Joint hypermobility syndromes: The pathophysiologic role of tenascin-X gene defects

Arthritis and Rheumatism

Volumn 50, Issue 9, 2004, Pages 2742-2749

  Zweers, Manon C ^a   Hakim, Alan J ^b   Grahame, Rodney ^c   Schalkwijk, Joost ^a  

^a RADBOUD UNIVERSITY MEDICAL CENTER   (Netherlands)

^b WHIPPS CROSS UNIVERSITY HOSPITAL   (United Kingdom)

^c UNIVERSITY COLLEGE LONDON HOSPITALS   (United Kingdom)

Author keywords

[No Author keywords available]

Indexed keywords

COLLAGEN; COLLAGEN FIBRIL; COLLAGEN TYPE 1; GELATINASE A; TENASCIN;

BENIGN JOINT HYPERMOBILITY SYNDROME; CHRONIC FATIGUE SYNDROME; CLINICAL FEATURE; COLLAGEN METABOLISM; EHLERS DANLOS SYNDROME; ELASTIC FIBER; EXTRACELLULAR MATRIX; GENE; GENE DOSAGE; GENE EXPRESSION; GENETIC ANALYSIS; GENETIC DISORDER; GENETIC HETEROGENEITY; GENOTYPE; HAPLOINSUFFICIENCY; HAPLOTYPE; JOINT HYPERMOBILITY; OSTEOARTHRITIS; OSTEOGENESIS IMPERFECTA; PRIORITY JOURNAL; PROTEIN ANALYSIS; REVIEW; SYNDROME DELINEATION; TENASCIN X DEFICIENCY; TENASCIN X GENE;

COLLAGEN; EHLERS-DANLOS SYNDROME; HUMANS; JOINT INSTABILITY; MICROFILAMENT PROTEINS; TENASCIN;

EID: 4444358278     PISSN: 00043591     EISSN: None     Source Type: Journal    
DOI: 10.1002/art.20488     Document Type: Review

References (80)

1. Beighton P, Solomon L, Soskolne CL. Articular mobility in an African population. Ann Rheum Dis 1973;32:413-8.
2. Larsson LG, Baum J, Mudholkar GS. Hypermobility: features and differential incidence between the sexes. Arthritis Rheum 1987; 30:1426-30.
3. Rikken-Bultman DG, Wellink L, van Dongen PW. Hypermobility in two Dutch school populations. Eur J Obstet Gynecol Reprod Biol 1997;73:189-92.
4. Hakim AJ, MacGregor AJ, Spector TD. Joint hypermobility in the general population is common and strongly genetically determined: results of a study of female twins from a national sample [abstract]. Arthritis Rheum 2003;48 Suppl 9:S682.
5. Kirk JA, Ansell BM, Bywaters EG. The hypermobility syndrome: musculoskeletal complaints associated with generalized joint hypermobility. Ann Rheum Dis 1967;26:419-25.
6. Robinson PN, Godfrey M. The molecular genetics of Marfan syndrome and related microfibrillopathies. J Med Genet 2000;37: 9-25.
7. Beighton P, De Paepe A, Steinmann B, Tsipouras P, Wenstrup RJ, for the Ehlers-Danlos National Foundation (USA) and Ehlers-Danlos Support Group (UK). Ehlers-Danlos syndromes: revised nosology, Villefranche, 1997. Am J Med Genet 1988;77:31-7.
8. Grahame R, Bird HA, Child A. The revised (Brighton 1998) criteria for the diagnosis of benign joint hypermobility syndrome (BJHS). J Rheumatol 2000;27:1777-9.
9. Grahame R. Joint hypermobility and genetic collagen disorders: are they related? Arch Dis Child 1999;80:188-91.
10. Hudson N, Fitzcharles MA, Cohen M, Starr MR, Esdaile JM. The association of soft-tissue rheumatism and hypermobility. Br J Rheumatol 1998;37:382-6.
11. Grahame R, Hakim AJ. High prevalence of joint hypermobility syndrome in clinic referrals to a north London community hospital [abstract]. Rheumatology 2004;43 Suppl 2:91.
12. Acasuso-Diaz M, Collantes-Estevez E. Joint hypermobility in patients with fibromyalgia syndrome. Arthritis Care Res 1998;11: 39-42.
13. Gedalia A, Press J, Klein M, Buskila D. Joint hypermobility and fibromyalgia in schoolchildren. Ann Rheum Dis 1993;52:494-6.
14. Barron DF, Cohen BA, Geraghty MT, Violand R, Rowe PC. Joint hypermobility is more common in children with chronic fatigue syndrome than in healthy controls. J Pediatr 2002;141:421-5.
15. Rowe PC, Barron DF, Calkins H, Maumenee IH, Tong PY, Geraghty MT. Orthostatic intolerance and chronic fatigue syndrome associated with Ehlers-Danlos syndrome. J Pediatr 1999; 135:494-9.
16. Goldstein DS, Robertson D, Esler M, Straus SE, Eisenhofer G. Dysautonomias: clinical disorders of the autonomic nervous system. Ann Intern Med 2002;137:753-63.
17. Gazit Y, Nahir AM, Grahame R, Jacob G. Dysautonomia in the joint hypermobility syndrome. Am J Med 2003;115:33-40.
18. Uiterwaal CS, Grobbee DE, Sakkers RJ, Helders PJ, Bank RA, Engelbert RH. A relation between blood pressure and stiffness of joints and skin. Epidemiology 2003;14:223-7.
19. Martin-Santos R, Bulbena A, Porta M, Gago J, Molina L, Duro JC. Association between joint hypermobility syndrome and panic disorder. Am J Psychiatry 1998;155:1578-83.
20. Bulbena A, Duro JC, Porta M, Martin-Santos R, Mateo A, Molina L, et al. Anxiety disorders in the joint hypermobility syndrome. Psychiatry Res 1993;46:59-68.
21. Hakim A, Grahame R. Joint hypermobility syndrome: an update for clinicians. Int J Adv Rheumatol 2003;1:131-8.
22. Jonsson H, Valtysdottir ST, Kjartansson O, Brekkan A. Hypermobility associated with osteoarthritis of the thumb base: a clinical and radiological subset of hand osteoarthritis. Ann Rheum Dis 1996;55:540-3.
23. Jonsson H, Valtysdottir ST. Hypermobility features in patients with hand osteoarthritis. Osteoarthritis Cartilage 1995;3:1-5.
24. Bridges AJ, Smith E, Reid J. Joint hypermobility in adults referred to rheumatology clinics. Ann Rheum Dis 1992;51:793-6.
25. Martin JR, Ives EJ. Familial articular hypermobility and scaphotrapezial/trapezoid osteoarthritis in two siblings. Rheumatology (Oxford) 2002;41:1203-6.
26. Dolan AL, Hart DJ, Doyle DV, Grahame R, Spector TD. The relationship of joint hypermobility, bone mineral density, and osteoarthritis in the general population: the Chingford Study. J Rheumatol 2003;30:799-803.
27. Holbrook KA, Byers PH. Structural abnormalities in the dermal collagen and elastic matrix from the skin of patients with inherited connective tissue disorders. J Invest Dermatol 1982;79 Suppl 1:7s-16s.
28. Byers PH. Ehlers-Danlos syndrome: recent advances and current understanding of the clinical and genetic heterogeneity. J Invest Dermatol 1994;103 Suppl 5:47S-52S.
29. Narcisi P, Richards AJ, Ferguson SD, Pope FM. A family with Ehlers-Danlos syndrome type III/articular hypermobility syndrome has a glycine 637 to serine substitution in type III collagen. Hum Mol Genet 1994;3:1617-20.
30. Henney AM, Brotherton DH, Child AH, Humphries SE, Grahame R. Segregation analysis of collagen genes in two families with joint hypermobility syndrome. Br J Rheumatol 1992;31:169-74.
31. Wordsworth P, Ogilvie D, Smith R, Sykes B. Joint mobility with particular reference to racial variation and inherited connective tissue disorders. Br J Rheumatol 1987;26:9-12.
32. Ameye L, Young MF. Mice deficient in small leucine-rich proteoglycans: novel in vivo models for osteoporosis, osteoarthritis, Ehlers-Danlos syndrome, muscular dystrophy, and corneal diseases. Glycobiology 2002;12:107R-16R.
33. Reed CC, Iozzo RV. The role of decorin in collagen fibrillogenesis and skin homeostasis. Glycoconj J 2002;19:249-55.
34. Chakravarti S. Functions of lumican and fibromodulin: lessons from knockout mice. Glycoconj J 2002;19:287-93.
35. Kao WW, Liu CY. Roles of lumican and keratocan on corneal transparency. Glycoconj J 2002;19:275-85.
36. Young MF, Bi Y, Ameye L, Chen XD. Biglycan knockout mice: new models for musculoskeletal diseases. Glycoconj J 2002;19: 257-62.
37. Sztrolovics R, Rimoin DL, Rodriguez E, Roughley RJ. Single-strand conformation polymorphism analysis of human decorin, biglycan and fibromodulin cDNAs. Matrix Biol 1994;14:307-12.
38. Schalkwijk J, Zweers MC, Steijlen PM, Dean WB, Taylor G, Van Vlijmen IM, et al. A recessive form of the Ehlers-Danlos syndrome caused by tenascin-X deficiency. N Engl J Med 2001;345:1167-75.
39. Weber P, Montag D, Schachner M, Bernhardt RR. Zebrafish tenascin-W, a new member of the tenascin family. J Neurobiol 1998;35:1-16.
40. Chiquet M, Fambrough DM. Chick myotendinous antigen. I. A monoclonal antibody as a marker for tendon and muscle morphogenesis. J Cell Biol 1984;98:1926-36.
41. Bourdon MA, Wikstrand CJ, Furthmayr H, Matthews TJ, Bigner DD. Human glioma-mesenchymal extracellular matrix antigen defined by monoclonal antibody. Cancer Res 1983;43:2796-805.
42. Bristow J, Tee MK, Gitelman SE, Mellon SH, Miller WL. Tenascin-X: a novel extracellular matrix protein encoded by the human XB gene overlapping P450c21B. J Cell Biol 1993;122:265-78.
43. Leprini A, Gherzi R, Siri A, Querze G, Viti F, Zardi L. The human tenascin-R gene. J Biol Chem 1996;271:31251-4.
44. Hagios C, Brown LM, Chiquet ER. Tenascin-Y, a component of distinctive connective tissues, supports muscle cell growth. Exp Cell Res 1999;253:607-17.
45. Jones FS, Jones PL. The tenascin family of ECM glycoproteins: structure, function, and regulation during embryonic development and tissue remodeling. Dev Dyn 2000;218:235-59.
46. Chiquet-Ehrismann R, Chiquet M. Tenascins: regulation and putative functions during pathological stress. J Pathol 2003;200: 488-99.
47. Siri A, Carnemolla B, Saginati M, Leprini A, Casari G, Baralle F, et al. Human tenascin: primary structure, pre-mRNA splicing patterns and localization of the epitopes recognized by two monoclonal antibodies. Nucleic Acids Res 1991;19:525-31.
48. Burch GH, Bedolli MA, McDonough S, Rosenthal SM, Bristow J. Embryonic expression of tenascin-X suggests a role in limb, muscle, and heart development. Dev Dyn 1995;203:491-504.
49. Geffrotin C, Garrido JJ, Tremet L, Vaiman M. Distinct tissue distribution in pigs of tenascin-X and tenascin-C transcripts. Eur J Biochem 1995;231:83-92.
50. Matsumoto K, Saga Y, Ikemura T, Sakakura T, Chiquet ER. The distribution of tenascin-X is distinct and often reciprocal to that of tenascin-C. J Cell Biol 1994;125:483-93.
51. Saga Y, Yagi T, Ikawa Y, Sakakura T, Aizawa S. Mice develop normally without tenascin. Genes Dev 1992;6:1821-31.
52. Freitag S, Schachner M, Morellini F. Behavioral alterations in mice deficient for the extracellular matrix glycoprotein tenascin-R. Behav Brain Res 2003;145:189-207.
53. Weber P, Bartsch U, Rasband MN, Czaniera R, Lang Y, Bluethmann H, et al. Mice deficient for tenascin-R display alterations of the extracellular matrix and decreased axonal conduction velocities in the CNS. J Neurosci 1999;19:4245-62.
54. Saghatelyan A, De Chevigny A, Schachner M, Lledo PM. Tenascin-R mediates activity-dependent recruitment of neuroblasts in the adult mouse forebrain. Nat Neurosci 2004;7:347-56.
55. Blanchong CA, Zhou B, Rupert KL, Chung EK, Jones KN, Sotos JF, et al. Deficiencies of human complement component C4A and C4B and heterozygosity in length variants of RP-C4-CYP21-TNX (RCCX) modules in Caucasians: the load of RCCX genetic diversity on major histocompatibility complex-associated disease. J Exp Med 2000;191:2183-96.
56. Yang Z, Mendoza AR, Welch TR, Zipf WB, Yu CY. Modular variations of the human major histocompatibility complex class III genes for serine/threonine kinase RP, complement component C4, steroid 21-hydroxylase CYP21, and tenascin TNX (the RCCX module): a mechanism for gene deletions and disease associations. J Biol Chem 1999;274:12147-56.
57. Burch GH, Gong Y, Liu W, Dettman RW, Curry CJ, Smith L, et al. Tenascin-X deficiency is associated with Ehlers-Danlos syndrome. Nat Genet 1997;17:104-8.
58. Zweers MC, Bristow J, Steijlen PM, Dean WB, Hamel BC, Otero M, et al. Haploinsufficiency of TNXB is associated with hypermobility type of Ehlers-Danlos syndrome. Am J Hum Genet 2003;73: 214-7.
59. Jessee EF, Owen DS Jr, Sagar KB. The benign hypermobile joint syndrome. Arthritis Rheum 1980;23:1053-6.
60. Hardy GH. Mendelian proportions in a mixed population. Science 1908;28:49-50.
61. Zweers MC, van Vlijmen-Willems IM, van Kuppeveit TH, Mecham RP, Steijlen PM, Bristow J, et al. Deficiency of tenascin-X causes abnormalities in dermal elastic fiber morphology. J Invest Dermatol 2004;122:885-91.
62. Holbrook KA, Byers PH. Skin is a window on heritable disorders of connective tissue. Am J Med Genet 1989;34:105-21.
63. Mao JR, Taylor G, Dean WB, Wagner DR, Afzal V, Lotz JC, et al. Tenascin-X deficiency mimics Ehlers-Danlos syndrome in mice through alteration of collagen deposition. Nat Genet 2002;30: 421-5.
64. Matsumoto K, Takayama N, Ohnishi J, Ohnishi E, Shirayoshi Y, Nakatsuji N, et al. Tumour invasion and metastasis are promoted in mice deficient in tenascin-X. Genes Cells 2001;6:1101-11.
65. Elefteriou F, Exposito JY, Garrone R, Lethias C. Cell adhesion to tenascin-X mapping of cell adhesion sites and identification of integrin receptors. Eur J Biochem 1999;263:840-8.
66. Ikuta T, Sogawa N, Ariga H, Ikemura T, Matsumoto K. Structural analysis of mouse tenascin-X: evolutionary aspects of reduplication of FNIII repeats in the tenascin gene family. Gene 1998;217: 1-13.
67. Lethias C, Descollonges Y, Boutillon MM, Garrone R. Flexilin: a new extracellular matrix glycoprotein localized on collagen fibrils. Matrix Biol 1996;15:11-9.
68. Elefteriou F, Exposito J, Garrone R, Lethias C. Binding of tenascin-X to decorin. FEBS Lett 2001;495:44-7.
69. Pogany G, Vogel KG. The interaction of decorin core protein fragments with type I collagen. Biochem Biophys Res Commun 1992;189:165-72.
70. Bidanset DJ, Guidry C, Rosenberg LC, Choi HU, Timpl R, Hook M. Binding of the proteoglycan decorin to collagen type VI. J Biol Chem 1992;267:5250-6.
71. Schonherr E, Hausser H, Beavan L, Kresse H. Decorin-type I collagen interaction: presence of separate core protein-binding domains. J Biol Chem 1995;270:8877-83.
72. Danielson KG, Baribault H, Holmes DF, Graham H, Kadler KE, Iozzo RV. Targeted disruption of decorin leads to abnormal collagen fibril morphology and skin fragility. J Cell Biol 1997;136: 729-43.
73. Kielty CM, Sherratt MJ, Shuttleworth CA. Elastic fibres. J Cell Sci 2002;115(Pt 14):2817-28.
74. Chiquet-Ehrismann R, Hagios C, Matsumoto K. The tenascin gene family. Perspect Dev Neurobiol 1994;2:3-7.
75. Reinboth BJ, Finnis ML, Gibson MA, Sandberg LB, Cleary EG. Developmental expression of dermatan sulfate proteoglycans in the elastic bovine nuchal ligament. Matrix Biol 2000;19:149-62.
76. Reinboth B, Hanssen E, Cleary EG, Gibson MA. Molecular interactions of biglycan and decorin with elastic fiber components: biglycan forms a ternary complex with tropoelastin and microfibril-associated glycoprotein 1. J Biol Chem 2002;277:3950-7.
77. Trask BC, Trask TM, Broekelmann T, Mecham RP. The microfibrillar proteins MAGP-1 and fibrillin-1 form a ternary complex with the chondroitin sulfate proteoglycan decorin. Mol Biol Cell 2000;11:1499-507.
78. Baccarani-Contri M, Vincenzi D, Cicchetti F, Mori G, Pasquali-Ronchetti I. Immunocytochemical localization of proteogiycans within normal elastin fibers. Eur J Cell Biol 1990;53:305-12.
79. Lethias C, Elefteriou F, Parsiegla G, Exposito JY, Garrone R. Identification and characterization of a conformational heparin-binding site involving two fibronectin type III modules of bovine tenascin-X. J Biol Chem 2001;276:16432-8.
80. Grahame R, Pyeritz RE. The Marfan syndrome: joint and skin manifestations are prevalent and correlated. Br J Rheumatol 1995;34:126-31.