Proteome-wide analysis of temporal phosphorylation dynamics in lysophosphatidic acid-induced signaling

Proteomics

Volumn 12, Issue 23-24, 2012, Pages 3485-3498

  Mäusbacher, Nina ^a,c   Schreiber, Thiemo B ^a   Machatti, Manuela ^b   Schaab, Christoph ^a,b   Daub, Henrik ^a,b  

^a MAX PLANCK INSTITUTE OF BIOCHEMISTRY   (Germany)

^b EVOTEC AG   (Germany)

^c TECHNICAL UNIVERSITY OF MUNICH   (Germany)

Author keywords

Kinases; Lysophosphatidic acid; Phosphoproteomics; Seven transmembrane receptors; SILAC; Systems biology

Indexed keywords

6 PHOSPHOFRUCTO 2 KINASE; CALCIUM CALMODULIN DEPENDENT PROTEIN KINASE II; EPIDERMAL GROWTH FACTOR RECEPTOR; LYSOPHOSPHATIDIC ACID; MITOGEN ACTIVATED PROTEIN KINASE 1; MITOGEN ACTIVATED PROTEIN KINASE 14; MITOGEN ACTIVATED PROTEIN KINASE 3; MITOGEN ACTIVATED PROTEIN KINASE 9; NUCLEOPORIN; PAXILLIN; PHOSPHOTRANSFERASE; POLYCYSTIN 2; PROTEIN KINASE C DELTA; STRESS ACTIVATED PROTEIN KINASE 1; TUMOR NECROSIS FACTOR RECEPTOR ASSOCIATED FACTOR 2;

ARTICLE; BIOINFORMATICS; CONTROLLED STUDY; ENZYME ACTIVITY; PRIORITY JOURNAL; PROTEIN ANALYSIS; PROTEIN PHOSPHORYLATION; REPRODUCIBILITY; SIGNAL TRANSDUCTION;

CELL LINE; HUMANS; LYSOPHOSPHOLIPIDS; MASS SPECTROMETRY; PHOSPHOPROTEINS; PHOSPHORYLATION; PHOSPHOTRANSFERASES; PROTEIN INTERACTION MAPS; PROTEOME; PROTEOMICS; REPRODUCIBILITY OF RESULTS; SIGNAL TRANSDUCTION;

EID: 84871259137     PISSN: 16159853     EISSN: 16159861     Source Type: Journal    
DOI: 10.1002/pmic.201200172     Document Type: Article

References (60)

1. Ubersax, J. A., Ferrell, J. E., Jr., Mechanisms of specificity in protein phosphorylation. Nat. Rev. Mol. Cell Biol. 2007, 8, 530-541.
2. Manning, G., Whyte, D. B., Martinez, R., Hunter, T., Sudarsanam, S., The protein kinase complement of the human genome. Science 2002, 298, 1912-1934.
3. Mallick, P., Kuster, B., Proteomics: a pragmatic perspective. Nat. Biotechnol. 2010, 28, 695-709.
4. Villen, J., Gygi, S. P., The SCX/IMAC enrichment approach for global phosphorylation analysis by mass spectrometry. Nat. Protoc. 2008, 3, 1630-1638.
5. Trost, M., Bridon, G., Desjardins, M., Thibault, P., Subcellular phosphoproteomics. Mass Spectrom. Rev. 2010, 29, 962-990.
6. Olsen, J. V., de Godoy, L. M., Li, G., Macek, B. et al., Parts per million mass accuracy on an Orbitrap mass spectrometer via lock mass injection into a C-trap. Mol. Cell Proteomics 2005, 4, 2010-2021.
7. Mann, M., Functional and quantitative proteomics using SILAC. Nat. Rev. Mol. Cell Biol. 2006, 7, 952-958.
8. Cox, J., Mann, M., MaxQuant enables high peptide identification rates, individualized p.p.b.-range mass accuracies and proteome-wide protein quantification. Nat. Biotechnol. 2008, 26, 1367-1372.
9. Olsen, J. V., Vermeulen, M., Santamaria, A., Kumar, C. et al., Quantitative phosphoproteomics reveals widespread full phosphorylation site occupancy during mitosis. Sci. Signal 2010, 3, ra3.
10. Weintz, G., Olsen, J. V., Fruhauf, K., Niedzielska, M. et al., The phosphoproteome of toll-like receptor-activated macrophages. Mol. Syst. Biol. 2010, 6, 371.
11. Dephoure, N., Zhou, C., Villen, J., Beausoleil, S. A. et al., A quantitative atlas of mitotic phosphorylation. Proc. Natl. Acad. Sci. USA 2008, 105, 10762-10767.
12. Van Hoof, D., Munoz, J., Braam, S. R., Pinkse, M. W. et al., Phosphorylation dynamics during early differentiation of human embryonic stem cells. Cell Stem Cell 2009, 5, 214-226.
13. Chen, R. Q., Yang, Q. K., Lu, B. W., Yi, W. et al., CDC25B mediates rapamycin-induced oncogenic responses in cancer cells. Cancer Res. 2009, 69, 2663-2668.
14. Bennetzen, M. V., Larsen, D. H., Bunkenborg, J., Bartek, J. et al., Site-specific phosphorylation dynamics of the nuclear proteome during the DNA damage response. Mol. Cell Proteomics 2010, 9, 1314-1323.
15. Olsen, J. V., Blagoev, B., Gnad, F., Macek, B. et al., Global, in vivo, and site-specific phosphorylation dynamics in signaling networks. Cell 2006, 127, 635-648.
16. Hoffert, J. D., Pisitkun, T., Saeed, F., Song, J. H. et al., Dynamics of the G protein-coupled vasopressin V2 receptor signaling network revealed by quantitative phosphoproteomics. Mol. Cell Proteomics 2012, 11, M111.014613.
17. Xiao, K., Sun, J., Kim, J., Rajagopal, S. et al., Global phosphorylation analysis of beta-arrestin-mediated signaling downstream of a seven transmembrane receptor (7TMR). Proc. Natl. Acad. Sci. USA 2010, 107, 15299-15304.
18. Christensen, G. L., Kelstrup, C. D., Lyngso, C., Sarwar, U. et al., Quantitative phosphoproteomics dissection of seven-transmembrane receptor signaling using full and biased agonists. Mol. Cell Proteomics 2010, 9, 1540-1553.
19. Rinschen, M. M., Yu, M. J., Wang, G., Boja, E. S. et al., Quantitative phosphoproteomic analysis reveals vasopressin V2-receptor-dependent signaling pathways in renal collecting duct cells. Proc. Natl. Acad. Sci. USA 2010, 107, 3882-3887.
20. Schreiber, T. B., Mausbacher, N., Keri, G., Cox, J., Daub, H., An integrated phosphoproteomics workflow reveals extensive network regulation in early lysophosphatidic acid signaling. Mol. Cell Proteomics 2010, 9, 1047-1062.
21. Pierce, K. L., Premont, R. T., Lefkowitz, R. J., Seven-transmembrane receptors. Nat. Rev. Mol. Cell Biol. 2002, 3, 639-650.
22. Radeff-Huang, J., Seasholtz, T. M., Matteo, R. G., Brown, J. H., G protein mediated signaling pathways in lysophospholipid induced cell proliferation and survival. J. Cell Biochem. 2004, 92, 949-966.
23. Gschwind, A., Hart, S., Fischer, O. M., Ullrich, A., TACE cleavage of proamphiregulin regulates GPCR-induced proliferation and motility of cancer cells. EMBO J. 2003, 22, 2411-2421.
24. Prenzel, N., Zwick, E., Daub, H., Leserer, M. et al., EGF receptor transactivation by G-protein-coupled receptors requires metalloproteinase cleavage of proHB-EGF. Nature 1999, 402, 884-888.
25. Mills, G. B., Moolenaar, W. H., The emerging role of lysophosphatidic acid in cancer. Nat. Rev. Cancer 2003, 3, 582-591.
26. Mausbacher, N., Schreiber, T. B., Daub, H., Glycoprotein capture and quantitative phosphoproteomics indicate coordinated regulation of cell migration upon lysophosphatidic acid stimulation. Mol. Cell Proteomics 2010, 9, 2337-2353.
27. Oppermann, F. S., Grundner-Culemann, K., Kumar, C., Gruss, O. J. et al., Combination of chemical genetics and phosphoproteomics for kinase signaling analysis enables confident identification of cellular downstream targets. Mol. Cell Proteomics 2012, 11, O111.012351.
28. Daub, H., Olsen, J. V., Bairlein, M., Gnad, F. et al., Kinase-selective enrichment enables quantitative phosphoproteomics of the kinome across the cell cycle. Mol. Cell 2008, 31, 438-448.
29. Schroeder, M. J., Shabanowitz, J., Schwartz, J. C., Hunt, D. F. et al., A neutral loss activation method for improved phosphopeptide sequence analysis by quadrupole ion trap mass spectrometry. Anal. Chem. 2004, 76, 3590-3598.
30. Elias, J. E., Haas, W., Faherty, B. K., Gygi, S. P., Comparative evaluation of mass spectrometry platforms used in large-scale proteomics investigations. Nat. Methods 2005, 2, 667-675.
31. Cox, J., Mann, M., MaxQuant enables high peptide identification rates, individualized p.p.b.-range mass accuracies and proteome-wide protein quantification. Nat. Biotechnol. 2008, 26, 1367-1372.
32. Zhou, Y., Cras-Meneur, C., Ohsugi, M., Stormo, G. D., Permutt, M. A., A global approach to identify differentially expressed genes in cDNA (two-color) microarray experiments. Bioinformatics 2007, 23, 2073-2079.
33. Gnad, F., Gunawardena, J., Mann, M., PHOSIDA 2011: the posttranslational modification database. Nucleic Acids Res. 2011, 39, D253-D260.
34. Harris, M. A., Clark, J., Ireland, A., Lomax, J. et al., The gene ontology (GO) database and informatics resource. Nucleic Acids Res. 2004, 32, D258-D261.
35. Klammer, M., Godl, K., Tebbe, A., Schaab, C., Identifying differentially regulated subnetworks from phosphoproteomic data. BMC Bioinformatics 2010, 11, 351.
36. Jensen, L. J., Kuhn, M., Stark, M., Chaffron, S. et al., STRING 8-a global view on proteins and their functional interactions in 630 organisms. Nucl. Acids Res. 2009, 37, D412-D416.
37. Cline, M. S., Smoot, M., Cerami, E., Kuchinsky, A. et al., Integration of biological networks and gene expression data using Cytoscape. Nat. Protoc. 2007, 2, 2366-2382.
38. Weber, C., Schreiber, T. B., Daub, H., Dual phosphoproteomics and chemical proteomics analysis of erlotinib and gefitinib interference in acute myeloid leukemia cells. J. Proteomics 2012, 75, 1343-1356.
39. Songyang, Z., Lu, K. P., Kwon, Y. T., Tsai, L. H. et al., A structural basis for substrate specificities of protein Ser/Thr kinases: primary sequence preference of casein kinases I and II, NIMA, phosphorylase kinase, calmodulin-dependent kinase II, CDK5, and Erk1. Mol. Cell Biol. 1996, 16, 6486-6493.
40. Amanchy, R., Periaswamy, B., Mathivanan, S., Reddy, R. et al., A curated compendium of phosphorylation motifs. Nat. Biotechnol. 2007, 25, 285-286.
41. Nishikawa, K., Toker, A., Johannes, F. J., Songyang, Z. et al., Determination of the specific substrate sequence motifs of protein kinase C isozymes. J. Biol. Chem. 1997, 272, 952-960.
42. Durgan, J., Michael, N., Totty, N., Parker, P. J., Novel phosphorylation site markers of protein kinase C delta activation. FEBS Lett. 2007, 581, 3377-3381.
43. Sturany, S., Van Lint, J., Gilchrist, A., Vandenheede, J. R. et al., Mechanism of activation of protein kinase D2(PKD2) by the CCK(B)/gastrin receptor. J. Biol. Chem. 2002, 277, 29431-29436.
44. Miller, M. L., Jensen, L. J., Diella, F., Jorgensen, C. et al., Linear motif atlas for phosphorylation-dependent signaling. Sci. Signal 2008, 1, ra2.
45. Trencia, A., Perfetti, A., Cassese, A., Vigliotta, G. et al., Protein kinase B/Akt binds and phosphorylates PED/PEA-15, stabilizing its antiapoptotic action. Mol. Cell Biol. 2003, 23, 4511-4521.
46. Bando, H., Atsumi, T., Nishio, T., Niwa, H. et al., Phosphorylation of the 6-phosphofructo-2-kinase/fructose 2, 6-bisphosphatase/PFKFB3 family of glycolytic regulators in human cancer. Clin. Cancer Res. 2005, 11, 5784-5792.
47. Esteve, P. O., Chang, Y., Samaranayake, M., Upadhyay, A. K. et al., A methylation and phosphorylation switch between an adjacent lysine and serine determines human DNMT1 stability. Nat. Struct. Mol. Biol. 2011, 18, 42-48.
48. Puc, J., Keniry, M., Li, H. S., Pandita, T. K. et al., Lack of PTEN sequesters CHK1 and initiates genetic instability. Cancer Cell 2005, 7, 193-204.
49. Palamarchuk, A., Efanov, A., Maximov, V., Aqeilan, R. I. et al., Akt phosphorylates and regulates Pdcd4 tumor suppressor protein. Cancer Res. 2005, 65, 11282-11286.
50. Kitani, T., Okuno, S., Fujisawa, H., Regulation of Ca(2+)/calmodulin-dependent protein kinase kinase alpha by cAMP-dependent protein kinase: II. Mutational analysis. J. Biochem. 2001, 130, 515-525.
51. Dorsch, M., Wang, A., Cheng, H., Lu, C. et al., Identification of a regulatory autophosphorylation site in the serine-threonine kinase RIP2. Cell Signal 2006, 18, 2223-2229.
52. Raman, M., Earnest, S., Zhang, K., Zhao, Y., Cobb, M. H., TAO kinases mediate activation of p38 in response to DNA damage. EMBO J. 2007, 26, 2005-2014.
53. Benjamini, Y., Hochberg, Y., Controlling the false discovery rate: a practical and powerful approach to multiple testing. J. Roy. Stat. Soc. B Met. 1995, 57, 289-300.
54. Ouwens, D. M., de Ruiter, N. D., van der Zon, G. C., Carter, A. P. et al., Growth factors can activate ATF2 via a two-step mechanism: phosphorylation of Thr71 through the Ras-MEK-ERK pathway and of Thr69 through RalGDS-Src-p38. EMBO J. 2002, 21, 3782-3793.
55. Blackwell, K., Zhang, L., Thomas, G. S., Sun, S. et al., TRAF2 phosphorylation modulates tumor necrosis factor alpha-induced gene expression and cell resistance to apoptosis. Mol. Cell Biol. 2009, 29, 303-314.
56. White, C. D., Erdemir, H. H., Sacks, D. B., IQGAP1 and its binding proteins control diverse biological functions. Cell Signal 2012, 24, 826-834.
57. Li, Z., McNulty, D. E., Marler, K. J., Lim, L. et al., IQGAP1 promotes neurite outgrowth in a phosphorylation-dependent manner. J. Biol. Chem. 2005, 280, 13871-13878.
58. McNulty, D. E., Li, Z., White, C. D., Sacks, D. B. et al., MAPK scaffold IQGAP1 binds the EGF receptor and modulates its activation. J. Biol. Chem. 2011, 286, 15010-15021.
59. Kosako, H., Yamaguchi, N., Aranami, C., Ushiyama, M. et al., Phosphoproteomics reveals new ERK MAP kinase targets and links ERK to nucleoporin-mediated nuclear transport. Nat. Struct. Mol. Biol. 2009, 16, 1026-1035.
60. Lappano, R., Maggiolini, M., G protein-coupled receptors: novel targets for drug discovery in cancer. Nat. Rev. Drug Discov. 2011, 10, 47-60.