TGF-β signaling and the development of osteoarthritis

Bone Research

Volumn 2, Issue , 2014, Pages

  Shen, Jie ^a   Li, Shan ^b   Chen, Di ^b  

^a UNIVERSITY OF ROCHESTER SCHOOL OF MEDICINE AND DENTISTRY   (United States)

^b RUSH UNIVERSITY MEDICAL CENTER   (United States)

Author keywords

[No Author keywords available]

Indexed keywords

EID: 84922199194     PISSN: 20954700     EISSN: 20956231     Source Type: Journal    
DOI: 10.1038/boneres.2014.2     Document Type: Review

References (82)

1. Wang M, Shen J, Jin H, Im HJ, Sandy J, Chen D. Recent progress in understanding molecular mechanisms of cartilage degeneration during osteoarthritis. Ann NY Acad Sci 2011; 1240: 61-69.
2. Felson DT. Clinical practice. Osteoarthritis of the knee. New Engl J Med 2006; 354: 841-848.
3. Bijlsma JW, Berenbaum F, Lafeber FP. Osteoarthritis: an update with relevance for clinical practice. Lancet 2011; 377: 2115-2126.
4. Anderson DD, Chubinskaya S, Guilak F et al. Post-traumatic osteoarthritis: improved understanding and opportunities for early intervention. J Orthop Res 2011; 29: 802-809.
5. van den Berg WB. Osteoarthritis year 2010 in review: pathomechanisms. Osteoarthr Cartilage 2011; 19: 338-341.
6. Yamada Y, Okuizumi H, Miyauchi A, Takagi Y, Ikeda K, Harada A. Association of transforming growth factor beta1 genotype with spinal osteophytosis in Japanese women. Arthritis Rheum 2000; 43: 452-460.
7. Lau HH, Ho AY, Luk KD, Kung AW. Transforming growth factor-beta1 gene polymorphisms and bone turnover, bone mineral density and fracture risk in southern Chinesewomen. Calcif Tissue Int 2004; 74: 516-521.
8. Kinoshita A, Saito T, TomitaHet al. Domain-specific mutations in TGFB1 result in Camurati-Engelmann disease. Nat Genet 2000; 26: 19-20.
9. Whyte MP, Totty WG, Novack DV, Zhang X, Wenkert D, Mumm S. Camurati-Engelmann disease: unique variant featuring a novel mutation in TGFbeta1 encoding transforming growth factor beta 1 and a missense change in TNFSF11 encoding RANK ligand. J Bone Miner Res 2011; 26: 920-933.
10. Dequeker J, Aerssens J, Luyten FP. Osteoarthritis and osteoporosis: clinical and research evidence of inverse relationship. Aging Clinl Exp Res 2003; 15: 426-439.
11. Hunter DJ, Spector TD. The role of bone metabolism in osteoarthritis. Curr Rheum Rep 2003; 5: 15-19.
12. Kizawa H, Kou I, Iida A et al. An aspartic acid repeat polymorphism in asporin inhibits chondrogenesis and increases susceptibility to osteoarthritis. Nat Genet 2005; 37: 138-144.
13. Jiang Q, Shi D, Yi L et al. Replication of the association of the aspartic acid repeat polymorphism in the asporin gene with knee-osteoarthritis susceptibility in Han Chinese. J Hum Genet 2006; 51: 1068-1072.
14. Mustafa Z, Dowling B, Chapman K, Sinsheimer JS, Carr A, Loughlin J. Investigating the aspartic acid (D) repeat of asporin as a risk factor for osteoarthritis in a UK Caucasian population. Arthritis Rheum 2005; 52: 3502-3506.
15. Song YQ, Cheung KM, HoDWet al. Association of the asporin D14 allele with lumbar-disc degeneration in Asians. Am J Hum Genet 2008; 82: 744-747.
16. KaliakatsosM, TzetisM, Kanavakis E et al. Asporin and knee osteoarthritis in patients of Greek origin. Osteoarthr Cartilage 2006; 14: 609-611.
17. Valdes AM, Spector TD, Tamm A et al. Genetic variation in the SMAD3 gene is associated with hip and knee osteoarthritis. Arthritis Rheum 2010; 62: 2347-2352.
18. van der Linde D, Verhagen HJ,Moelker A et al. Aneurysm-osteoarthritis syndrome with visceral and iliac artery aneurysms. J Vasc Surg 2013; 57: 96-102.
19. Martens T, van Herzeele I, de Ryck F et al. Multiple aneurysms in a patient with aneurysms-osteoarthritis syndrome. Ann Thorac Surg 2013; 95: 332-335.
20. van der Linde D, van de Laar IM, Bertoli-Avella AM et al. Aggressive cardiovascular phenotype of aneurysms-osteoarthritis syndrome caused by pathogenic SMAD3 variants. J Am Coll Cardiol 2012; 60: 397-403.
21. van de Laar IM, Oldenburg RA, Pals G et al. Mutations in SMAD3 cause a syndromic form of aortic aneurysms and dissections with early-onset osteoarthritis. Nat Genet 2011; 43: 121-126.
22. van de Laar IM, van der Linde D, Oei EHet al. Phenotypic spectrum of the SMAD3-related aneurysms-osteoarthritis syndrome. J Med Genet 2012; 49: 47-57.
23. Kainulainen K, Karttunen L, Puhakka L, Sakai L, Peltonen L. Mutations in the fibrillin gene responsible for dominant ectopia lentis and neonatal Marfan syndrome. Nat Genet 1994; 6: 64-69.
24. Loeys BL, Schwarze U, Holm T et al. Aneurysm syndromes caused by mutations in the TGF-beta receptor. New Engl J Med 2006; 355: 788-798.
25. Gordon KJ, Blobe GC. Role of transforming growth factor-beta superfamily signaling pathways in human disease. Biochim Biophys Acta 2008; 1782: 197-228.
26. van der Kraan PM, Blaney Davidson EN, Blom A, van den Berg WB. TGFbeta signaling in chondrocyte terminal differentiation and osteoarthritis: modulation and integration of signaling pathways through receptor-Smads. Osteoarthr Cartilage 2009; 17: 1539-1545.
27. Miyazawa K, Shinozaki M, Hara T, Furuya T, Miyazono K. Two major Smad pathways in TGF-beta superfamily signalling. Genes Cells 2002; 7: 1191-1204.
28. Blaney Davidson EN, Remst DF, Vitters EL 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: 7937-7945.
29. Goumans MJ,Valdimarsdottir G, Itoh S, Rosendahl A, Sideras P, ten Dijke P. Balancing the activation state of the endothelium via two distinct TGFbeta type I receptors. EMBO J 2002; 21: 1743-1753.
30. Goumans MJ, Valdimarsdottir G, Itoh S et al. Activin receptor-like kinase (ALK)1 is an antagonistic mediator of lateral TGFbeta/ALK5 signaling. Mol Cell 2003; 12: 817-828.
31. Finnson KW, Parker WL, ten Dijke P, Thorikay M, Philip A. ALK1 opposes ALK5/Smad3 signaling and expression of extracellular matrix components in human chondrocytes. J Bone Miner Res 2008; 23: 896-906.
32. Xiao YT, Xiang LX, Shao JZ. Bone morphogenetic protein. Biochem Bioph Res Commun 2007; 362: 550-553.
33. ten Dijke P, Arthur HM. Extracellular control of TGFbeta signalling in vascular development and disease. Nature reviews. Mol Cell Biol 2007; 8: 857-869.
34. Di Guglielmo GM, Le Roy C, Goodfellow AF, Wrana JL. Distinct endocytic pathways regulate TGF-beta receptor signalling and turnover. Nat Cell Biol 2003; 5: 410-421.
35. Chen YG. Endocytic regulation of TGF-beta signaling. Cell Res 2009; 19: 58-70.
36. WuQ, Huang JH, Sampson ER et al. Smurf2 induces degradation of GSK-3beta and upregulates beta-catenin in chondrocytes: a potential mechanism for Smurf2-induced degeneration of articular cartilage. Exp Cell Res 2009; 315: 2386-2398.
37. Wu Q, Chen D, Zuscik MJ, O'Keefe RJ, Rosier RN. Overexpression of Smurf2 stimulates endochondral ossification through upregulation of beta-catenin. J Bone Miner Res 2008; 23: 552-563.
38. Wu Q, Kim KO, Sampson ER et al. Induction of an osteoarthritis-like phenotype and degradation of phosphorylated Smad3 by Smurf2 in transgenic mice. Arthritis Rheum 2008; 58: 3132-3144.
39. Song JJ, Aswad R, Kanaan RA et al. Connective tissue growth factor (CTGF) acts as a downstream mediator of TGF-beta1 to induce mesenchymal cell condensation. J Cell Physiol 2007; 210: 398-410.
40. Tuli R, Tuli S, Nandi S et al. Transforming growth factor-beta-mediated chondrogenesis of human mesenchymal progenitor cells involves Ncadherin and mitogen-activated protein kinase and Wnt signaling cross-talk. J Biol Chem 2003; 278: 41227-41236.
41. Leonard CM, Fuld HM, Frenz DA, Downie SA, Massague J, Newman SA. Role of transforming growth factor-beta in chondrogenic pattern formation in the embryonic limb: stimulation of mesenchymal condensation and fibronectin gene expression by exogenenous TGFbeta and evidence for endogenous TGF-beta-like activity. Dev Biol 1991; 145: 99-109.
42. Kulyk WM, Rodgers BJ, Greer K, Kosher RA. Promotion of embryonic chick limb cartilage differentiation by transforming growth factor-beta. Dev Biol 1989; 135: 424-430.
43. van der Kraan PM, van den Berg WB. Osteophytes: relevance and biology. Osteoarthr Cartilage 2007; 15: 237-244.
44. Blom AB, van Lent PL, Holthuysen AE, et al. Synovial liningmacrophages mediate osteophyte formation during experimental osteoarthritis. Osteoarthr Cartilage 2004; 12: 627-635.
45. Buckwalter JA,Mankin HJ. Articular cartilage. J Bone Joint Surg Am 1997; 79: 600-632.
46. Buckwalter JA, Mankin HJ, Grodzinsky AJ. Articular cartilage and osteoarthritis. Instr Course Lect 2005; 54: 465-480.
47. Buckwalter JA, Brown TD. Joint injury, repair, and remodeling: roles in post-traumatic osteoarthritis. Clin Orthop Relat Res 2004; (423): 7-16.
48. Brandt KD, Dieppe P, Radin E. Etiopathogenesis of osteoarthritis. Med Clin North Am 2009; 93: 1-24.
49. Pullig O, Weseloh G, Ronneberger D, Kakonen S, Swoboda B. Chondrocyte differentiation in human osteoarthritis: expression of osteocalcin in normal and osteoarthritic cartilage and bone. Calcif Tissue Int 2000; 63: 230-240.
50. van den Berg WB. Pathophysiology of osteoarthritis. Joint Bone Spine 2000; 67: 555-556.
51. Shen J, Li J, Wang B et al.Deletion of the Type II TGF-beta receptor gene in articular chondrocytes leads to a progressive OA-like phenotype inmice. Arthritis Rheum 2013; 65: 3107-3119
52. Serra R, Johnson M, Filvaroff EH et al. Expression of a truncated, kinasedefective TGF-beta type II receptor in mouse skeletal tissue promotes terminal chondrocyte differentiation and osteoarthritis. J Cell Biol 1997; 139: 541-552.
53. Yang X, Chen L, Xu X, Li C, Huang C, Deng CX. TGF-beta/Smad3 signals repress chondrocyte hypertrophic differentiation and are required for maintaining articular cartilage. J Cell Biol 2001; 153: 35-46.
54. Blaney Davidson EN, Scharstuhl A, Vitters EL, van der Kraan PM, van den Berg WB. Reduced transforming growth factor-beta signaling in cartilage of old mice: role in impaired repair capacity. Arthritis Res Ther 2005; 7: R1338-R13347.
55. Blaney Davidson EN, van der Kraan PM, van den Berg WB. TGF-beta and osteoarthritis. Osteoarthr Cartilage 2007; 15: 597-604.
56. Dunker N, Krieglstein K. Targeted mutations of transforming growth factor-beta genes reveal important roles in mouse development and adult homeostasis. Eur J Biochem/FEBS 2000; 267: 6982-6988.
57. Chen M, Lichtler AC, Sheu TJ et al. Generation of a transgenic mouse model with chondrocyte-specific and tamoxifen-inducible expression of Cre recombinase. Genesis 2007; 45: 44-50.
58. Zhu M, Chen M, Lichtler AC, O'Keefe RJ, Chen D. Tamoxifen-inducible Cre-recombination in articular chondrocytes of adult Col2a1-CreER(T2) transgenic mice. Osteoarthr Cartilage 2008; 16: 129-130.
59. Little CB, Barai A, Burkhardt D et al. Matrix metalloproteinase 13-deficient mice are resistant to osteoarthritic cartilage erosion but not chondrocyte hypertrophy or osteophyte development. Arthritis Rheum 2009; 60: 3723-3733.
60. Wang M, Sampson ER, Jin H et al. MMP13 is a critical target gene during the progression of osteoarthritis. Arthritis Res Ther 2013; 15: R5.
61. Blaney Davidson EN, Vitters EL, van Beuningen HM, van de Loo FA, van den Berg WB, van der Kraan PM. Resemblance of osteophytes in experimental osteoarthritis to transforming growth factor beta-induced osteophytes: limited role of bone morphogenetic protein in early osteoarthritic osteophyte formation. Arthritis Rheum 2007; 56: 4065-4073.
62. Bakker AC, van de Loo FA, van Beuningen HM et al. Overexpression of active TGF-beta-1 in the murine knee joint: evidence for synovial-layerdependent chondro-osteophyte formation. Osteoarthr Cartilage 2001; 9: 128-136.
63. Kronenberg HM. Developmental regulation of the growth plate. Nature 2003; 423: 332-336.
64. van Beuningen HM, van der Kraan PM, Arntz OJ, van den Berg WB. Transforming growth factor-beta 1 stimulates articular chondrocyte proteoglycan synthesis and induces osteophyte formation in the murine knee joint. Lab Invest 1994; 71: 279-290.
65. van Beuningen HM, Glansbeek HL, van der Kraan PM, van den Berg WB. Differential effects of local application of BMP-2 or TGF-beta 1 on both articular cartilage composition and osteophyte formation. Osteoarthr Cartilage 1998; 6: 306-317.
66. van Beuningen HM, Glansbeek HL, van der Kraan PM, van den Berg WB. Osteoarthritis-like changes in the murine knee joint resulting from intraarticular transforming growth factor-beta injections. Osteoarthr Cartilage 2000; 8: 25-33.
67. Scharstuhl A, Glansbeek HL, van Beuningen HM, Vitters EL, van der Kraan PM, van den Berg WB. Inhibition of endogenous TGF-beta during experimental osteoarthritis prevents osteophyte formation and impairs cartilage repair. J Immunol 2002; 169: 507-514.
68. Zhen G, Wen C, Jia X et al. Inhibition of TGF-beta signaling in mesenchymal stem cells of subchondral bone attenuates osteoarthritis. Nat Med 2013; 19: 704-712.
69. Tang Y, Wu X, Lei W et al. TGF-beta1-induced migration of bone mesenchymal stem cells couples bone resorption with formation. Nat Med 2009; 15: 757-765.
70. Scanzello CR, Goldring SR. The role of synovitis in osteoarthritis pathogenesis. Bone 2012; 51: 249-257.
71. Fan J, Varshney RR, Ren L, Cai D, Wang DA. Synovium-derived mesenchymal stem cells: a new cell source for musculoskeletal regeneration. Tissue Erng Part B Rev 2009; 15: 75-86.
72. Hui AY, McCarty WJ,Masuda K, Firestein GS, Sah RL.Asystems biology approach to synovial joint lubrication in health, injury, and disease. Wiley interdisciplinary reviews. Syst Biol Med 2012; 4: 15-37.
73. Rhee DK, Marcelino J, Baker M et al. The secreted glycoprotein lubricin protects cartilage surfaces and inhibits synovial cell overgrowth. J Clin Invest 2005; 115: 622-631.
74. Oehler S, Neureiter D, Meyer-Scholten C, Aigner T. Subtyping of osteoarthritic synoviopathy. Clin Exp Rheumatol 2002; 20: 633-640.
75. Ayral X, Pickering EH, Woodworth TG, Mackillop N, Dougados M. Synovitis: a potential predictive factor of structural progression of medial tibiofemoral knee osteoarthritis-results of a 1 year longitudinal arthroscopic study in 422 patients. Osteoarthr Cartilage 2005; 13: 361-367.
76. Scharstuhl A, Vitters EL, van der Kraan PM, van den Berg WB. Reduction of osteophyte formation and synovial thickening by adenoviral overexpression of transforming growth factor beta/bone morphogenetic protein inhibitors during experimental osteoarthritis. Arthritis Rheum 2003; 48: 3442-3451.
77. Blaney Davidson EN, Vitters EL, van den Berg WB, van der Kraan PM. TGF beta-induced cartilage repair is maintained but fibrosis is blocked in the presence of Smad7. Arthritis Res Ther 2006; 8: R65.
78. Mirando AJ, Liu Z, Moore T et al. RBP-Jkappa-dependent Notch signaling is required for murine articular cartilage and joint maintenance. Arthritis Rheum 2013; 65: 2623-2633.
79. Lin AC, Seeto BL, Bartoszko JMet al.Modulating hedgehog signaling can attenuate the severity of osteoarthritis. Nat Med 2009; 15: 1421-1425.
80. Wang M, Tang D, Shu B et al. Conditional activation of beta-catenin signaling in mice leads to severe defects in intervertebral disc tissue. Arthritis Rheum 2012; 64: 2611-2623.
81. Goldring MB, Marcu KB. Epigenomic and microRNA-mediated regulation in cartilage development, homeostasis, and osteoarthritis. Trends Mol Med 2012; 18: 109-118.
82. Miyaki S, Sato T, Inoue A et al. MicroRNA-140 plays dual roles in both cartilage development and homeostasis. Genes Dev 2010; 24: 1173-1185.