Assignment of protein function in the postgenomic era

Nature Chemical Biology

Volumn 1, Issue 3, 2005, Pages 129-

  Saghatelian, Alan ^a   Cravatt, Benjamin F ^a  

^a SCRIPPS RESEARCH INSTITUTE   (United States)

Author keywords

[No Author keywords available]

Indexed keywords

PROTEIN;

AMINO ACID SEQUENCE; BACTERIUM; BIOLOGICAL MODEL; CHEMICAL STRUCTURE; CHEMISTRY; ENZYMOLOGY; METHODOLOGY; PHYSIOLOGY; PROTEIN PROCESSING; PROTEOMICS; REVIEW; SEQUENCE ALIGNMENT;

AMINO ACID SEQUENCE; BACTERIA; MODELS, BIOLOGICAL; MOLECULAR STRUCTURE; PROTEIN PROCESSING, POST-TRANSLATIONAL; PROTEINS; PROTEOMICS; SEQUENCE ALIGNMENT;

EID: 84984752764     PISSN: 15524450     EISSN: 15524469     Source Type: Journal    
DOI: 10.1038/nchembio0805-130     Document Type: Article

References (113)

1. Gerlt, J.A. & Babbitt, P.C. Divergent evolution of enzymatic function: mechanistically diverse superfamilies and functionally distinct suprafamilies. Annu. Rev. Biochem. 70, 209-246 (2001).
2. Walsh, C.T. Posttranslational Modification of Proteins. Expanding Natures lnventory (Roberts & Company, Greenwood Village, Colorado, USA, 2005).
3. Austin, C.P. et al. The knockout mouse project. Nat. Genet. 36, 921-924 (2004).
4. Carpenter, A.E. & Sabatini, D.M. Systematic genome-wide screens of gene function. Nat. Rev. Genet. 5, 11-22 (2004).
5. Clardy, J. & Walsh, C. Lessons from natural molecules. Nature 432, 829-837 (2004).
6. 8-barrel enzymes. Curr. Opin. Chem. Biol. 7, 252-264 (2003).
7. Neidhart, D.J., Kenyon, G.L., Gerlt, J.A. & Petsko, G.A. Mandelate racemase and muconate lactonizing enzyme are mechanistically distinct and structurally homolo-gous. Nature 347, 692-694 (1990).
8. Osterman, A. & Overbeek, R. Missing genes in metabolic pathways: a comparative genomics approach. Curr. Opin. Chem. Biol. 7, 238-251 (2003).
9. Schmidt, D.M., Hubbard, B.K. & Gerlt, J.A. Evolution of enzymatic activities in the enolase superfamily: functional assignment of unknown proteins in Bacillus subtilis and Escherichia coli as L-Ala-D/L-Glu epimerases. Biochemistry40, 15707-15715 (2001).
10. Wise, E., Yew, W.S., Babbitt, P.C., Gerlt, J.A. & Rayment, I. Homologous (p/a)8-barrel enzymes that catalyze unrelated reactions: orotidine 5′-monophosphate decarboxyl- ase and 3-keto-L-gulonate 6-phosphate decarboxylase. Biochemistry41, 3861-3869 (2002).
11. Wang, S.C., Person, M.D., Johnson, W.H., Jr & Whitman, C.P. Reactions of trans-3-chloroacrylic acid dehalogenase with acetylene substrates: consequences of and evidence for a hydration reaction. Biochemistry 42, 8762-8773 (2003).
12. de Jong, R.M., Brugman, W., Poelarends, G.J., Whitman, C.P. & Dijkstra, B.W. The X-ray structure of trans-3-chloroacrylic acid dehalogenase reveals a novel hydration mechanism in the tautomerase superfamily. J. Biol. Chem. 279, 11546-11552 (2004).
13. Mizanur, R.M., Jaipuri, F.A. & Pohl, N.L. One-step synthesis of labeled sugar nucleo-tides for protein O-GlcNAc modification studies by chemical function analysis of an archaeal protein. J. Am. Chem. Soc. 127, 836-837 (2005).
14. Kurnasov, O. et al. NAD biosynthesis: identification of the tryptophan to quinolinate pathway in bacteria. Chem. Biol. 10, 1195-1204 (2003).
15. Zhuang, Z., Gartemann, K.H., Eichenlaub, R. & Dunaway-Mariano, D. Characterization of the 4-hydroxybenzoyl-coenzyme A thioesterase from Arthrobacter sp. strain SU. Appl. Environ. Microbiol. 69, 2707-2711 (2003).
16. Patterson, S.D. & Aebersold, R. Proteomics: the first decade and beyond. Nat. Genet. 33, 311-323 (2003).
17. de Hoog, C.L. & Mann, M. Proteomics. Annu. Rev. Genomics Hum. Genet. 5, 267-293 (2004).
18. Corthals, G.L., Wasinger, V.C., Hochstrasser, D.F. & Sanchez, J.C. The dynamic range of protein expressioin: a challenge for proteomic research. Electrophoresis 21, 1104-1115 (2000).
19. Adam, G.C., Sorensen, E.J. & Cravatt, B.F. Chemical strategies for functional pro-teomics. Mol. Cell. Proteomics 1, 781-790 (2002).
20. Verhelst, S.H. & Bogyo, M. Chemical proteomics applied to target identification and drug discovery. Biotechniques 38, 175-177 (2005).
21. Brown, P.O. & Botstein, D. Exploring the new world of the genome with DNA microar-rays. Nat. Genet. 21, 33-37 (1999).
22. Aebersold, R. & Mann, M. Mass spectrometry-based proteomics. Nature 422, 198-207 (2003).
23. Kobe, B. & Kemp, B.E. Active site-directed protein regulation. Nature 402, 373-376 (1999).
24. Liu, Y., Patricelli, M.P. & Cravatt, B.F. Activity-based protein profiling: the serine hydrolases. Proc. Natl. Acad. Sci. USA 96, 14694-14699 (1999).
25. Jessani, N. & Cravatt, B.F. The development and application of methods for activity-based protein profiling. Curr. Opin. Chem. Biol. 8, 54-59 (2004).
26. Berger, A.B., Vitorino, P.M. & Bogyo, M. Activity-based protein profiling: applications to biomarker discovery, in vivo imaging and drug discovery. Am. J. Pharmacogenomics 4, 371-381 (2004).
27. Kidd, D., Liu, Y. & Cravatt, B.F. Profiling serine hydrolase activities in complex proteomes. Biochemistry 40, 4005-4015 (2001).
28. Jessani, N., Liu, Y., Humphrey, M. & Cravatt, B.F. Enzyme activity profiles of the secreted and membrane proteome that depict cancer invasiveness. Proc. Natl. Acad. Sci. USA 99, 10335-10340 (2002).
29. Greenbaum, D. et al. Chemical approaches for functionally probing the proteome. Mol. Cell. Proteomics 1, 60-68 (2002).
30. Sieber, S.A., Mondala, T.S., Head, S.R. & Cravatt, B.F. Microarray platform for profiling enzyme activities in complex proteomes. J. Am. Chem. Soc. 126, 15640-15641 (2004).
31. Adam, G.C., Burbaum, J.J., Kozarich, J.W., Patricelli, M.P. & Cravatt, B.F. Mapping enzyme active sites in complex proteomes. J. Am. Chem. Soc. 126, 1363-1368 (2004).
32. Okerberg, E.S. et al. High-resolution functional proteomics by active-site peptide profiling. Proc. Natl. Acad. Sci. USA 102, 4996-5001 (2005).
33. Jessani, N. et al. Carcinoma and stromal enzyme activity profiles associated with breast tumor growth in vivo. Proc. Natl. Acad. Sci. USA 101, 13756-13761 (2004).
34. Joyce, J.A. et al. Cathepsin cysteine proteases are effectors of invasive growth and angiogenesis during multistage tumorigenesis. Cancer Cell 5, 443-453 (2004).
35. Greenbaum, D.C. et al. A role for the protease falcipain 1 in host cell invasion by the human malaria parasite. Science 298, 2002-2006 (2002).
36. Barglow, K.T. & Cravatt, B.F. Discovering disease-associated enzymes by proteome reactivity profiling. Chem. Biol. 11, 1523-1531 (2004).
37. Greenbaum, D., Medzihradszky, K.F., Burlingame, A. & Bogyo, M. Epoxide electro-philes as activity-dependent cysteine protease profiling and discovery tools. Chem. Biol. 7, 569-581 (2000).
38. Thornberry, N.A. et al. Inactivation of interleukin-1 p converting enzyme by peptide (acyloxy)methyl ketones. Biochemistry 33, 3934-3940 (1994).
39. Faleiro, L., Kobayashi, R., Fearnhead, H. & Lazebnik, Y. Multiple species of CPP32 and Mch2 are the major active caspases present in apoptotic cells. EMBO J. 16, 2271-2281 (1997).
40. Borodovsky, A. et al. Chemistry-based functional proteomics reveals novel members of the deubiquitinating enzyme family. Chem. Biol. 9, 1149-1159 (2002).
41. Kato, D. et al. Activity-based probes that targe diverse cysteine protease families. Nat. Chem. Biol. 1, 33-38 (2005).
42. Saghatelian, A., Jessani, N., Joseph, A., Humphrey, M. & Cravatt, B.F. Activity-based probes for the proteomic profiling of metalloproteases. Proc. Natl. Acad. Sci. USA 101, 10000-10005 (2004).
43. Chan, E.W., Chattopadhaya, S., Panicker, R.C., Huang, X. & Yao, S.Q. Developing photoactive affinity probes for proteomic profiling: hydroxamate-based probes for metalloproteases. J. Am. Chem. Soc. 126, 14435-14446 (2004).
44. Li, Y.M. et al. Photoactivated y-secretase inhibitors directed to the active site covalently label presenilin 1. Nature 405, 689-694 (2000).
45. Groll, M., Nazif, T., Huber, R. & Bogyo, M. Probing structural determinants distal to the site of hydrolysis that control substrate specificity of the 20S proteasome. Chem. Biol. 9, 655-662 (2002).
46. Ovaa, H. et al. Chemistry in living cells: detection of active proteasomes by a two-step labeling strategy. Angew. Chem. Int. Edn Engl. 42, 3626-3629 (2003).
47. Kumar, S. et al. Activity-based probes for protein tyrosine phosphatases. Proc. Natl. Acad. Sci. USA 101, 7943-7948 (2004).
48. Shreder, K.R. et al. Design and synthesis of AX7574: a microcystin-derived, fluo-rescent probe for serine/threonine phosphatases. Bioconjug. Chem. 15, 790-798 (2004).
49. Liu, Y. et al. Wortmannin, a widely used phosphoinositide 3-kinase inhibitor, also potently inhibits mammalian polo-like kinase. Chem. Biol. 12, 99-107 (2005).
50. Vocadlo, D.J. & Bertozzi, C.R. A strategy for functional proteomic analysis of gly-cosidase activity from cell lysates. Angew. Chem. Int. Edn Engl. 43, 5338-5342 (2004).
51. Adam, G.C., Sorensen, E.J. & Cravatt, B.F. Proteomic profiling of mechanistically distinct enzyme classes using a common chemotype. Nat. Biotechnol. 20, 805-809 (2002).
52. Adam, G.C., Cravatt, B.F. & Sorensen, E.J. Profiling the specific reactivity of the proteome with non-directed activity-based probes. Chem. Biol. 8, 81-95 (2001).
53. Adam, G.C., Sorensen, E.J. & Cravatt, B.F. Trifunctional chemical probes for the con-solidated detection and identification of enzyme activities from complex proteomes. Mol. Cell. Proteomics 1, 828-835 (2002).
54. Speers, A.E. & Cravatt, B.F. Chemical strategies for activity-based proteomics. Chem Bio Chem 5, 41-47 (2004).
55. Jessani, N. et al. Class assignment of sequence-unrelated members of enzyme superfamilies by activity-based protein profiling. Angew. Chem. Int. Edn Engl. 44, 2400-2403 (2005).
56. Baxter, S.M. et al. Synergistic computational and experimental proteomics approaches for more accurate detection of active serine hydrolases in yeast. Mol. Cell. Proteomics 3, 209-225 (2004).
57. Leung, D., Hardouin, C., Boger, D.L. & Cravatt, B.F. Discovering potent and selec-tive reversible inhibitors of enzymes in complex proteomes. Nat. Biotechnol. 21, 687-691 (2003).
58. Greenbaum, D.C. et al. Small molecule affinity fingerprinting. A tool for enzyme family subclassification, target identification, and inhibitor design. Chem. Biol. 9, 1085-1094 (2002).
59. Speers, A.E., Adam, G.C. & Cravatt, B.F. Activity-based protein profiling in vivo using a copper(I)-catalyzed azide-alkyne [3 + 2] cycloaddition. J. Am. Chem. Soc. 125, 4686-4687 (2003).
60. Speers, A.E. & Cravatt, B.F. Profiling enzyme activities in vivo using click chemistry methods. Chem. Biol. 11, 535-546 (2004).
61. Johnson, S.A. & Hunter, T. Kinomics: methods for deciphering the kinome. Nat. Methods 2, 17-25 (2005).
62. Zhou, H., Watts, J.D. & Aebersold, R. A systematic approach to the analysis of protein phosphorylation. Nat. Biotechnol. 19, 375-378 (2001).
63. Oda, Y., Nagasu, T. & Chait, B.T. Enrichment analysis of phosphorylated proteins as a tool for probing the phosphoproteome. Nat. Biotechnol. 19, 379-382 (2001).
64. Rusnak, F., Zhou, J. & Hathaway, G.M. Identification of phosphorylated and glyco-sylated sites in peptides by chemically targeted proteolysis. J. Biomol. Tech. 13, 228-237 (2002).
65. Knight, Z.A. et al. Phosphospecific proteolysis for mapping sites of protein phosphorylation. Nat. Biotechnol. 21, 1047-1054 (2003).
66. Zachara, N.E. & Hart, G.W. O-GlcNAc a sensor of cellular state: the role of nucleocy-toplasmic glycosylation in modulating cellular function in response to nutrition and stress. Biochim. Biophys. Acta 1673, 13-28 (2004).
67. Zhang, F. et al. O-GlcNAc modification is an endogenous inhibitor of the proteasome. Cell 115, 715-725 (2003).
68. Yang, X., Zhang, F. & Kudlow, J.E. Recruitment of O-GlcNAc transferase to promoters by corepressor mSin3A: coupling protein O-GlcNAcylation to transcriptional repression. Cell 110, 69-80 (2002).
69. Wells, L. et al. Mapping sites of O-GlcNAc modification using affinity tags for serine and threonine post-translational modifications. Mol. Cell. Proteomics 1, 791-804 (2002).
70. Vocadlo, D.J., Hang, H.C., Kim, E.J., Hanover, J.A. & Bertozzi, C.R. A chemical approach for identifying O-GlcNAc-modified proteins in cells. Proc. Natl. Acad. Sci. USA 100, 9116-9121 (2003).
71. Hang, H.C., Yu, C., Kato, D.L. & Bertozzi, C.R. A metabolic labeling approach toward proteomic analysis of mucin-type O-linked glycosylation. Proc. Natl. Acad. Sci. USA 100, 14846-14851 (2003).
72. Kho, Y. et al. A tagging-via-substrate technology for detection and proteomics of farnesylated proteins. Proc. Natl. Acad. Sci. USA 101, 12479-12484 (2004).
73. Rose, M.W. et al. Enzymatic incorporation of orthogonally reactive prenylazide groups into peptides using geranylazide diphosphate via protein farnesyltransferase: implica-tions for selective protein labeling. Biopolymers 80, 164-171 (2005).
74. Khidekel, N. et al. A chemoenzymatic approach toward the rapid and sensitive detection of O-GlcNAc posttranslational modifications. J. Am. Chem. Soc. 125, 16162-16163 (2003).
75. Khidekel, N., Ficarro, S.B., Peters, E.C. & Hsieh-Wilson, L.C. Exploring the O-GlcNAc proteome: direct identification of O-GlcNAc-modified proteins from the brain. Proc. Natl. Acad. Sci. USA 101, 13132-13137 (2004).
76. Zhang, H., Li, X.J., Martin, D.B. & Aebersold, R. Identification and quantification of N-linked glycoproteins using hydrazide chemistry, stable isotope labeling and mass spectrometry. Nat. Biotechnol. 21, 660-666 (2003).
77. Davies, S.P., Reddy, H., Caivano, M. & Cohen, P. Specificity and mechanism of action of some commonly used protein kinase inhibitors. Biochem. J. 351, 95-105 (2000).
78. Manning, G., Whyte, D.B., Martinez, R., Hunter, T. & Sudarsanam, S. The protein kinase complement of the human genome. Science 298, 1912-1934 (2002).
79. Shah, K., Liu, Y., Deirmengian, C. & Shokat, K.M. Engineering unnatural nucleotide specificity for Rous sarcoma virus tyrosine kinase to uniquely label its direct substrates. Proc. Natl. Acad. Sci. USA 94, 3565-3570 (1997).
80. Bishop, A.C. et al. A chemical switch for inhibitor-sensitive alleles of any protein kinase. Nature 407, 395-401 (2000).
81. Sekiya-Kawasaki, M. et al. Dynamic phosphoregulation of the cortical actin cyto-skeleton and endocytic machinery revealed by real-time chemical genetic analysis. J. Cell Biol. 162, 765-772 (2003).
82. Wang, H. et al. Inducible protein knockout reveals temporal requirement of CaMKII reactivation for memory consolidation in the brain. Proc. Natl. Acad. Sci. USA 100, 4287-4292 (2003).
83. Wong, S. et al. Sole BCR-ABL inhibition is insufficient to eliminate all myeloproliferative disorder cell populations. Proc. Natl. Acad. Sci. USA 101, 17456-17461 (2004).
84. Ubersax, J.A. et al. Targets of the cyclin-dependent kinase Cdk1. Nature 425, 859-864 (2003).
85. Holt, J.R. et al. A chemical-genetic strategy implicates myosin-1c in adaptation by hair cells. Cell 108, 371-381 (2002).
86. Weijland, A. & Parmeggiani, A. Toward a model for the interaction between elongation factor Tu and the ribosome. Science 259, 1311-1314 (1993).
87. Powers, T. & Walter, P. Reciprocal stimulation of GTP hydrolysis by two directly interacting GTPases. Science 269, 1422-1424 (1995).
88. Levitsky, K., Ciolli, C.J. & Belshaw, P.J. Selective inhibition of engineered receptors via proximity-accelerated alkylation. Org. Lett. 5, 693-696 (2003).
89. Hoffman, H.E., Blair, E.R., Johndrow, J.E. & Bishop, A.C. Allele-specific inhibitors of protein tyrosine phosphatases. J. Am. Chem. Soc. 127, 2824-2825 (2005).
90. Zhang, C. et al. A second-site suppressor strategy for chemical genetic analysis of diverse protein kinases. Nat. Methods 2, 435-441 (2005).
91. Muir, T.W. Semisynthesis of proteins by expressed protein ligation. Annu. Rev. Biochem. 72, 249-289 (2003).
92. Lu, W., Gong, D., Bar-Sagi, D. & Cole, P.A. Site-specific incorporation of a phosphoty-rosine mimetic reveals a role for tyrosine phosphorylation of SHP-2 in cell signaling. Mol. Cell 8, 759-769 (2001).
93. Lu, W., Shen, K. & Cole, P.A. Chemical dissection of the effects of tyrosine phosphorylation of SHP-2. Biochemistry 42, 5461-5468 (2003).
94. Ottesen, J.J., Huse, M., Sekedat, M.D. & Muir, T.W. Semisynthesis of phosphovariants of Smad2 reveals a substrate preference of the activated T p RI kinase. Biochemistry 43, 5698-5706 (2004).
95. Zou, K., Cheley, S., Givens, R.S. & Bayley, H. Catalytic subunit of protein kinase A caged at the activating phosphothreonine. J. Am. Chem. Soc. 124, 8220-8229 (2002).
96. Rothman, D.M., Vazquez, M.E., Vogel, E.M. & Imperiali, B. General method for the synthesis of caged phosphopeptides: tools for the exploration of signal transduction pathways. Org. Lett. 4, 2865-2868 (2002).
97. Vazquez, M.E., Nitz, M., Stehn, J., Yaffe, M.B. & Imperiali, B. Fluorescent caged phosphoserine peptides as probes to investigate phosphorylation-dependent protein associations. J. Am. Chem. Soc. 125, 10150-10151 (2003).
98. Rothman, D.M. et al. Caged phosphoproteins. J. Am. Chem. Soc. 127, 846-847 (2005).
99. Hahn, M.E. & Muir, T.W. Photocontrol of Smad2, a multiphosphorylated cell-signaling protein, through caging of activating phosphoserines. Angew. Chem. Int. Edn Engl. 43, 5800-5803 (2004).
100. Nguyen, A., Rothman, D.M., Stehn, J., Imperiali, B. & Yaffe, M.B. Caged phosphopeptides reveal a temporal role for 14-3-3 in G1 arrest and S-phase checkpoint function. Nat. Biotechnol. 22, 993-1000 (2004).
101. Ghosh, M. et al. Cofilin promotes actin polymerization and defines the direction of cell motility. Science 304, 743-746 (2004).
102. Wang, L., Brock, A., Herberich, B. & Schultz, P.G. Expanding the genetic code of Escherichia coli. Science 292, 498-500 (2001).
103. Chin, J.W. et al. An expanded eukaryotic genetic code. Science 301, 964-967 (2003).
104. Giriat, I. & Muir, T.W. Protein semi-synthesis in living cells. J. Am. Chem. Soc. 125, 7180-7181 (2003).
105. Rohde, A. et al. Molecular phenotyping of the pal1 and pal2 mutants of Arabidopsis thaliana reveals far-reaching consequences on phenylpropanoid, amino acid, and carbohydrate metabolism. Plant Cell 16, 2749-2771 (2004).
106. Wu, J.Y. et al. ENU mutagenesis identifies mice with mitochondrial branched-chain aminotransferase deficiency resembling human maple syrup urine disease. J. Clin. Invest. 113, 434-440 (2004).
107. Saghatelian, A. et al. Assignment of endogenous substrates to enzymes by global metabolite profiling. Biochemistry 43, 14332-14339 (2004).
108. Cravatt, B.F. et al. Molecular characterization of an enzyme that degrades neuro-modulatory fatty-acid amides. Nature 384, 83-87 (1996).
109. Cravatt, B.F. et al. Supersensitivity to anandamide and enhanced endogenous can-nabinoid signaling in mice lacking fatty acid amide hydrolase. Proc. Natl. Acad. Sci. USA 98, 9371-9376 (2001).
110. Hirai, M.Y. et al. Elucidation of gene-to-gene and metabolite-to-gene networks in Arabidopsis by integration of metabolomics and transcriptomics. J. Biol. Chem., published online May 2005 (doi:10.1074/jbc.M502332200).
111. Babbitt, P.C. Definitions of enzyme function for the structural genomics era. Curr. Opin. Chem. Biol. 7, 230-237 (2003).
112. Pegg, S.C. & Babbitt, P.C. Shotgun: getting more from sequence similarity searches. Bioinformatics 15, 729-740 (1999).
113. Copley, S.D., Novak, W.R. & Babbitt, P.C. Divergence of function in the thioredoxin fold suprafamily: evidence for evolution of peroxiredoxins from a thioredoxin-like ancestor. Biochemistry 43, 13981-13995 (2004).