Receptor tyrosine kinases fall into distinct classes based on their inferred signaling networks

Science Signaling

Volumn 6, Issue 284, 2013, Pages

  Wagner, Joel P ^a,e   Wolf Yadlin, Alejandro ^b,f   Sevecka, Mark ^b,g   Grenier, Jennifer K ^c   Root, David E ^c   Lauffenburger, Douglas A ^a   MacBeath, Gavin ^b,d  

^a USA   (United States)

^b HARVARD UNIVERSITY   (United States)

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

^d HARVARD MEDICAL SCHOOL   (United States)

^e JACKSON LABORATORY   (United States)

^f UNIVERSITY OF WASHINGTON   (United States)

^g MERRIMACK PHARMACEUTICALS   (United States)

Author keywords

[No Author keywords available]

Indexed keywords

EPIDERMAL GROWTH FACTOR RECEPTOR; FIBROBLAST GROWTH FACTOR RECEPTOR 1; LIGAND; PROTEIN TYROSINE KINASE; SCATTER FACTOR RECEPTOR; SOMATOMEDIN C RECEPTOR;

ARTICLE; CANCER CELL CULTURE; HUMAN; HUMAN CELL; PRIORITY JOURNAL; PROTEIN EXPRESSION; PROTEIN FUNCTION; RNA INTERFERENCE;

CELL LINE, TUMOR; GENE EXPRESSION REGULATION, ENZYMOLOGIC; HEK293 CELLS; HUMANS; MODELS, BIOLOGICAL; RECEPTOR PROTEIN-TYROSINE KINASES; SIGNAL TRANSDUCTION;

EID: 84880886028     PISSN: 19450877     EISSN: 19379145     Source Type: Journal    
DOI: 10.1126/scisignal.2003994     Document Type: Article

References (56)

1. M. A. Lemmon, J. Schlessinger, Cell signaling by receptor tyrosine kinases. Cell 141, 1117-1134 (2010).
2. S. R. Hubbard, J. H. Till, Protein tyrosine kinase structure and function. Annu. Rev. Biochem. 69, 373-398 (2000).
3. J. M. Stommel, A. C. Kimmelman, H. Ying, R. Nabioullin, A. H. Ponugoti, R. Wiedemeyer, A. H. Stegh, J. E. Bradner, K. L. Ligon, C. Brennan, L. Chin, R. A. DePinho, Coactivation of receptor tyrosine kinases affects the response of tumor cells to targeted therapies. Science 318, 287-290 (2007). (Pubitemid 47574858)
4. A. B. Turke, K. Zejnullahu, Y. L. Wu, Y. Song, D. Dias-Santagata, E. Lifshits, L. Toschi, A. Rogers, T. Mok, L. Sequist, N. I. Lindeman, C. Murphy, S. Akhavanfard, B. Y. Yeap, Y. Xiao, M. Capelletti, A. J. Iafrate, C. Lee, J. G. Christensen, J. A. Engelman, P. A. Jänne, Preexistence and clonal selection of MET amplification in EGFR mutant NSCLC. Cancer Cell 17, 77-88 (2010).
5. J. Qi, M. A. McTigue, A. Rogers, E. Lifshits, J. G. Christensen, P. A. Jänne, J. A. Engelman, Multiple mutations and bypass mechanisms can contribute to development of acquired resistance to MET inhibitors. Cancer Res. 71, 1081-1091 (2011).
6. Z. Zhang, J. C. Lee, L. Lin, V. Olivas, V. Au, T. LaFramboise, M. Abdel-Rahman, X. Wang, A. D. Levine, J. K. Rho, Y. J. Choi, C. M. Choi, S. W. Kim, S. J. Jang, Y. S. Park, W. S. Kim, D. H. Lee, J. S. Lee, V. A. Miller, M. Arcila, M. Ladanyi, P. Moonsamy, C. Sawyers, T. J. Boggon, P. C. Ma, C. Costa, M. Taron, R. Rosell, B. Halmos, T. G. Bivona, Activation of the AXL kinase causes resistance to EGFR-targeted therapy in lung cancer. Nat. Genet. 44, 852-860 (2012).
7. F. Harbinski, V. J. Craig, S. Sanghavi, D. Jeffery, L. Liu, K. A. Sheppard, S. Wagner, C. Stamm, A. Buness, C. Chatenay-Rivauday, Y. Yao, F. He, C. X. Lu, V. Guagnano, T. Metz, P. M. Finan, F. Hofmann, W. R. Sellers, J. A. Porter, V. E. Myer, D. Graus-Porta, C. J. Wilson, A. Buckler, R. Tiedt, Rescue screens with secreted proteins reveal compensatory potential of receptor tyrosine kinases in driving cancer growth. Cancer Discov. 2, 948-959 (2012).
8. T. R. Wilson, J. Fridlyand, Y. Yan, E. Penuel, L. Burton, E. Chan, J. Peng, E. Lin, Y. Wang, J. Sosman, A. Ribas, J. Li, J. Moffat, D. P. Sutherlin, H. Koeppen, M. Merchant, R. Neve, J. Settleman, Widespread potential for growth-factor-driven resistance to anticancer ki-nase inhibitors. Nature 487, 505-509 (2012).
9. M. Bansal, V. Belcastro, A. Ambesi-Impiombato, D. di Bernardo, How to infer gene networks from expression profiles. Mol. Syst. Biol. 3, 78 (2007).
10. K. Sachs, O. Perez, D. Pe'er, D. A. Lauffenburger, G. P. Nolan, Causal protein-signaling networks derived from multiparameter single-cell data. Science 308, 523-529 (2005). (Pubitemid 40570578)
11. J. Tegner, M. K. S. Yeung, J. Hasty, J. J. Collins, Reverse engineering gene networks: Integrating genetic perturbations with dynamical modeling. Proc. Natl. Acad. Sci. U.S.A. 100, 5944-5949 (2003). (Pubitemid 36576912)
12. R. J. Prill, J. Saez-Rodriguez, L. G. Alexopoulos, P. K. Sorger, G. Stolovitzky, Crowdsourcing network inference: The DREAM predictive signaling network challenge. Sci. Signal. 4, mr7 (2011).
13. A. Gordus, J. A. Krall, E. M. Beyer, A. Kaushansky, A. Wolf-Yadlin, M. Sevecka, B. H. Chang, J. Rush, G. MacBeath, Linear combinations of docking affinities explain quantitative differences in RTK signaling. Mol. Syst. Biol. 5, 235 (2009).
14. J. Moffat, D. A. Grueneberg, X. Yang, S. Y. Kim, A. M. Kloepfer, G. Hinkle, B. Piqani, T. M. Eisenhaure, B. Luo, J. K. Grenier, A. E. Carpenter, S. Y. Foo, S. A. Stewart, B. R. Stockwell, N. Hacohen, W. C. Hahn, E. S. Lander, D. M. Sabatini, D. E. Root, A lentiviral RNAi library for human and mouse genes applied to an arrayed viral highcontent screen. Cell 124, 1283-1298 (2006).
15. M. D. Marmor, K. B. Skaria, Y. Yarden, Signal transduction and oncogenesis by ErbB/HER receptors. Int. J. Radiat. Oncol. Biol. Phys. 58, 903-913 (2004). (Pubitemid 38221150)
16. C. P. Paweletz, L. Charboneau, V. E. Bichsel, N. L. Simone, T. Chen, J. W. Gillespie, M. R. Emmert-Buck, M. J. Roth, E. F. Petricoin III, L. A. Liotta, Reverse phase protein microarrays which capture disease progression show activation of pro-survival pathways at the cancer invasion front. Oncogene 20, 1981-1989 (2001). (Pubitemid 32458030)
17. M. Sevecka, A. Wolf-Yadlin, G. MacBeath, Lysate microarrays enable high-throughput, quantitative investigations of cellular signaling. Mol. Cell. Proteomics 10, M110.005363 (2011).
18. O. E. Sturm, R. Orton, J. Grindlay, M. Birtwistle, V. Vyshemirsky, D. Gilbert, M. Calder, A. Pitt, B. Kholodenko, W. Kolch, The mammalian MAPK/ERK pathway exhibits properties of a negative feedback amplifier. Sci. Signal. 3, ra90 (2010).
19. Q. Wang, Y. Zhou, X. Wang, B. M. Evers, Glycogen synthase kinase-3 is a negative regulator of extracellular signal-regulated kinase. Oncogene 25, 43-50 (2006). (Pubitemid 43050002)
20. J. E. Ferrell Jr., What do scaffold proteins really do? Sci. STKE 2000, pe1 (2000).
21. Y. Kim, Z. Paroush, K. Nairz, E. Hafen, G. Jiménez, S. Y. Shvartsman, Substrate-dependent control of MAPK phosphorylation in vivo. Mol. Syst. Biol. 7, 467 (2011).
22. M. L. Wynn, A. C. Ventura, J. A. Sepulchre, H. J. García, S. D. Merajver, Kinase inhibitors can produce off-target effects and activate linked pathways by retroactivity. BMC Syst. Biol. 5, 156 (2011).
23. D. Marbach, J. C. Costello, R. Küffner, N. M. Vega, R. J. Prill, D. M. Camacho, K. R. Allison; DREAM5 Consortium, M. Kellis, J. J. Collins, G. Stolovitzky, Wisdom of crowds for robust gene network inference. Nat. Methods 9, 796-804 (2012).
24. M. Koivisto, K. Sood, Exact Bayesian structure discovery in Bayesian networks. J. Mach. Learn. Res. 5, 549-573 (2004).
25. R. Steuer, J. Kurths, C. O. Daub, J. Weise, J. Selbig, The mutual information: Detecting and evaluating dependencies between variables. Bioinformatics 18 (suppl. 2), S231-S240 (2002). (Pubitemid 41073239)
26. J. J. Faith, B. Hayete, J. T. Thaden, I. Mogno, J. Wierzbowski, G. Cottarel, S. Kasif, J. J. Collins, T. S. Gardner, Large-scale mapping and validation of Escherichia coli transcriptional regulation from a compendium of expression profiles. PLoS Biol. 5, e8 (2007).
27. G. A. F. Seber, Multivariate Observations (Wiley, Hoboken, NJ, 1984).
28. M. I. Davis, J. P. Hunt, S. Herrgard, P. Ciceri, L. M. Wodicka, G. Pallares, M. Hocker, D. K. Treiber, P. P. Zarrinkar, Comprehensive analysis of kinase inhibitor selectivity. Nat. Biotechnol. 29, 1046-1051 (2011).
29. J. Barretina, G. Caponigro, N. Stransky, K. Venkatesan, A. A. Margolin, S. Kim, C. J. Wilson, J. Lehár, G. V. Kryukov, D. Sonkin, A. Reddy, M. Liu, L. Murray, M. F. Berger, J. E. Monahan, P. Morais, J. Meltzer, A. Korejwa, J. Jané-Valbuena, F. A. Mapa, J. Thibault, E. Bric-Furlong, P. Raman, A. Shipway, I. H. Engels, J. Cheng, G. K. Yu, J. Yu, P. Aspesi Jr., M. de Silva, K. Jagtap, M. D. Jones, L. Wang, C. Hatton, E. Palescandolo, S. Gupta, S. Mahan, C. Sougnez, R. C. Onofrio, T. Liefeld, L. MacConaill, W. Winckler, M. Reich, N. Li, J. P. Mesirov, S. B. Gabriel, G. Getz, K. Ardlie, V. Chan, V. E. Myer, B. L. Weber, J. Porter, M. Warmuth, P. Finan, J. L. Harris, M. Meyerson, T. R. Golub, M. P. Morrissey, W. R. Sellers, R. Schlegel, L. A. Garraway, The Cancer Cell Line Encyclopedia enables predictive modelling of anticancer drug sensitivity. Nature 483, 603-607 (2012).
30. R. C. Harris, E. Chung, R. J. Coffey, EGF receptor ligands. Exp. Cell Res. 284, 2-13 (2003). (Pubitemid 36331964)
31. X. Zhang, O. A. Ibrahimi, S. K. Olsen, H. Umemori, M. Mohammadi, D. M. Ornitz, Receptor specificity of the fibroblast growth factor family. The complete mammalian FGF family. J. Biol. Chem. 281, 15694-15700 (2006). (Pubitemid 43848456)
32. S. P. Squinto, T. N. Stitt, T. H. Aldrich, S. Davis, S. M. Bianco, C. Radziejewski, D. J. Glass, P. Masiakowski, M. E. Furth, D. M. Valenzuela, P. S. DiStefano, G. D. Yancopoulos, trkB encodes a functional receptor for brain-derived neurotrophic factor and neurotrophin-3 but not nerve growth factor. Cell 65, 885-893 (1991). (Pubitemid 121001319)
33. J. Andrae, R. Gallini, C. Betsholtz, Role of platelet-derived growth factors in physiology and medicine. Genes Dev. 22, 1276-1312 (2008). (Pubitemid 351717519)
34. R. Straussman, T. Morikawa, K. Shee, M. Barzily-Rokni, Z. R. Qian, J. Du, A. Davis, M. M. Mongare, J. Gould, D. T. Frederick, Z. A. Cooper, P. B. Chapman, D. B. Solit, A. Ribas, R. S. Lo, K. T. Flaherty, S. Ogino, J. A. Wargo, T. R. Golub, Tumour microenvironment elicits innate resistance to RAF inhibitors through HGF secretion. Nature 487, 500-504 (2012).
35. 1-integrin regulates ovarian cancer invasion and metastasis. Oncogene 30, 1566-1576 (2011).
36. S. Corso, E. Ghiso, V. Cepero, J. R. Sierra, C. Migliore, A. Bertotti, L. Trusolino, P. M. Comoglio, S. Giordano, Activation of HER family members in gastric carcinoma cells mediates resistance to MET inhibition. Mol. Cancer 9, 121 (2010).
37. M. E. Marshall, T. K. Hinz, S. A. Kono, K. R. Singleton, B. Bichon, K. E. Ware, L. Marek, B. A. Frederick, D. Raben, L. E. Heasley, Fibroblast growth factor receptors are components of autocrine signaling networks in head and neck squamous cell carcinoma cells. Clin. Cancer Res. 17, 5016-5025 (2011).
38. H. Fischer, N. Taylor, S. Allerstorfer, M. Grusch, G. Sonvilla, K. Holzmann, U. Setinek, L. Elbling, H. Cantonati, B. Grasl-Kraupp, C. Gauglhofer, B. Marian, M. Micksche, W. Berger, Fibroblast growth factor receptor-mediated signals contribute to the malignant phenotype of non-small cell lung cancer cells: Therapeutic implications and synergism with epidermal growth factor receptor inhibition. Mol. Cancer Ther. 7, 3408-3419 (2008).
39. L. Marek, K. E. Ware, A. Fritzsche, P. Hercule, W. R. Helton, J. E. Smith, L. A. McDermott, C. D. Coldren, R. A. Nemenoff, D. T. Merrick, B. A. Helfrich, P. A. Bunn Jr., L. E. Heasley, Fibroblast growth factor (FGF) and FGF receptor-mediated autocrine signaling in non-small-cell lung cancer cells. Mol. Pharmacol. 75, 196-207 (2009).
40. K. E. Ware, M. E. Marshall, L. R. Heasley, L. Marek, T. K. Hinz, P. Hercule, B. A. Helfrich, R. C. Doebele, L. E. Heasley, Rapidly acquired resistance to EGFR tyrosine kinase inhibitors in NSCLC cell lines through de-repression of FGFR2 and FGFR3 expression. PLoS One 5, e14117 (2010).
41. M. Guix, A. C. Faber, S. E. Wang, M. G. Olivares, Y. Song, S. Qu, C. Rinehart, B. Seidel, D. Yee, C. L. Arteaga, J. A. Engelman, Acquired resistance to EGFR tyrosine kinase inhibitors in cancer cells is mediated by loss of IGF-binding proteins. J. Clin. Invest. 118, 2609-2619 (2008). (Pubitemid 351949788)
42. F. Huang, A. Greer, W. Hurlburt, X. Han, R. Hafezi, G. M. Wittenberg, K. Reeves, J. Chen, D. Robinson, A. Li, F. Y. Lee, M. M. Gottardis, E. Clark, L. Helman, R. M. Attar, A. Dongre, J. M. Carboni, The mechanisms of differential sensitivity to an insulin-like growth factor-1 receptor inhibitor (BMS-536924) and rationale for combining with EGFR/HER2 inhibitors. Cancer Res. 69, 161-170 (2009).
43. C. Garofalo, M. C. Manara, G. Nicoletti, M. T. Marino, P. L. Lollini, A. Astolfi, G. Pandini, J. A. López-Guerrero, K. L. Schaefer, A. Belfiore, P. Picci, K. Scotlandi, Efficacy of and resistance to anti-IGF-1R therapies in Ewing's sarcoma is dependent on insulin receptor signaling. Oncogene 30, 2730-2740 (2011).
44. D. Milojkovic, J. Apperley, Mechanisms of resistance to imatinib and second-generation tyrosine inhibitors in chronic myeloid leukemia. Clin. Cancer Res. 15, 7519-7527 (2009).
45. K. Inaki, E. T. Liu, Structural mutations in cancer: Mechanistic and functional insights. Trends Genet. 28, 550-559 (2012).
46. R. Beroukhim, G. Getz, L. Nghiemphu, J. Barretina, T. Hsueh, D. Linhart, I. Vivanco, J. C. Lee, J. H. Huang, S. Alexander, J. Du, T. Kau, R. K. Thomas, K. Shah, H. Soto, S. Perner, J. Prensner, R. M. Debiasi, F. Demichelis, C. Hatton, M. A. Rubin, L. A. Garraway, S. F. Nelson, L. Liau, P. S. Mischel, T. F. Cloughesy, M. Meyerson, T. A. Golub, E. S. Lander, I. K. Mellinghoff, W. R. Sellers, Assessing the significance of chromosomal aberrations in cancer: Methodology and application to glioma. Proc. Natl. Acad. Sci. U.S.A. 104, 20007-20012 (2007).
47. A. Hellman, E. Zlotorynski, S. W. Scherer, J. Cheung, J. B. Vincent, D. I. Smith, L. Trakhtenbrot, B. Kerem, A role for common fragile site induction in amplification of human oncogenes. Cancer Cell 1, 89-97 (2002). (Pubitemid 41039179)
48. H. Riedel, T. J. Dull, A. M. Honegger, J. Schlessinger, A. Ullrich, Cytoplasmic domains determine signal specificity, cellular routing characteristics and influence ligand binding of epidermal growth factor and insulin receptors. EMBO J. 8, 2943-2954 (1989). (Pubitemid 19274996)
49. A. P. Won, J. E. Garbarino, W. A. Lim, Recruitment interactions can override catalytic interactions in determining the functional identity of a protein kinase. Proc. Natl. Acad. Sci. U.S.A. 108, 9809-9814 (2011).
50. L. Naldini, U. Blömer, P. Gallay, D. Ory, R. Mulligan, F. H. Gage, I. M. Verma, D. Trono, In vivo gene delivery and stable transduction of nondividing cells by a lentiviral vector. Science 272, 263-267 (1996). (Pubitemid 26119138)
51. S. M. Chan, J. Ermann, L. Su, C. G. Fathman, P. J. Utz, Protein microarrays for multiplex analysis of signal transduction pathways. Nat. Med. 10, 1390-1396 (2004). (Pubitemid 40022723)
52. M. Sevecka, G. MacBeath, State-based discovery: A multidimensional screen for small-molecule modulators of EGF signaling. Nat. Methods 3, 825-831 (2006). (Pubitemid 44445830)
53. J. D. Storey, R. Tibshirani, Statistical significance for genomewide studies. Proc. Natl. Acad. Sci. U.S.A. 100, 9440-9445 (2003). (Pubitemid 37033947)
54. Y. Benjamini, Y. Hochberg, Controlling the false discovery rate: A practical and powerful approach to multiple testing. J. Roy. Stat. Soc. B Met. 57, 289-300 (1995).
55. M. F. Ciaccio, J. P. Wagner, C. P. Chuu, D. A. Lauffenburger, R. B. Jones, Systems analysis of EGF receptor signaling dynamics with microwestern arrays. Nat. Methods 7, 148-155 (2010).
56. D. Eaton, K. Murphy, Bayesian structure learning using dynamic programming and MCMC, paper presented at the 23rd Conference on Uncertainty in Artificial Intelligence, Vancouver, British Columbia, Canada, 19 to 22 July 2007.