The high affinity ALK1-ligand BMP9 induces a hypertrophy-like state in chondrocytes that is antagonized by TGFβ1

Osteoarthritis and Cartilage

Volumn 23, Issue 6, 2015, Pages 985-995

  van Caam, A ^a   Blaney Davidson, E ^a   Garcia de Vinuesa, A ^b   van Geffen, E ^a   van den Berg, W ^a   Goumans, M J ^b   ten Dijke, P ^b   van der Kraan, P ^a  

^a RADBOUD UNIVERSITY MEDICAL CENTER   (Netherlands)

^b LEIDEN UNIVERSITY MEDICAL CENTER   (Netherlands)

Author keywords

BMP 9; Chondrocyte; Hypertrophy; Smad signaling; TGF beta1

Indexed keywords

ALKALINE PHOSPHATASE; BONE MORPHOGENETIC PROTEIN 9; CAGA PROTEIN; COLLAGEN TYPE 10; COLLAGEN TYPE 10A1; SMAD1 PROTEIN; SMAD2 PROTEIN; SMAD3 PROTEIN; SMAD5 PROTEIN; TRANSFORMING GROWTH FACTOR BETA1; UNCLASSIFIED DRUG; BETAIG-H3 PROTEIN; LIGAND; SCLEROPROTEIN; TRANSFORMING GROWTH FACTOR BETA;

ANIMAL CELL; ARTICLE; BINDING AFFINITY; CARTILAGE CELL; CONTROLLED STUDY; DOSE RESPONSE; HYPERTROPHY; INTRACELLULAR SIGNALING; NONHUMAN; PRIORITY JOURNAL; PROTEIN EXPRESSION; PROTEIN PHOSPHORYLATION; PROTEIN PROTEIN INTERACTION; ANIMAL; ANTAGONISTS AND INHIBITORS; ARTICULAR CARTILAGE; BOVINE; CELL CULTURE; CYTOLOGY; DRUG EFFECTS; GENE EXPRESSION REGULATION; METABOLISM; PATHOLOGY; PHOSPHORYLATION; SIGNAL TRANSDUCTION;

ANIMALS; CARTILAGE, ARTICULAR; CATTLE; CELLS, CULTURED; CHONDROCYTES; EXTRACELLULAR MATRIX PROTEINS; GENE EXPRESSION REGULATION; GROWTH DIFFERENTIATION FACTOR 2; HYPERTROPHY; LIGANDS; PHOSPHORYLATION; SIGNAL TRANSDUCTION; SMAD1 PROTEIN; SMAD2 PROTEIN; SMAD5 PROTEIN; TRANSFORMING GROWTH FACTOR BETA;

EID: 84929708247     PISSN: 10634584     EISSN: 15229653     Source Type: Journal    
DOI: 10.1016/j.joca.2015.02.007     Document Type: Article

References (52)

1. van der Kraan P.M., van den Berg W.B. Chondrocyte hypertrophy and osteoarthritis: role in initiation and progression of cartilage degeneration?. Osteoarthritis Cartilage 2012, 20:223-232.
2. Dreier R. Hypertrophic differentiation of chondrocytes in osteoarthritis: the developmental aspect of degenerative joint disorders. Arthritis Res Ther 2010, 12:216.
3. Tchetina E.V., Squires G., Poole A.R. Increased type II collagen degradation and very early focal cartilage degeneration is associated with upregulation of chondrocyte differentiation related genes in early human articular cartilage lesions. JRheumatol 2005, 32:876-886.
4. Finnson K.W., Chi Y., Bou-Gharios G., Leask A., Philip A. TGF-b signaling in cartilage homeostasis and osteoarthritis. Front Biosci (Schol Ed) 2012, 4:251-268.
5. Heldin C.H., Miyazono K., ten Dijke P. TGF-beta signalling from cell membrane to nucleus through SMAD proteins. Nature 1997, 390:465-471.
6. Yang X., Chen L., Xu X., Li C., Huang C., Deng C.X. TGF-beta/Smad3 signals repress chondrocyte hypertrophic differentiation and are required for maintaining articular cartilage. JCell Biol 2001, 153:35-46.
7. Ferguson C.M., Schwarz E.M., Reynolds P.R., Puzas J.E., Rosier R.N., O'Keefe R.J. Smad2 and 3 mediate transforming growth factor-beta1-induced inhibition of chondrocyte maturation. Endocrinology 2000, 141:4728-4735.
8. Song B., Estrada K.D., Lyons K.M. Smad signaling in skeletal development and regeneration. Cytokine Growth Factor Rev 2009, 20:379-388.
9. Hellingman C.A., Davidson E.N., Koevoet W., Vitters E.L., van den Berg W.B., van Osch G.J., et al. Smad signaling determines chondrogenic differentiation of bone-marrow-derived mesenchymal stem cells: inhibition of Smad1/5/8P prevents terminal differentiation and calcification. Tissue Eng Part A 2011, 17:1157-1167.
10. Horiki M., Imamura T., Okamoto M., Hayashi M., Murai J., Myoui A., et al. Smad6/Smurf1 overexpression in cartilage delays chondrocyte hypertrophy and causes dwarfism with osteopenia. JCell Biol 2004, 165:433-445.
11. Valcourt U., Gouttenoire J., Moustakas A., Herbage D., Mallein-Gerin F. Functions of transforming growth factor-beta family type I receptors and Smad proteins in the hypertrophic maturation and osteoblastic differentiation of chondrocytes. JBiol Chem 2002, 277:33545-33558.
12. Retting K.N., Song B., Yoon B.S., Lyons K.M. BMP canonical Smad signaling through Smad1 and Smad5 is required for endochondral bone formation. Development 2009, 136:1093-1104.
13. Blaney Davidson E.N., Remst D.F., Vitters E.L., van Beuningen H.M., Blom A.B., Goumans M.J., et al. Increase in ALK1/ALK5 ratio as a cause for elevated MMP-13 expression in osteoarthritis in humans and mice. JImmunol 2009, 182:7937-7945.
14. David L., Mallet C., Mazerbourg S., Feige J.J., Bailly S. Identification of BMP9 and BMP10 as functional activators of the orphan activin receptor-like kinase 1 (ALK1) in endothelial cells. Blood 2007, 109:1953-1961.
15. Scharpfenecker M., van Dinther M., Liu Z., van Bezooijen R.L., Zhao Q.H., Pukac L., et al. BMP-9 signals via ALK1 and inhibits bFGF-induced endothelial cell proliferation and VEGF-stimulated angiogenesis. JCell Sci 2007, 120:964-972.
16. Herrera B., Inman G.J. Arapid and sensitive bioassay for the simultaneous measurement of multiple bone morphogenetic proteins. Identification and quantification of BMP4, BMP6 and BMP9 in bovine and human serum. BMC Cell Biol 2009, 10:20.
17. David L., Mallet C., Keramidas M., Lamande N., Gasc J.M., Dupuis-Girod S., et al. Bone morphogenetic protein-9 is a circulating vascular quiescence factor. Circ Res 2008, 102:914-922.
18. Bidart M., Ricard N., Levet S., Samson M., Mallet C., David L., et al. BMP9 is produced by hepatocytes and circulates mainly in an active mature form complexed to its prodomain. Cell Mol Life Sci 2012 Jan, 69(2):313-324. Epub 2011 Jun 28. (the PMID:21710321). 10.1007/s00018-011-0751-1.
19. Wu N.N., Zhao Y.Z., Yin Y.B., Zhang Y., Luo J.Y. Identification and analysis of type II TGF-beta receptors in BMP-9-induced osteogenic differentiation of C3H10T1/2 mesenchymal stem cells. Acta Biochim Biophys Sin 2010, 42:699-708.
20. Zhang W., Deng Z.L., Chen L., Zuo G.W., Luo Q., Shi Q., et al. Retinoic acids potentiate BMP9-induced osteogenic differentiation of mesenchymal progenitor cells. PLoS One 2010, 5:e11917.
21. Upton P.D., Davies R.J., Trembath R.C., Morrell N.W. Bone morphogenetic protein (BMP) and activin type II receptors balance BMP9 signals mediated by activin receptor-like kinase-1 in human pulmonary artery endothelial cells. JBiol Chem 2009, 284:15794-15804.
22. Star G.P., Giovinazzo M., Langleben D. Bone morphogenic protein-9 stimulates endothelin-1 release from human pulmonary microvascular endothelial cells: a potential mechanism for elevated ET-1 levels in pulmonary arterial hypertension. Microvasc Res 2010, 80:349-354.
23. Cunha S.I., Pardali E., Thorikay M., Anderberg C., Hawinkels L., Goumans M.J., et al. Genetic and pharmacological targeting of activin receptor-like kinase 1 impairs tumor growth and angiogenesis. JExp Med 2010, 207:85-100.
24. Dennler S., Itoh S., Vivien D., ten Dijke P., Huet S., Gauthier J.M. Direct binding of Smad3 and Smad4 to critical TGF beta-inducible elements in the promoter of human plasminogen activator inhibitor-type 1 gene. EMBO J 1998, 17:3091-3100.
25. Herrera B., van Dinther M., Ten Dijke P., Inman G.J. Autocrine bone morphogenetic protein-9 signals through activin receptor-like kinase-2/Smad1/Smad4 to promote ovarian cancer cell proliferation. Cancer Res 2009, 69:9254-9262.
26. Piek E., Ju W.J., Heyer J., Escalante-Alcalde D., Stewart C.L., Weinstein M., et al. Functional characterization of transforming growth factor beta signaling in Smad2- and Smad3-deficient fibroblasts. JBiol Chem 2001, 276:19945-19953.
27. Yang Y.C., Piek E., Zavadil J., Liang D., Xie D., Heyer J., et al. Hierarchical model of gene regulation by transforming growth factor beta. Proc Natl Acad Sci USA 2003, 100:10269-10274.
28. Liu Y., Meyer C., Muller A., Herweck F., Li Q., Mullenbach R., et al. IL-13 induces connective tissue growth factor in rat hepatic stellate cells via TGF-beta-independent Smad signaling. JImmunol 2011, 187:2814-2823.
29. Weng H., Mertens P.R., Gressner A.M., Dooley S. IFN-gamma abrogates profibrogenic TGF-beta signaling in liver by targeting expression of inhibitory and receptor Smads. JHepatol 2007, 46:295-303.
30. Zhang Y., Handley D., Kaplan T., Yu H., Bais A.S., Richards T., et al. High throughput determination of TGFbeta1/SMAD3 targets in A549 lung epithelial cells. PLoS One 2011, 6:e20319.
31. Brodin G., Ahgren A., ten Dijke P., Heldin C.H., Heuchel R. Efficient TGF-beta induction of the Smad7 gene requires cooperation between AP-1, Sp1, and Smad proteins on the mouse Smad7 promoter. JBiol Chem 2000, 275:29023-29030.
32. Jonk L.J., Itoh S., Heldin C.H., ten Dijke P., Kruijer W. Identification and functional characterization of a Smad binding element (SBE) in the JunB promoter that acts as a transforming growth factor-beta, activin, and bone morphogenetic protein-inducible enhancer. JBiol Chem 1998, 273:21145-21152.
33. Caron M.M., Emans P.J., Cremers A., Surtel D.A., Coolsen M.M., van Rhijn L.W., et al. Hypertrophic differentiation during chondrogenic differentiation of progenitor cells is stimulated by BMP-2 but suppressed by BMP-7. Osteoarthritis Cartilage 2013, 21:604-613.
34. ten Dijke P., Yamashita H., Sampath T.K., Reddi A.H., Estevez M., Riddle D.L., et al. Identification of type I receptors for osteogenic protein-1 and bone morphogenetic protein-4. JBiol Chem 1994, 269:16985-16988.
35. Leboy P., Grasso-Knight G., D'Angelo M., Volk S.W., Lian J.V., Drissi H., et al. Smad-Runx interactions during chondrocyte maturation. JBone Joint Surg Am 2001, 83-A(Suppl 1):S15-S22.
36. Kang J.S., Alliston T., Delston R., Derynck R. Repression of Runx2 function by TGF-beta through recruitment of class II histone deacetylases by Smad3. EMBO J 2005, 24:2543-2555.
37. van der Kraan P.M., Blaney Davidson E.N., Blom A., van den Berg W.B. TGF-beta signaling in chondrocyte terminal differentiation and osteoarthritis: modulation and integration of signaling pathways through receptor-Smads. Osteoarthritis Cartilage 2009, 17:1539-1545.
38. Oh S.P., Seki T., Goss K.A., Imamura T., Yi Y., Donahoe P.K., et al. Activin receptor-like kinase 1 modulates transforming growth factor-beta 1 signaling in the regulation of angiogenesis. Proc Natl Acad Sci USA 2000, 97:2626-2631.
39. Goumans M.J., Valdimarsdottir G., Itoh S., Lebrin F., Larsson J., Mummery C., et al. Activin receptor-like kinase (ALK)1 is an antagonistic mediator of lateral TGFbeta/ALK5 signaling. Mol Cell 2003, 12:817-828.
40. Finnson K.W., Parker W.L., ten Dijke P., Thorikay M., Philip A. ALK1 opposes ALK5/Smad3 signaling and expression of extracellular matrix components in human chondrocytes. JBone Miner Res 2008, 23:896-906.
41. Zhang S., Fei T., Zhang L., Zhang R., Chen F., Ning Y., et al. Smad7 antagonizes transforming growth factor beta signaling in the nucleus by interfering with functional Smad-DNA complex formation. Mol Cell Biol 2007, 27:4488-4499.
42. Yan X., Chen Y.G. Smad7: not only a regulator, but also a cross-talk mediator of TGF-beta signalling. Biochem J 2011, 434:1-10.
43. Scharstuhl A., Diepens R., Lensen J., Vitters E., van Beuningen H., van der Kraan P., et al. Adenoviral overexpression of Smad-7 and Smad-6 differentially regulates TGF-beta-mediated chondrocyte proliferation and proteoglycan synthesis. Osteoarthritis Cartilage 2003, 11:773-782.
44. Enomoto H., Enomoto-Iwamoto M., Iwamoto M., Nomura S., Himeno M., Kitamura Y., et al. Cbfa1 is a positive regulatory factor in chondrocyte maturation. JBiol Chem 2000, 275:8695-8702.
45. Hatakeyama Y., Nguyen J., Wang X., Nuckolls G.H., Shum L. Smad signaling in mesenchymal and chondroprogenitor cells. JBone Joint Surg Am 2003, 85-A(Suppl 3):13-18.
46. Mattot V., Raes M.B., Henriet P., Eeckhout Y., Stehelin D., Vandenbunder B., et al. Expression of interstitial collagenase is restricted to skeletal tissue during mouse embryogenesis. JCell Sci 1995, 108(Pt 2):529-535.
47. Prasadam I., van Gennip S., Friis T., Shi W., Crawford R., Xiao Y. ERK-1/2 and p38 in the regulation of hypertrophic changes of normal articular cartilage chondrocytes induced by osteoarthritic subchondral osteoblasts. Arthritis Rheum 2010, 62:1349-1360.
48. Reilly G.C., Golden E.B., Grasso-Knight G., Leboy P.S. Differential effects of ERK and p38 signaling in BMP-2 stimulated hypertrophy of cultured chick sternal chondrocytes. Cell Commun Signal 2005, 3:3.
49. Derynck R., Zhang Y.E. Smad-dependent and Smad-independent pathways in TGF-beta family signalling. Nature 2003, 425:577-584.
50. Morales T.I., Joyce M.E., Sobel M.E., Danielpour D., Roberts A.B. Transforming growth factor-beta in calf articular cartilage organ cultures: synthesis and distribution. Arch Biochem Biophys 1991, 288:397-405.
51. Kushner I., Somerville J.A. Permeability of human synovial membrane to plasma proteins. Relationship to molecular size and inflammation. Arthritis Rheum 1971, 14:560-570.
52. Shen J., Li J., Wang B., Jin H., Wang M., Zhang Y., et al. Deletion of the transforming growth factor beta receptor type II gene in articular chondrocytes leads to a progressive osteoarthritis-like phenotype in mice. Arthritis Rheum 2013, 65:3107-3119.