Articular cartilage calcification in osteoarthritis: Insights into crystal-induced stress

Arthritis and Rheumatism

Volumn 63, Issue 1, 2011, Pages 10-18

  Ea, Hang Korng ^a   Nguyen, Christelle ^a   Bazin, Dominique ^b   Bianchi, Arnaud ^c   Guicheux, Jérôme ^d   Reboul, Pascal ^c   Daudon, Michel ^e   Lioté, Frédéric ^a  

^a INSERM   (France)

^b UNIVERSITÉ PARIS SACLAY   (France)

^c UNIVERSITÉ DE LORRAINE   (France)

^d Universite de Nantes   (France)

^e HÔPITAL NECKER ENFANTS MALADES   (France)

Author keywords

[No Author keywords available]

Indexed keywords

CALCIUM PHOSPHATE; CALCIUM PYROPHOSPHATE; OSTEOCALCIN;

ARTICULAR CARTILAGE; ARTICULAR CARTILAGE CALCIFICATION; CALCIFICATION; CARTILAGE CELL; CHONDROCALCINOSIS; CLINICAL ASSESSMENT; CYTOKINE PRODUCTION; DISEASE ASSOCIATION; EXTRACELLULAR MATRIX; HUMAN; IN VITRO STUDY; JOINT DEGENERATION; JOINT SWELLING; MUTATION; NONHUMAN; OSTEOARTHRITIS; PRIORITY JOURNAL; REVIEW; RHEUMATOID ARTHRITIS;

CALCINOSIS; CARTILAGE, ARTICULAR; HUMANS; JOINTS; OSTEOARTHRITIS;

EID: 78650781142     PISSN: 00043591     EISSN: 15290131     Source Type: Journal    
DOI: 10.1002/art.27761     Document Type: Review

References (77)

1. Arden N, Nevitt MC,. Osteoarthritis: epidemiology. Best Pract Res Clin Rheumatol 2006; 20: 3-25.
2. Hunter DJ, Felson DT,. Osteoarthritis. BMJ 2006; 332: 639-42.
3. McCarthy GM, Cheung HS,. Point: hydroxyapatite crystal deposition is intimately involved in the pathogenesis and progression of human osteoarthritis. Curr Rheumatol Rep 2009; 11: 141-7.
4. Pritzker KP,. Counterpoint: hydroxyapatite crystal deposition is not intimately involved in the pathogenesis and progression of human osteoarthritis. Curr Rheumatol Rep 2009; 11: 148-53.
5. McCarty DJ, Lehr JR, Halverson PB,. Crystal populations in human synovial fluid: identification of apatite, octacalcium phosphate, and tricalcium phosphate. Arthritis Rheum 1983; 26: 1220-4.
6. Scotchford CA, Ali SY,. Magnesium whitlockite deposition in articular cartilage: a study of 80 specimens from 70 patients. Ann Rheum Dis 1995; 54: 339-44.
7. Mitsuyama H, Healey RM, Terkeltaub RA, Coutts RD, Amiel D,. Calcification of human articular knee cartilage is primarily an effect of aging rather than osteoarthritis. Osteoarthritis Cartilage 2007; 15: 559-65.
8. Gordon GV, Villanueva T, Schumacher HR, Gohel V,. Autopsy study correlating degree of osteoarthritis, synovitis and evidence of articular calcification. J Rheumatol 1984; 11: 681-6.
9. Kirsch T, Swoboda B, Nah H,. Activation of annexin II and V expression, terminal differentiation, mineralization and apoptosis in human osteoarthritic cartilage. Osteoarthritis Cartilage 2000; 8: 294-302.
10. Fuerst M, Bertrand J, Lammers L, Dreier R, Echtermeyer F, Nitschke Y, et al. Calcification of articular cartilage in human osteoarthritis. Arthritis Rheum 2009; 60: 2694-703.
11. Fuerst M, Niggemeyer O, Lammers L, Schafer F, Lohmann C, Ruther W,. Articular cartilage mineralization in osteoarthritis of the hip. BMC Musculoskelet Disord 2009; 10: 166.
12. Nguyen C, Ea HK, Meyer M, Weil R, Nizard R, Daudon M, et al. Diversité chimique et morphologique des cristaux calciques dans le cartilage humain arthrosique. Rev Rhum 2009; 76: 986-7.
13. Scotchford CA, Greenwald S, Ali SY,. Calcium phosphate crystal distribution in the superficial zone of human femoral head articular cartilage. J Anat 1992; 181: 293-300.
14. Nalbant S, Martinez JA, Kitumnuaypong T, Clayburne G, Sieck M, Schumacher HR Jr., Synovial fluid features and their relations to osteoarthritis severity: new findings from sequential studies. Osteoarthritis Cartilage 2003; 11: 50-4.
15. McCarty DJ Jr, Hogan JM, Gatter RA, Grossman M,. Studies on pathological calcifications in human cartilage. I. Prevalence and types of crystal deposits in the menisci of two hundred fifteen cadavera. J Bone Joint Surg Am 1966; 48: 309-25.
16. Mitrovic DR,. Pathology of articular deposition of calcium salts and their relationship to osteoarthrosis. Ann Rheum Dis 1983; 42 Suppl 1: 19-26.
17. Macmullan PA, McCarthy GM,. The meniscus, calcification and osteoarthritis: a pathologic team. Arthritis Res Ther 2010; 12: 116.
18. Sun Y, Mauerhan DR, Honeycutt PR, Kneisl JS, Norton HJ, Zinchenko N, et al. Calcium deposition in osteoarthritic meniscus and meniscal cell culture. Arthritis Res Ther 2010; 12: R56.
19. Bendele AM, White SL,. Early histopathologic and ultrastructural alterations in femorotibial joints of partial medial meniscectomized guinea pigs. Vet Pathol 1987; 24: 436-43.
20. Evans RG, Collins C, Miller P, Ponsford FM, Elson CJ,. Radiological scoring of osteoarthritis progression in STR/ORT mice. Osteoarthritis Cartilage 1994; 2: 103-9.
21. Magne D, Bluteau G, Faucheux C, Palmer G, Vignes-Colombeix C, Pilet P, et al. Phosphate is a specific signal for ATDC5 chondrocyte maturation and apoptosis-associated mineralization: possible implication of apoptosis in the regulation of endochondral ossification. J Bone Miner Res 2003; 18: 1430-42.
22. Ea HK, Liote F,. Advances in understanding calcium-containing crystal disease. Curr Opin Rheumatol 2009; 21: 150-7.
23. Terkeltaub RA,. What does cartilage calcification tell us about osteoarthritis? J Rheumatol 2002; 29: 411-5.
24. Chen CC, Boskey AL, Rosenberg LC,. The inhibitory effect of cartilage proteoglycans on hydroxyapatite growth. Calcif Tissue Int 1984; 36: 285-90.
25. Kirsch T, Nah HD, Shapiro IM, Pacifici M,. Regulated production of mineralization-competent matrix vesicles in hypertrophic chondrocytes. J Cell Biol 1997; 137: 1149-60.
26. Derfus B, Steinberg M, Mandel N, Buday M, Daft L, Ryan L,. Characterization of an additional articular cartilage vesicle fraction that generates calcium pyrophosphate dihydrate crystals in vitro. J Rheumatol 1995; 22: 1514-9.
27. Hashimoto S, Ochs RL, Rosen F, Quach J, McCabe G, Solan J, et al. Chondrocyte-derived apoptotic bodies and calcification of articular cartilage. Proc Natl Acad Sci U S A 1998; 95: 3094-9.
28. Anderson HC,. Molecular biology of matrix vesicles. Clin Orthop Relat Res 1995: 266-80.
29. Jubeck B, Gohr C, Fahey M, Muth E, Matthews M, Mattson E, et al. Promotion of articular cartilage matrix vesicle mineralization by type I collagen. Arthritis Rheum 2008; 58: 2809-17.
30. Julien M, Magne D, Masson M, Rolli-Derkinderen M, Chassande O, Cario-Toumaniantz C, et al. Phosphate stimulates matrix Gla protein expression in chondrocytes through the extracellular signal regulated kinase signaling pathway. Endocrinology 2007; 148: 530-7.
31. Terkeltaub RA,. Inorganic pyrophosphate generation and disposition in pathophysiology. Am J Physiol Cell Physiol 2001; 281: C1-11.
32. Thouverey C, Bechkoff G, Pikula S, Buchet R,. Inorganic pyrophosphate as a regulator of hydroxyapatite or calcium pyrophosphate dihydrate mineral deposition by matrix vesicles. Osteoarthritis Cartilage 2009; 17: 64-72.
33. Ho AM, Johnson MD, Kingsley DM,. Role of the mouse ank gene in control of tissue calcification and arthritis. Science 2000; 289: 265-70.
34. Johnson K, Vaingankar S, Chen Y, Moffa A, Goldring MB, Sano K, et al. Differential mechanisms of inorganic pyrophosphate production by plasma cell membrane glycoprotein-1 and B10 in chondrocytes. Arthritis Rheum 1999; 42: 1986-97.
35. Rosenthal AK, Cheung HS, Ryan LM,. Transforming growth factor β1 stimulates inorganic pyrophosphate elaboration by porcine cartilage. Arthritis Rheum 1991; 34: 904-11.
36. Rosen F, McCabe G, Quach J, Solan J, Terkeltaub R, Seegmiller JE, et al. Differential effects of aging on human chondrocyte responses to transforming growth factor β: increased pyrophosphate production and decreased cell proliferation. Arthritis Rheum 1997; 40: 1275-81.
37. Hirose J, Ryan LM, Masuda I,. Up-regulated expression of cartilage intermediate-layer protein and ANK in articular hyaline cartilage from patients with calcium pyrophosphate dihydrate crystal deposition disease. Arthritis Rheum 2002; 46: 3218-29.
38. Cailotto F, Bianchi A, Sebillaud S, Venkatesan N, Moulin D, Jouzeau JY, et al. Inorganic pyrophosphate generation by transforming growth factor-β-1 is mainly dependent on ANK induction by Ras/Raf-1/extracellular signal-regulated kinase pathways in chondrocytes. Arthritis Res Ther 2007; 9: R122.
39. Johnson K, Hashimoto S, Lotz M, Pritzker K, Terkeltaub R,. Interleukin-1 induces pro-mineralizing activity of cartilage tissue transglutaminase and factor XIIIa. Am J Pathol 2001; 159: 149-63.
40. Okawa A, Nakamura I, Goto S, Moriya H, Nakamura Y, Ikegawa S,. Mutation in Npps in a mouse model of ossification of the posterior longitudinal ligament of the spine. Nat Genet 1998; 19: 271-3. (Pubitemid 28309341)
41. Rutsch F, Ruf N, Vaingankar S, Toliat MR, Suk A, Hohne W, et al. Mutations in ENPP1 are associated with 'idiopathic' infantile arterial calcification. Nat Genet 2003; 34: 379-81.
42. Rutsch F, Vaingankar S, Johnson K, Goldfine I, Maddux B, Schauerte P, et al. PC-1 nucleoside triphosphate pyrophosphohydrolase deficiency in idiopathic infantile arterial calcification. Am J Pathol 2001; 158: 543-54.
43. Pendleton A, Johnson MD, Hughes A, Gurley KA, Ho AM, Doherty M, et al. Mutations in ANKH cause chondrocalcinosis. Am J Hum Genet 2002; 71: 933-40.
44. Williams CJ,. Familial calcium pyrophosphate dihydrate deposition disease and the ANKH gene. Curr Opin Rheumatol 2003; 15: 326-31.
45. Rutsch F, Terkeltaub R,. Deficiencies of physiologic calcification inhibitors and low-grade inflammation in arterial calcification: lessons for cartilage calcification. Joint Bone Spine 2005; 72: 110-8. (Pubitemid 41388961)
46. Luo G, Ducy P, McKee MD, Pinero GJ, Loyer E, Behringer RR, et al. Spontaneous calcification of arteries and cartilage in mice lacking matrix GLA protein. Nature 1997; 386: 78-81.
47. Zebboudj AF, Imura M, Bostrom K,. Matrix GLA protein, a regulatory protein for bone morphogenetic protein-2. J Biol Chem 2002; 277: 4388-94.
48. Zebboudj AF, Shin V, Bostrom K,. Matrix GLA protein and BMP-2 regulate osteoinduction in calcifying vascular cells. J Cell Biochem 2003; 90: 756-65.
49. Munroe PB, Olgunturk RO, Fryns JP, Van Maldergem L, Ziereisen F, Yuksel B, et al. Mutations in the gene encoding the human matrix Gla protein cause Keutel syndrome. Nat Genet 1999; 21: 142-4.
50. Sauer GR, Wuthier RE,. Fourier transform infrared characterization of mineral phases formed during induction of mineralization by collagenase-released matrix vesicles in vitro. J Biol Chem 1988; 263: 13718-24.
51. Pritzker KP, Chateauvert JM, Grynpas MD,. Osteoarthritic cartilage contains increased calcium, magnesium and phosphorus. J Rheumatol 1987; 14: 806-10.
52. Bonen DK, Schmid TM,. Elevated extracellular calcium concentrations induce type X collagen synthesis in chondrocyte cultures. J Cell Biol 1991; 115: 1171-8.
53. Gigout A, Jolicoeur M, Buschmann MD,. Low calcium levels in serum-free media maintain chondrocyte phenotype in monolayer culture and reduce chondrocyte aggregation in suspension culture. Osteoarthritis Cartilage 2005; 13: 1012-24.
54. Garancis JC, Cheung HS, Halverson PB, McCarty DJ,. "Milwaukee shoulder" âassociation of microspheroids containing hydroxyapatite crystals, active collagenase, and neutral protease with rotator cuff defects. III. Morphologic and biochemical studies of an excised synovium showing chondromatosis. Arthritis Rheum 1981; 24: 484-91.
55. Halverson PB, Cheung HS, McCarty DJ, Garancis J, Mandel N,. "Milwaukee shoulder"âassociation of microspheroids containing hydroxyapatite crystals, active collagenase, and neutral protease with rotator cuff defects. II. Synovial fluid studies. Arthritis Rheum 1981; 24: 474-83.
56. McCarty DJ, Halverson PB, Carrera GF, Brewer BJ, Kozin F,. "Milwaukee shoulder"âassociation of microspheroids containing hydroxyapatite crystals, active collagenase, and neutral protease with rotator cuff defects. I. Clinical aspects. Arthritis Rheum 1981; 24: 464-73.
57. Dieppe PA, Crocker P, Huskisson EC, Willoughby DA,. Apatite deposition disease: a new arthropathy. Lancet 1976; 1: 266-9.
58. Pons-Estel BA, Gimenez C, Sacnun M, Gentiletti S, Battagliotti CA, de la Pena LS, et al. Familial osteoarthritis and Milwaukee shoulder associated with calcium pyrophosphate and apatite crystal deposition. J Rheumatol 2000; 27: 471-80.
59. Muehleman C, Li J, Aigner T, Rappoport L, Mattson E, Hirschmugl C, et al. Association between crystals and cartilage degeneration in the ankle. J Rheumatol 2008; 35: 1108-17.
60. Fam AG, Morava-Protzner I, Purcell C, Young BD, Bunting PS, Lewis AJ,. Acceleration of experimental lapine osteoarthritis by calcium pyrophosphate microcrystalline synovitis. Arthritis Rheum 1995; 38: 201-10.
61. Cheung HS, Sallis JD, Demadis KD, Wierzbicki A,. Phosphocitrate blocks calcification-induced articular joint degeneration in a guinea pig model. Arthritis Rheum 2006; 54: 2452-61.
62. Ea HK, Uzan B, Rey C, Liote F,. Octacalcium phosphate crystals directly stimulate expression of inducible nitric oxide synthase through p38 and JNK mitogen-activated protein kinases in articular chondrocytes. Arthritis Res Ther 2005; 7: R915-26.
63. Ea HK, Monceau V, Camors E, Cohen-Solal M, Charlemagne D, Liote F,. Annexin 5 overexpression increased articular chondrocyte apoptosis induced by basic calcium phosphate crystals. Ann Rheum Dis 2008; 67: 1617-25.
64. Liu-Bryan R, Pritzker K, Firestein GS, Terkeltaub R,. TLR2 signaling in chondrocytes drives calcium pyrophosphate dihydrate and monosodium urate crystal-induced nitric oxide generation. J Immunol 2005; 174: 5016-23.
65. Liu-Bryan R, Scott P, Sydlaske A, Rose DM, Terkeltaub R,. Innate immunity conferred by Toll-like receptors 2 and 4 and myeloid differentiation factor 88 expression is pivotal to monosodium urate monohydrate crystal-induced inflammation. Arthritis Rheum 2005; 52: 2936-46.
66. Grandjean-Laquerriere A, Tabary O, Jacquot J, Richard D, Frayssinet P, Guenounou M, et al. Involvement of Toll-like receptor 4 in the inflammatory reaction induced by hydroxyapatite particles. Biomaterials 2007; 28: 400-4.
67. Martinon F, Petrilli V, Mayor A, Tardivel A, Tschopp J,. Gout-associated uric acid crystals activate the NALP3 inflammasome. Nature 2006; 440: 237-41.
68. Asplin JR, Donahue SE, Lindeman C, Michalenka A, Strutz KL, Bushinsky DA,. Thiosulfate reduces calcium phosphate nephrolithiasis. J Am Soc Nephrol 2009; 20: 1246-53.
69. Hall AH, Dart R, Bogdan G,. Sodium thiosulfate or hydroxocobalamin for the empiric treatment of cyanide poisoning? Ann Emerg Med 2007; 49: 806-13.
70. Hayden MR,. Calciphylaxis and the cardiometabolic syndrome: the emerging role of sodium thiosulfate as a novel treatment option. J Cardiometab Syndr 2008; 3: 55-9.
71. Hayden MR, Goldsmith D, Sowers JR, Khanna R,. Calciphylaxis: calcific uremic arteriolopathy and the emerging role of sodium thiosulfate. Int Urol Nephrol 2008; 40: 443-51.
72. Pasch A, Schaffner T, Huynh-Do U, Frey BM, Frey FJ, Farese S,. Sodium thiosulfate prevents vascular calcifications in uremic rats. Kidney Int 2008; 74: 1444-53.
73. Yatzidis H,. Successful sodium thiosulphate treatment for recurrent calcium urolithiasis. Clin Nephrol 1985; 23: 63-7.
74. Meissner M, Kaufmann R, Gille J,. Sodium thiosulphate: a new way of treatment for calciphylaxis? Dermatology 2007; 214: 278-82.
75. Glatz AC, Pawel BR, Hsu DT, Weinberg P, Chrisant MR,. Idiopathic infantile arterial calcification: two case reports, a review of the literature and a role for cardiac transplantation. Pediatr Transplant 2006; 10: 225-33.
76. Ramjan KA, Roscioli T, Rutsch F, Sillence D, Munns CF,. Generalized arterial calcification of infancy: treatment with bisphosphonates. Nat Clin Pract Endocrinol Metab 2009; 5: 167-72.
77. Rothschild B, Yakubov LE,. Prospective 6-month, double-blind trial of hydroxychloroquine treatment of CPDD. Compr Ther 1997; 23: 327-31.