation in the SMAD3 gene is associated with hip and knee osteoarthritis. Arthritis Rheum 2010; 62: 2347-52.
9. Alvarez J, Sohn P, Zeng X, Doetschman T, Robbins DJ, Serra R. TGF-2 mediates the effects of hedgehog on hypertrophic differentiation and PTHrP expression. Development 2002; 129: 1913-24.
10. Serra R, Karaplis A, Sohn P. Parathyroid hormone-related peptide (PTHrP)-dependent and -independent effects of transforming growth factor - (TGF-) on endochondral bone formation. J Cell Biol 1999; 145: 783-94. (Pubitemid 29240855)
11. Alvarez J, Serra R. Unique and redundant roles of Smad3 in TGF-mediated regulation of long bone development in organ culture. Dev Dyn 2004; 230: 685-99.
12. Ashcroft GS, Yang X, Glick AB, Weinstein M, Letterio JL, Mizel DE, et al. Mice lacking Smad3 show accelerated wound healing and an impaired local inflammatory response. Nat Cell Biol 1999; 1: 260-6. (Pubitemid 129495775)
13. Zhu Y, Richardson JA, Parada LF, Graff JM. Smad3 mutant mice develop metastatic colorectal cancer. Cell 1998; 94: 703-14. (Pubitemid 28436003)
14. Tomic D, Miller KP, Kenny HA, Woodruff TK, Hoyer P, Flaws JA. Ovarian follicle development requires Smad3. Mol Endocrinol 2004; 18: 2224-40. (Pubitemid 39215252)
15. Balooch G, Balooch M, Nalla RK, Schilling S, Filvaroff EH, Marshall GW, et al. TGF-regulates the mechanical properties and composition of bone matrix. Proc Natl Acad Sci U S A 2005; 102: 18813-8. (Pubitemid 43049527)
16. Ferguson CM, Schwarz EM, Reynolds PR, Puzas JE, Rosier RN, O'Keefe RJ. Smad2 and 3 mediate transforming growth factor-1- induced inhibition of chondrocyte maturation. Endocrinology 2000; 141: 4728-35.
17. Selvamurugan N, Kwok S, Partridge NC. Smad3 interacts with JunB and Cbfa1/Runx2 for transforming growth factor-1-stimulated collagenase-3 expression in human breast cancer cells. J Biol Chem 2004; 279: 27764-73.
18. Selvamurugan N, Kwok S, Alliston T, Reiss M, Partridge NC. Transforming growth factor-1 regulation of collagenase-3 expression in osteoblastic cells by cross-talk between the Smad and MAPK signaling pathways and their components, Smad2 and Runx2. J Biol Chem 2004; 279: 19327-34.
19. Rydziel S, Varghese S, Canalis E. Transforming growth factor -1 inhibits collagenase 3 expression by transcriptional and posttranscriptional mechanisms in osteoblast cultures. J Cell Physiol 1997; 170: 145-52. (Pubitemid 27076215)
20. Alliston T, Choy L, Ducy P, Karsenty G, Derynck R. TGF- induced repression of CBFA1 by Smad3 decreases cbfa1 and osteocalcin expression and inhibits osteoblast differentiation. EMBO J 2001; 20: 2254-72.
21. Ovchinnikov DA, Deng JM, Ogunrinu G, Behringer RR. Col2a1- directed expression of Cre recombinase in differentiating chondrocytes in transgenic mice. Genesis 2000; 26: 145-6. (Pubitemid 30158102)
22. Li Q, Pangas SA, Jorgez CJ, Graff JM, Weinstein M, Matzuk MM. Redundant roles of SMAD2 and SMAD3 in ovarian granulosa cells in vivo. Mol Cell Biol 2008; 28: 7001-11.
23. Xu L, Flahiff CM, Waldman BA, Wu D, Olsen BR, Setton LA, et al. Osteoarthritis-like changes and decreased mechanical function of articular cartilage in the joints of mice with the chondrodysplasia gene (cho). Arthritis Rheum 2003; 48: 2509-18. (Pubitemid 37129428)
24. Shibata S, Fukada K, Suzuki S, Ogawa T, Yamashita Y. Histochemical localisation of versican, aggrecan and hyaluronan in the developing condylar cartilage of the fetal rat mandible. J Anat 2001; 198: 129-35. (Pubitemid 32177976)
25. Singer II, Kawka DW, Bayne EK, Donatelli SA, Weidner JR, Williams HR, et al. VDIPEN, a metalloproteinase-generated neoepitope, is induced and immunolocalized in articular cartilage during inflammatory arthritis. J Clin Invest 1995; 95: 2178-86.
26. Billinghurst RC, Dahlberg L, Ionescu M, Reiner A, Bourne R, Rorabeck C, et al. Enhanced cleavage of type II collagen by collagenases in osteoarthritic articular cartilage. J Clin Invest 1997; 99: 1534-45. (Pubitemid 27163804)
27. Thirion S, Berenbaum F. Culture and phenotyping of chondrocytes in primary culture. Methods Mol Med 2004; 100: 1-14.
28. Suter SE, Gouthro TA, McSweeney PA, Nash RA, Haskins ME, Felsburg PJ, et al. Optimized transduction of canine paediatric CD34-cells using an MSCV-based bicistronic vector. Vet Res Commun 2006; 30: 881-901. (Pubitemid 46195455)
29. Ducy P, Karsenty G. Two distinct osteoblast-specific cis-acting elements control expression of a mouse osteocalcin gene. Mol Cell Biol 1995; 15: 1858-69.
30. Carcamo J, Zentella A, Massague J. Disruption of transforming growth factor - signaling by a mutation that prevents transphosphorylation within the receptor complex. Mol Cell Biol 1995;15: 1573-81.
31. Im HJ, Pacione C, Chubinskaya S, Van Wijnen AJ, Sun Y, Loeser RF. Inhibitory effects of insulin-like growth factor-1 and osteogenic protein-1 on fibronectin fragment- and interleukin-1-stimulated matrix metalloproteinase-13 expression in human chondrocytes. J Biol Chem 2003; 278: 25386-94.
32. Feng XH, Filvaroff EH, Derynck R. Transforming growth factor-(TGF-)-induced down-regulation of cyclin A expression requires a functional TGF-receptor complex: characterization of chimeric and truncated type I and type II receptors. J Biol Chem 1995; 270: 24237-45.
33. Fosang AJ, Last K, Knauper V, Murphy G, Neame PJ. Degradation of cartilage aggrecan by collagenase-3 (MMP-13). FEBS Lett 1996; 380: 17-20. (Pubitemid 26058726)
34. Jimenez MJ, Balbin M, Lopez JM, Alvarez J, Komori T, Lopez- Otin C. Collagenase 3 is a target of Cbfa1, a transcription factor of the runt gene family involved in bone formation. Mol Cell Biol 1999; 19: 4431-42. (Pubitemid 29242017)
35. Van de Laar IM, Oldenburg RA, Pals G, Roos-Hesselink JW, de Graaf BM, Verhagen JM, et al. Mutations in SMAD3 cause a syndromic form of aortic aneurysms and dissections with earlyonset osteoarthritis. Nat Genet 2011; 43: 121-6.
36. Tardif G, Pelletier JP, Dupuis M, Geng C, Cloutier JM, Martel- Pelletier J. Collagenase 3 production by human osteoarthritic chondrocytes in response to growth factors and cytokines is a function of the physiologic state of the cells. Arthritis Rheum 1999; 42: 1147-58. (Pubitemid 29268951)
37. Furumatsu T, Tsuda M, Taniguchi N, Tajima Y, Asahara H. Smad3 induces chondrogenesis through the activation of SOX9 via CREB-binding protein/p300 recruitment. J Biol Chem 2005;280: 8343-50. (Pubitemid 40349737)
38. Kang JS, Alliston T, Delston R, Derynck R. Repression of Runx2 function by TGF-through recruitment of class II histone deacetylases by Smad3. EMBO J 2005; 24: 2543-55. (Pubitemid 41076311)
39. Shimizu E, Selvamurugan N, Westendorf JJ, Olson EN, Partridge NC. HDAC4 represses matrix metalloproteinase-13 transcription in osteoblastic cells, and parathyroid hormone controls this repression. J Biol Chem 2010; 285: 9616-26.
40. Vega RB, Matsuda K, Oh J, Barbosa AC, Yang X, Meadows E, et al. Histone deacetylase 4 controls chondrocyte hypertrophy during skeletogenesis. Cell 2004; 119: 555-66. (Pubitemid 39482354)
41. Takeda S, Bonnamy JP, Owen MJ, Ducy P, Karsenty G. Continuous expression of Cbfa1 in nonhypertrophic chondrocytes uncovers its ability to induce hypertrophic chondrocyte differentiation and partially rescues Cbfa1-deficient mice. Genes Dev 2001;15: 467-81. (Pubitemid 32187007)
42. Li F, Lu Y, Ding M, Napierala D, Abbassi S, Chen Y, et al. Runx2 contributes to murine Col10a1 gene regulation through direct interaction with its cis-enhancer. J Bone Miner Res 2011;26: 2899-910.
43. Zheng Q, Zhou G, Morello R, Chen Y, Garcia-Rojas X, Lee B. Type X collagen gene regulation by Runx2 contributes directly to its hypertrophic chondrocyte-specific expression in vivo. J Cell Biol 2003; 162: 833-42. (Pubitemid 37087723)
44. Dong YF, Soung DY, Schwarz EM, O'Keefe RJ, Drissi H. Wnt induction of chondrocyte hypertrophy through the Runx2 transcription factor. J Cell Physiol 2006; 208: 77-86. (Pubitemid 43848991)
45. Li TF, Darowish M, Zuscik MJ, Chen D, Schwarz EM, Rosier RN, et al. Smad3-deficient chondrocytes have enhanced BMP signaling and accelerated differentiation. J Bone Miner Res 2006; 21: 4-16. (Pubitemid 43023222)
46. Blaney Davidson EN, Remst DF, Vitters EL, van Beuningen HM, Blom AB, Goumans MJ, et al. Increase in ALK1/ALK5 ratio as a cause for elevated MMP-13 expression in osteoarthritis in humans and mice. J Immunol 2009; 182: 7937-45.
47. Finnson KW, Parker WL, Chi Y, Hoemann CD, Goldring MB, Antoniou J, et al. Endoglin differentially regulates TGF-induced Smad2/3 and Smad1/5 signalling and its expression correlates with extracellular matrix production and cellular differentiation state in human chondrocytes. Osteoarthritis Cartilage 2010; 18: 1518-27.
48. Ijiri K, Zerbini LF, Peng H, Correa RG, Lu B, Walsh N, et al. A novel role for GADD45-as a mediator of MMP-13 gene expression during chondrocyte terminal differentiation. J Biol Chem 2005; 280: 38544-55. (Pubitemid 43853754)
49. Correa D, Hesse E, Seriwatanachai D, Kiviranta R, Saito H, Yamana K, et al. Zfp521 is a target gene and key effector of parathyroid hormone-related peptide signaling in growth plate chondrocytes. Dev Cell 2010; 19: 533-46.
50. Chang JL, Brauer DS, Johnson J, Chen CG, Akil O, Balooch G, et al. Tissue-specific calibration of extracellular matrix material properties by transforming growth factor-and Runx2 in bone is required for hearing. EMBO Rep 2010; 11: 765-71.