Reduced-representation phosphosignatures measured by quantitative targeted MS capture cellular states and enable large-scale comparison of drug-induced phenotypes

Molecular and Cellular Proteomics

Volumn 15, Issue 5, 2016, Pages 1622-1641

  Abelin, Jennifer G ^a   Patel, Jinal ^a   Lu, Xiaodong ^a   Feeney, Caitlin M ^a   Fagbami, Lola ^a   Creech, Amanda L ^a   Hu, Roger ^a   Lam, Daniel ^a   Davison, Desiree ^a   Pino, Lindsay ^a   Qiao, Jana W ^a   Kuhn, Eric ^a   Officer, Adam ^a   Li, Jianxue ^b   Abbatiello, Susan ^a   Subramanian, Aravind ^a   Sidman, Richard ^b   Snyder, Evan ^c   Carr, Steven A ^a   Jaffe, Jacob D ^a  

^a BROAD INSTITUTE OF MIT AND HARVARD   (United States)

^b BETH ISRAEL DEACONESS MEDICAL CENTER   (United States)

^c Sanford Burhnam Research Institute   (United States)

Author keywords

[No Author keywords available]

Indexed keywords

CYCLIN DEPENDENT KINASE; MAMMALIAN TARGET OF RAPAMYCIN; MITOGEN ACTIVATED PROTEIN KINASE; PHOSPHATIDYLINOSITOL 3 KINASE; PHOSPHOPEPTIDE; MOLECULAR LIBRARY; PHOSPHOPROTEIN;

ARTICLE; AUTOMATION; CONTROLLED STUDY; EMBRYO; HUMAN; HUMAN CELL; HUMAN EMBRYONIC STEM CELL; MASS SPECTROMETRY; MCF 7 CELL LINE; NEURAL STEM CELL; PRIORITY JOURNAL; PROTEIN ANALYSIS; PROTEIN DEGRADATION; PROTEIN PROCESSING; PROTEOMICS; QUANTITATIVE ANALYSIS; REPRODUCIBILITY; SENSITIVITY ANALYSIS; SIGNAL TRANSDUCTION; ANIMAL; CELL CULTURE; COMPARATIVE STUDY; CYTOLOGY; DRUG EFFECTS; EMBRYONIC STEM CELL; HIGH THROUGHPUT SCREENING; MCF-7 CELL LINE; METABOLISM; MOLECULAR LIBRARY; MOUSE; PHARMACOLOGY; PROCEDURES;

ANIMALS; CELLS, CULTURED; EMBRYONIC STEM CELLS; HIGH-THROUGHPUT SCREENING ASSAYS; HUMANS; MCF-7 CELLS; MICE; PHOSPHOPROTEINS; PROTEOMICS; SIGNAL TRANSDUCTION; SMALL MOLECULE LIBRARIES;

EID: 84964727338     PISSN: 15359476     EISSN: 15359484     Source Type: Journal    
DOI: 10.1074/mcp.M116.058354     Document Type: Article

References (59)

1. Edgar, R., Domrachev, M., and Lash, A. E. Gene Expression Omnibus: NCBI gene expression and hybridization array data repository. (2002) Nucleic Acids Res. 30, 207-210
2. Barrett, T., Troup D. B., Wilhite S. E., Ledoux P., Evangelista C., Kim I. F., Tomashevsky M., Marshall, K. A., Phillippy, K. H., Sherman, P. M., Muertter, R. N., Holko, M., Ayanbule, O., Yefanov, A., and Soboleva, A. (2013) NCBI GEO: archive for functional genomics data sets-update. Nucleic Acids Res. 41, D991-D995
3. Lamb, J., Crawford, E. D., Peck, D., Modell, J. W., Blat, I. C., Wrobel, M. J., Lerner, J., Brunet, J. P., Subramanian, A., Ross, K. N., Reich, M., Hieronymus, H., Wei, G., Armstrong, S. A., Haggarty, S. J., Clemons, P. A., Wei, R., Carr, S. A., Lander, E. S., and Golub, T. R. (2006) The connectivity map: Using gene-expression signatures to connect small molecules, genes, and disease. Science 313, 1929-1935
4. Lamb, J. (2007) The Connectivity Map: a new tool for biomedical research. Nat. Rev. Cancer 7, 54-60
5. Freeman, M. (2000) Feedback control of intercellular signalling in development. Nature 408, 313-319
6. Lalli, E., and Sassone-Corsi, P. (1994) Signal transduction and gene regulation: the nuclear response to cAMP. J. Biol. Chem. 269, 17359-17362
7. Nishi, H., Hashimoto, K., and Panchenko, A. R. (2011) Phosphorylation in protein-protein binding: effect on stability and function. Structure 19, 1807-1815
8. Ubersax, J. A., and Ferrell Jr, J. E. (2007) Mechanisms of specificity in protein phosphorylation. Nat Rev Mol Cell Biol 8, 530-541
9. Ozer, R. S., and Halpain, S. (2000) Phosphorylation-dependent Localization of microtubule-associated protein MAP2c to the actin cytoskeleton. Mol. Biol. Cell 11, 3573-3587
10. Suter, B., and Steward, R. (1991) Requirement for phosphorylation and localization of the Bicaudal-D protein in Drosophila oocyte differentiation. Cell 67, 917-926
11. Jimeno, A., Rubio-Viqueira, B., Rajeshkumar, N. V., Chan, A., Solomon, A., and Hidalgo, M. (2010) A fine-needle aspirate-based vulnerability assay identifies polo-like kinase 1 as a mediator of gemcitabine resistance in pancreatic cancer. Mol. Cancer Ther. 9, 311-318
12. Firestein, R., Bass, A. J., Kim, S. Y., Dunn, I. F., Silver, S. J., Guney, I., Freed, E., Ligon, A. H., Vena, N., Ogino, S., Chheda, M. G., Tamayo, P., Finn, S., Shrestha, Y., Boehm, J. S., Jain, S., Bojarski, E., Mermel, C., Barretina, J., Chan, J. A., Baselga, J., Tabernero, J., Root, D. E., Fuchs, C. S., Loda, M., Shivdasani, R. A., Meyerson, M., and Hahn, W. C. (2008) CDK8 is a colorectal cancer oncogene that regulates [bgr]-catenin activity. Nature 455, 547-551
13. Sharma, S. V., Bell, D. W., Settleman, J., and Haber, D. A. (2007) Epidermal growth factor receptor mutations in lung cancer. Nat. Rev. Cancer 7, 169-181
14. Amit, I. W., and Ron Yarden, Y. (2007) Evolvable signaling networks of receptor tyrosine kinases: relevance of robustness to malignancy and to cancer therapy. Mol. Syst. Biol. 3
15. Zoncu, R., Efeyan, A., and Sabatini, D. M. (2011) mTOR: from growth signal integration to cancer, diabetes and ageing. Nat. Rev. Mol. Cell Biol. 12, 21-35
16. Scholl, C., Fröhling, S., Dunn, I. F., Schinzel, A. C., Barbie, D. A., Kim, S. Y., Silver, S. J., Tamayo, P., Wadlow, R. C., Ramaswamy, S., Döhner, K., Bullinger, L., Sandy, P., Boehm, J. S., Root, D. E., Jacks, T., Hahn, W. C., and Gilliland, D. G. (2009) Synthetic lethal interaction between oncogenic KRAS dependency and STK33 suppression in human cancer cells. Cell 137, 821-834
17. Barbie, D. A., Tamayo, P., Boehm, J. S., Kim, S. Y., Moody, S. E., Dunn, I. F., Schinzel, A. C., Sandy, P., Meylan, E., Scholl, C., Fröhling, S., Chan, E. M., Sos, M. L., Michel, K., Mermel, C., Silver, S. J., Weir, B. A., Reiling, J. H., Sheng, Q., Gupta, P. B., Wadlow, R. C., Le, H., Hoersch, S., Wittner, B. S., Ramaswamy, S., Livingston, D. M., Sabatini, D. M., Meyerson, M., Thomas, R. K., Lander, E. S., Mesirov, J. P., Root, D. E., Gilliland, D. G., Jacks, T., and Hahn, W. C. (2009) Systematic RNA interference reveals that oncogenic KRAS-driven cancers require TBK1. Nature 462, 108-112
18. Hornbeck, P. V., Chabra, I., Kornhauser, J. M., Skrzypek, E. and Zhang, B. PhosphoSite: A bioinformatics resource dedicated to physiological protein phosphorylation. Proteomics 4, 1551-1561 (2004)
19. Manning, G., Whyte, D. B., Martinez, R., Hunter, T., and Sudarsanam, S. (2002) The protein kinase complement of the human genome. Science 298, 1912-1934
20. Tinti, M., Nardozza, A. P., Ferrari, E., Sacco, F., Corallino, S., Castagnoli, L., and Cesareni, G. (2012) The 4G10, pY20 and p-TYR-100 antibody specificity: profiling by peptide microarrays. Affin. Proteomics 29, 571-577
21. Bergström Lind, S., Molin, M., Savitski, M. M., Emilsson, L., Aström, J., Hedberg, L., Adams, C., Nielsen, M. L., Engström, A., Elfineh, L., Andersson, E., Zubarev, R. A., and Pettersson, U. (2008) Immunoaffinity enrichments followed by mass spectrometric detection for studying global protein tyrosine phosphorylation. J. Proteome Res. 7, 2897-2910
22. Ficarro, S. B., Adelmant, G., Tomar, M. N., Zhang, Y., Cheng, V. J., and Marto, J. A. (2009) Magnetic bead processor for rapid evaluation and optimization of parameters for phosphopeptide enrichment. Anal. Chem. 81, 4566-4575
23. Villen, J., and Gygi, S. P. (2008) The SCX/IMAC enrichment approach for global phosphorylation analysis by mass spectrometry. Nat. Protoc. 3, 1630-1638
24. Mertins, P., Yang, F., Liu, T., Mani, D. R., Petyuk, V. A., Gillette, M. A., Clauser, K. R., Qiao, J. W., Gritsenko, M. A., Moore, R. J., Levine, D. A., Townsend, R., Erdmann-Gilmore, P., Snider, J. E., Davies, S. R., Ruggles, K. V., Fenyo, D., Kitchens, R. T., Li S., Olvera, N., Dao, F., Rodriguez, H., Chan, D. W., Liebler, D., White, F., Rodland, K. D., Mills, G. B., Smith, R. D., Paulovich, A. G., Ellis, M., and Carr, S. A. (2014) Ischemia in tumors induces early and sustained phosphorylation changes in stress kinase pathways but does not affect global protein levels. Mol. Cell. Proteomics 13, 1690-1704
25. Choudhary, A., Hu, H. K., Mertins, P., Udeshi, N. D., Dančík, V., Fomina-Yadlin, D., Kubicek, S., Clemons, P. A., Schreiber, S. L., Carr, S. A., and Wagner, B. K. (2014) Quantitative-Proteomic comparison of alpha and beta cells to uncover novel targets for lineage reprogramming. PLoS ONE 9, e95194
26. Macek, B., Mann, M., and Olsen, J. V. (2009) Global and site-specific quantitative phosphoproteomics: principles and applications. Annu. Rev. Pharmacol. Toxicol. 49, 199-221
27. Olsen, J. V. V. Santamaria, M., Kumar, A., Miller, C., Jensen, M. L., Gnad, L. J., Cox, F., Jensen, J., Nigg, T. S., Brunak, E. A., and Mann, S. M. (2010) Quantitative phosphoproteomics reveals widespread full phosphorylation site occupancy during mitosis. Sci. Signal. 3, ra3-ra3
28. Jedrychowski, M. P., Huttlin, E. L., Haas, W., Sowa, M. E., Rad, R., and Gygi, S. P. (2011) Evaluation of HCD- and CID-type fragmentation within their respective detection platforms for murine phosphoproteomics. Mol. Cell. Proteomics 10, M111.009910
29. Bodenmiller, B., Mueller, L. N., Mueller, M., Domon, B., and Aebersold, R. (2007) Reproducible isolation of distinct, overlapping segments of the phosphoproteome. Nat. Meth. 4, 231-237
30. Rudomin, E. L., Carr, S. A., and Jaffe, J. D. (2009) Directed sample interrogation utilizing an accurate mass exclusion-based data-dependent acquisition strategy (AMEx) J. Proteome Res. 8, 3154-3160
31. Liu, H., Sadygov, R. G., and Yates, J. R. (2004) A model for random sampling and estimation of relative protein abundance in shotgun proteomics. Anal. Chem. 76, 4193-4201
32. Alcolea, M. P., Casado, P., Rodríguez-Prados, J.-C., Vanhaesebroeck, B. and Cutillas, P. R. (2012) Phosphoproteomic analysis of leukemia cells under basal and drug-treated conditions identifies markers of kinase pathway activation and mechanisms of resistance. Mol. Cell. Proteomics 11, 453-466
33. Duan, Q., Flynn, C., Niepel, M., Hafner, M., Muhlich, J. L., Fernandez, N. F., Rouillard, A. D., Tan, C. M., Chen, E. Y., Golub, T. R., Sorger, P. K., Subramanian, A. and Ma'ayan, A. (2014) LINCS canvas browser: interactive web app to query, browse and interrogate LINCS L1000 gene expression signatures. Nucleic Acids Res. 42, W449-W460
34. Soste, M., Hrabakova, R., Wanka, S., Melnik, A., Boersema, P., Maiolica, A., Wernas, T., Tognetti, M., von Mering, C., and Picotti, P. (2014) A sentinel protein assay for simultaneously quantifying cellular processes. Nat. Meth. 11, 1045-1048
35. Creech, A. L., Taylor, J. E., Maier, V. K., Wu, X., Feeney, C. M., Udeshi, N. D., Peach, S. E., Boehm, J. S., Lee, J. T., Carr, S. A., and Jaffe, J. D. (2015) Building the connectivity map of epigenetics: chromatin profiling by quantitative targeted mass spectrometry. Methods 72, 57-64
36. Jaffe, J. D., Wang, Y., Chan, H. M., Zhang, J., Huether, R., Kryukov, G. V., Bhang, H. E., Taylor, J. E., Hu, M., Englund, N. P., Yan, F., Wang, Z., Robert McDonald, E. 3rd, Wei, L., Ma, J., Easton, J., Yu, Z., deBeaumount, R., Gibaja, V., Venkatesan, K., Schlegel, R., Sellers, W. R., Keen, N., Liu, J., Caponigro, G., Barretina, J., Cooke, V. G., Mullighan, C., Carr, S. A., Downing, J. R., Garraway, L. A., and Stegmeier, F. (2013) Global chromatin profiling reveals NSD2 mutations in pediatric acute lymphoblastic leukemia. Nat. Genet. 45, 1386-1391
37. Mertins, P., Qiao, J. W., Patel, J., Udeshi, N. D., Clauser, K. R., Mani, D. R., Burgess, M. W., Gillette, M. A., Jaffe, J. D., and Carr, S. A. (2013) Integrated proteomic analysis of post-translational modifications by serial enrichment. Nat. Meth. 10, 634-637
38. Rappsilber, J., Mann, M., and Ishihama, Y. (2007) Protocol for micropurification, enrichment, pre-fractionation and storage of peptides for proteomics using StageTips. Nat. Protoc. 2, 1896-1906
39. Jaffe, J. D., Keshishian, H., Chang, B., Addona, T. A., Gillette, M. A., and Carr, S. A. (2008) Accurate inclusion mass screening: a bridge from unbiased discovery to targeted assay development for biomarker verification. Mol. Cell. Proteomics 7, 1952-1962
40. MacLean, B., Tomazela, D. M., Shulman, N., Chambers, M., Finney, G. L., Frewen, B., Kern, R., Tabb, D. L., Liebler, D. C., and MacCoss, M. J. (2010) Skyline: an open source document editor for creating and analyzing targeted proteomics experiments. Bioinformatics 26, 966-968
41. Shannon, P., Markiel, A., Ozier, O., Baliga, N. S., Wang, J. T., Ramage, D., Amin, N., Schwikowski, B., and Ideker, T. (2003) Cytoscape: A software environment for integrated models of biomolecular interaction networks. Genome Res. 13, 2498-2504
42. Gheorghiade, M., Adams, K. F., and Colucci, W. S. (2004) Digoxin in the management of cardiovascular disorders. Circulation 109, 2959-2964
43. Franceschini, A., Szklarczyk, D., Frankild, S., Kuhn, M., Simonovic, M., Roth, A., Lin, J., Minguez, P., Bork, P., von Mering, C., and Jensen, L. J. (2013) STRING v9.1: protein-protein interaction networks, with increased coverage and integration. Nucleic Acids Res. 41, D808-D815
44. Amanchy, R., Periaswamy, B., Mathivanan, S., Reddy, R., Tattikota, S. G., and Pandey, A. (2007) A curated compendium of phosphorylation motifs. Nat. Biotech. 25, 285-286
45. Kanehisa, M., and Goto, S. (2000) KEGG: Kyoto Encyclopedia of Genes and Genomes. Nucleic Acids Res. 28, 27-30
46. StemBook [Internet]. Cambridge (MA): Harvard Stem Cell Institute; 2008-. Available from: http://www.ncbi.nlm.nih.gov/books/NBK27044/
47. Krumm, N., O'Roak, B. J., Shendure, J., and Eichler, E. E. (2014) A de novo convergence of autism genetics and molecular neuroscience. Trends Neurosci. 37, 95-105
48. Kanehisa, M., Goto, S., Sato, Y., Kawashima, M., Furumichi, M., and Tanabe, M. (2014) Data, information, knowledge and principle: back to metabolism in KEGG. Nucleic Acids Res. 42, D199-D205
49. Wu, G., Xing, M., Mambo, E., Huang, X., Liu, J., Guo, Z., Chatterjee, A., Goldenberg, D., Gollin, S. M., Sukumar, S., Trink, B., and Sidransky, D. (2005) Somatic mutation and gain of copy number of PIK3CA in human breast cancer. Breast Cancer Res. 7, R609-R616
50. Holliday, D. L., and Speirs, V. (2011) Choosing the right cell line for breast cancer research. Breast Cancer Res. BCR 13, 215-215
51. Kim, E. K., and Choi, E. J. (2010) Pathological roles of MAPK signaling pathways in human diseases. Biochim. Biophys. Acta BBA - Mol. Basis Dis. 1802, 396-405
52. Lawrence, M. C., Jivan, A., Shao, C., Duan, L., Goad, D., Zaganjor, E., Osborne, J., McGlynn, K., Stippec, S., Earnest, S., Chen, W., and Cobb, M. H. (2008) The roles of MAPKs in disease. Cell Res 18, 436-442
53. Mihaylova, M. M., and Shaw, R. J. (2011) The AMP-activated protein kinase (AMPK) signaling pathway coordinates cell growth, autophagy, and metabolism. Nat. Cell Biol. 13, 1016-1023
54. Steinberg, G. R., and Kemp, B. E. (2009) AMPK in health and disease. Physiol. Rev. 89, 1025-1078
55. Salminen, A., and Kaarniranta, K. (2012) AMP-activated protein kinase (AMPK) controls the aging process via an integrated signaling network. Ageing Res. Rev. 11, 230-241
56. Bublil, E. M., and Yarden, Y. (2007) The EGF receptor family: spearheading a merger of signaling and therapeutics. Cell Regul. 19, 124-134
57. Wieduwilt, M. J., and Moasser, M. M. (2008) The epidermal growth factor receptor family: Biology driving targeted therapeutics. Cell. Mol. Life Sci. 65, 1566-1584
58. Foster, F. M., Traer, C. J., Abraham, S. M., and Fry, M. J. (2003) The phosphoinositide (PI) 3-kinase family. J. Cell Sci. 116, 3037-3040
59. Tang, H., Fang H., Yin E., Brasier A. R., Sowers L. C., and Zhang K. (2014) Multiplexed parallel reaction monitoring targeting histone modifications on the QExactive mass spectrometer. Anal. Chem. 86, 5526-5534