The raine syndrome protein FAM20C is a golgi kinase that phosphorylates bio-mineralization proteins

PLoS ONE

Volumn 7, Issue 8, 2012, Pages

  Ishikawa, Hiroyuki O ^a,b   Xu, Aiguo ^b,d   Ogura, Eri ^a   Manning, Gerard ^c,e   Irvine, Kenneth D ^b  

^a CHIBA UNIVERSITY   (Japan)

^b RUTGERS UNIVERSITY   (United States)

^c SALK INSTITUTE FOR BIOLOGICAL STUDIES   (United States)

^d Simcere Pharmaceutical   (China)

^e GENENTECH INC   (United States)

Author keywords

[No Author keywords available]

Indexed keywords

AMINO ACID; CASEIN; FAMILY WITH SEQUENCE SIMILARITY 20 PROTEIN; PEPTIDE; PHOSPHOPROTEIN; PHOSPHOTRANSFERASE; PROTEIN SIBLING; UNCLASSIFIED DRUG;

ANIMAL CELL; ARTICLE; AUTOPHOSPHORYLATION; BIOMINERALIZATION; BONE DYSPLASIA; EMBRYO; ENZYME ACTIVITY; ENZYME LOCALIZATION; HUMAN; HUMAN CELL; NONHUMAN; POINT MUTATION; PROTEIN FUNCTION; PROTEIN PHOSPHORYLATION; RAINE SYNDROME;

ABNORMALITIES, MULTIPLE; CELL LINE; CLEFT PALATE; ENZYME ACTIVATION; EXOPHTHALMOS; EXTRACELLULAR MATRIX PROTEINS; GENE EXPRESSION; GOLGI APPARATUS; HUMANS; MICROCEPHALY; MUTATION; OSTEOSCLEROSIS; PHOSPHOPROTEINS; PHOSPHORYLATION; PROTEIN KINASES; PROTEIN TRANSPORT;

EID: 84865021971     PISSN: None     EISSN: 19326203     Source Type: Journal    
DOI: 10.1371/journal.pone.0042988     Document Type: Article

References (47)

1. Hulskamp G, Wieczorek D, Rieder H, Louwen F, Hornig-Franz I, et al. ((2003)) Raine syndrome: report of a family with three affected sibs and further delineation of the syndrome. Clin Dysmorphol 12:: 153--160.
2. Raine J, Winter RM, Davey A, Tucker SM, ((1989)) Unknown syndrome: microcephaly, hypoplastic nose, exophthalmos, gum hyperplasia, cleft palate, low set ears, and osteosclerosis. J Med Genet 26:: 786--788.
3. Rejjal A, ((1998)) Raine syndrome. Am J Med Genet 78:: 382--385.
4. Fradin M, Stoetzel C, Muller J, Koob M, Christmann D, et al. ((2011)) Osteosclerotic bone dysplasia in siblings with a Fam20C mutation. Clin Genet 80:: 177--183.
5. Simpson MA, Hsu R, Keir LS, Hao J, Sivapalan G, et al. ((2007)) Mutations in FAM20C are associated with lethal osteosclerotic bone dysplasia (Raine syndrome), highlighting a crucial molecule in bone development. Am J Hum Genet 81:: 906--912.
6. Simpson MA, Scheuerle A, Hurst J, Patton MA, Stewart H, et al. ((2009)) Mutations in FAM20C also identified in non-lethal osteosclerotic bone dysplasia. Clin Genet 75:: 271--276.
7. Hao J, Narayanan K, Muni T, Ramachandran A, George A, ((2007)) Dentin matrix protein 4, a novel secretory calcium-binding protein that modulates odontoblast differentiation. J Biol Chem 282:: 15357--15365.
8. Wang X, Hao J, Xie Y, Sun Y, Hernandez B, et al. ((2010)) Expression of FAM20C in the osteogenesis and odontogenesis of mouse. The journal of histochemistry and cytochemistry: official journal of the Histochemistry Society 58:: 957--967.
9. Qin C, Baba O, Butler WT, ((2004)) Post-translational modifications of sibling proteins and their roles in osteogenesis and dentinogenesis. Crit Rev Oral Biol Med 15:: 126--136.
10. Fisher LW, Fedarko NS, ((2003)) Six genes expressed in bones and teeth encode the current members of the SIBLING family of proteins. Connect Tissue Res 44 (Suppl 1):: 33--40.
11. Bellahcene A, Castronovo V, Ogbureke KU, Fisher LW, Fedarko NS, ((2008)) Small integrin-binding ligand N-linked glycoproteins (SIBLINGs): multifunctional proteins in cancer. Nat Rev Cancer 8:: 212--226.
12. George A, Veis A, ((2008)) Phosphorylated proteins and control over apatite nucleation, crystal growth, and inhibition. Chem Rev 108:: 4670--4693.
13. Addison WN, Masica DL, Gray JJ, McKee MD, ((2010)) Phosphorylation-dependent inhibition of mineralization by osteopontin ASARM peptides is regulated by PHEX cleavage. J Bone Miner Res 25:: 695--705.
14. Gericke A, Qin C, Spevak L, Fujimoto Y, Butler WT, et al. ((2005)) Importance of phosphorylation for osteopontin regulation of biomineralization. Calcif Tissue Int 77:: 45--54.
15. Jono S, Peinado C, Giachelli CM, ((2000)) Phosphorylation of osteopontin is required for inhibition of vascular smooth muscle cell calcification. J Biol Chem 275:: 20197--20203.
16. Kazanecki CC, Uzwiak DJ, Denhardt DT, ((2007)) Control of osteopontin signaling and function by post-translational phosphorylation and protein folding. J Cell Biochem 102:: 912--924.
17. Deshpande AS, Fang P-A, Zhang X, Jayaraman T, Sfeir C, et al. ((2011)) Primary structure and phosphorylation of dentin matrix protein 1 (DMP1) and dentin phosphophoryn (DPP) uniquely determine their role in biomineralization. Biomacromolecules 12:: 2933--2945.
18. Hammarsten O, ((1883)) Zur Frage ob Caseín ein einheitlicher Stoff sei. Zeitschrift für Physiologische Chemie 7:: 227--273.
19. Burnett G, Kennedy EP, ((1954)) The enzymatic phosphorylation of proteins. The Journal of biological chemistry 211:: 969--980.
20. Bingham EW, Farrel HM Jr, ((1974)) Casein kinase from the Golgi apparatus of lactating mammary gland. J Biol Chem 249:: 3647--3651.
21. Lasa-Benito M, Marin O, Meggio F, Pinna LA, ((1996)) Golgi apparatus mammary gland casein kinase: monitoring by a specific peptide substrate and definition of specificity determinants. FEBS Lett 382:: 149--152.
22. Ishikawa HO, Takeuchi H, Haltiwanger RS, Irvine KD, ((2008)) Four-jointed is a Golgi kinase that phosphorylates a subset of cadherin domains. Science 321:: 401--404.
23. Simon MA, Xu A, Ishikawa HO, Irvine KD, ((2010)) Modulation of Fat:Dachsous binding by the cadherin domain kinase four-jointed. Curr Biol 20:: 811--817.
24. Brittle AL, Repiso A, Casal J, Lawrence PA, Strutt D, ((2010)) Four-jointed modulates growth and planar polarity by reducing the affinity of dachsous for fat. Curr Biol 20:: 803--810.
25. Nalbant D, Youn H, Nalbant SI, Sharma S, Cobos E, et al. ((2005)) FAM20: an evolutionarily conserved family of secreted proteins expressed in hematopoietic cells. BMC Genomics 6:: 11.
26. El-Battari A, Prorok M, Angata K, Mathieu S, Zerfaoui M, et al. ((2003)) Different glycosyltransferases are differentially processed for secretion, dimerization, and autoglycosylation. Glycobiology 13:: 941--953.
27. Buckles GR, Rauskolb C, Villano JL, Katz FN, ((2001)) four-jointed interacts with dachs, abelson and enabled and feeds back onto the Notch pathway to affect growth and segmentation in the Drosophila leg. Development 128:: 3533--3542.
28. Wu C, Orozco C, Boyer J, Leglise M, Goodale J, et al. ((2009)) BioGPS: an extensible and customizable portal for querying and organizing gene annotation resources. Genome Biol 10:: R130.
29. Lattin JE, Schroder K, Su AI, Walker JR, Zhang J, et al. ((2008)) Expression analysis of G Protein-Coupled Receptors in mouse macrophages. Immunome Res 4:: 5.
30. Su AI, Wiltshire T, Batalov S, Lapp H, Ching KA, et al. ((2004)) A gene atlas of the mouse and human protein-encoding transcriptomes. Proc Natl Acad Sci U S A 101:: 6062--6067.
31. Jonchère V, Réhault-Godbert S, Hennequet-Antier C, Cabau C, Sibut V, et al. ((2010)) Gene expression profiling to identify eggshell proteins involved in physical defense of the chicken egg. BMC Genomics 11:: 57.
32. Mann K, Poustka AJ, Mann M, ((2010)) Phosphoproteomes of Strongylocentrotus purpuratus shell and tooth matrix: identification of a major acidic sea urchin tooth phosphoprotein, phosphodontin. Proteome Sci 8:: 6.
33. Tomancak P, Berman BP, Beaton A, Weiszmann R, Kwan E, et al. ((2007)) Global analysis of patterns of gene expression during Drosophila embryogenesis. Genome biology 8:: R145.
34. Wheeler SR, Kearney JB, Guardiola AR, Crews ST, ((2006)) Single-cell mapping of neural and glial gene expression in the developing Drosophila CNS midline cells. Developmental Biology 294:: 509--524.
35. Bingham EW, Groves ML, ((1979)) Properties of casein kinase from lactating bovine mammary gland. J Biol Chem 254:: 4510--4515.
36. Sorensen ES, Hojrup P, Petersen TE, ((1995)) Posttranslational modifications of bovine osteopontin: identification of twenty-eight phosphorylation and three O-glycosylation sites. Protein Sci 4:: 2040--2049.
37. Lasa M, Chang PL, Prince CW, Pinna LA, ((1997)) Phosphorylation of osteopontin by Golgi apparatus casein kinase. Biochem Biophys Res Commun 240:: 602--605.
38. Tagliabracci VS, Engel JL, Wen J, Wiley SE, Worby CA, et al. ((2012)) Secreted Kinase Phosphorylates Extracellular Proteins that Regulate Biomineralization. Science 336:: 1150--1153.
39. Wang X, Wang S, Li C, Gao T, Liu Y, et al. ((2012)) Inactivation of a Novel FGF23 Regulator, FAM20C, Leads to Hypophosphatemic Rickets in Mice. PLoS genetics 8:: e1002708.
40. Steitz SA, Speer MY, McKee MD, Liaw L, Almeida M, et al. ((2002)) Osteopontin inhibits mineral deposition and promotes regression of ectopic calcification. Am J Pathol 161:: 2035--2046.
41. Feng JQ, Ward LM, Liu S, Lu Y, Xie Y, et al. ((2006)) Loss of DMP1 causes rickets and osteomalacia and identifies a role for osteocytes in mineral metabolism. Nat Genet 38:: 1310--1315.
42. Ye L, MacDougall M, Zhang S, Xie Y, Zhang J, et al. ((2004)) 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 279:: 19141--19148.
43. Salvi M, Cesaro L, Tibaldi E, Pinna LA, ((2010)) Motif analysis of phosphosites discloses a potential prominent role of the Golgi casein kinase (GCK) in the generation of human plasma phospho-proteome. Journal of proteome research 9:: 3335--3338.
44. Koike T, Izumikawa T, Tamura J, Kitagawa H, ((2009)) FAM20B is a kinase that phosphorylates xylose in the glycosaminoglycan-protein linkage region. Biochem J 421:: 157--162.
45. Hardie DG, ((2000)) Peptide assay of protein kinases and use of variant peptides to determine recognition motifs. Methods Mol Biol 99:: 191--201.
46. Oh H, Irvine KD, ((2009)) In vivo analysis of Yorkie phosphorylation sites. Oncogene 28:: 1916--1927.
47. Hemsley A, Arnheim N, Toney MD, Cortopassi G, Galas DJ, ((1989)) A simple method for site-directed mutagenesis using the polymerase chain reaction. Nucleic Acids Res 17:: 6545--6551.