Phosphoproteomic analysis of the mouse brain cytosol reveals a predominance of protein phosphorylation in regions of intrinsic sequence diorder

Molecular and Cellular Proteomics

Volumn 7, Issue 7, 2008, Pages 1331-1348

  Collins, Mark O ^a   Yu, Lu ^a   Campuzano, Iain ^b   Grant, Seth G N ^a   Choudhary, Jyoti S ^a  

^a WELLCOME TRUST SANGER INSTITUTE   (United Kingdom)

^b WATERS CORPORATION   (United States)

Author keywords

[No Author keywords available]

Indexed keywords

BINDING PROTEIN; PHOSPHATASE; PHOSPHOPROTEIN; PHOSPHOTRANSFERASE; PROTEIN 14 3 3; STRUCTURAL PROTEIN;

AMINO ACID COMPOSITION; AMINO ACID SEQUENCE; ANIMAL TISSUE; ARTICLE; BINDING SITE; CELLULAR DISTRIBUTION; CONTROLLED STUDY; CYTOSOL; DEPHOSPHORYLATION; FOREBRAIN; LIQUID CHROMATOGRAPHY; MOUSE; NONHUMAN; NUCLEOTIDE SEQUENCE; PRIORITY JOURNAL; PROTEIN ANALYSIS; PROTEIN CONFORMATION; PROTEIN DOMAIN; PROTEIN INTERACTION; PROTEIN PHOSPHORYLATION; PROTEIN PURIFICATION; PROTEIN STRUCTURE; PROTEOMICS; SEQUENCE ANALYSIS; TANDEM MASS SPECTROMETRY;

ANIMALS; BRAIN CHEMISTRY; CLUSTER ANALYSIS; CYTOSOL; MICE; NEURODEGENERATIVE DISEASES; PHOSPHOPROTEINS; PHOSPHORYLATION; PROTEIN CONFORMATION; PROTEIN FOLDING; PROTEIN STRUCTURE, TERTIARY; PROTEOME; PROTEOMICS; SEQUENCE ANALYSIS, PROTEIN;

EID: 47849089500     PISSN: 15359476     EISSN: None     Source Type: Journal    
DOI: 10.1074/mcp.M700564-MCP200     Document Type: Article

References (80)

1. Ficarro, S. B., McCleland, M. L., Stukenberg, P. T., Burke, D. J., Ross, M. M., Shabanowitz, J., Hunt, D. F., and White, F. M. (2002) Phosphoproteome analysis by mass spectrometry and its application to Saccharomyces cerevisiae. Nat. Biotechnol. 20, 301-305
2. Nuhse, T. S., Stensballe, A., Jensen, O. N., and Peck, S. C. (2003) Large-scale analysis of in vivo phosphorylated membrane proteins by immobilized metal ion affinity chromatography and mass spectrometry. Mol. Cell. Proteomics 2, 1234-1243
3. Collins, M. O., Yu, L., Coba, M. P., Husi, H., Campuzano, I., Blackstock, W. P., Choudhary, J. S., and Grant, S. G. (2005) Proteomic analysis of in vivo phosphorylated synaptic proteins. J. Biol. Chem. 280, 5972-5982
4. Trinidad, J. C., Specht, C. G., Thalhammer, A., Schoepfer, R., and Burlingame, A. L. (2006) Comprehensive identification of phosphorylation sites in postsynaptic density preparations. Mol. Cell. Proteomics 5, 914-922
5. Olsen, J. V., Blagoev, B., Gnad, F., Macek, B., Kumar, C., Mortensen, P., and Mann, M. (2006) Global, in vivo, and site-specific phosphorylation dynamics in signaling networks. Cell 127, 635-648
6. Bodenmiller, B., Mueller, L. N., Mueller, M., Domon, B., and Aebersold, R. (2007) Reproducible isolation of distinct, overlapping segments of the phosphoproteome. Nat. Methods 4, 231-237
7. Villen, J., Beausoleil, S. A., Gerber, S. A., and Gygi, S. P. (2007) Large-scale phosphorylation analysis of mouse liver. Proc. Natl. Acad. Sci. U. S. A. 104, 1488-1493
8. Peters, E. C., Brock, A., and Ficarro, S. B. (2004) Exploring the phosphoproteome with mass spectrometry. Mini Rev. Med. Chem. 4, 313-324
9. Reinders, J., and Sickmann, A. (2005) State-of-the-art in phosphoproteomics. Proteomics 5, 4052-4061
10. Collins, M. O., Yu, L., and Choudhary, J. S. (2007) Analysis of protein phosphorylation on a proteome-scale. Proteomics 7, 2751-2768
11. Stensballe, A., Jensen, O. N., Olsen, J. V., Haselmann, K. F., and Zubarev, R. A. (2000) Electron capture dissociation of singly and multiply phosphorylated peptides. Rapid Commun. Mass Spectrom. 14, 1793-1800
12. Molina, H., Horn, D. M., Tang, N., Mathivanan, S., and Pandey, A. (2007) Global proteomic profiling of phosphopeptides using electron transfer dissociation tandem mass spectrometry. Proc. Natl. Acad. Sci. U. S. A. 104, 2199-2204
13. Chi, A., Huttenhower, C., Geer, L. Y., Coon, J. J., Syka, J. E. P., Bai, D. L., Shabanowitz, J., Burke, D. J., Troyanskaya, O. G., and Hunt, D. F. (2007) Analysis of phosphorylation sites on proteins from Saccharomyces cerevisiae by electron transfer dissociation (ETD) mass spectrometry. Proc. Natl. Acad. Sci. U. S. A. 104, 2193-2198
14. Johansen, J. W., and Ingebritsen, T. S. (1987) Effects of phosphorylation of protein phosphatase 1 by pp60v-src on the interaction of the enzyme with substrates and inhibitor proteins. Biochim. Biophys. Acta 928, 63-75
15. Ridsdale, R. A., Beniac, D. R., Tompkins, T. A., Moscarello, M. A., and Harauz, G. (1997) Three-dimensional structure of myelin basic protein. II. Molecular modeling and considerations of predicted structures in multiple sclerosis. J. Biol. Chem. 272, 4269-4275
16. Shen, T., Zong, C., Hamelberg, D., McCammon, J. A., and Wolynes, P. G. (2005) The folding energy landscape and phosphorylation: modeling the conformational switch of the NFAT regulatory domain. FASEB J. 19, 1389-1395
17. Iakoucheva, L. M., Radivojac, P., Brown, C. J., O'Connor, T. R., Sikes, J. G., Obradovic, Z., and Dunker, A. K. (2004) The importance of intrinsic disorder for protein phosphorylation. Nucleic Acids Res. 32, 1037-1049
18. Collins, M. O., Yu, L., Husi, H., Blackstock, W. P., Choudhary, J. S., and Grant, S. G. (2005) Robust enrichment of phosphorylated species in complex mixtures by sequential protein and peptide metal-affinity chromatography and analysis by tandem mass spectrometry. Sci. STKE 2005, pl6
19. Wright, P. E., and Dyson, H. J. (1999) Intrinsically unstructured proteins: re-assessing the protein structure-function paradigm. J. Mol. Biol. 293, 321-331
20. Obenauer, J. C., Cantley, L. C., and Yaffe, M. B. (2003) Scansite 2.0: proteome-wide prediction of cell signaling interactions using short sequence motifs. Nucleic Acids Res. 31, 3635-3641
21. Finn, R. D., Mistry, J., Schuster-Bockler, B., Griffiths-Jones, S., Hollich, V., Lassmann, T., Moxon, S., Marshall, M., Khanna, A., Durbin, R., Eddy, S. R., Sonnhammer, E. L., and Bateman, A. (2006) Pfam: clans, web tools and services. Nucleic Acids Res. 34, D247-D251
22. Vacic, V., Uversky, V. N., Dunker, A. K., and Lonardi, S. (2007) Composition Profiler: a tool for discovery and visualization of amino acid composition differences. BMC Bioinformatics 8, 211
23. Li, X., Romero, P., Rani, M., Dunker, A. K., and Obradovic, Z. (1999) Predicting protein disorder for N-, C-, and internal regions. Genome Inform. Ser. Workshop Genome Inform. 10, 30-40
24. Guex, N., and Peitsch, M. C. (1997) SWISS-MODEL and the Swiss-Pdb-Viewer: an environment for comparative protein modeling. Electrophoresis 18, 2714-2723
25. Schwartz, D., and Gygi, S. P. (2005) An iterative statistical approach to the identification of protein phosphorylation motifs from large-scale data sets. Nat. Biotechnol. 23, 1391-1398
26. Zhang, B., Kirov, S., and Snoddy, J. (2005) WebGestalt: an integrated system for exploring gene sets in various biological contexts. Nucleic Acids Res. 33, W741-W748
27. Halpain, S., and Dehmelt, L. (2006) The MAP1 family of microtubule-associated proteins. Genome Biol. 7, 224
28. Mukhopadhyay, R., and Hoh, J. H. (2001) AFM force measurements on microtubule-associated proteins: the projection domain exerts a long-range repulsive force. FEBS Lett. 505, 374-378
29. Ballif, B. A., Villen, J., Beausoleil, S. A., Schwartz, D., and Gygi, S. P. (2004) Phosphoproteomic analysis of the developing mouse brain. Mol. Cell. Proteomics 3, 1093-1101
30. Munton, R. P., Tweedie-Cullen, R., Livingstone-Zatchej, M., Weinandy, F., Waidelich, M., Longo, D., Gehrig, P., Potthast, F., Rutishauser, D., Gerrits, B., Panse, C., Schlapbach, R., and Mansuy, I. M. (2007) Qualitative and quantitative analyses of protein phosphorylation in naive and stimulated mouse synaptosomal preparations. Mol. Cell. Proteomics 6, 283-293
31. Trinidad, J. C., Thalhammer, A., Specht, C. G., Lynn, A. J., Baker, P. R., Schoepfer, R., and Burlingame, A. L. (2008) Quantitative analysis of synaptic phosphorylation and protein expression. Mol. Cell. Proteomics 7, 684-696
32. Xie, H., Vucetic, S., Iakoucheva, L. M., Oldfield, C. J., Dunker, A. K., Uversky, V. N., and Obradovic, Z. (2007) Functional anthology of intrinsic disorder. 1. Biological processes and functions of proteins with long disordered regions. J. Proteome Res. 6, 1882-1898
33. Barghorn, S., Davies, P., and Mandelkow, E. (2004) Tau paired helical filaments from Alzheimer's disease brain and assembled in vitro are based on β-structure in the core domain. Biochemistry 43, 1694-1703
34. Imanishi, S. Y., Kochin, V., Ferraris, S. E., de Thonel, A., Pallari, H. M., Corthals, G. L., and Eriksson, J. E. (2007) Reference-facilitated phosphoproteomics: fast and reliable phosphopeptide validation by μLC-ESI-Q-TOF MS/MS. Mol. Cell. Proteomics 6, 1380-1391
35. Marcantonio, M., Trost, M., Courcelles, M., Desjardins, M., and Thibault, P. (2008) Combined enzymatic and data mining approaches for comprehensive phosphoproteome analyses. Application to cell signaling events of interferon-stimulated macrophages. Mol. Cell. Proteomics 7, 645-660
36. Honnappa, S., Jahnke, W., Seelig, J., and Steinmetz, M. O. (2006) Control of intrinsically disordered stathmin by multisite phosphorylation. J. Biol. Chem. 281, 16078-16083
37. Nikolakaki, E., Drosou, V., Sanidas, I., Peidis, P., Papamarcaki, T., Iakoucheva, L. M., and Giannakouros, T. (2008) RNA association or phosphorylation of the RS domain prevents aggregation of RS domain-containing proteins. Biochim. Biophys. Acta 1780, 214-225
38. Tanoue, T., Adachi, M., Moriguchi, T., and Nishida, E. (2000) A conserved docking motif in MAP kinases common to substrates, activators and regulators. Nat. Cell Biol. 2, 110-116
39. Holland, P. M., and Cooper, J. A. (1999) Protein modification: docking sites for kinases. Curr. Biol. 9, R329-R331
40. Gavin, A. C., and Nebreda, A. R. (1999) A MAP kinase docking site is required for phosphorylation and activation of p90(rsk)/MAPKAP kinase-1. Curr. Biol. 9, 281-284
41. Dyson, H. J., and Wright, P. E. (2005) Intrinsically unstructured proteins and their functions. Nat. Rev. Mol. Cell Biol. 6, 197-208
42. Haynes, C., Oldfield, C. J., Ji, F., Klitgord, N., Cusick, M. E., Radivojac, P., Uversky, V. N., Vidal, M., and lakoucheva, L. M. (2006) Intrinsic disorder is a common feature of hub proteins from four eukaryotic interactomes. PLoS Comput. Biol. 2, e100
43. Dunker, A. K., Cortese, M. S., Romero, P., lakoucheva, L. M., and Uversky, V. N. (2005) Flexible nets. The roles of intrinsic disorder in protein interaction networks. FEBS J. 272, 5129-5148
44. Tompa, P. (2003) Intrinsically unstructured proteins evolve by repeat expansion. BioEssays 25, 847-855
45. Linding, R., Jensen, L. J., Diella, F., Bork, P., Gibson, T. J., and Russell, R. B. (2003) Protein disorder prediction: implications for structural proteomics. Structure (Camb.) 11, 1453-1459
46. Cao, W., and Garcia-Blanco, M. A. (1998) A serine/arginine-rich domain in the human U1 70k protein is necessary and sufficient for ASIF/SF2 binding. J. Biol. Chem. 273, 20629-20635
47. Xiao, S. H., and Manley, J. L. (1997) Phosphorylation of the ASF/SF2 RS domain affects both protein-protein and protein-RNA interactions and is necessary for splicing. Genes Dev. 11, 334-344
48. Cao, W., Jamison, S. F., and Garcia-Blanco, M. A. (1997) Both phosphorylation and dephosphorylation of ASF/SF2 are required for pre-mRNA splicing in vitro. RNA 3,1456-1467
49. Graveley, B. R. (2000) Sorting out the complexity of SR protein functions. RNA 6, 1197-1211
50. Blencowe, B. J., Bauren, G., Eldridge, A. G., Issner, R., Nickerson, J. A., Rosonina, E., and Sharp, P. A. (2000) The SRml60/300 splicing coactivator subunits. RNA 6, 111-120
51. Kojima, T., Zama, T., Wade, K., Onogi, H., and Hagiwara, M. (2001) Cloning of human PRP4 reveals interaction with Clk1. J. Biol. Chem. 276, 32247-32256
52. Colwill, K., Pawson, T., Andrews, B., Prasad, J., Manley, J. L., Bell, J. C., and Duncan, P. I. (1996) The Clk/Sty protein kinase phosphorylates SR splicing factors and regulates their intranuclear distribution. EMBO J. 15, 265-275
53. Lin, C. L., Leu, S., Lu, M. C., and Ouyang, P. (2004) Over-expression of SR-cyclophilin, an interaction partner of nuclear pinin, releases SR family splicing factors from nuclear speckles. Biochem. Biophys. Res. Commun. 321, 638-647
54. Hughes, C. A., and Bennett, V. (1995) Adducin: a physical model with implications for function in assembly of spectrin-actin complexes. J. Biol. Chem. 270, 18990-18996
55. Matsuoka, Y., Li, X., and Bennett, V. (1998) Adducin is an in vivo substrate for protein kinase C: phosphorylation in the MARCKS-related domain inhibits activity in promoting spectrin-actin complexes and occurs in many cells, including dendritic spines of neurons. J. Cell Biol. 142, 485-497
56. Orosz, F., Kovacs, G. G., Lehotzky, A., Olah, J., Vincze, O., and Ovadi, J. (2004) TPPP/p25: from unfolded protein to misfolding disease: prediction and experiments. Biol. Cell 96, 701-711
57. Otzen, D. E., Lundvig, D. M., Wimmer, R., Nielsen, L. H., Pedersen, J. R., and Jensen, P. H. (2005) p25α is flexible but natively folded and binds tubulin with oligomeric stoichiometry. Protein Sci. 14, 1396-1409
58. Tirian, L., Hlavanda, E., Olah, J., Horvath, I., Orosz, F., Szabo, B., Kovacs, J., Szabad, J., and Ovadl, J. (2003) TPPP/p25 promotes tubulin assemblies and blocks mitotic spindle formation. Proc. Natl. Acad. Sci. U. S. A. 100, 13976-13981
59. Takahashi, M., Tomizawa, K., Ishiguro, K., Sato, K., Omori, A., Sato, S., Shiratsuchi, A., Uchida, T., and Imahori, K. (1991) A novel brain-specific 25 kDa protein (p25) is phosphorylated by a Ser/Thr-Pro kinase (TPK II) from tau protein kinase fractions. FEBS Lett. 289, 37-43
60. Lee, G., Neve, R. L., and Kosik, K. S. (1989) The microtubule binding domain of tau protein. Neuron 2, 1615-1624
61. Jiang, Z., Tang, H., Havlioglu, N., Zhang, X., Stamm, S., Yan, R., and Wu, J. Y. (2003) Mutations in tau gene exon 10 associated with FTDP-17 alter the activity of an exonic splicing enhancer to interact with Tra2β. J. Biol. Chem. 278, 18997-19007
62. Kondo, S., Yamamoto, N., Murakami, T., Okumura, M., Mayeda, A., and Imaizumi, K. (2004) Tra2β, SF2/ASF and SRp30c modulate the function of an exonic splicing enhancer in axon 10 of tau pre-mRNA. Genes Cells 9, 121-130
63. Goode, B. L., Denis, P. E., Panda, D., Radeke, M. J., Miller, H. P., Wilson, L., and Feinstein, S. C. (1997) Functional interactions between the proline-rich and repeat regions of tau enhance microtubule binding and assembly. Mol. Biol. Cell 8, 353-365
64. Mandelkow, E. (1999) Alzheimer's disease. The tangled tale of tau. Nature 402, 588-589
65. Yau, J. L., Rasmuson, S., Andrew, R., Graham, M., Noble, J., Olsson, T., Fuchs, E., Lathe, R., and Seckl, J. R. (2003) Dehydroepiandrosterone 7-hydroxylase CYP7B: predominant expression in primate hippocampus and reduced expression in Alzheimer's disease. Neuroscience 121, 307-314
66. Shim, K. S., and Lubec, G. (2002) Drebrin, a dendritic spine protein, is manifold decreased in brains of patients with Alzheimer's disease and Down syndrome. Neurosci. Lett. 324, 209-212
67. Del Villar, K., and Miller, C. A. (2004) Down-regulation of DENN/MADD, a TNF receptor binding protein, correlates with neuronal cell death in Alzheimer's disease brain and hippocampal neurons. Proc. Natl. Acad. Sci. U. S. A. 101, 4210-4215
68. Goehler, H., Lalowski, M., Stelzl, U., Waelter, S., Stroedicke, M., Worm, U., Droege, A., Lindenberg, K. S., Knoblich, M., Haenig, C., Herbst, M., Suopanki, J., Scherzinger, E., Abraham, C., Bauer, B., Hasenbank, R., Fritzsche, A., Ludewig, A. H., Bussow, K., Coleman, S. H., Gutekunst, C. A., Landwehrmeyer, B. G., Lehrach, H., and Wanker, E. E. (2004) A protein interaction network links GIT1, an enhancer of huntingtin aggregation, to Huntington's disease. Mol. Cell 15, 853-865
69. Yin, G., Zheng, Q., Yan, C., and Berk, B. C. (2005) GIT1 is a scaffold for ERK1/2 activation in focal adhesions. J. Biol. Chem. 280, 27705-27712
70. Cole, A. R., Knebel, A., Morrice, N. A., Robertson, L. A., Irving, A. J., Connolly, C. N., and Sutherland, C. (2004) GSK-3 phosphorylation of the Alzheimer epitope within collapsin response mediator proteins regulates axon elongation in primary neurons. J. Biol. Chem. 279, 50176-50180
71. Gu, Y., Hamajima, N., and Ihara, Y. (2000) Neurofibrillary tangle-associated collapsin response mediator protein-2 (CRMP-2) is highly phosphorylated on Thr-509, Ser-518, and Ser-522. Biochemistry 39, 4267-4275
72. Uchida, Y., Ohshima, T., Sasaki, Y., Suzuki, H., Yanai, S., Yamashita, N., Nakamura, F., Takei, K., Ihara, Y., Mikoshiba, K., Kolattukudy, P., Honnorat, J., and Goshima, Y. (2005) Semaphorin3A signalling is mediated via sequential Cdk5 and GSK3β phosphorylation of CRMP2: implication of common phosphorylating mechanism underlying axon guidance and Alzheimer's disease. Genes Cells 10, 165-179
73. Zoghbi, H. Y. (1995) Spinocerebellar ataxia type 1. Clin. Neurosci. 3, 5-11
74. Chen, H. K., Fernandez-Funez, P., Acevedo, S. F., Lam, Y. C., Kaytor, M. D., Fernandez, M. H., Aitken, A., Skoulakis, E. M., Orr, H. T., Botas, J., and Zoghbi, H. Y. (2003) Interaction of Akt-phosphorylated ataxin-1 with 14-3-3 mediates neurodegeneration in spinocerebellar ataxia type 1. Cell 113, 457-468
75. Emamian, E. S., Kaytor, M. D., Duvick, L. A., Zu, T., Tousey, S. K., Zoghbi, H. Y., Clark, H. B., and Orr, H. T. (2003) Serine 776 of ataxin-1 is critical for polyglutamine-induced disease in SCA1 transgenic mice. Neuron 38, 375-387
76. Ralser, M., Albrecht, M., Nonhoff, U., Lengauer, T., Lehrach, H., and Krobitsch, S. (2005) An integrative approach to gain insights into the cellular function of human ataxin-2. J. Mol. Biol. 346, 203-214
77. Nagafuchi, S., Yanagisawa, H., Ohsaki, E., Shirayama, T., Tadokoro, K., Inoue, T., and Yamada, M. (1994) Structure and expression of the gene responsible for the triplet repeat disorder, dentatorubral and pallidoluysian atrophy (DRPLA). Nat. Genet. 8, 177-182
78. Fountain, J. W., Wallace, M. R., Bruce, M. A., Seizinger, B. R., Menon, A. G., Gusella, J. F., Michels, V. V., Schmidt, M. A., Dewald, G. W., and Collins, F. S. (1989) Physical mapping of a translocation breakpoint in neurofibromatosis. Science 244, 1085-1087
79. Zhao, C., Takita, J., Tanaka, Y., Setou, M., Nakagawa, T., Takeda, S., Yang, H. W., Terada, S., Nakata, T., Takei, Y., Saito, M., Tsuji, S., Hayashi, Y., and Hirokawa, N. (2001) Charcot-Marie-Tooth disease type 2A caused by mutation in a microtubule motor KIF1Bβ. Cell 105, 587-597
80. Villard, L., Toutain, A., Lossi, A. M., Gecz, J., Houdayer, C., Moraine, C., and Fontes, M. (1996) Splicing mutation in the ATR-X gene can lead to a dysmorphic mental retardation phenotype without α-thalassemia. Am. J. Hum. Genet. 58, 499-505