Mineralizing enthesopathy is a common feature of renal phosphate-wasting disorders attributed to FGF23 and is exacerbated by standard therapy in hyp mice

Endocrinology

Volumn 153, Issue 12, 2012, Pages 5906-5917

  Karaplis, Andrew C ^a   Bai, Xiuying ^b   Falet, Jean Pierre ^a   Macica, Carolyn M ^c  

^a MCGILL UNIVERSITY   (Canada)

^b MCGILL UNIVERSITY   (Canada)

^c YALE UNIVERSITY SCHOOL OF MEDICINE   (United States)

Author keywords

[No Author keywords available]

Indexed keywords

CALCITRIOL; COMPLEMENTARY DNA; DENTIN MATRIX PROTEIN 1; FIBROBLAST GROWTH FACTOR 23; PHOSPHATE;

ACHILLES TENDON; ADULT; ANIMAL EXPERIMENT; ANIMAL MODEL; ANIMAL TISSUE; ARTICLE; CARTILAGE CELL; CASE REPORT; CONTROLLED STUDY; DISEASE EXACERBATION; ENTHESOPATHY; GENE MUTATION; HUMAN; MALE; MINERALIZATION; MOUSE; NONHUMAN; PRIORITY JOURNAL; X LINKED HYPOPHOSPHATEMIC RICKETS;

ANIMALS; EXTRACELLULAR MATRIX PROTEINS; FEMALE; FIBROBLAST GROWTH FACTORS; HYPOPHOSPHATEMIC RICKETS, X-LINKED DOMINANT; IMMUNOHISTOCHEMISTRY; KIDNEY; MALE; MICE; MICE, INBRED C57BL; MICE, TRANSGENIC; MODELS, GENETIC; MUTATION; PEDIGREE; PHOSPHATES; PHOSPHOPROTEINS; RHEUMATIC DISEASES; TRANSGENES; UP-REGULATION;

EID: 84870168690     PISSN: 00137227     EISSN: 19457170     Source Type: Journal    
DOI: 10.1210/en.2012-1551     Document Type: Article

References (64)

1. Eicher EM, Southard JL, Scriver CR, Glorieux FH 1976 Hypophosphatemia: mouse model for human familial hypophosphatemic (vitamin D-resistant) rickets. Proc Natl Acad Sci USA 73:4667-4671
2. Liu S, Guo R, Simpson LG, Xiao ZS, Burnham CE, Quarles LD 2003 Regulation of fibroblastic growth factor 23 expression but not degradation by PHEX. J Biol Chem 278:37419-37426
3. Bowe AE, Finnegan R, Jan de Beur SM, Cho J, Levine MA, Kumar R, Schiavi SC 2001 FGF-23 inhibits renal tubular phosphate transport and is a PHEX substrate. Biochem Biophys Res Commun 284:977-981
4. Liu S, Tang W, Zhou J, Stubbs JR, Luo Q, Pi M, Quarles LD 2006 Fibroblast growth factor 23 is a counter-regulatory phosphaturic hormone for vitamin D. J Am Soc Nephrol 17:1305-1315
5. Liu S, Vierthaler L, Tang W, Zhou J, Quarles LD 2008 FGFR3 and FGFR4 do not mediate renal effects of FGF23. J Am Soc Nephrol 19:2342-2350
6. Saito H, Kusano K, Kinosaki M, Ito H, Hirata M, Segawa H, Miyamoto K, Fukushima N 2003 Human fibroblast growth factor-23 mutants suppress Na+-dependent phosphate co-transport activity and 1α,25-dihydroxyvitamin D3 production. J Biol Chem 278:2206-2211
7. Urakawa I, Yamazaki Y, Shimada T, Iijima K, Hasegawa H, Okawa K, Fujita T, Fukumoto S, Yamashita T 2006 Klotho converts canonical FGF receptor into a specific receptor for FGF23. Nature 444:770-774
8. Brownstein CA, Zhang J, Stillman A, Ellis B, Troiano N, Adams DJ, Gundberg CM, Lifton RP, Carpenter TO 2010 Increased bone volume and correction of HYP mouse hypophosphatemia in the Klotho/HYP mouse. Endocrinology 151:492-501
9. Kurosu H, Ogawa Y, Miyoshi M, Yamamoto M, Nandi A, Rosenblatt KP, Baum MG, Schiavi S, Hu MC, Moe OW, Kuro-o M 2006 Regulation of fibroblast growth factor-23 signaling by klotho. J Biol Chem 281:6120-6123
10. Feng JQ, Ward LM, Liu S, Lu Y, Xie Y, Yuan B, Yu X, Rauch F, Davis SI, Zhang S, Rios H, Drezner MK, Quarles LD, Bonewald LF, White KE 2006 Loss of DMP1 causes rickets and osteomalacia and identifies a role for osteocytes in mineral metabolism. Nat Genet 38:1310-1315
11. Fukumoto S, Yamashita T 2002 Fibroblast growth factor-23 is the phosphaturic factor in tumor-induced osteomalacia and may be phosphatonin. Curr Opin Nephrol Hypertens 11:385-389
12. Lorenz-Depiereux B, Bastepe M, Benet-Pagès A, Amyere M, Wagenstaller J, Müller-Barth U, Badenhoop K, Kaiser SM, Rittmaster RS, Shlossberg AH, Olivares JL, Loris C, Ramos FJ, Glorieux F, Vikkula M, Jüppner H, Strom TM 2006 DMP1 mutations in autosomal recessive hypophosphatemia implicate a bone matrix protein in the regulation of phosphate homeostasis. Nat Genet 38:1248-1250
13. White KE, Carn G, Lorenz-Depiereux B, Benet-Pages A, Strom TM, Econs MJ 2001 Autosomal-dominant hypophosphatemic rickets (ADHR) mutations stabilize FGF-23. Kidney Int 60:2079-2086
14. Yu X, White KE 2005 FGF23 and disorders of phosphate homeostasis. Cytokine Growth Factor Rev 16:221-232
15. Saito T, Shimizu Y, Hori M, Taguchi M, Igarashi T, Fukumoto S, Fujitab T 2011 A patient with hypophosphatemic rickets and ossification of posterior longitudinal ligament caused by a novel homozygous mutation in ENPP1 gene. Bone 49:913-916
16. Holm IA, Econs MJ, T. O. C 2003 Familial hypophosphatemia and related disorders. In: Glorieux F, Juppner H, Pettifor JM, eds. Pediatric bone: biology, diseases. San Diego: Academic Press; 603-631
17. Francis F, Strom TM, Hennig S, Böddrich A, Lorenz B, Brandau O, Mohnike KL, Cagnoli M, Steffens C, Klages S, Borzym K, Pohl T, Oudet C, Econs MJ, Rowe PS, Reinhardt R, Meitinger T, Lehrach H 1997 Genomic organization of the human PEX gene mutated in X-linked dominant hypophosphatemic rickets. Genome Res 7:573-585
18. Wang L, Du L, Ecarot B 1999 Evidence for Phex haploinsufficiency in murine X-linked hypophosphatemia. Mamm Genome 10:385-389
19. Carpenter TO, Imel EA, Holm IA, Jan de Beur SM, Insogna KL 2011 A clinician's guide to X-linked hypophosphatemia. J Bone Miner Res 26:1381-1388
20. Burnstein MI, Lawson JP, Kottamasu SR, Ellis BI, Micho J 1989 The enthesopathic changes of hypophosphatemic osteomalacia in adults: radiologic findings. AJR Am J Roentgenol 153:785-790
21. Polisson RP, Martinez S, Khoury M, Harrell RM, Lyles KW, Friedman N, Harrelson JM, Reisner E, Drezner MK 1985 Calcification of entheses associated with X-linked hypophosphatemic osteomalacia. N Engl J Med 313:1-6
22. Hardy DC, Murphy WA, Siegel BA, Reid IR, Whyte MP 1989 X-linked hypophosphatemia in adults: prevalence of skeletal radiographic and scintigraphic features. Radiology 171:403-414
23. Jacobson JA, Kalume-Brigido M 2006 Case 97: X-linked hypophosphatemic osteomalacia with insufficiency fracture. Radiology 240:607-610
24. Ramonda R, Sfriso P, Podswiadek M, Oliviero F, Valvason C, Punzi L 2005 [The enthesopathy of vitamin D-resistant osteomalacia in adults]. Reumatismo 57:52-56
25. Reid IR, Hardy DC, Murphy WA, Teitelbaum SL, Bergfeld MA, Whyte MP 1989 X-linked hypophosphatemia: a clinical, biochemical, and histopathologic assessment of morbidity in adults. Medicine 68:336-352
26. Van de Wiele C, Dierckx RA, Weynants L, Simons M, Kaufman JM 1996 Whole-body bone scan findings in X-linked hypophosphatemia. Clin Nucl Med 21:483
27. Yost JH, Spencer-Green G, Brown LA 1994 Radiologic vignette. X-linked hypophosphatemia (familial vitamin D-resistant rickets). Arthritis Rheum 37:435-438
28. Liang G, Katz LD, Insogna KL, Carpenter TO, Macica CM 2009 Survey of the enthesopathy of X-linked hypophosphatemia and its characterization in Hyp mice. Calcif Tissue Int 85:235-246
29. Soehle M, Casey AT 2002 Cervical spinal cord compression attributable to a calcified intervertebral disc in a patient with X-linked hypophosphatemic rickets: case report and review of the literature. Neurosurgery 51:239-242; discussion 242-233
30. Glorieux FH, Marie PJ, Pettifor JM, Delvin EE 1980 Bone response to phosphate salts, ergocalciferol, and calcitriol in hypophosphatemic vitamin D-resistant rickets. N Engl J Med 303:1023-1031
31. Sullivan W, Carpenter T, Glorieux F, Travers R, Insogna K 1992 A prospective trial of phosphate and 1,25-dihydroxyvitamin D3 therapy in symptomatic adults with X-linked hypophosphatemic rickets. J Clin Endocrinol Metab 75:879-885
32. Mäkitie O, Pereira RC, Kaitila I, Turan S, Bastepe M, Laine T, Kröger H, Cole WG, Jüppner H 2010 Long-term clinical outcome and carrier phenotype in autosomal recessive hypophosphatemia caused by a novel DMP1 mutation. J Bone Miner Res 25:2165-2174
33. Miao D, Bai X, Panda DK, Karaplis AC, Goltzman D, McKee MD 2004 Cartilage abnormalities are associated with abnormal Phex expression and with altered matrix protein and MMP-9 localization in Hyp mice. Bone 34:638-647
34. Thompson DL, Sabbagh Y, Tenenhouse HS, Roche PC, Drezner MK, Salisbury JL, Grande JP, Poeschla EM, Kumar R 2002 Ontogeny of Phex/PHEX protein expression in mouse embryo and subcellular localization in osteoblasts. J Bone Miner Res 17:311-320
35. Benjamin M, Ralphs JR 2000 The cell and developmental biology of tendons and ligaments. Int Rev Cytol 196:85-130
36. Benjamin M, Toumi H, Ralphs JR, Bydder G, Best TM, Milz S 2006 Where tendons and ligaments meet bone: attachment sites ('entheses') in relation to exercise and/or mechanical load. J Anat 208:471-490
37. Liu S, Brown TA, Zhou J, Xiao ZS, Awad H, Guilak F, Quarles LD 2005 Role of matrix extracellular phosphoglycoprotein in the pathogenesis of X-linked hypophosphatemia. J Am Soc Nephrol 16:1645-1653
38. Liu S, Zhou J, Tang W, Jiang X, Rowe DW, Quarles LD 2006 Pathogenic role of Fgf23 in Hyp mice. Am J Physiol Endocrinol Metab 291:E38-E49
39. Bai X, Miao D, Li J, Goltzman D, Karaplis AC 2004 Transgenic mice overexpressing human fibroblast growth factor 23 (R176Q) delineate a putative role for parathyroid hormone in renal phosphate wasting disorders. Endocrinology 145:5269-5279
40. Liang G, Vanhouten J, Macica CM 2011 An atypical degenerative osteoarthropathy in Hyp mice is characterized by a loss in the mineralized zone of articular cartilage. Calcif Tissue Int 89:151-162
41. Benjamin M, Kumai T, Milz S, Boszczyk BM, Boszczyk AA, Ralphs JR 2002 The skeletal attachment of tendons - tendon "entheses."Comp Biochem Physiol 133:931-945
42. de Bernard B, Bianco P, Bonucci E, Costantini M, Lunazzi GC, Martinuzzi P, Modricky C, Moro L, Panfili E, Pollesello P, et al. 1986 Biochemical and immunohistochemical evidence that in cartilage an alkaline phosphatase is a Ca2+-binding glycoprotein. J Cell Biol 103:1615-1623
43. Rufai A, Benjamin M, Ralphs JR 1992 Development and ageing of phenotypically distinct fibrocartilages associated with the rat Achilles tendon. Anat Embryol 186:611-618
44. Gao J, Messner K, Ralphs JR, Benjamin M 1996 An immunohistochemical study of enthesis development in the medial collateral ligament of the rat knee joint. Anat Embryol 194:399-406
45. Brown DC, Vogel KG 1989 Characteristics of the in vitro interaction of a small proteoglycan (PG II) of bovine tendon with type I collagen. Matrix 9:468-478
46. Vogel KG 2004 What happens when tendons bend and twist? Proteoglycans. J Musculoskelet Neuronal Interact 4:202-203
47. Benjamin M, Ralphs JR 1998 Fibrocartilage in tendons and ligaments - an adaptation to compressive load. J Anat 193 ( Pt 4):481-494
48. Waggett AD, Ralphs JR, Kwan AP, Woodnutt D, Benjamin M 1998 Characterization of collagens and proteoglycans at the insertion of the human Achilles tendon. Matrix Biol 16:457-470
49. Lu XL, Miller C, Chen FH, Guo XE, Mow VC 2007 The generalized triphasic correspondence principle for simultaneous determination of the mechanical properties and proteoglycan content of articular cartilage by indentation. J Biomech 40:2434-2441
50. Lu XL, Mow VC, Guo XE 2009 Proteoglycans and mechanical behavior of condylar cartilage. J Dent Res 88:244-248
51. Lu XL, Sun DD, Guo XE, Chen FH, Lai WM, Mow VC 2004 Indentation determined mechanoelectrochemical properties and fixed charge density of articular cartilage. Ann Biomed Eng 32:370-379
52. Carpenter TO, Keller M, Schwartz D, Mitnick M, Smith C, Ellison A, Carey D, Comite F, Horst R, Travers R, Glorieux FH, Gundberg CM, Poole AR, Insogna KL 1996 24,25 Dihydroxyvitamin D supplementation corrects hyperparathyroidism and improves skeletal abnormalities in X-linked hypophosphatemic rickets - a clinical research center study. J Clin Endocrinol Metab 81:2381-2388
53. Adams JE, Davies M 1986 Intra-spinal new bone formation and spinal cord compression in familial hypophosphataemic vitamin D resistant osteomalacia. Q J Med 61:1117-1129
54. Dugger GS, Vandiver RW 1966 Spinal cord compression caused by vitamin D resistant rickets. J Neurosurg 25:300-303
55. Dunlop DJ, Stirling AJ 1996 Thoracic spinal cord compression caused by hypophosphataemic rickets: a case report and review of the world literature. Eur Spine J 5:272-274
56. Highman JH, Sanderson PH, Sutcliffe MM 1970 Vitamin-D-resistant osteomalacia as a cause of cord compression. QJ Med 39:529-537
57. Johnston Jr CC, Kurlander GJ, Smith DM, Goodman JM, Campbell RL 1966 Familial vitamin D resistant rickets in untreated adult. Bony proliferation of neural arches with cord compression. Arch Intern Med 117:141-147
58. Yoshikawa S, Shiba M, Suzuki A 1968 Spinal-cord compression in untreated adult cases of vitamin-D resistant rickets. J Bone Joint Surg Am 50:743-752
59. Vogel KG, Peters JA 2005 Histochemistry defines a proteoglycan-rich layer in bovine flexor tendon subjected to bending. J Musculoskelet Neuronal Interact 5:64-69
60. Kolek OI, Hines ER, Jones MD, LeSueur LK, Lipko MA, Kiela PR, Collins JF, Haussler MR, Ghishan FK 2005 1α,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 289:G1036-G1042
61. Perwad F, Azam N, Zhang MY, Yamashita T, Tenenhouse HS, Portale AA 2005 Dietary and serum phosphorus regulate fibroblast growth factor 23 expression and 1,25-dihydroxyvitamin d metabolism in mice. Endocrinology 146:5358-5364
62. Benjamin M, Ralphs JR 2001 Entheses - the bony attachments of tendons and ligaments. Ital J Anat Embryol 106:151-157
63. Thomopoulos S, Kim HM, Rothermich SY, Biederstadt C, Das R, Galatz LM 2007 Decreased muscle loading delays maturation of the tendon enthesis during postnatal development. J Orthop Res 25:1154-1163
64. Aono Y, Yamazaki Y, Yasutake J, Kawata T, Hasegawa H, Urakawa I, Fujita T, Wada M, Yamashita T, Fukumoto S, Shimada T 2009 Therapeutic effects of anti-FGF23 antibodies in hypophosphatemic rickets/osteomalacia. J Bone Miner Res 24:1879-1888