Functional analysis of mutant FAM20C in Raine syndrome with FGF23-related hypophosphatemia

Bone

Volumn 67, Issue , 2014, Pages 145-151

  Kinoshita, Yuka ^a   Hori, Michiko ^a   Taguchi, Manabu ^a   Fukumoto, Seiji ^a  

^a UNIVERSITY OF TOKYO HOSPITAL   (Japan)

Author keywords

DMP1; FAM20C; FGF23 related hypophosphatemia; Raine syndrome

Indexed keywords

DENTIN MATRIX PROTEIN 1; FAM20C PROTEIN; FIBROBLAST GROWTH FACTOR 23; MITOGEN ACTIVATED PROTEIN KINASE; PROTEIN KINASE; UNCLASSIFIED DRUG; CASEIN KINASE I; DMP1 PROTEIN, HUMAN; FAM20C PROTEIN, HUMAN; FIBROBLAST GROWTH FACTOR; PHOSPHOPROTEIN; SCLEROPROTEIN;

ANIMAL EXPERIMENT; ANIMAL MODEL; ARTICLE; BONE DYSPLASIA; COMPARATIVE STUDY; CONTROLLED STUDY; DMP1 GENE; ENDOPLASMIC RETICULUM STRESS; ENZYME ACTIVITY; FAM20C GENE; FGF23 GENE; GENE OVEREXPRESSION; GENETIC TRANSCRIPTION; HUMAN; HUMAN CELL; HYPOPHOSPHATEMIA; IN VITRO STUDY; MOUSE; NONHUMAN; PROMOTER REGION; PROTEIN ANALYSIS; PROTEIN FUNCTION; PROTEIN SECRETION; RAINE SYNDROME; CELL LINE; CLEFT PALATE; EXOPHTHALMOS; GENETICS; METABOLISM; MICROCEPHALY; MULTIPLE MALFORMATION SYNDROME; OSTEOSCLEROSIS; REVERSE TRANSCRIPTION POLYMERASE CHAIN REACTION;

ABNORMALITIES, MULTIPLE; CASEIN KINASE I; CELL LINE; CLEFT PALATE; ENDOPLASMIC RETICULUM STRESS; EXOPHTHALMOS; EXTRACELLULAR MATRIX PROTEINS; FIBROBLAST GROWTH FACTORS; HUMANS; HYPOPHOSPHATEMIA; MICROCEPHALY; OSTEOSCLEROSIS; PHOSPHOPROTEINS; PROMOTER REGIONS, GENETIC; REVERSE TRANSCRIPTASE POLYMERASE CHAIN REACTION;

EID: 84904619926     PISSN: 87563282     EISSN: None     Source Type: Journal    
DOI: 10.1016/j.bone.2014.07.009     Document Type: Article

References (35)

1. Raine J., Winter R.M., Davey A., Tucker S.M. Unknown syndrome: microcephaly, hypoplastic nose, exophthalmos, gum hyperplasia, cleft palate, low set ears, and osteosclerosis. J Med Genet 1989, 26:786-788.
2. Simpson M.A., Hsu R., Keir L.S., Hao J., Sivapalan G., Ernst L.M., et al. Mutations in FAM20C are associated with lethal osteosclerotic bone dysplasia (Raine syndrome), highlighting a crucial molecule in bone development. Am J Hum Genet 2007, 81:906-912.
3. Simpson M.A., Scheuerle A., Hurst J., Patton M.A., Stewart H., Crosby A.H. Mutations in FAM20C also identified in non-lethal osteosclerotic bone dysplasia. Clin Genet 2009, 75:271-276.
4. Fradin M., Stoetzel C., Muller J., Koob M., Christmann D., Debry C., et al. Osteosclerotic bone dysplasia in siblings with a Fam20C mutation. Clin Genet 2011, 80:177-183.
5. Rafaelsen S.H., Raeder H., Fagerheim A.K., Knappskog P., Carpenter T.O., Johansson S., et al. Exome sequencing reveals FAM20c mutations associated with fibroblast growth factor 23-related hypophosphatemia, dental anomalies, and ectopic calcification. J Bone Miner Res 2013, 28:1378-1385.
6. Ishikawa H.O., Takeuchi H., Haltiwanger R.S., Irvine K.D. Four-jointed is a Golgi kinase that phosphorylates a subset of cadherin domains. Science 2008, 321:401-404.
7. O'Sullivan J., Bitu C.C., Daly S.B., Urquhart J.E., Barron M.J., Bhaskar S.S., et al. Whole-exome sequencing identifies FAM20A mutations as a cause of amelogenesis imperfecta and gingival hyperplasia syndrome. Am J Hum Genet 2011, 88:616-620.
8. Nalbant D., Youn H., Nalbant S.I., Sharma S., Cobos E., Beale E.G., et al. FAM20: an evolutionarily conserved family of secreted proteins expressed in hematopoietic cells. BMC Genomics 2005, 6:11.
9. Wang X., Hao J., Xie Y., Sun Y., Hernandez B., Yamoah A.K., et al. Expression of FAM20C in the osteogenesis and odontogenesis of mouse. J Histochem Cytochem 2010, 58:957-967.
10. Kawasaki K., Weiss K.M. Mineralized tissue and vertebrate evolution: the secretory calcium-binding phosphoprotein gene cluster. Proc Natl Acad Sci U S A 2003, 100:4060-4065.
11. Steitz S.A., Speer M.Y., McKee M.D., Liaw L., Almeida M., Yang H., et al. Osteopontin inhibits mineral deposition and promotes regression of ectopic calcification. Am J Pathol 2002, 161:2035-2046.
12. Narayanan K., Srinivas R., Ramachandran A., Hao J., Quinn B., George A. Differentiation of embryonic mesenchymal cells to odontoblast-like cells by overexpression of dentin matrix protein 1. Proc Natl Acad Sci U S A 2001, 98:4516-4521.
13. Tagliabracci V.S., Engel J.L., Wen J., Wiley S.E., Worby C.A., Kinch L.N., et al. Secreted kinase phosphorylates extracellular proteins that regulate biomineralization. Science 2012, 336:1150-1153.
14. Ishikawa H.O., Xu A., Ogura E., Manning G., Irvine K.D. The Raine syndrome protein FAM20C is a Golgi kinase that phosphorylates bio-mineralization proteins. PLoS One 2012, 7:e42988.
15. Shimada T., Hasegawa H., Yamazaki Y., Muto T., Hino R., Takeuchi Y., et al. FGF-23 is a potent regulator of vitamin D metabolism and phosphate homeostasis. J Bone Miner Res 2004, 19:429-435.
16. Consortium T. A gene (PEX) with homologies to endopeptidases is mutated in patients with X-linked hypophosphatemic rickets. Nat Genet 1995, 11:130-136.
17. Consortium A. Autosomal dominant hypophosphataemic rickets is associated with mutations in FGF23. Nat Genet 2000, 26:345-348.
18. 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.
19. 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.
20. 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. United States 2006, 1310-1315.
21. 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.
22. Levy-Litan V., Hershkovitz E., Avizov L., Leventhal N., Bercovich D., Chalifa-Caspi V., et al. Autosomal-recessive hypophosphatemic rickets is associated with an inactivation mutation in the ENPP1 gene. Am J Hum Genet 2010, 86:273-278.
23. Lorenz-Depiereux B., Schnabel D., Tiosano D., Hausler G., Strom T.M. Loss-of-function ENPP1 mutations cause both generalized arterial calcification of infancy and autosomal-recessive hypophosphatemic rickets. Am J Hum Genet 2010, 86:267-272.
24. Wang X., Wang S., Li C., Gao T., Liu Y., Rangiani A., et al. Inactivation of a novel FGF23 regulator, FAM20C, leads to hypophosphatemic rickets in mice. PLoS Genet 2012, 8:e1002708.
25. Lutz M.P., Pinon D.I., Miller L.J. A nonradioactive fluorescent gel-shift assay for the analysis of protein phosphatase and kinase activities toward protein-specific peptide substrates. Anal Biochem 1994, 220:268-274.
26. Wang Y., Shen J., Arenzana N., Tirasophon W., Kaufman R.J., Prywes R. Activation of ATF6 and an ATF6 DNA binding site by the endoplasmic reticulum stress response. J Biol Chem 2000, 275:27013-27020.
27. Kolek O.I., Hines E.R., Jones M.D., LeSueur L.K., Lipko M.A., Kiela P.R., et al. 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-G1042.
28. Liu S., Tang W., Zhou J., Stubbs J.R., Luo Q., Pi M., et al. Fibroblast growth factor 23 is a counter-regulatory phosphaturic hormone for vitamin D. J Am Soc Nephrol 2006, 17:1305-1315.
29. 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.
30. Wang S.K., Samann A.C., Hu J.C., Simmer J.P. FAM20C functions intracellularly within both ameloblasts and odontoblasts in vivo. J Bone Miner Res 2013, 28:2508-2511.
31. Wu H., Teng P.N., Jayaraman T., Onishi S., Li J., Bannon L., et al. Dentin matrix protein 1 (DMP1) signals via cell surface integrin. J Biol Chem 2011, 286:29462-29469.
32. Samadfam R., Richard C., Nguyen-Yamamoto L., Bolivar I., Goltzman D. Bone formation regulates circulating concentrations of fibroblast growth factor 23. Endocrinology 2009, 150:4835-4845.
33. Narayanan K., Gajjeraman S., Ramachandran A., Hao J., George A. Dentin matrix protein 1 regulates dentin sialophosphoprotein gene transcription during early odontoblast differentiation. J Biol Chem 2006, 281:19064-19071.
34. Wang X., Wang J., Yuan B., Lu Y., Feng J.Q., Qin C. Overexpression of Dmp1 fails to rescue the bone and dentin defects, in Fam20C knockout mice. Connect Tissue Res 2014, 1-16.
35. Tagliabracci V.S., Engel J.L., Wiley S.E., Xiao J., Gonzalez D.J., Nidumanda Appaiah H., et al. Dynamic regulation of FGF23 by Fam20C phosphorylation, GalNAc-T3 glycosylation, and furin proteolysis. Proc Natl Acad Sci U S A 2014, 111:5520-5525.