The expanding family of hypophosphatemic syndromes

Journal of Bone and Mineral Metabolism

Volumn 30, Issue 1, 2012, Pages 1-9

  Carpenter, Thomas O ^a  

^a YALE UNIVERSITY SCHOOL OF MEDICINE   (United States)

Author keywords

FGF23; Osteomalacia; Phosphate; Rickets

Indexed keywords

AMILORIDE; CALCITONIN; CALCITRIOL; CINACALCET; CYTOCHROME P450; CYTOCHROME P450 27B1; DOXERCALCIFEROL; ECTONUCLEOTIDE PYROPHOSPHATASE PHOSPHODIESTERASE 1; FIBROBLAST GROWTH FACTOR 23; HUMAN GROWTH HORMONE; PARATHYROID HORMONE; PARICALCITOL; PHOSPHATE; PHOSPHODIESTERASE; PHOSPHORUS; SODIUM PHOSPHATE COTRANSPORTER 2; THIAZIDE DIURETIC AGENT; UNCLASSIFIED DRUG;

ADJUVANT THERAPY; AUTOSOMAL DOMINANT HYPOPHOSPHATEMIC RICKETS; AUTOSOMAL RECESSIVE DISORDER; AUTOSOMAL RECESSIVE HYPOPHOSPHATEMIC RICKETS; DENT DISEASE; ENTHESOPATHY; FAMILY HISTORY; FANCONI RENOTUBULAR SYNDROME; GENE; HEREDITARY HYPOPHOSPHATEMIC RICKETS WITH HYPERCALCIURIA; HUMAN; HYPERPARATHYROIDISM; HYPOPHOSPHATEMIC RICKETS; KIDNEY TUBULE DISORDER; LEG MALFORMATION; LOSS OF FUNCTION MUTATION; LOWE SYNDROME; NONHUMAN; ONCOGENIC OSTEOMALACIA; OSTEOARTHRITIS; OSTEOPHYTE; PHOSPHATE METABOLISM; PRIORITY JOURNAL; RENAL PHOSPHATE WASTING; REVIEW; SHORT STATURE; SLC34A1 GENE; X LINKED HYPOPHOSPHATEMIC RICKETS;

ANIMALS; FIBROBLAST GROWTH FACTORS; HUMANS; HYPOPHOSPHATEMIC RICKETS, X-LINKED DOMINANT; SYNDROME;

EID: 84858819813     PISSN: 09148779     EISSN: 14355604     Source Type: Journal    
DOI: 10.1007/s00774-011-0340-2     Document Type: Review

References (66)

1. Winters RW, Graham JB, Williams TF, McFalls VW, Burnett CH (1958) A genetic study of familial hypophosphatemia and vitamin D-resistant rickets with a review of the literature. Medicine 37:97
2. Francis F (1995) A gene (PEX) with homologies to endopeptidases is mutated in patients with X-linked hypophosphatemic rickets. The HYP Consortium. Nat Genet 11:130-136
3. Ruchon AF, Marcinkiewicz M, Siegfried G, Tenenhouse HS, DesGroseillers L, Crine P, Boileau G (1998) Pex mRNA is localized in developing mouse osteoblasts and odontoblasts. J Histochem Cytochem 46:459-468 (Pubitemid 28158465)
4. Sabbagh Y, Boileau G, DesGroseillers L, Tenenhouse HS (2001) Disease-causing missense mutations in the PHEX gene interfere with membrane targeting of the recombinant protein. Hum Mol Genet 10:1539-1546 (Pubitemid 32734305)
5. 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 (Pubitemid 32924744)
6. Shimada T, Mizutani S, Muto T, Yoneya T, Hino R, Takeda S, Takeuchi Y, Fujita T, Fukumoto S, Yamashita T (2001) Cloning and characterization of FGF23 as a causative factor of tumorinduced osteomalacia. Proc Natl Acad Sci USA 98:6500-6505 (Pubitemid 32488266)
7. 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 (Pubitemid 41653049)
8. Antoniucci DM, Yamashita T, Portale AA (2006) Dietary phosphorus regulates serum fibroblast growth factor-23 concentrations in healthy men. J Clin Endocrinol Metab 91:3144-3149 (Pubitemid 44271770)
9. Perwad F, Zhang MY, Tenenhouse HS, Portale AA (2007) Fibroblast growth factor 23 impairs phosphorus and vitamin D metabolism in vivo and suppresses 25-hydroxyvitamin D-1alphahydroxylase expression in vitro. Am J Physiol Renal Physiol 293:F1577-F1583 (Pubitemid 350085994)
10. Strom TM, Francis F, Lorenz B, Böddrich A, Econs MJ, Lehrach H, Meitinger T (1997) Pex gene deletions in Gy and Hyp mice provide mouse models for X-linked hypophosphatemia. Hum Mol Genet 6:165-171 (Pubitemid 27078072)
11. 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 (Pubitemid 33070451)
12. White KE (2000) Autosomal dominant hypophosphataemic rickets is associated with mutations in FGF23. Nat Genet 26:345-348
13. 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 (Pubitemid 44949607)
14. Ranch D, Zhang MY, Portale AA, Perwad F (2011) Fibroblast growth factor 23 regulates renal 1, 25-dihydroxyvitamin D and phosphate metabolism via the MAP kinase signaling pathway in Hyp mice. J Bone Miner Res 26:1883-1890
15. Xiao L, Naganawa T, Lorenzo J, Carpenter TO, Coffin JD, Hurley MM (2010) Nuclear isoforms of fibroblast growth factor 2 are novel inducers of hypophosphatemia via modulation of FGF23 and KLOTHO. J Biol Chem 285:2843-2846
16. Martin A, Liu S, David V, Li H, Karydis A, Feng JQ, Quarles LD (2011) Bone proteins PHEX and DMP1 regulate fibroblastic growth factor Fgf23 expression in osteocytes through a common pathway involving FGF receptor (FGFR) signaling. FASEB J 25:2551-2562
17. Yoshida T, Fujimori T, Nabeshima Y-I (2002) Mediation of unusually high concentrations of 1,25-dihydroxyvitamin D in homozygous klotho mutant mice by increased expression of renal 1a-hydroxylase gene. Endocrinology 143:683-689 (Pubitemid 34107224)
18. Brownstein CA, Adler F, Nelson-Williams C, Iijima J, Li P, Imura A, Nabeshima Y, Reyes-Mugica M, Carpenter TO, Lifton RP (2008) A translocation causing increased alpha-klotho level results in hypophosphatemic rickets and hyperparathyroidism. Proc Natl Acad Sci USA 105:3455-3460 (Pubitemid 351723574)
19. 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 (Pubitemid 19286654)
20. Marie PJ, Glorieux FH (1982) Bone histomorphometry in asymptomatic adults with hereditary hypophosphatemic vitamin D-resistant osteomalacia. Metab Bone Dis Relat Res 4:249-253
21. Marie PJ, Glorieux FH (1981) Histomorphometric study of bone remodeling in hypophosphatemic vitamin D-resistant rickets. Metab Bone Dis Relat Res 3:31-38
22. Abe K, Ooshima T, Lily TS, Yasufuku Y, Sobue S (1988) Structural deformities of deciduous teeth in patients with hypophosphatemic vitamin D-resistant rickets. Oral Surg Oral Med Oral Pathol 65:191-198
23. Hillmann G, Geurtsen W (1996) Pathohistology of undecalcified primary teeth in vitamin D-resistant rickets: review and report of two cases. Oral Surg Oral Med Oral Pathol Oral Radiol Endod 82:218-224 (Pubitemid 126808191)
24. Seeto E, Seow WK (1991) Scanning electron microscopic analysis of dentin in vitamin D-resistant rickets-assessment of mineralization and correlation with clinical findings. Pediatr Dent 13:43-48
25. Goodman JR, Gelbier MJ, Bennett JH, Winter GB (1998) Dental problems associated with hypophosphataemic vitamin D resistant rickets. Int J Paediatr Dent 8:19-28 (Pubitemid 128506658)
26. 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
27. 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
28. Megerian CA, Semaan MT, Aftab S, Kisley LB, Zheng QY, Pawlowski KS, Wright CG, Alagramam KN (2008) A mouse model with postnatal endolymphatic hydrops and hearing loss. Hear Res 237:90-105
29. Lorenz-Depiereux B, Guido VE, Johnson KR, Zheng QY, Gagnon LH, Bauschatz JD, Davisson MT, Washburn LL, Donahue LR, Strom TM, Eicher EM (2004) New intragenic deletions in the Phex gene clarify X-linked hypophosphatemia-related abnormalities in mice. Mamm Genome 15:151-161 (Pubitemid 38293807)
30. 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
31. 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
32. Goetz R, Nakada Y, Hu MC, Kurosu H, Wang L, Nakatani T, Shi M, Eliseenkova AV, Razzaque MS, Moe OW, Kuro-o M, Mohammadi M (2010) Isolated C-terminal tail of FGF23 alleviates hypophosphatemia by inhibiting FGF23-FGFR-Klotho complex formation. Proc Natl Acad Sci USA 107:407-412
33. Yuan B, Bowman S, Meudt J, Blank R, Feng J, Drezner M (2010) Hexa-D-arginine reversal of osteoblast 7B2 dysregulation in Hypmice normalizes the HYP biochemical phenotype. J Bone Miner Res 25:S4
34. Yuan B, Meudt J, Blank R, Lindberg I, Drezner M (2011) Mechanism of hexa-D-arginine curative effects on the HYP phenotype. J Bone Miner Res 26:S90
35. Liu ES, Carpenter TO, Gundberg CM, Simpson C, Insogna KL (2011) Calcitonin administration in X-linked hypophosphatemia. N Engl J Med 364:1678-1680
36. Seikaly MG, Brown R, Baum M (1997) The effect of recombinant human growth hormone in children with X-linked hypophosphatemia. Pediatrics 100:879-884 (Pubitemid 27463326)
37. Haffner D, Wuhl E, Blum WF, Schaefer F, Mehls O (1995) Disproportionate growth following long-term growth hormone treatment in short children with X-linked hypophosphataemia. Eur J Pediatr 154:610-613
38. Patel L, Clayton PE, Brain C, Pelekouda E, Addison GM, Price DA, Mughal MZ (1996) Acute biochemical effects of growth hormone treatment compared with conventional treatment in familial hypophosphataemic rickets. Clin Endocrinol 44:687-696 (Pubitemid 26225185)
39. 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 (Pubitemid 26175972)
40. Alon US, Levy-Olomucki R, Moore WV, Stubbs J, Liu S, Quarles LD (2008) Calcimimetics as an adjuvant treatment for familial hypophosphatemic rickets. Clin J Am Soc Nephrol 3:658-664
41. Alon U, Chan JC (1985) Effects of hydrochlorothiazide and amiloride in renal hypophosphatemic rickets. Pediatrics 75:754-763 (Pubitemid 15079532)
42. Weidner N, Santa Cruz D (1987) Phosphaturic mesenchymal tumors. A polymorphous group causing osteomalacia or rickets. Cancer 59:144-154
43. Chong WH, Molinolo AA, Chen CC, Collins MT (2011) Tumorinduced osteomalacia. Endocr Relat Cancer 18:R53-R77
44. Bergwitz C, Collins MT, Kamath RS, Rosenberg AE (2011) Case records of the Massachusetts General Hospital. Case 33-2011. A 56-year-old man with hypophosphatemia. N Engl J Med 365:1625-1635
45. Harrison HE, Harrison HC (1979) Rickets and osteomalacia. In: Disorders of calcium and phosphate metabolism in childhood and adolescence. W.B. Saunders Company, Philadelphia, pp 141-256
46. Econs M, McEnery P (1997) Autosomal dominant hypophosphatemic rickets/osteomalacia: clinical characterization of a novel renal phosphate wasting disorder. J Clin Endocrinol Metab 82:674-681 (Pubitemid 27068650)
47. Imel EA, Hui SL, Econs MJ (2007) FGF23 concentrations vary with disease status in autosomal dominant hypophosphatemic rickets. J Bone Miner Res 22:520-526 (Pubitemid 47457428)
48. Imel EA, Peacock M, Gray AK, Padgett LR, Hui SL, Econs MJ (2011) Iron modifies plasma fgf23 differently in autosomal dominant hypophosphatemic rickets and healthy humans. J Clin Endocrinol Metab 96:3541-3549
49. Farrow EG, Yu X, Summers LJ, Davis SI, Fleet JC, Allen MR, Robling AG, Stayrook KR, Jideonwo V, Magers MJ, Garringer HJ, Vidal R, Chan RJ, Goodwin CB, Hui SL, Peacock M, White KE (2011) Iron deficiency drives an autosomal dominant hypophosphatemic rickets (ADHR) phenotype in fibroblast growth factor-23 (Fgf23) knock-in mice. Proc Natl Acad Sci USA 108:E1146-E1155 (Epub ahead of print)
50. 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 (Pubitemid 44646294)
51. Lorenz-Depiereux B, Bastepe M, Benet-Pages 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 (Pubitemid 44646286)
52. Lorenz-Depiereux B, Schnabel D, Tiosano D, Häusler G, Strom TM (2010) Loss-of-function ENPP1 mutations cause both generalized arterial calcification of infancy and autosomal-recessive hypophosphatemic rickets. Am J Hum Genet 86:267-272
53. Levy-Litan V, Hershkovitz E, Avizov L, Leventhal N, Bercovich D, Chalifa-Caspi V, Manor E, Buriakovsky S, Hadad Y, Goding J, Parvari R (2010) Autosomal-recessive hypophosphatemic rickets is associated with an inactivation mutation in the ENPP1 gene. Am J Hum Genet 86:273-278
54. Rutsch F, Ruf N, Vaingankar S, Toliat MR, Suk A, Höhne W, Schauer G, Lehmann M, Roscioli T, Schnabel D, Epplen JT, Knisely A, Superti-Furga A, McGill J, Filippone M, Sinaiko AR, Vallance H, Hinrichs B, Smith W, Ferre M, Terkeltaub R, Nürnberg P (2003) Mutations in ENPP1 are associated with 'idiopathic' infantile arterial calcification. Nat Genet 34:379-381 (Pubitemid 36935330)
55. Dumitrescu CE, Collins MT (2008) McCune-Albright syndrome. Orphanet J Rare Dis 3:12
56. Sethi SK, Hari P, Bagga A (2010) Elevated FGF-23 and parathormone in linear nevus sebaceous syndrome with resistant rickets. Pediatr Nephrol 25:1577-1578
57. Konishi K, Nakamura M, Yamakawa H, Suzuki H, Saruta T, Hanaoka H, Davatchi F (1991) Hypophosphatemic osteomalacia in von Recklinghausen neurofibromatosis. Am J Med Sci 301:322-328
58. White KE, Cabral JM, Davis SI, Fishburn T, Evans WE, Ichikawa S, Fields J, Yu X, Shaw NJ, McLellan NJ, McKeown C, Fitzpatrick D, Yu K, Ornitz DM, Econs MJ (2005) Mutations that cause osteoglophonic dysplasia define novel roles for FGFR1 in bone elongation. Am J Hum Genet 76:361-367 (Pubitemid 40129563)
59. Tieder M, Modai D, Samuel R, Tieder M, Modai D, Samuel R, Arie R, Halabe A, Bab I, Gabizon D, Liberman UA (1985) Hereditary hypophosphatemic rickets with hypercalciuria. N Engl J Med 312:611-617 (Pubitemid 15133676)
60. Bergwitz C, Roslin NM, Tieder M, Loredo-Osti JC, Bastepe M, Abu-Zahra H, Frappier D, Burkett K, Carpenter TO, Anderson D, Garabedian M, Sermet I, Fujiwara TM, Morgan K, Tenenhouse HS, Juppner H (2006) SLC34A3 mutations in patients with hereditary hypophosphatemic rickets with hypercalciuria predict a key role for the sodium-phosphate cotransporter NaPi-IIc in maintaining phosphate homeostasis. Am J Hum Genet 78:179-192 (Pubitemid 43157559)
61. Lorenz-Depiereux B, Benet-Pages A, Eckstein G, Tenenbaum- Rakover Y, Wagenstaller J, Tiosano D, Gershoni-Baruch R, Albers N, Lichtner P, Schnabel D, Hochberg Z, Strom TM (2006) Hereditary hypophosphatemic rickets with hypercalciuria is caused by mutations in the sodium-phosphate cotransporter gene SLC34A3. Am J Hum Genet 78:193-201 (Pubitemid 43157560)
62. Xia W-B (2011) Clinical features and genetic analysis of patients with hypophosphatemic rickets. Japanese Bone and Mineral Society, Osaka
63. Jaureguiberry G, Carpenter TO, Forman S, Jüppner H, Bergwitz C (2008) A novel missense mutation in SLC34A3 that causes hereditary hypophosphatemic rickets with hypercalciuria in humans identifies threonine 137 as an important determinant of sodium-phosphate cotransport in NaPi-IIc. Am J Physiol Renal Physiol 295:F371-F379
64. Magen D, Berger L, Coady MJ, Ilivitzki A, Militianu D, Tieder M, Selig S, Lapointe JY, Zelikovic I, Skorecki K (2010) A lossof- function mutation in NaPi-IIa and renal Fanconi's syndrome. N Engl J Med 362:1102-1109
65. Scheinman SJ (1998) X-linked hypercalciuric nephrolithiasis: clinical syndromes and chloride channel mutations. Kidney Int 53:3-17
66. Karim Z, Gérard B, Bakouh N, Alili R, Leroy C, Beck L, Silve C, Planelles G, Urena-Torres P, Grandchamp B, Friedlander G, PriéD (2008) NHERF1 mutations and responsiveness of renal parathyroid hormone. N Engl J Med 359:1128-1135