A Single Kinase Generates the Majority of the Secreted Phosphoproteome

Cell

Volumn 161, Issue 7, 2015, Pages 1619-1632

  Tagliabracci, Vincent S ^a,c,i   Wiley, Sandra E ^a,c   Guo, Xiao ^b   Kinch, Lisa N ^c   Durrant, Eric ^a   Wen, Jianzhong ^a   Xiao, Junyu ^a,j   Cui, Jixin ^a   Nguyen, Kim B ^a   Engel, James L ^a,j   Coon, Joshua J ^b,d   Grishin, Nick ^c,e   Pinna, Lorenzo A ^f,g   Pagliarini, David J ^b   Dixon, Jack E ^a,h  

^a San Diego   (United States)

^b UNIVERSITY OF WISCONSIN MADISON   (United States)

^c UNIVERSITY OF TEXAS AT DALLAS   (United States)

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

^e HOWARD HUGHES MEDICAL INSTITUTE   (United States)

^f UNIVERSITY OF PADOVA   (Italy)

^g VENETIAN INSTITUTE OF MOLECULAR MEDICINE   (Italy)

^h UNIVERSITY OF CALIFORNIA   (United States)

ⁱ UNIVERSITY OF CALIFORNIA   (United States)

^j PEKING UNIVERSITY   (China)

more..

Author keywords

[No Author keywords available]

Indexed keywords

PHOSPHOPROTEIN; PHOSPHOTRANSFERASE; PROTEOGLYCAN; CASEIN KINASE I; FAM20C PROTEIN, HUMAN; PLASMA PROTEIN; PROTEIN CEREBROSPINAL FLUID LEVEL; SCLEROPROTEIN;

ARTICLE; BIOMINERALIZATION; ENZYME SPECIFICITY; EXTRACELLULAR MATRIX; LIPID HOMEOSTASIS; PHYLOGENETIC TREE; PRIORITY JOURNAL; PROTEIN PHOSPHORYLATION; SECRETORY PATHWAY; WOUND HEALING; AMINO ACID SEQUENCE; CELL ADHESION; CELL MOTION; CHEMISTRY; GENE INACTIVATION; GENE ONTOLOGY; GENETICS; HUMAN; METABOLISM; MOLECULAR GENETICS; PROTEIN CEREBROSPINAL FLUID LEVEL;

AMINO ACID SEQUENCE; BLOOD PROTEINS; CASEIN KINASE I; CELL ADHESION; CELL MOVEMENT; CEREBROSPINAL FLUID PROTEINS; EXTRACELLULAR MATRIX PROTEINS; GENE KNOCKOUT TECHNIQUES; GENE ONTOLOGY; HUMANS; MOLECULAR SEQUENCE DATA; PHOSPHOPROTEINS; SECRETORY PATHWAY; SUBSTRATE SPECIFICITY;

EID: 84934956347     PISSN: 00928674     EISSN: 10974172     Source Type: Journal    
DOI: 10.1016/j.cell.2015.05.028     Document Type: Article

References (54)

1. A. Aziz, S.P. Harrop, and N.E. Bishop Characterization of the deleted in autism 1 protein family: implications for studying cognitive disorders PLoS ONE 6 2011 e14547
2. A. Aziz, S.P. Harrop, and N.E. Bishop DIA1R is an X-linked gene related to Deleted In Autism-1 PLoS ONE 6 2011 e14534
3. J.M. Bahl, S.S. Jensen, M.R. Larsen, and N.H. Heegaard Characterization of the human cerebrospinal fluid phosphoproteome by titanium dioxide affinity chromatography and mass spectrometry Anal. Chem. 80 2008 6308 6316
4. P. Bakrania, M. Efthymiou, J.C. Klein, A. Salt, D.J. Bunyan, A. Wyatt, C.P. Ponting, A. Martin, S. Williams, and V. Lindley Mutations in BMP4 cause eye, brain, and digit developmental anomalies: overlap between the BMP4 and hedgehog signaling pathways Am. J. Hum. Genet. 82 2008 304 319
5. R.C. Baxter IGF binding proteins in cancer: mechanistic and clinical insights Nat. Rev. Cancer 14 2014 329 341
6. A. Bellahcène, V. Castronovo, K.U. Ogbureke, L.W. Fisher, and N.S. Fedarko Small integrin-binding ligand N-linked glycoproteins (SIBLINGs): multifunctional proteins in cancer Nat. Rev. Cancer 8 2008 212 226
7. I. Bieche, F. Lerebours, S. Tozlu, M. Espie, M. Marty, and R. Lidereau Molecular profiling of inflammatory breast cancer: identification of a poor-prognosis gene expression signature Clinical cancer research 10 2004 6789 6795
8. M.R. Bordoli, J. Yum, S.B. Breitkopf, J.N. Thon, J.E. Italiano Jr., J. Xiao, C. Worby, S.K. Wong, G. Lin, and M. Edenius A secreted tyrosine kinase acts in the extracellular environment Cell 158 2014 1033 1044
9. A.M. Brunati, O. Marin, A. Bisinella, A. Salviati, and L.A. Pinna Novel consensus sequence for the Golgi apparatus casein kinase, revealed using proline-rich protein-1 (PRP1)-derived peptide substrates Biochem. J. 351 2000 765 768
10. M. Carrascal, M. Gay, D. Ovelleiro, V. Casas, E. Gelpí, and J. Abian Characterization of the human plasma phosphoproteome using linear ion trap mass spectrometry and multiple search engines J. Proteome Res. 9 2010 876 884
11. E. Cerami, J. Gao, U. Dogrusoz, B.E. Gross, S.O. Sumer, B.A. Aksoy, A. Jacobsen, C.J. Byrne, M.L. Heuer, and E. Larsson The cBiol. cancer genomics portal: an open platform for exploring multidimensional cancer genomics data Cancer discovery 2 2012 401 404
12. H.C. Chan, L. Mai, A. Oikonomopoulou, H.L. Chan, A.S. Richardson, S.K. Wang, J.P. Simmer, and J.C. Hu Altered enamelin phosphorylation site causes amelogenesis imperfecta J. Dent. Res. 89 2010 695 699
13. C. Chen, and B.E. Turk Analysis of serine-threonine kinase specificity using arrayed positional scanning peptide libraries Curr. Protoc. Mol. Biol Chapter 18 2010 Unit 18.14
14. L. Cong, F.A. Ran, D. Cox, S. Lin, R. Barretto, N. Habib, P.D. Hsu, X. Wu, W. Jiang, L.A. Marraffini, and F. Zhang Multiplex genome engineering using CRISPR/Cas systems Science 339 2013 819 823
15. T. Dewpura, A. Raymond, J. Hamelin, N.G. Seidah, M. Mbikay, M. Chrétien, and J. Mayne PCSK9 is phosphorylated by a Golgi casein kinase-like kinase ex vivo and circulates as a phosphoprotein in humans FEBS J. 275 2008 3480 3493
16. M. Dudkiewicz, A. Lenart, and K. Pawłowski A novel predicted calcium-regulated kinase family implicated in neurological disorders PLoS ONE 8 2013 e66427
17. L. Gagnoux-Palacios, M. Allegra, F. Spirito, O. Pommeret, C. Romero, J.P. Ortonne, and G. Meneguzzi The short arm of the laminin gamma2 chain plays a pivotal role in the incorporation of laminin 5 into the extracellular matrix and in cell adhesion J. Cell Biol. 153 2001 835 850
18. J. Gao, B.A. Aksoy, U. Dogrusoz, G. Dresdner, B. Gross, S.O. Sumer, Y. Sun, A. Jacobsen, R. Sinha, and E. Larsson Integrative analysis of complex cancer genomics and clinical profiles using the cBioPortal Sci. Signal. 6 2013 pl1
19. R.B. Georges, H. Adwan, H. Hamdi, T. Hielscher, U. Linnemann, and M.R. Berger The insulin-like growth factor binding proteins 3 and 7 are associated with colorectal cancer and liver metastasis Cancer Biol. Ther. 12 2011 69 79
20. O. Hammarsten Zur Frage ob Caseín ein einheitlicher Stoff sei Hoppe Seylers Z. Physiol. Chem. 7 1883 227 273
21. W. Huang, B.T. Sherman, and R.A. Lempicki Systematic and integrative analysis of large gene lists using DAVID bioinformatics resources Nat. Protoc. 4 2009 44 57
22. J.E. Hutti, E.T. Jarrell, J.D. Chang, D.W. Abbott, P. Storz, A. Toker, L.C. Cantley, and B.E. Turk A rapid method for determining protein kinase phosphorylation specificity Nat. Methods 1 2004 27 29
23. H.O. Ishikawa, H. Takeuchi, R.S. Haltiwanger, and K.D. Irvine Four-jointed is a Golgi kinase that phosphorylates a subset of cadherin domains Science 321 2008 401 404
24. H.O. Ishikawa, A. Xu, E. Ogura, G. Manning, and K.D. Irvine The Raine syndrome protein FAM20C is a Golgi kinase that phosphorylates bio-mineralization proteins PLoS ONE 7 2012 e42988
25. L.T. Jae, M. Raaben, M. Riemersma, E. van Beusekom, V.A. Blomen, A. Velds, R.M. Kerkhoven, J.E. Carette, H. Topaloglu, and P. Meinecke Deciphering the glycosylome of dystroglycanopathies using haploid screens for lassa virus entry Science 340 2013 479 483
26. W. Jiang, C. Xiang, S. Cazacu, C. Brodie, and T. Mikkelsen Insulin-like growth factor binding protein 7 mediates glioma cell growth and migration Neoplasia 10 2008 1335 1342
27. T. Koike, T. Izumikawa, J. Tamura, and H. Kitagawa FAM20B is a kinase that phosphorylates xylose in the glycosaminoglycan-protein linkage region Biochem. J. 421 2009 157 162
28. I.K. Kotowski, A. Pertsemlidis, A. Luke, R.S. Cooper, G.L. Vega, J.C. Cohen, and H.H. Hobbs A spectrum of PCSK9 alleles contributes to plasma levels of low-density lipoprotein cholesterol Am. J. Hum. Genet. 78 2006 410 422
29. M. Lasa-Benito, O. Marin, F. Meggio, and L.A. Pinna Golgi apparatus mammary gland casein kinase: monitoring by a specific peptide substrate and definition of specificity determinants FEBS Lett. 382 1996 149 152
30. I. Lindberg, H.W. Pang, J.P. Stains, D. Clark, A.J. Yang, L. Bonewald, and K.Z. Li FGF23 is endogenously phosphorylated in bone cells J. Bone Miner. Res. 30 2015 449 454
31. P. Mali, L. Yang, K.M. Esvelt, J. Aach, M. Guell, J.E. DiCarlo, J.E. Norville, and G.M. Church RNA-guided human genome engineering via Cas9 Science 339 2013 823 826
32. G. Manning, D.B. Whyte, R. Martinez, T. Hunter, and S. Sudarsanam The protein kinase complement of the human genome Science 298 2002 1912 1934
33. F. Meggio, J.W. Perich, H.E. Meyer, E. Hoffmann-Posorske, D.P. Lennon, R.B. Johns, and L.A. Pinna Synthetic fragments of beta-casein as model substrates for liver and mammary gland casein kinases Eur. J. Biochem. 186 1989 459 464
34. J. Mok, P.M. Kim, H.Y. Lam, S. Piccirillo, X. Zhou, G.R. Jeschke, D.L. Sheridan, S.A. Parker, V. Desai, and M. Jwa Deciphering protein kinase specificity through large-scale analysis of yeast phosphorylation site motifs Sci. Signal. 3 2010 ra12
35. E.M. Morrow, S.Y. Yoo, S.W. Flavell, T.K. Kim, Y. Lin, R.S. Hill, N.M. Mukaddes, S. Balkhy, G. Gascon, and A. Hashmi Identifying autism loci and genes by tracing recent shared ancestry Science 321 2008 218 223
36. D. Nalbant, H. Youn, S.I. Nalbant, S. Sharma, E. Cobos, E.G. Beale, Y. Du, and S.C. Williams FAM20: an evolutionarily conserved family of secreted proteins expressed in hematopoietic cells BMC Genomics 6 2005 11
37. A.K. O'Neill, L.L. Gallegos, V. Justilien, E.L. Garcia, M. Leitges, A.P. Fields, R.A. Hall, and A.C. Newton Protein kinase Cα promotes cell migration through a PDZ-dependent interaction with its novel substrate discs large homolog 1 (DLG1) J. Biol. Chem. 286 2011 43559 43568
38. J. Raine, R.M. Winter, A. Davey, and S.M. Tucker Unknown syndrome: microcephaly, hypoplastic nose, exophthalmos, gum hyperplasia, cleft palate, low set ears, and osteosclerosis J. Med. Genet. 26 1989 786 788
39. M.A. Simpson, R. Hsu, L.S. Keir, J. Hao, G. Sivapalan, L.M. Ernst, E.H. Zackai, L.I. Al-Gazali, G. Hulskamp, and H.M. Kingston Mutations in FAM20C are associated with lethal osteosclerotic bone dysplasia (Raine syndrome), highlighting a crucial molecule in bone development Am. J. Hum. Genet. 81 2007 906 912
40. K.L. Sodek, T.J. Brown, and M.J. Ringuette Collagen I but not Matrigel matrices provide an MMP-dependent barrier to ovarian cancer cell penetration BMC Cancer 8 2008 223
41. V.S. Tagliabracci, J.L. Engel, J. Wen, S.E. Wiley, C.A. Worby, L.N. Kinch, J. Xiao, N.V. Grishin, and J.E. Dixon Secreted kinase phosphorylates extracellular proteins that regulate biomineralization Science 336 2012 1150 1153
42. V.S. Tagliabracci, L.A. Pinna, and J.E. Dixon Secreted protein kinases Trends Biochem. Sci. 38 2013 121 130
43. V.S. Tagliabracci, J. Xiao, and J.E. Dixon Phosphorylation of substrates destined for secretion by the Fam20 kinases Biochem. Soc. Trans. 41 2013 1061 1065
44. V.S. Tagliabracci, J.L. Engel, S.E. Wiley, J. Xiao, D.J. Gonzalez, H. Nidumanda Appaiah, A. Koller, V. Nizet, K.E. White, and J.E. Dixon Dynamic regulation of FGF23 by Fam20C phosphorylation, GalNAc-T3 glycosylation, and furin proteolysis Proc. Natl. Acad. Sci. USA 111 2014 5520 5525
45. A.J. Tennant-Eyles, H. Moffitt, C.A. Whitehouse, and R.G. Roberts Characterisation of the FAM69 family of cysteine-rich endoplasmic reticulum proteins Biochem. Biophys. Res. Commun. 406 2011 471 477
46. M. Valiente, A.C. Obenauf, X. Jin, Q. Chen, X.H. Zhang, D.J. Lee, J.E. Chaft, M.G. Kris, J.T. Huse, E. Brogi, and J. Massagué Serpins promote cancer cell survival and vascular co-option in brain metastasis Cell 156 2014 1002 1016
47. A. von Renesse, M.V. Petkova, S. Lützkendorf, J. Heinemeyer, E. Gill, C. Hübner, A. von Moers, W. Stenzel, and M. Schuelke POMK mutation in a family with congenital muscular dystrophy with merosin deficiency, hypomyelination, mild hearing deficit and intellectual disability J. Med. Genet. 51 2014 275 282
48. X. Wang, S. Wang, C. Li, T. Gao, Y. Liu, A. Rangiani, Y. Sun, J. Hao, A. George, and Y. Lu Inactivation of a novel FGF23 regulator, FAM20C, leads to hypophosphatemic rickets in mice PLoS Genet. 8 2012 e1002708
49. S. Weber, J.C. Taylor, P. Winyard, K.F. Baker, J. Sullivan-Brown, R. Schild, T. Knüppel, A.M. Zurowska, A. Caldas-Alfonso, and M. Litwin SIX2 and BMP4 mutations associate with anomalous kidney development J. Am. Soc. Nephrol. 19 2008 891 903
50. J. Wen, J. Xiao, M. Rahdar, B.P. Choudhury, J. Cui, G.S. Taylor, J.D. Esko, and J.E. Dixon Xylose phosphorylation functions as a molecular switch to regulate proteoglycan biosynthesis Proc. Natl. Acad. Sci. USA 111 2014 15723 15728
51. J. Xiao, V.S. Tagliabracci, J. Wen, S.A. Kim, and J.E. Dixon Crystal structure of the Golgi casein kinase Proc. Natl. Acad. Sci. USA 110 2013 10574 10579
52. T. Yoshida-Moriguchi, T. Willer, M.E. Anderson, D. Venzke, T. Whyte, F. Muntoni, H. Lee, S.F. Nelson, L. Yu, and K.P. Campbell SGK196 is a glycosylation-specific O-mannose kinase required for dystroglycan function Science 341 2013 896 899
53. A.M. Zawadzka, B. Schilling, M.P. Cusack, A.K. Sahu, P. Drake, S.J. Fisher, C.C. Benz, and B.W. Gibson Phosphoprotein secretome of tumor cells as a source of candidates for breast cancer biomarkers in plasma Mol. Cell. Proteomics 13 2014 1034 1049
54. W. Zhou, M.M. Ross, A. Tessitore, D. Ornstein, A. Vanmeter, L.A. Liotta, and E.F. Petricoin 3rd An initial characterization of the serum phosphoproteome J. Proteome Res. 8 2009 5523 5531