Cross-species proteomics reveals specific modulation of signaling in cancer and stromal cells by Phosphoinositide 3-kinase (PI3K) inhibitors

Molecular and Cellular Proteomics

Volumn 13, Issue 6, 2014, Pages 1457-1470

  Rajeeve, Vinothini ^a   Vendrell, Iolanda ^b,c   Wilkes, Edmund ^a   Torbett, Neil ^b,c   Cutillas, Pedro R ^a  

^a QUEEN MARY UNIVERSITY OF LONDON   (United Kingdom)

^b Activiomics   (United Kingdom)

^c Retroscreen Virology   (United Kingdom)

Author keywords

[No Author keywords available]

Indexed keywords

CASEIN KINASE; IDELALISIB; PHOSPHATIDYLINOSITOL 3 KINASE; PHOSPHATIDYLINOSITOL 3 KINASE INHIBITOR; PHOSPHOPEPTIDE; PICTILISIB; PROTEIN KINASE; PURINE DERIVATIVE; QUINAZOLINONE DERIVATIVE;

AMINO ACID SEQUENCE; ANIMAL EXPERIMENT; ANIMAL MODEL; APOPTOSIS; ARTICLE; CANCER CELL; CONTROLLED STUDY; ENZYME ACTIVITY; FEMALE; HUMAN; HUMAN CELL; MOUSE; NONHUMAN; PRIORITY JOURNAL; PROTEIN EXPRESSION; PROTEIN MOTIF; PROTEIN PHOSPHORYLATION; PROTEOMICS; SIGNAL TRANSDUCTION; STROMA CELL; TUMOR GROWTH; TUMOR MICROENVIRONMENT; ANIMAL; ANTAGONISTS AND INHIBITORS; CANCER STEM CELL; COLORECTAL TUMOR; DRUG SCREENING; GENETICS; METABOLISM; MORTALITY; PATHOLOGY; PHOSPHORYLATION; TUMOR CELL LINE;

ANIMALS; CELL LINE, TUMOR; COLORECTAL NEOPLASMS; HUMANS; MICE; NEOPLASTIC STEM CELLS; PHOSPHATIDYLINOSITOL 3-KINASES; PHOSPHORYLATION; PROTEOMICS; PURINES; QUINAZOLINONES; SIGNAL TRANSDUCTION; STROMAL CELLS; TUMOR MICROENVIRONMENT; XENOGRAFT MODEL ANTITUMOR ASSAYS;

EID: 84901928401     PISSN: 15359476     EISSN: 15359484     Source Type: Journal    
DOI: 10.1074/mcp.M113.035204     Document Type: Article

References (63)

1. Elenbaas, B., and Weinberg, R. A. (2001) Heterotypic signaling between epithelial tumor cells and fibroblasts in carcinoma formation. Exp. Cell Res. 264, 169-184 (Pubitemid 32989090)
2. Fang, H., and Declerck, Y. A. (2013) Targeting the tumor microenvironment: from understanding pathways to effective clinical trials. Cancer Res. 73, 4965-4977
3. Krutovskikh, V. A., Piccoli, C., and Yamasaki, H. (2002) Gap junction intercellular communication propagates cell death in cancerous cells. Oncogene 21, 1989-1999 (Pubitemid 34270887)
4. Buess, M., Nuyten, D. S., Hastie, T., Nielsen, T., Pesich, R., and Brown, P. O. (2007) Characterization of heterotypic interaction effects in vitro to deconvolute global gene expression profiles in cancer. Genome Biol. 8, R191
5. Hanahan, D., and Weinberg, R. A. (2011) Hallmarks of cancer: the next generation. Cell 144, 646-674
6. Liotta, L. A., and Kohn, E. C. (2001) The microenvironment of the tumour-host interface. Nature 411, 375-379
7. Fidler, I. J., and Poste, G. (2008) The "seed and soil" hypothesis revisited. Lancet Oncol. 9, 808
8. Lowery, F. J., and Yu, D. (2012) Growth factor signaling in metastasis: current understanding and future opportunities. Cancer Metast. Rev. 31, 479-491
9. Park, E. S., Kim, S. J., Kim, S. W., Yoon, S. L., Leem, S. H., Kim, S. B., Kim, S. M., Park, Y. Y., Cheong, J. H., Woo, H. G., Mills, G. B., Fidler, I. J., and Lee, J. S. (2011) Cross-species hybridization of microarrays for studying tumor transcriptome of brain metastasis. Proc. Natl. Acad. Sci. U.S.A. 108, 17456-17461
10. Straussman, R., Morikawa, T., Shee, K., Barzily-Rokni, M., Qian, Z. R., Du, J., Davis, A., Mongare, M. M., Gould, J., Frederick, D. T., Cooper, Z. A., Chapman, P. B., Solit, D. B., Ribas, A., Lo, R. S., Flaherty, K. T., Ogino, S., Wargo, J. A., and Golub, T. R. (2012) Tumour micro-environment elicits innate resistance to RAF inhibitors through HGF secretion. Nature 487, 500-504
11. Hofmeister, V., Schrama, D., and Becker, J. C. (2008) Anti-cancer therapies targeting the tumor stroma. Cancer Immunol. Immun. 57, 1-17 (Pubitemid 350043655)
12. Chin, Y. R., and Toker, A. (2009) Function of Akt/PKB signaling to cell motility, invasion and the tumor stroma in cancer. Cell. Signal. 21, 470-476
13. Folkes, A. J., Ahmadi, K., Alderton, W. K., Alix, S., Baker, S. J., Box, G., Chuckowree, I. S., Clarke, P. A., Depledge, P., Eccles, S. A., Friedman, L. S., Hayes, A., Hancox, T. C., Kugendradas, A., Lensun, L., Moore, P., Olivero, A. G., Pang, J., Patel, S., Pergl-Wilson, G. H., Raynaud, F. I., Robson, A., Saghir, N., Salphati, L., Sohal, S., Ultsch, M. H., Valenti, M., Wallweber, H. J., Wan, N. C., Wiesmann, C., Workman, P., Zhyvoloup, A., Zvelebil, M. J., and Shuttleworth, S. J. (2008) The identification of 2-(1H-indazol-4-yl)-6-(4- methanesulfonyl-piperazin-1-ylmethyl)-4-morpholin-4-yl-t hieno[3,2-d]pyrimidine (GDC-0941) as a potent, selective, orally bioavailable inhibitor of class I PI3 kinase for the treatment of cancer. J. Med. Chem. 51, 5522-5532
14. Herman, S. E., Gordon, A. L., Wagner, A. J., Heerema, N. A., Zhao, W., Flynn, J. M., Jones, J., Andritsos, L., Puri, K. D., Lannutti, B. J., Giese, N. A., Zhang, X., Wei, L., Byrd, J. C., and Johnson, A. J. (2010) Phosphatidylinositol 3-kinase-delta inhibitor CAL-101 shows promising preclinical activity in chronic lymphocytic leukemia by antagonizing intrinsic and extrinsic cellular survival signals. Blood 116, 2078-2088
15. Vanhaesebroeck, B., Welham, M. J., Kotani, K., Stein, R., Warne, P. H., Zvelebil, M. J., Higashi, K., Volinia, S., Downward, J., and Waterfield, M. D. (1997) P110delta, a novel phosphoinositide 3-kinase in leukocytes. Proc. Natl. Acad. Sci. U.S.A. 94, 4330-4335 (Pubitemid 27194241)
16. Wong, K. K., Engelman, J. A., and Cantley, L. C. (2010) Targeting the PI3K signaling pathway in cancer. Curr. Opin. Gen. Dev. 20, 87-90
17. Samuels, Y., Wang, Z., Bardelli, A., Silliman, N., Ptak, J., Szabo, S., Yan, H., Gazdar, A., Powell, S. M., Riggins, G. J., Willson, J. K., Markowitz, S., Kinzler, K. W., Vogelstein, B., and Velculescu, V. E. (2004) High frequency of mutations of the PIK3CA gene in human cancers. Science 304, 554 (Pubitemid 38541907)
18. Robak, P., and Robak, T. (2012) A targeted therapy for protein and lipid kinases in chronic lymphocytic leukemia. Curr. Med. Chem. 19, 5294-5318
19. Hoeflich, K. P., Merchant, M., Orr, C., Chan, J., Den Otter, D., Berry, L., Kasman, I., Koeppen, H., Rice, K., Yang, N. Y., Engst, S., Johnston, S., Friedman, L. S., and Belvin, M. (2012) Intermittent administration of MEK inhibitor GDC-0973 plus PI3K inhibitor GDC-0941 triggers robust apoptosis and tumor growth inhibition. Cancer Res. 72, 210-219
20. Lannutti, B. J., Meadows, S. A., Herman, S. E., Kashishian, A., Steiner, B., Johnson, A. J., Byrd, J. C., Tyner, J. W., Loriaux, M. M., Deininger, M., Druker, B. J., Puri, K. D., Ulrich, R. G., and Giese, N. A. (2011) CAL-101, a p110delta selective phosphatidylinositol-3-kinase inhibitor for the treatment of B-cell malignancies, inhibits PI3K signaling and cellular viability. Blood 117, 591-594
21. Alcolea, M. P., Casado, P., Rodriguez-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: MCP 11, 453-466
22. Montoya, A., Beltran, L., Casado, P., Rodriguez-Prados, J. C., and Cutillas, P. R. (2011) Characterization of a TiO(2) enrichment method for label-free quantitative phosphoproteomics. Methods 54, 370-378
23. Larsen, M. R., Thingholm, T. E., Jensen, O. N., Roepstorff, P., and Jorgensen, T. J. (2005) Highly selective enrichment of phosphorylated peptides from peptide mixtures using titanium dioxide microcolumns. Mol. Cell. Proteomics 4, 873-886 (Pubitemid 41309146)
24. Savitski, M. M., Lemeer, S., Boesche, M., Lang, M., Mathieson, T., Bantscheff, M., and Kuster, B. (2011) Confident phosphorylation site localization using the Mascot Delta Score. Mol. Cell. Proteomics 10, M110 003830
25. Cutillas, P. R., and Vanhaesebroeck, B. (2007) Quantitative profile of five murine core proteomes using label-free functional proteomics. Mol. Cell. Proteomics 6, 1560-1573 (Pubitemid 47506167)
26. Wisniewski, J. R., Ostasiewicz, P., Dus, K., Zielinska, D. F., Gnad, F., and Mann, M. (2012) Extensive quantitative remodeling of the proteome between normal colon tissue and adenocarcinoma. Mol. Sys. Biol. 8, 611
27. Huang da, W., Sherman, B. T., and Lempicki, R. A. (2009) Systematic and integrative analysis of large gene lists using DAVID bioinformatics resources. Nat. Protoc. 4, 44-57
28. Vizcaino, J. A., Cote, R. G., Csordas, A., Dianes, J. A., Fabregat, A., Foster, J. M., Griss, J., Alpi, E., Birim, M., Contell, J., O'Kelly, G., Schoenegger, A., Ovelleiro, D., Perez-Riverol, Y., Reisinger, F., Rios, D., Wang, R., and Hermjakob, H. (2013) The PRoteomics IDEntifications (PRIDE) database and associated tools: status in 2013. Nucleic Acids Res. 41, D1063-1069
29. Casado, P., and Cutillas, P. R. (2011) A self-validating quantitative mass spectrometry method for assessing the accuracy of high-content phosphoproteomic experiments. Mol. Cell. Proteomics 10, M110 003079
30. Bodenmiller, B., Wanka, S., Kraft, C., Urban, J., Campbell, D., Pedrioli, P. G., Gerrits, B., Picotti, P., Lam, H., Vitek, O., Brusniak, M. Y., Roschitzki, B., Zhang, C., Shokat, K. M., Schlapbach, R., Colman-Lerner, A., Nolan, G. P., Nesvizhskii, A. I., Peter, M., Loewith, R., von Mering, C., and Aebersold, R. (2010) Phosphoproteomic analysis reveals interconnected system-wide responses to perturbations of kinases and phosphatases in yeast. Sci. Signal. 3, rs4
31. Stulemeijer, I. J., Joosten, M. H., and Jensen, O. N. (2009) Quantitative phosphoproteomics of tomato mounting a hypersensitive response reveals a swift suppression of photosynthetic activity and a differential role for hsp90 isoforms. J. Proteome Res. 8, 1168-1182
32. Schilling, B., Rardin, M. J., MacLean, B. X., Zawadzka, A. M., Frewen, B. E., Cusack, M. P., Sorensen, D. J., Bereman, M. S., Jing, E., Wu, C. C., Verdin, E., Kahn, C. R., Maccoss, M. J., and Gibson, B. W. (2012) Platform-independent and label-free quantitation of proteomic data using MS1 extracted ion chromatograms in skyline: application to protein acetylation and phosphorylation. Mol. Cell. Proteomics 11, 202-214
33. Rardin, M. J., Newman, J. C., Held, J. M., Cusack, M. P., Sorensen, D. J., Li, B., Schilling, B., Mooney, S. D., Kahn, C. R., Verdin, E., and Gibson, B. W. (2013) Label-free quantitative proteomics of the lysine acetylome in mitochondria identifies substrates of SIRT3 in metabolic pathways. Proc. Natl. Acad. Sci. U.S.A. 110, 6601-6606
34. Wang, M., Weiss, M., Simonovic, M., Haertinger, G., Schrimpf, S. P., Hengartner, M. O., and von Mering, C. (2012) PaxDb, a database of protein abundance averages across all three domains of life. Mol. Cell. Proteomics 11, 492-500
35. Lolli, G., Pinna, L. A., and Battistutta, R. (2012) Structural determinants of protein kinase CK2 regulation by autoinhibitory polymerization. ACS Chem. Biol. 7, 1158-1163
36. Deshiere, A., Duchemin-Pelletier, E., Spreux, E., Ciais, D., Combes, F., Vandenbrouck, Y., Coute, Y., Mikaelian, I., Giusiano, S., Charpin, C., Cochet, C., and Filhol, O. (2013) Unbalanced expression of CK2 kinase subunits is sufficient to drive epithelial-to-mesenchymal transition by Snail1 induction. Oncogene 32, 1373-1383
37. Korn, I., Jacob, G., Allende, C. C., and Allende, J. E. (2001) The activity of CK2 in the extracts of COS-7 cells transfected with wild type and mutant subunits of protein kinase CK2. Mol. Cell. Biochem. 227, 37-44 (Pubitemid 34051305)
38. Battistutta, R., and Lolli, G. (2011) Structural and functional determinants of protein kinase CK2alpha: facts and open questions. Mol. Cell. Biochem. 356, 67-73
39. Niefind, K., and Issinger, O. G. (2010) Conformational plasticity of the catalytic subunit of protein kinase CK2 and its consequences for regulation and drug design. Biochim. Biophys. Acta 1804, 484-492
40. Llorens, F., Duarri, A., Sarro, E., Roher, N., Plana, M., and Itarte, E. (2006) The N-terminal domain of the human eIF2beta subunit and the CK2 phosphorylation sites are required for its function. Biochem. J. 394, 227-236 (Pubitemid 43259672)
41. Montagnoli, A., Valsasina, B., Brotherton, D., Troiani, S., Rainoldi, S., Tenca, P., Molinari, A., and Santocanale, C. (2006) Identification of Mcm2 phosphorylation sites by S-phase-regulating kinases. J. Biol. Chem. 281, 10281-10290 (Pubitemid 43864566)
42. Bignone, P. A., King, M. D., Pinder, J. C., and Baines, A. J. (2007) Phosphorylation of a threonine unique to the short C-terminal isoform of betaII-spectrin links regulation of alpha-beta spectrin interaction to neuritogenesis. J. Biol. Chem. 282, 888-896 (Pubitemid 47076581)
43. Ponce, D. P., Maturana, J. L., Cabello, P., Yefi, R., Niechi, I., Silva, E., Armisen, R., Galindo, M., Antonelli, M., and Tapia, J. C. (2011) Phosphorylation of AKT/PKB by CK2 is necessary for the AKT-dependent upregulation of beta-catenin transcriptional activity. J. Cell. Physiol. 226, 1953-1959
44. Clevers, H. (2006) Wnt/beta-catenin signaling in development and disease. Cell 127, 469-480
45. Shitashige, M., Satow, R., Jigami, T., Aoki, K., Honda, K., Shibata, T., Ono, M., Hirohashi, S., and Yamada, T. (2010) Traf2- and Nck-interacting kinase is essential for Wnt signaling and colorectal cancer growth. Cancer Res. 70, 5024-5033
46. Casado, P., Rodriguez-Prados, J. C., Cosulich, S. C., Guichard, S., Vanhaesebroeck, B., Joel, S., and Cutillas, P. R. (2013) Kinase-substrate enrichment analysis provides insights into the heterogeneity of signaling pathway activation in leukemia cells. Sci. Sig. 6, rs6
47. Alessi, D. R., Caudwell, F. B., Andjelkovic, M., Hemmings, B. A., and Cohen, P. (1996) Molecular basis for the substrate specificity of protein kinase B; comparison with MAPKAP kinase-1 and p70 S6 kinase. FEBS letters 399, 333-338 (Pubitemid 26426877)
48. Watanabe, F., Teraoka, H., Iijima, S., Mimori, T., and Tsukada, K. (1994) Molecular properties, substrate specificity and regulation of DNA-dependent protein kinase from Raji Burkitt's lymphoma cells. Biochim. Biophys. Acta 1223, 255-260 (Pubitemid 24278286)
49. Vander Haar, E., Lee, S. I., Bandhakavi, S., Griffin, T. J., and Kim, D. H. (2007) Insulin signalling to mTOR mediated by the Akt/PKB substrate PRAS40. Nat. Cell Biol. 9, 316-323 (Pubitemid 46344611)
50. Mukherjee, B., Kessinger, C., Kobayashi, J., Chen, B. P., Chen, D. J., Chatterjee, A., and Burma, S. (2006) DNA-PK phosphorylates histone H2AX during apoptotic DNA fragmentation in mammalian cells. DNA Repair 5, 575-590
51. Saelens, X., Kalai, M., and Vandenabeele, P. (2001) Translation inhibition in apoptosis: caspase-dependent PKR activation and eIF2-alpha phosphorylation. J. Biol. Chem. 276, 41620-41628
52. Walter, P., and Ron, D. (2011) The unfolded protein response: from stress pathway to homeostatic regulation. Science 334, 1081-1086
53. Wiita, A. P., Ziv, E., Wiita, P. J., Urisman, A., Julien, O., Burlingame, A. L., Weissman, J. S., and Wells, J. A. (2013) Global cellular response to chemotherapy-induced apoptosis. eLife 2, e01236
54. McAllister, S. S., and Weinberg, R. A. (2010) Tumor-host interactions: a far-reaching relationship. J. Clin. Oncol. 28, 4022-4028
55. Emes, R. D., Goodstadt, L., Winter, E. E., and Ponting, C. P. (2003) Comparison of the genomes of human and mouse lays the foundation of genome zoology. Hum. Mol. Genet. 12, 701-709 (Pubitemid 36416957)
56. Cascante, M., Boros, L. G., Comin-Anduix, B., de Atauri, P., Centelles, J. J., and Lee, P. W. (2002) Metabolic control analysis in drug discovery and disease. Nat. Biotechnol. 20, 243-249 (Pubitemid 34205416)
57. Cobb, M. H. (1999) MAP kinase pathways. Prog. Biophys. Mol. Bio. 71, 479-500
58. Ferrell, J. E., Jr. (1996) Tripping the switch fantastic: how a protein kinase cascade can convert graded inputs into switch-like outputs. Trends Biochem. Sci. 21, 460-466
59. Casagolda, D., Del Valle-Perez, B., Valls, G., Lugilde, E., Vinyoles, M., Casado-Vela, J., Solanas, G., Batlle, E., Reynolds, A. B., Casal, J. I., de Herreros, A. G., and Dunach, M. (2010) A p120-catenin-CK1epsilon complex regulates Wnt signaling. J. Cell Sci. 123, 2621-2631
60. Tapia, J. C., Torres, V. A., Rodriguez, D. A., Leyton, L., and Quest, A. F. (2006) Casein kinase 2 (CK2) increases survivin expression via enhanced beta-catenin-T cell factor/lymphoid enhancer binding factor-dependent transcription. Proc. Natl. Acad. Sci. U.S.A. 103, 15079-15084 (Pubitemid 44583167)
61. Vermeulen, L., De Sousa, E. M. F., van der Heijden, M., Cameron, K., de Jong, J. H., Borovski, T., Tuynman, J. B., Todaro, M., Merz, C., Rodermond, H., Sprick, M. R., Kemper, K., Richel, D. J., Stassi, G., and Medema, J. P. (2010) Wnt activity defines colon cancer stem cells and is regulated by the microenvironment. Nat. Cell Biol. 12, 468-476
62. Fruman, D. A., and Rommel, C. (2011) PI3Kdelta inhibitors in cancer: rationale and serendipity merge in the clinic. Cancer Disc. 1, 562-572
63. Chen, B. P., Chan, D. W., Kobayashi, J., Burma, S., Asaithamby, A., Morotomi-Yano, K., Botvinick, E., Qin, J., and Chen, D. J. (2005) Cell cycle dependence of DNA-dependent protein kinase phosphorylation in response to DNA double strand breaks. J. Biol. Chem. 280, 14709-14715 (Pubitemid 40562818)