1,25-Dihydroxyvitamin D3 and extracellular inorganic phosphate activate mitogen-activated protein kinase pathway through fibroblast growth factor 23 contributing to hypertrophy and mineralization in osteoarthritic chondrocytes

Experimental Biology and Medicine

Volumn 237, Issue 3, 2012, Pages 241-253

  Orfanidou, Timoklia ^a,b   Malizos, Konstantinos N ^a,b   Varitimidis, Sokratis ^a   Tsezou, Aspasia ^a,b  

^a UNIVERSITY OF THESSALY   (Greece)

^b INSTITUTE OF HUMAN PERFORMANCE AND REHABILITATION   (Greece)

Author keywords

1a,25(OH)2D3; ERK1 2; FGF23; Osteoarthritis; Phosphate; Phosphate inorganic transporter 1 and 2

Indexed keywords

CALCITRIOL; CASPASE 9; COLLAGENASE 3; FIBROBLAST GROWTH FACTOR 23; FIBROBLAST GROWTH FACTOR RECEPTOR 1; MESSENGER RNA; MITOGEN ACTIVATED PROTEIN KINASE; MITOGEN ACTIVATED PROTEIN KINASE 1; MITOGEN ACTIVATED PROTEIN KINASE 3; OSTEOCALCIN; OSTEOPONTIN; PHOSPHATE;

ADULT; AGED; ARTICLE; ARTICULAR CARTILAGE; BONE DEMINERALIZATION; CARTILAGE CELL; CHROMATIN IMMUNOPRECIPITATION; CLINICAL EVALUATION; ENZYME PHOSPHORYLATION; FEMALE; HUMAN; HUMAN CELL; HYPERTROPHY; MALE; MOLECULAR BIOLOGY; OSTEOARTHRITIS; PROTEIN BINDING; PROTEIN EXPRESSION; TOTAL KNEE REPLACEMENT; UPREGULATION;

AGED; BLOTTING, WESTERN; CALCINOSIS; CARTILAGE, ARTICULAR; CHONDROCYTES; FEMALE; FIBROBLAST GROWTH FACTORS; HUMANS; HYPERTROPHY; IMMUNOPRECIPITATION; MALE; MIDDLE AGED; MITOGEN-ACTIVATED PROTEIN KINASES; OLIGONUCLEOTIDE ARRAY SEQUENCE ANALYSIS; OSTEOARTHRITIS; PHOSPHATES; PROMOTER REGIONS, GENETIC; REAL-TIME POLYMERASE CHAIN REACTION; VITAMIN D; VITAMIN D RESPONSE ELEMENT;

EID: 84858783231     PISSN: 15353702     EISSN: 15353699     Source Type: Journal    
DOI: 10.1258/ebm.2011.011301     Document Type: Article

References (43)

1. Karpouzas GA, Terkeltaub RA. New developments in the pathogenesis of articular cartilage calcification. Curr Rheumatol Rep 1999;1:121-7
2. Arden N, Nevitt MC. Osteoarthritis: epidemiology. Best Pract Res Clin Rheumatol 2006;20:3-25
3. Kamekura S, Kawasaki Y, Hoshi K, Shimoaka T, Chikuda H, Maruyama Z, Komori T, Sato S, Takeda S, Karsenty G, Nakamura K, Chung UI, Kawaguchi H. Contribution of runt-related transcription factor 2 to the pathogenesis of osteoarthritis in mice after induction of knee joint instability. Arthritis Rheum 2006;54:2462-70
4. Pfander D, Swoboda B, Kirsch T. Expression of early and late differentiation markers (proliferating cell nuclear antigen, syndecan-3, annexin VI, and alkaline phosphatase) by human osteoarthritic chondrocytes. Am J Pathol 2001;159:1777-83
5. 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
6. Schwartz Z, Sylvia VL, Luna MH, DeVeau P, Whetstone R, Dean DD, Boyan BD. The effect of 24R,25-(OH)(2)D(3) on protein kinase C activity in chondrocytes is mediated by phospholipase D whereas the effect of 1alpha,25-(OH)(2)D(3) is mediated by phospholipase C. Steroids 2001;66:683-94
7. Denison TA, Koch CF, Shapiro IM, Schwartz Z, Boyan BD. Inorganic phosphate modulates responsiveness to 24,25(OH)2D3 in chondrogenic ATDC5 cells. J Cell Biochem 2009;107:155-62
8. Dean DD, Boyan BD, Muniz OE, Howell DS, Schwartz Z. Vitamin D metabolites regulate matrix vesicle metalloproteinase content in a cell maturation-dependent manner. Calcif Tissue Int 1996;59:109-16
9. Dean DD, Boyan BD, Schwart Z, Muniz OE, Carreno MR, Maeda S, Howell DS. Effect of 1alpha,25-dihydroxyvitamin D3 and 24R,25-dihydroxyvitamin D3 on metalloproteinase activity and cell maturation in growth plate cartilage in vivo. Endocrine 2001;14:311-23
10. Maeda S, Dean DD, Gay I, Schwartz Z, Boyan BD. Activation of latent transforming growth factor beta1 by stromelysin 1 in extracts of growth plate chondrocyte-derived matrix vesicles. J Bone Miner Res 2001;16:1281-90
11. Tetlow LC, Smith SJ, Mawer EB, Woolley DE. Vitamin D receptors in the rheumatoid lesion: expression by chondrocytes, macrophages, and synoviocytes. Ann Rheum Dis 1999;58:118-21
12. Whitfield GK, Jurutka PW, Haussler CA, Hsieh JC, Barthel TK, Jacobs ET, Dominguez CE, Thatcher ML, Haussler MR. Nuclear vitamin D receptor: structure-function, molecular control of gene transcription, and novel bioactions. In: Feldman D, Pike JW, Glorieux FH, eds. Vitamin D. Oxford, UK: Elsevier Academic Press, 2005:219-61
13. Julien M, Magne D, Masson M, Rolli-Derkinderen M, Chassande O, Cario-Toumaniantz C, Cherel Y, Weiss P, Guicheux J. Phosphate stimulates matrix Gla protein expression in chondrocytes through the extracellular signal regulated kinase signaling pathway. Endocrinology 2007;148:530-7
14. Terkeltaub RA. Inorganic pyrophosphate generation and disposition in pathophysiology. Am J Physiol Cell Physiol 2001;281:C1-C11
15. Ho AM, Johnson MD, Kingsley DM. Role of the mouse ank gene in control of tissue calcification and arthritis. Science 2000;289:265-70
16. Palmer G, Zhao J, Bonjour J, Hofstetter W, Caverzasio J. In vivo expression of transcripts encoding the Glvr-1 phosphate transporter/retrovirus receptor during bone development. Bone 1999;24:1-7
17. Cecil DL, Rose DM, Terkeltaub R, Liu-Bryan R. Role of interleukin-8 in PiT-1 expression and CXCR1-mediated inorganic phosphate uptake in chondrocytes. Arthritis Rheum 2005;52:144-54
18. Beck GR Jr, Moran E, Knecht N. Inorganic phosphate regulates multiple genes during osteoblast differentiation, including Nrf2. Exp Cell Res 2003;288:288-300
19. Beck GR Jr, Zerler B, Moran E. Phosphate is a specific signal for induction of osteopontin gene expression. Proc Natl Acad Sci USA 2000;97:8352-7
20. Bringhurst FR, Deway MB, Kronenberg HM. Hormones and disorders of mineral metabolism. In: Larsen PR, Kronenberg HM, Melmed S, eds. Williams Textbook of Endocrinology. Philadelphia: WB Saunders Company, 1998:1155-209
21. Fukumoto S. Physiological regulation and disorders of phosphate metabolism-pivotal role of fibroblast growth factor 23. Intern Med 2008;47:337-43
22. Mirams M, Robinson BG, Mason RS, Nelson AE. Bone as a source of FGF23: regulation by phosphate? Bone 2004;35:1192-9
23. Saito H, Maeda A, Ohtomo S, Hirata M, Kusano K, Kato S, Ogata E, Segawa H, Miyamoto K, Fukushima N. Circulating FGF-23 is regulated by 1alpha,25-dihydroxyvitamin D3 and phosphorus in vivo. J Biol Chem 2005;280:2543-9
24. Shimada T, Hasegawa H, Yamazaki Y, Muto T, Hino R, Takeuchi Y, Fujita T, Nakahara K, Fukumoto S, Yamashita T. FGF-23 is a potent regulator of vitamin D metabolism and phosphate homeostasis. J Bone Miner Res 2004;19:429-35
25. Quarles LD. Endocrine functions of bone in mineral metabolism regulation. J Clin Invest 2008;118:3820-8
26. Lanske B, Razzaque MS. Vitamin D and aging: old concepts and new insights. J Nutr Biochem 2007;18:771-7
27. Gattineni J, Bates C, Twombley K, Dwarakanath V, Robinson ML, Goetz R, Mohammadi M, Baum M. FGF23 decreases renal NaPi-2a and NaPi-2c expression and induces hypophosphatemia in vivo predominantly via FGF receptor 1. Am J Physiol Renal Physiol 2009;297:F282-91
28. Liu S, Vierthaler L, Tang W, Zhou J, Quarles LD. FGFR3 and FGFR4 do not mediate renal effects of FGF23. J Am Soc Nephrol 2008;19: 2342-50
29. Yu X, Ibrahimi OA, Goetz R, Zhang F, Davis SI, Garringer HJ, Linhardt RJ, Ornitz DM, Mohammadi M, White KE. Analysis of the biochemical mechanisms for the endocrine actions of fibroblast growth factor-23. Endocrinology 2005;146:4647-56
30. von der Mark K, Kirsch T, Nerlich A, Kuss A, Weseloh G, Gluckert K, Stoss H. Type X collagen synthesis in human osteoarthritic cartilage. Indication of chondrocyte hypertrophy. Arthritis Rheum 1992;35: 806-11
31. Ryan LM, McCarthy DJ. Calcium pyrophosphate crystal deposition disease, pseudogout and articular chondrocalcinosis. In: Koopman WJ, ed. Arthritis and Allied Conditions: A Textbook of Rheumatology. Baltimore: Williams and Wilkins, 1997: 2103-5
32. Fuerst M, Bertrand J, Lammers L, Dreier R, Echtermeyer F, Nitschke Y, Rutsch F, Schafer FK, Niggemeyer O, Steinhagen J, Lohmann CH, Pap T, Ruther W. Calcification of articular cartilage in human osteoarthritis. Arthritis Rheum 2009;60:2694-703
33. Kavanaugh MP, Kabat D. Identification and characterization of a widely expressed phosphate transporter/retrovirus receptor family. Kidney Int 1996;49:959-63
34. Kavanaugh MP, Miller DG, Zhang W, LawW, Kozak SL, Kabat D, Miller AD. Cell-surface receptors for gibbon ape leukemia virus and amphotropic murine retrovirus are inducible sodium-dependent phosphate symporters. Proc Natl Acad Sci USA 1994;91:7071-5
35. Sutton AL, MacDonald PN. Vitamin D: more than a 'bone-a-fide' hormone. Mol Endocrinol 2003;17:777-91
36. Tetlow LC, Adlam DJ, Woolley DE. Matrix metalloproteinase and proinflammatory cytokine production by chondrocytes of human osteoarthritic cartilage: associations with degenerative changes. Arthritis Rheum 2001;44:585-94
37. Sanchez CP, He YZ. Bone growth during daily or intermittent calcitriol treatment during renal failure with advanced secondary hyperparathyroidism. Kidney Int 2007;72:582-91
38. Orfanidou T, Iliopoulos D, Malizos KN, Tsezou A. Involvement of SOX-9 and FGF-23 in RUNX-2 regulation in osteoarthritic chondrocytes. J Cell Mol Med 2009;13:3186-94
39. Yu X, Sabbagh Y, Davis SI, Demay MB, White KE. Genetic dissection of phosphate-and vitamin D-mediated regulation of circulating Fgf23 concentrations. Bone 2005;36:971-7
40. Kolek OI, Hines ER, Jones MD, LeSueur LK, Lipko MA, Kiela PR, Collins JF, Haussler MR, Ghishan FK. 1alpha,25-Dihydroxyvitamin D3 upregulates FGF23 gene expression in bone: the final link in a renal-gastrointestinal-skeletal axis that controls phosphate transport. Am J Physiol Gastrointest Liver Physiol 2005;289:G1036-42
41. Provot S, Nachtrab G, Paruch J, Chen AP, Silva A, Kronenberg HM. A-raf and B-raf are dispensable for normal endochondral bone development, and parathyroid hormone-related peptide suppresses extracellular signal-regulated kinase activation in hypertrophic chondrocytes. Mol Cell Biol 2008;28:344-57
42. Canadillas S, Canalejo R, Rodriguez-Ortiz ME, Martinez-Moreno JM, Estepa JC, Zafra R, Perez J, Munoz-Castaneda JR, Canalejo A, Rodriguez M, Almaden Y. The up-regulation of the parathyroid VDR expression by extracellular calcium is mediated by the ERK1/2-MAPK signaling pathway. Am J Physiol Renal Physiol 2010 [Epub ahead of print]
43. Beck GR Jr, Knecht N. Osteopontin regulation by inorganic phosphate is ERK1/2-, protein kinase C-, and proteasome-dependent. J Biol Chem 2003;278:41921-9