Using Bacteria to Determine Protein Kinase Specificity and Predict Target Substrates

PLoS ONE

Volumn 7, Issue 12, 2012, Pages

  Chou, Michael F ^a   Prisic, Sladjana ^b   Lubner, Joshua M ^c   Church, George M ^a   Husson, Robert N ^b   Schwartz, Daniel ^c  

^a HARVARD MEDICAL SCHOOL   (United States)

^b BOSTON CHILDREN S HOSPITAL   (United States)

^c UNIVERSITY OF CONNECTICUT   (United States)

Author keywords

[No Author keywords available]

Indexed keywords

CASEIN KINASE II; CYCLIC AMP DEPENDENT PROTEIN KINASE; PROTEOME; RECOMBINANT ENZYME;

ACCURACY; AMINO ACID SEQUENCE; ARTICLE; BACTERIUM; BINDING SITE; COMPUTER PROGRAM; CONTROLLED STUDY; ENZYME SPECIFICITY; ENZYME SUBSTRATE; HUMAN; IN VIVO STUDY; MASS SPECTROMETRY; NONHUMAN; PEPTIDE LIBRARY; PREDICTION; PROTEIN EXPRESSION; PROTEIN MOTIF; PROTEIN PHOSPHORYLATION; VALIDATION STUDY;

AMINO ACID MOTIFS; AMINO ACID SEQUENCE; CASEIN KINASE II; CONSENSUS SEQUENCE; CYCLIC AMP-DEPENDENT PROTEIN KINASES; ESCHERICHIA COLI; ESCHERICHIA COLI PROTEINS; HUMANS; HYDROPHOBIC AND HYDROPHILIC INTERACTIONS; MOLECULAR SEQUENCE DATA; PEPTIDE LIBRARY; PHOSPHORYLATION; PROTEIN PROCESSING, POST-TRANSLATIONAL; RECOMBINANT PROTEINS; ROC CURVE; SEQUENCE ANALYSIS, PROTEIN; SIGNAL TRANSDUCTION; SUBSTRATE SPECIFICITY;

BACTERIA (MICROORGANISMS);

EID: 84871590810     PISSN: None     EISSN: 19326203     Source Type: Journal    
DOI: 10.1371/journal.pone.0052747     Document Type: Article

References (49)

1. Cohen P, (2002) The origins of protein phosphorylation. Nat Cell Biol 4: E127-130.
2. Ozlu N, Akten B, Timm W, Haseley N, Steen H, et al. (2010) Phosphoproteomics. Wiley Interdiscip Rev Syst Biol Med 2: 255-276.
3. Alessi DR, Caudwell FB, Andjelkovic M, Hemmings BA, Cohen P, (1996) Molecular basis for the substrate specificity of protein kinase B; comparison with MAPKAP kinase-1 and p70 S6 kinase. FEBS Lett 399: 333-338.
4. Shoelson SE, Chatterjee S, Chaudhuri M, White MF, (1992) YMXM motifs of IRS-1 define substrate specificity of the insulin receptor kinase. Proc Natl Acad Sci U S A 89: 2027-2031.
5. Hutti JE, Jarrell ET, Chang JD, Abbott DW, Storz P, et al. (2004) A rapid method for determining protein kinase phosphorylation specificity. Nat Methods 1: 27-29.
6. Songyang Z, Blechner S, Hoagland N, Hoekstra MF, Piwnica-Worms H, et al. (1994) Use of an oriented peptide library to determine the optimal substrates of protein kinases. Curr Biol 4: 973-982.
7. Huang SY, Tsai ML, Chen GY, Wu CJ, Chen SH, (2007) A systematic MS-based approach for identifying in vitro substrates of PKA and PKG in rat uteri. J Proteome Res 6: 2674-2684.
8. Kettenbach AN, Wang T, Faherty BK, Madden DR, Knapp S, et al. (2012) Rapid determination of multiple linear kinase substrate motifs by mass spectrometry. Chem Biol 19: 608-618.
9. Knight JD, Tian R, Lee RE, Wang F, Beauvais A, et al. (2012) A novel whole-cell lysate kinase assay identifies substrates of the p38 MAPK in differentiating myoblasts. Skelet Muscle 2: 5.
10. Douglass J, Gunaratne R, Bradford D, Saeed F, Hoffert JD, et al. (2012) Identifying Protein Kinase Target Preferences Using Mass Spectrometry. Am J Physiol Cell Physiol 303: C715-C727.
11. Villen J, Gygi SP, (2008) The SCX/IMAC enrichment approach for global phosphorylation analysis by mass spectrometry. Nat Protoc 3: 1630-1638.
12. Schwartz D, Gygi SP, (2005) An iterative statistical approach to the identification of protein phosphorylation motifs from large-scale data sets. Nat Biotechnol 23: 1391-1398.
13. Schwartz D, Chou MF, Church GM, (2009) Predicting protein post-translational modifications using meta-analysis of proteome scale data sets. Mol Cell Proteomics 8: 365-379.
14. Macek B, Gnad F, Soufi B, Kumar C, Olsen JV, et al. (2008) Phosphoproteome analysis of E. coli reveals evolutionary conservation of bacterial Ser/Thr/Tyr phosphorylation. Mol Cell Proteomics 7: 299-307.
15. Sarno S, Vaglio P, Meggio F, Issinger OG, Pinna LA, (1996) Protein kinase CK2 mutants defective in substrate recognition. Purification and kinetic analysis. J Biol Chem 271: 10595-10601.
16. Hornbeck PV, Kornhauser JM, Tkachev S, Zhang B, Skrzypek E, et al. (2012) PhosphoSitePlus: a comprehensive resource for investigating the structure and function of experimentally determined post-translational modifications in man and mouse. Nucleic Acids Res 40: D261-270.
17. Zhang M, Han G, Wang C, Cheng K, Li R, et al. (2011) A bead-based approach for large-scale identification of in vitro kinase substrates. Proteomics 11: 4632-4637.
18. Obenauer JC, Cantley LC, Yaffe MB, (2003) Scansite 2.0: Proteome-wide prediction of cell signaling interactions using short sequence motifs. Nucleic Acids Res 31: 3635-3641.
19. Guo Z, Tang W, Yuan J, Chen X, Wan B, et al. (2006) BRSK2 is activated by cyclic AMP-dependent protein kinase A through phosphorylation at Thr260. Biochem Biophys Res Commun 347: 867-871.
20. Chemnitz J, Pieper D, Gruttner C, Hauber J, (2009) Phosphorylation of the HuR ligand APRIL by casein kinase 2 regulates CD83 expression. Eur J Immunol 39: 267-279.
21. Miller ML, Jensen LJ, Diella F, Jorgensen C, Tinti M, et al. (2008) Linear motif atlas for phosphorylation-dependent signaling. Sci Signal 1: ra2.
22. Nairn AC, Picciotto MR, (1994) Calcium/calmodulin-dependent protein kinases. Semin Cancer Biol 5: 295-303.
23. Suter M, Riek U, Tuerk R, Schlattner U, Wallimann T, et al. (2006) Dissecting the role of 5′-AMP for allosteric stimulation, activation, and deactivation of AMP-activated protein kinase. J Biol Chem 281: 32207-32216.
24. Seger R, Krebs EG, (1995) The MAPK signaling cascade. FASEB J 9: 726-735.
25. Frame S, Cohen P, (2001) GSK3 takes centre stage more than 20 years after its discovery. Biochem J 359: 1-16.
26. Chambers SP, Austen DA, Fulghum JR, Kim WM, (2004) High-throughput screening for soluble recombinant expressed kinases in Escherichia coli and insect cells. Protein Expr Purif 36: 40-47.
27. Macek B, Mijakovic I, Olsen JV, Gnad F, Kumar C, et al. (2007) The serine/threonine/tyrosine phosphoproteome of the model bacterium Bacillus subtilis. Mol Cell Proteomics 6: 697-707.
28. Rappsilber J, Mann M, Ishihama Y, (2007) Protocol for micro-purification, enrichment, pre-fractionation and storage of peptides for proteomics using StageTips. Nat Protoc 2: 1896-1906.
29. Eng JK, Mccormack AL, Yates JR, (1994) An Approach to Correlate Tandem Mass-Spectral Data of Peptides with Amino-Acid-Sequences in a Protein Database. Journal of the American Society for Mass Spectrometry 5: 976-989.
30. Elias JE, Gygi SP, (2007) Target-decoy search strategy for increased confidence in large-scale protein identifications by mass spectrometry. Nat Methods 4: 207-214.
31. Chiang CW, Derti A, Schwartz D, Chou MF, Hirschhorn JN, et al. (2008) Ultraconserved elements: analyses of dosage sensitivity, motifs and boundaries. Genetics 180: 2277-2293.
32. Prisic S, Dankwa S, Schwartz D, Chou MF, Locasale JW, et al. (2010) Extensive phosphorylation with overlapping specificity by Mycobacterium tuberculosis serine/threonine protein kinases. Proc Natl Acad Sci U S A 107: 7521-7526.
33. Chou MF, Schwartz D (2011) Biological sequence motif discovery using motif-x. Curr Protoc Bioinformatics Chapter 13: Unit 13 15-24.
34. Cui J, Melman Y, Palma E, Fishman GI, McDonald TV, (2000) Cyclic AMP regulates the HERG K(+) channel by dual pathways. Curr Biol 10: 671-674.
35. O'Donnell M RM, Lund L, Bond M (2011) Novel domains in chromodomain helicase binding protein 8. FASEB: 751.711.
36. Lauritzen I, Chemin J, Honore E, Jodar M, Guy N, et al. (2005) Cross-talk between the mechano-gated K2P channel TREK-1 and the actin cytoskeleton. EMBO Rep 6: 642-648.
37. Mant A, Elliott D, Eyers PA, O'Kelly IM, (2011) Protein kinase A is central for forward transport of two-pore domain potassium channels K2P3.1 and K2P9.1. J Biol Chem 286: 14110-14119.
38. Vergarajauregui S, Oberdick R, Kiselyov K, Puertollano R, (2008) Mucolipin 1 channel activity is regulated by protein kinase A-mediated phosphorylation. Biochem J 410: 417-425.
39. Chang CC, Naik MT, Huang YS, Jeng JC, Liao PH, et al. (2011) Structural and functional roles of Daxx SIM phosphorylation in SUMO paralog-selective binding and apoptosis modulation. Mol Cell 42: 62-74.
40. Montagnoli A, Valsasina B, Brotherton D, Troiani S, Rainoldi S, et al. (2006) Identification of Mcm2 phosphorylation sites by S-phase-regulating kinases. J Biol Chem 281: 10281-10290.
41. Brunati AM, Contri A, Muenchbach M, James P, Marin O, et al. (2000) GRP94 (endoplasmin) co-purifies with and is phosphorylated by Golgi apparatus casein kinase. FEBS Lett 471: 151-155.
42. Li D, Dobrowolska G, Krebs EG, (1996) The physical association of casein kinase 2 with nucleolin. J Biol Chem 271: 15662-15668.
43. Lees-Miller SP, Anderson CW, (1989) Two human 90-kDa heat shock proteins are phosphorylated in vivo at conserved serines that are phosphorylated in vitro by casein kinase II. J Biol Chem 264: 2431-2437.
44. Sugimoto K, Himeno M, (1992) Casein kinase II site of human centromere protein B (CENP-B) is phosphorylated in vitro. Biosci Biotechnol Biochem 56: 1174-1175.
45. Gonzalez-Santos JM, Cao H, Duan RC, Hu J, (2008) Mutation in the splicing factor Hprp3p linked to retinitis pigmentosa impairs interactions within the U4/U6 snRNP complex. Hum Mol Genet 17: 225-239.
46. Wang D, Jang DJ, (2009) Protein kinase CK2 regulates cytoskeletal reorganization during ionizing radiation-induced senescence of human mesenchymal stem cells. Cancer Res 69: 8200-8207.
47. Saad FA, Salih E, Wunderlich L, Fluckiger R, Glimcher MJ, (2005) Prokaryotic expression of bone sialoprotein and identification of casein kinase II phosphorylation sites. Biochem Biophys Res Commun 333: 443-447.
48. Wells NJ, Addison CM, Fry AM, Ganapathi R, Hickson ID, (1994) Serine 1524 is a major site of phosphorylation on human topoisomerase II alpha protein in vivo and is a substrate for casein kinase II in vitro. J Biol Chem 269: 29746-29751.
49. Escargueil AE, Plisov SY, Filhol O, Cochet C, Larsen AK, (2000) Mitotic phosphorylation of DNA topoisomerase II alpha by protein kinase CK2 creates the MPM-2 phosphoepitope on Ser-1469. J Biol Chem 275: 34710-34718.