Osteocyte regulation of phosphate homeostasis and bone mineralization underlies the pathophysiology of the heritable disorders of rickets and osteomalacia

Bone

Volumn 54, Issue 2, 2013, Pages 213-221

  Feng, Jian Q ^a   Clinkenbeard, Erica L ^b,c   Yuan, Baozhi ^c,d   White, Kenneth E ^b   Drezner, Marc K ^c,d  

^a BAYLOR COLLEGE OF DENTISTRY   (United States)

^b INDIANA UNIVERSITY SCHOOL OF MEDICINE   (United States)

^c UNIVERSITY OF WISCONSIN SCHOOL OF MEDICINE AND PUBLIC HEALTH   (United States)

^d WILLIAM S MIDDLETON MEMORIAL VETERANS HOSPITAL   (United States)

Author keywords

DMP1; Fibroblast growth factor 23; Osteocyte; Osteomalacia; PHEX; Rickets

Indexed keywords

BETA CATENIN; DENTIN MATRIX PROTEIN 1; DICKKOPF 1 PROTEIN; FIBROBLAST GROWTH FACTOR 23; MESSENGER RNA; PHOSPHATE REGULATING NEUTRAL ENDOPEPTIDASE;

AUTOSOMAL DOMINANT HYPOPHOSPHATEMIC RICKETS; AUTOSOMAL RECESSIVE HYPOPHOSPHATEMIC RICKETS; BONE MINERALIZATION; CARBOXY TERMINAL SEQUENCE; CLINICAL FEATURE; CYTOKINE PRODUCTION; CYTOKINE RELEASE; DENTIN MATRIX PROTEIN 1 GENE; DISEASE MODEL; FAMILIAL HYPOPHOSPHATEMIC RICKETS; FIBROBLAST GROWTH FACTOR 23 GENE; GENE; GENE DELETION; GENETIC SCREENING; HUMAN; HYPOPHOSPHATEMIA; IRON DEFICIENCY; LOSS OF FUNCTION MUTATION; METABOLIC REGULATION; MISSENSE MUTATION; MOLECULAR DYNAMICS; MOLECULAR GENETICS; NONHUMAN; OSTEOCYTE; OSTEOMALACIA; PATHOPHYSIOLOGY; PHENOTYPE; PHEX GENE; PHOSPHATE METABOLISM; POINT MUTATION; PROTEIN CLEAVAGE; PROTEIN DEGRADATION; REVIEW; RICKETS; X LINKED HYPOPHOSPHATEMIC RICKETS;

ANIMALS; CALCIFICATION, PHYSIOLOGIC; HOMEOSTASIS; HUMANS; OSTEOCYTES; OSTEOMALACIA; PHOSPHATES; RICKETS;

EID: 84875864123     PISSN: 87563282     EISSN: None     Source Type: Journal    
DOI: 10.1016/j.bone.2013.01.046     Document Type: Review

References (50)

1. Bonewald L.F. Osteocytes as dynamic multifunctional cells. Ann N Y Acad Sci 2007, 6:281-290.
2. Martin A., Liu S., David V., Li H., Karydis A., Feng J.Q., Quarles L.D. Bone proteins PHEX and DMP1 regulate fibroblastic growth factor Fgf23 expression in osteocytes through a common pathway involving FGF receptor (FGFR) signaling. FASEB J 2011, 25:2551-2562.
3. Bianchine J.W., Stambler A.A., Harrison H.E. Familial hypophosphatemic rickets showing autosomal dominant inheritance. Birth Defects Orig Artic Ser 1971, 7:287-295.
4. Econs M.J., McEnery P.T. Autosomal dominant hypophosphatemic rickets/osteomalacia: clinical characterization of a novel renal phosphate-wasting disorder. J Clin Endocrinol Metab 1997, 82:674-681.
5. Econs M.J., McEnery P.T., Lennon F., Speer M.C. Autosomal dominant hypophosphatemic rickets is linked to chromosome 12p13. J Clin Invest 1997, 100:2653-2657.
6. ADHR-Consortium Autosomal dominant hypophosphataemic rickets is associated with mutations in FGF23. Nat Genet 2000, 26:345-348.
7. Gribaa M., Younes M., Bouyacoub Y., Korbaa W., Ben Charfeddine I., Touzi M., et al. An autosomal dominant hypophosphatemic rickets phenotype in a Tunisian family caused by a new FGF23 missense mutation. J Bone Miner Metab 2010, 28:111-115.
8. Molloy S.S., Bresnahan P.A., Leppla S.H., Klimpel K.R., Thomas G. Human furin is a calcium-dependent serine endoprotease that recognizes the sequence Arg-X-X-Arg and efficiently cleaves anthrax toxin protective antigen. J Biol Chem 1992, 267:16396-16402.
9. Nakayama K. Furin: a mammalian subtilisin/Kex2p-like endoprotease involved in processing of a wide variety of precursor proteins. Biochem J 1997, 327(Pt 3):625-635.
10. Benet-Pages A., Lorenz-Depiereux B., Zischka H., White K.E., Econs M.J., Strom T.M. FGF23 is processed by proprotein convertases but not by PHEX. Bone 2004, 35:455-462.
11. Yuan B., Feng J.Q., Bowman S., Liu Y., Blank R.D., Lindberg I., et al. Hexa-d-arginine treatment increases 7B2•PC2 activity in hyp-mouse osteoblasts and rescues the HYP phenotype. J Bone Miner Res 2013, 28:56-72.
12. White K.E., Carn G., Lorenz-Depiereux B., Benet-Pages A., Strom T.M., Econs M.J. Autosomal-dominant hypophosphatemic rickets (ADHR) mutations stabilize FGF-23. Kidney Int 2001, 60:2079-2086.
13. Shimada T., Muto T., Urakawa I., Yoneya T., Yamazaki Y., Okawa K., et al. Mutant FGF-23 responsible for autosomal dominant hypophosphatemic rickets is resistant to proteolytic cleavage and causes hypophosphatemia in vivo. Endocrinology 2002, 143:3179-3182.
14. Imel E.A., Hui S.L., Econs M.J. FGF23 concentrations vary with disease status in autosomal dominant hypophosphatemic rickets. J Bone Miner Res 2007, 22:520-526.
15. Durham B.H., Joseph F., Bailey L.M., Fraser W.D. The association of circulating ferritin with serum concentrations of fibroblast growth factor-23 measured by three commercial assays. Ann Clin Biochem 2007, 44:463-466.
16. Farrow E.G., Yu X., Summers L.J., Davis S.I., Fleet J.C., Allen M.R., et al. Iron deficiency drives an autosomal dominant hypophosphatemic rickets (ADHR) phenotype in fibroblast growth factor-23 (Fgf23) knock-in mice. Proc Natl Acad Sci U S A 2011, 108:E1146-E1155.
17. Feng J.Q., Ward L.M., Liu S., Lu Y., Xie Y., Yuan B., et al. Loss of DMP1 causes rickets and osteomalacia and identifies a role for osteocytes in mineral metabolism. Nat Genet 2006, 38:1310-1315.
18. Lorenz-Depiereux B., Bastepe M., Benet-Pages A., Amyere M., Wagenstaller J., Muller-Barth U., et al. DMP1 mutations in autosomal recessive hypophosphatemia implicate a bone matrix protein in the regulation of phosphate homeostasis. Nat Genet 2006, 38:1248-1250.
19. Farrow E.G., Davis S.I., Ward L.M., Summers L.J., Bubbear J.S., Keen R., et al. Molecular analysis of DMP1 mutants causing autosomal recessive hypophosphatemic rickets. Bone 2009, 44:287-294.
20. Turan S., Aydin C., Bereket A., Akcay T., Guran T., Yaralioglu B.A., et al. Identification of a novel dentin matrix protein-1 (DMP-1) mutation and dental anomalies in a kindred with autosomal recessive hypophosphatemia. Bone 2010, 46:402-409.
21. Koshida R., Yamaguchi H., Yamasaki K., Tsuchimochi W., Yonekawa T., Nakazato M. A novel nonsense mutation in the DMP1 gene in a Japanese family with autosomal recessive hypophosphatemic rickets. J Bone Miner Metab 2010, 28:585-590.
22. Mäkitie O., Pereira R.C., Kaitila I., Turan S., Bastepe M., Laine T., et al. Long-term clinical outcome and carrier phenotype in autosomal recessive hypophosphatemia caused by a novel DMP1 mutation. J Bone Miner Res 2010, 25:2165-2174.
23. Ling Y., Rios H.F., Myers E.R., Lu Y., Feng J.Q., Boskey A.L. DMP1 depletion decreases bone mineralization in vivo: an FTIR imaging analysis. J Bone Miner Res 2005, 20:2169-2177.
24. Saito T., Shimizu Y., Hori M., Taguchi M., Igarashi T., Fukumoto S., et al. A patient with hypophosphatemic rickets and ossification of posterior longitudinal ligament caused by a novel homozygous mutation in ENPP1 gene. Bone 2011, 49:913-916.
25. Ye L., Mishina Y., Chen D., Huang H., Dallas S.L., Dallas M.R., et al. Dmp1-deficient mice display severe defects in cartilage formation responsible for a chondrodysplasia-like phenotype. J Biol Chem 2005, 280:6197-6203.
26. Ye L., MacDougall M., Zhang S., Xie Y., Zhang J., Li Z., et al. Deletion of dentin matrix protein-1 leads to a partial failure of maturation of predentin into dentin, hypomineralization, and expanded cavities of pulp and root canal during postnatal tooth development. J Biol Chem 2004, 279:19141-19148.
27. Zhang R., Lu Y., Ye L., Yuan B., Yu S., Qin C., et al. Unique roles of phosphorus in endochondral bone formation and osteocyte maturation. J Bone Miner Res 2011, 26:1047-1056.
28. Lu Y., Yuan B., Qin C., Cao Z., Xie Y., Dallas S.L., et al. The biological function of DMP-1 in osteocyte maturation is mediated by its 57-kDa C-terminal fragment. J Bone Miner Res 2011, 26:331-340.
29. Sun Y., Prasad M., Gao T., Wang X., Zhu Q., D'Souza R., et al. Failure to process dentin matrix protein 1 (DMP1) into fragments leads to its loss of function in osteogenesis. J Biol Chem 2010, 285:31713-31722.
30. Sun Y., Lu Y., Chen L., Gao T., D'Souza R., Feng J.Q., et al. DMP1 processing is essential to dentin and jaw formation. J Dent Res 2011, 90:619-624.
31. Lin S., Jiang Y., Zong Z., Liu M., Liu Y., Yuan B., et al. A key pathological role for the Wnt/β-catenin signaling pathway in hypophosphatemic rickets/osteomalacia. J Bone Miner Res 2012, 27(Suppl. 1). [Abstract, Available at http://www.asbmr.org/Meetings/AnnualMeeting/AbstractDetail.aspx?aid=fcb1fd30-26ae-4a68-9a65-6b44e78b71bc. Accessed December 24, 2012].
32. Jiang B., Cao Z., Lu Y., Janik C., Lauziere S., Xie Y., et al. DMP1 C-terminal mutant mice recapture the human ARHR tooth phenotype. J Bone Miner Res 2010, 25:2155-2164.
33. Ruppe M.D. X-linked hypophosphatemia. GeneReviews™ [Internet] 2012, University of Washington, Seattle, Seattle (WA), [1993-2012 Feb 09 updated 2012 Sep 27]. R.A. Pagon, T.D. Bird, C.R. Dolan, K. Stephens, M.P. Adam (Eds.).
34. Harrison H.E., Harrison H.C., Lifshitz F., Johnson A.D. Growth disturbance in hereditary hypophosphatemia. Am J Dis Child 1966, 112:290-297.
35. Polisson R.P., Martinez S., Khoury M., Harrell R.M., Lyles K.W., Friedman N., et al. Calcification of entheses associated with X-linked hypophosphatemic osteomalacia. N Engl J Med 1985, 313:1-6.
36. The HYP Consortium A gene (PEX) with homologies to endopeptidases is mutated in patients with X-linked hypophosphatemic rickets. Nat Genet 1995, 11:130-136.
37. Econs M.J., Fain P.R., Norman M., Speer M.C., Pericak-Vance M.A., Becker P.A., et al. Flanking markers define the X-linked hypophosphatemic rickets gene locus. J Bone Miner Res 1993, 8:1149-1152.
38. Econs M.J., Rowe P.S., Francis F., Barker D.F., Speer M.C., Norman M., et al. Fine structure mapping of the human X-linked hypophosphatemic rickets gene locus. J Clin Endocrinol Metab 1994, 79:1351-1354.
39. Econs M.J., Francis F., Rowe P.S., Speer M.C., O'Riordan J.L., Lehrach H., et al. Dinucleotide repeat polymorphism at the DXS1683 locus. Hum Mol Genet 1994, 3:680.
40. Francis F., Rowe P.S., Econs M.J., See C.G., Benham F., O'Riordan J.L., et al. A YAC contig spanning the hypophosphatemic rickets disease gene (HYP) candidate region. Genomics 1994, 21:229-237.
41. Rowe P.S., Goulding J.N., Francis F., Oudet C., Econs M.J., Hanauer A., et al. The gene for X-linked hypophosphataemic rickets maps to a 200-300kb region in Xp22.1, and is located on a single YAC containing a putative vitamin D response element (VDRE). Hum Genet 1996, 97:345-352.
42. Beck L., Soumounou Y., Martel J., Krishnamurthy G., Gauthier C., Goodyer C.G., et al. Pex/PEX tissue distribution and evidence for a deletion in the 3' region of the Pex gene in X-linked hypophosphatemic mice. J Clin Invest 1997, 99:1200-1209.
43. Strom T.M., Francis F., Lorenz B., Boddrich A., Econs M.J., Lehrach H., et al. Pex gene deletions in Gy and Hyp mice provide mouse models for X-linked hypophosphatemia. Hum Mol Genet 1997, 6:165-171.
44. Sabbagh Y., Tenenehouse H.S. PHEXdb http://www.phexdb.mcgill.ca.
45. Rowe P.S., Oudet C.L., Francis F., Sinding C., Pannetier S., Econs M.J., et al. Distribution of mutations in the PEX gene in families with X-linked hypophosphataemic rickets (HYP). Hum Mol Genet 1997, 6:539-549.
46. Yuan B., Takaiwa M., Clemens T.L., Feng J.Q., Kumar R., Rowe P.S., et al. Aberrant Phex function in osteoblasts and osteocytes alone underlies murine X-linked hypophosphatemia. J Clin Invest 2008, 118:722-734.
47. Nesbitt T., Coffman T.M., Griffiths R., Drezner M.K. Crosstransplantation of kidneys in normal and Hyp mice: evidence that the Hyp mouse phenotype is unrelated to an intrinsic renal defect. J Clin Invest 1992, 89:1453-1459.
48. Shimada T., Urakawa I., Yamazaki Y., Hasegawa H., Hino R., Yoneya T., et al. FGF-23 transgenic mice demonstrate hypophosphatemic rickets with reduced expression of sodium phosphate co-transporter type IIa. Biochem Biophys Res Commun 2004, 314:409-414.
49. Yamazaki Y., Okazaki R., Shibata M., Hasegawa Y., Satoh K., Tajima T. Increased circulator level of biologically active full-length FGF-23 in patients with hypophosphatemic rickets/osteomalacia. J Clin Endocrinol Metab 2002, 87:4957-4960.
50. Liu S., Zhou J., Tang W., Jiang X., Rowe D.W., Quarles L.D. Pathogenic role of Fgf23 in Hyp mice. Am J Physiol Endocrinol Metab 2006, 291:E38-E49.