Functional knockout of the matrilin-3 gene causes premature chondrocyte maturation to hypertrophy and increases bone mineral density and osteoarthritis

American Journal of Pathology

Volumn 169, Issue 2, 2006, Pages 515-527

  Van Der Weyden, Louise ^a   Wei, Lei ^b   Luo, Junming ^b   Yang, Xu ^b   Birk, David E ^c   Adams, David J ^a   Bradley, Allan ^a   Chen, Qian ^b,d  

^a WELLCOME TRUST SANGER INSTITUTE   (United Kingdom)

^b RHODE ISLAND HOSPITAL   (United States)

^c THOMAS JEFFERSON UNIVERSITY   (United States)

^d NONE   (United States)

Author keywords

[No Author keywords available]

Indexed keywords

MATRILIN 3; SCLEROPROTEIN; UNCLASSIFIED DRUG;

ANIMAL CELL; ANIMAL EXPERIMENT; ANIMAL MODEL; ANIMAL TISSUE; ARTICLE; BONE DENSITY; BONE DISEASE; BONE DYSPLASIA; CARTILAGE CELL; CELL MATURATION; CONTROLLED STUDY; DISEASE PREDISPOSITION; EMBRYO DEVELOPMENT; GENE; GENE MUTATION; GROWTH PLATE; HISTOPATHOLOGY; HYPERTROPHY; IMMUNOHISTOCHEMISTRY; KNOCKOUT MOUSE; MATN3 GENE; MOUSE; NONHUMAN; NUCLEOTIDE SEQUENCE; OSTEOARTHRITIS; PATHOGENESIS; PRIORITY JOURNAL; SKELETON MALFORMATION; SPONDYLOEPIPHYSEAL DYSPLASIA; STEM CELL;

EID: 33746641679     PISSN: 00029440     EISSN: None     Source Type: Journal    
DOI: 10.2353/ajpath.2006.050981     Document Type: Article

References (59)

1. Deak F, Wagener R, Kiss I, Paulsson M: The matrilins: a novel family of oligomeric extracellular matrix proteins. Matrix Biol 1999, 18:55-64
2. Paulsson M, Heinegard D: Radioimmunoassay of the 148-kilodalton cartilage protein: distribution of the protein among bovine tissues. Biochem J 1982, 207:207-213
3. Wagener R, Kobbe B, Paulsson M: Primary structure of matrilin-3, a new member of a family of extracellular matrix proteins related to cartilage matrix protein (matrilin-1) and von Willebrand factor. FEBS Lett 1997, 413:129-134
4. Klatt AR, Nitsche DP, Kobbe B, Morgelin M, Paulsson M, Wagener R: Molecular structure and tissue distribution of matrilin-3, a filament-forming extracellular matrix protein expressed during skeletal development. J Biol Chem 2000, 275:3999-4006
5. Piecha D, Muratoglu S, Morgelin M, Hauser N, Studer D, Kiss I, Paulsson M, Deak F: Matrilin-2, a large, oligomeric matrix protein, is expressed by a great variety of cells and forms fibrillar networks. J Biol Chem 1999, 274:13353-13361
6. Klatt A, Nitsche DP, Kobbe B, Macht M, Paulsson M, Wagener R: Molecular structure, processing, and tissue distribution of matrilin-4. J Biol Chem 2001, 276:17267-17275
7. Wu JJ, Eyre DR: Matrilin-3 forms disulfide-linked oligomers with matrilin-1 in bovine epiphyseal cartilage. J Biol Chem 1998, 273:17433-17438
8. Zhang Y, Chen Q: Changes of matrilin forms during endochondral ossification: molecular basis of oligomeric assembly. J Biol Chem 2000, 275:32628-32634
9. Winterbottom N, Tondravi MM, Harrington TL, Klier FG, Vertel BM, Goetinck PF: Cartilage matrix protein is a component of the collagen fibril of cartilage. Dev Dyn 1992, 193:266-276
10. Paulsson M, Heinegård D: Matrix proteins bound to associatively prepared proteoglycans from bovine cartilage. Biochem J 1979, 183:539-545
11. Hauser N, Paulsson M, Heinegård D, Morgelin M: Interaction of cartilage matrix protein with aggrecan: increased covalent crosslinking with tissue maturation. J Biol Chem 1996, 271:32247-32252
12. Wiberg C, Klatt AR, Wagener R, Paulsson M, Bateman JF, Heinegard D, Morgelin M: Complexes of matrilin-1 and biglycan or decorin connect collagen VI microfibrils to both collagen II and aggrecan. J Biol Chem 2003, 278:37698-37704
13. Jackson GC, Barker FS, Jakkula E, Czarny-Ratajczak M, Makitie O, Cole WG, Wright MJ. Smithson SF, Suri M, Rogala P, Mortier GR, Baldock C, Wallace A, Elles R, Ala-Kokko L, Briggs MD: Missense mutations in the beta strands of the single A-domain of matrilin-3 result in multiple epiphyseal dysplasia. J Med Genet 2004, 41:52-59
14. Chapman KL, Mortier GR, Chapman K, Loughlin J, Grant ME, Briggs MD: Mutations in the region encoding the von Willebrand factor A domain of matrilin-3 are associated with multiple epiphyseal dysplasia. Nat Genet 2001, 28:393-396
15. Mostert AK, Dijkstra PF, Jansen BR, van Horn JR, de Graaf B, Heutink P, Lindhout D: Familial multiple epiphyseal dysplasia due to a matrilin-3 mutation: further delineation of the phenotype including 40 years follow-up. Am J Med Genet 2003, 120A:490-497
16. Makitie O, Mortier GR, Czarny-Ratajczak M, Wright MJ, Suri M, Rogala P, Freund M, Jackson GC, Jakkula E, Ala-Kokko L, Briggs MD, Cole WG: Clinical and radiographic findings in multiple epiphyseal dysplasia caused by MATN3 mutations: description of 12 patients. Am J Med Genet 2004, 125A:278-284
17. Mabuchi A, Haga N, Maeda K, Nakashima E, Manabe N, Hiraoka H, Kitoh H, Kosaki R, Nishimura G, Ohashi H, Ikegawa S: Novel and recurrent mutations clustered in the von Willebrand factor A domain of MATN3 in multiple epiphyseal dysplasia. Hum Mutat 2004, 4:439-440
18. Borochowitz ZU, Scheffer D, Adir V, Dagoneau N, Munnich A, Cormier-DaireV: Spondylo-epi-metaphyseal dysplasia (SEMD) matrilin 3 type: homozygote matrilin 3 mutation in a novel form of SEMD. J Med Genet 2004, 41:366-372
19. Stefansson SE, Jonsson H, Ingvarsson T, Manolescu I, Jonsson HH, Olafsdottir G, Palsdottir E, Stefansdottir G, Sveinbjornsdottir G, Frigge ML, Kong A, Gulcher JR, Stefansson K: Genomewide scan for hand osteoarthritis: a novel mutation in matrilin-3. Am J Hum Genet 2003, 72:1448-1459
20. Pullig O, Weseloh G, Klatt AR, Wagener R, Swoboda B: Matrilin-3 in human articular cartilage: increased expression in osteoarthritis. Osteoarthritis Cartilage 2002, 10:253-263
21. Segat D, Frie C, Nitsche PD, Klatt AR, Piecha D, Korpos E, Deak F, Wagener R, Paulsson M, Smyth N: Expression of matrilin-1, -2 and -3 in developing mouse limbs and heart. Matrix Biol 2000, 19:649-655
22. Klatt AR, Paulsson M, Wagener R: Expression of matrilins during maturation of mouse skeletal tissues. Matrix Biol 2002, 21:289-296
23. Aszodi A, Bateman JF, Hirsch E, Baranyi M, Hunziker EB, Hauser N, Bosze Z, Fassler R: Normal skeletal development of mice lacking matrilin 1: redundant function of matrilins in cartilage? Mol Cell Biol 1999, 19:7841-7845
24. Huang X, Birk DE, Goetinck PF: Mice lacking matrilin-1 (cartilage matrix protein) have alterations in type II collagen fibrillogenesis and fibril organization. Dev Dyn 1999, 216:434-441
25. Ko Y, Kobbe B, Nicolae C, Miosge N, Paulsson M, Wagener R, Aszodi A: Matrilin-3 is dispensable for mouse skeletal growth and development. Mol Cell Biol 2004, 24:1691-1699
26. Ramirez-Solis R, Liu P, Bradley A: Chromosome engineering in mice. Nature 1995, 378:720-724
27. McMahon AP, Bradley A: The Wnt-1 (int-1) proto-oncogene is required for development of a large region of the mouse brain. Cell 1990, 62:1073-1085
28. Lufkin T, Mark M, Hart CP, Dolle P, LeMeur M, Chambon P: Homeotic transformation of the occipital bones of the skull by ectopic expression of a homeobox gene. Nature 1992, 359:835-841
29. Wilhelmi G, Faust R: Suitability of the C57 black mouse as an experimental animal for the study of skeletal changes due to ageing, with special reference to osteo-arthrosis and its response to tribenoside. Pharmacology 1976, 14:289-296
30. Chen Q, Johnson DM, Haudenschild DR, Tondravi MM, Goetinck PF: Cartilage matrix protein forms a type II collagen-independent filamentous network: analysis in primary cell cultures with a retrovirus expression system. Mol Biol Cell 1996, 6:1743-1753
31. Lee JO, Rieu P, Arnaout MA, Liddington R: Crystal structure of the A domain from the alpha subunit of integrin CR3 (CD11b/CD18). Cell 1995, 80:631-638
32. Birk DE, Trelstad RL: Extracellular compartments in tendon morphogenesis: collagen fibril, bundle, and macroaggregate formation. J Cell Biol 1986, 103:231-240
33. Morris NP, Keene DR, Horton WA: Cartilage morphology. Extracellular Matrix and Heritable Disorders of Connective Tissue, ed 2. Edited by PM Rocye, B Steinmann. New York, Alan R. Liss, 2002
34. Chapman KL, Briggs MD, Mortier GR: Review: clinical variability and genetic heterogeneity in multiple epiphyseal dysplasia. Pediatr Pathol Mol Med 2003, 22:53-75
35. Chen Q, Zhang Y, Johnson DM, Goetinck PF: Assembly of a novel cartilage matrix protein filamentous network: molecular basis of differential requirement of von Willebrand factor A domains. Mol Biol Cell 1999, 10:2149-2162
36. Makihira S, Yan W, Ohno S, Kawamoto T, Fujimoto K, Okimura A, Yoshida E, Noshiro M, Hamada T, Kato Y: Enhancement of cell adhesion and spreading by a cartilage-specific noncollagenous protein, cartilage matrix protein (CMP/Matrilin-1), via integrin alpha1beta1. J Biol Chem 1999, 274:11417-11423
37. Whittaker CA, Hynes RO: Distribution and evolution of von Willebrand/integrin A domains: widely dispersed domains with roles in cell adhesion and elsewhere. Mol Biol Cell 2002, 13:3369-3387
38. Vortkamp A, Lee K, Lanske B, Segre GV, Kronenberg HM, Tabin CJ: Regulation of rate of cartilage differentiation by Indian hedgehog and PTH-related protein. Science 1996, 273:613-622
39. Huang W, Chung UI, Kronenberg HM, de Crombrugghe B: The chondrogenic transcription factor Sox9 is a target of signaling by the parathyroid hormone-related peptide in the growth plate of endochondral bones. Proc Natl Acad Sci USA 2001, 98:160-165
40. Lanske B, Karaplis AC, Lee K, Luz A, Vortkamp A, Pirro A, Karperien M, Defize LH, Ho C, Mulligan RC, Abou-Samra AB, Juppner H, Segre GV, Kronenberg HM: PTH/PTHrP receptor in early development and Indian hedgehog-regulated bone growth. Science 1996, 273:663-666
41. Gerber HP, Vu TH, Ryan AM, Kolwalski J, Werb Z, Ferrara N: VEGF couples hypertrophic cartilage remodelling, ossification and angiogenesis during endochondral bone formation. Nat Med 1999, 5:623-628
42. Smits P, Dy P, Mitra S, Lefebvre V: Sox5 and Sox6 are needed to develop and maintain source, columnar, and hypertrophic chondrocytes in the cartilage growth plate. J Cell Biol 2004, 164:747-758
43. 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
44. Naski MC, Colvin JS, Coffin JD, Ornitz DM: Repression of hedgehog signaling and BMP4 expression in growth plate cartilage by fibroblast growth factor receptor 3. Development 1998, 125:4977-4988
45. Ornitz DM: Regulation of chondrocyte growth and differentiation by fibroblast growth factor receptor 3. Novartis Found Symp 2001, 232:63-76
46. Liu Z, Xu J, Colvin JS, Ornitz DM: Coordination of chondrogenesis and osteogenesis by fibroblast growth factor 18. Genes Dev 2002, 16:859-869
47. Ivkovic S, Yoon BS, Popoff SN, Safadi FF, Libuda DE, Stephenson RC, Daluiski A, Lyons KM: Connective tissue growth factor coordinates chondrogenesis and angiogenesis during skeletal development. Development 2003, 130:2779-2791
48. Brandi ML, Gennari L, Cerinic MM, Becherini L, Falchetti A, Masi L, Gennari C, Reginster JY: Genetic markers of osteoarticular disorders: facts and hopes. Arthritis Res 2001, 3:270-280
49. Beamer WG, Donahue LR, Rosen CJ, Baylink DJ: Genetic variability in adult bone density among inbred strains of mice. Bone 1996, 18:397-403
50. Liu Z, Shi W, Ji X, Sun C, Jee WSS, Wu Y, Mao Z, Nagy TR, Li Q, Cao X: Molecules mimicking Smad1 interacting with Hox stimulate bone formation. J Biol Chem 2004, 279:11313-11319
51. Hamrick MW: Increased bone mineral density in the femora of GDF8 knockout mice. Anat Rec A Discov Mol Cell Evol Biol 2003, 272:388-391
52. Xiao L, Naganawa T, Obugunde E, Gronowicz G, Ornitz DM, Coffin JD, Hurley MM: Stat1 controls postnatal bone formation by regulating fibroblast growth factor signaling in osteoblasts. J Biol Chem 2004, 279:27743-27752
53. Zerega B, Cermelli S, Bianco P, Cancedda R, Cancedda FD: Parathyroid hormone [PTH(1-34)] and parathyroid hormone-related protein [PTHrP(1-34)] promote reversion of hypertrophic chondrocytes to a prehypertrophic proliferating phenotype and prevent terminal differentiation of osteoblast-like cells. J Bone Miner Res 1999, 14:1281-1289
54. Hannan MT, Anderson JJ, Zhang Y, Levy D, Felson DT: Bone mineral density and knee osteoarthritis in elderly men and women: the Framingham Study. Arthritis Rheum 1993, 36:1671-1680
55. Hart DJ, Mootoosamy I, Doyle DV, Spector TD: The relationship between osteoarthritis and osteoporosis in the general population: the Chingford Study. Ann Rheum Dis 1994, 53:158-162
56. Nevitt MC, Lane NE, Scott JC, Hochberg MC, Pressman AR, Genant HK, Cummings SR: Radiographic osteoarthritis of the hip and bone mineral density: the Study of Osteoporotic Fractures Research Group. Arthritis Rheum 1995, 38:907-916
57. Burger H, van Daele PL, Odding E, Valkenburg HA, Hofman A, Grobbee DE, Schutte HE, Birkenhager JC, Pols HA: Association of radiographically evident osteoarthritis with higher bone mineral density and increased bone loss with age: the Rotterdam Study. Arthritis Rheum 1996, 39:81-86
58. Sowers M, Lachance L, Jamadar D, Hochberg MC, Hollis B, Crutchfield M, Jannausch ML: The associations of bone mineral density and bone turnover markers with osteoarthritis of the hand and knee in pre-and perimenopausal women. Arthritis Rheum 1999, 42:483-489
59. Korpos E, Molnar A, Papp P, Kiss I, Orosz L, Deak F: Expression pattern of matrilins and other extracellular matrix proteins characterize distinct stages of cell differentiation during antler development. Matrix Biol 2005, 24:124-135