Integration of protein abundance and structure data reveals competition in the ErbB signaling network

Science Signaling

Volumn 6, Issue 306, 2013, Pages

  Kiel, Christina ^a,b   Verschueren, Erik ^a,b   Yang, Jae Seong ^a,b   Serrano, Luis ^a,b,c  

^a CENTRE FOR GENOMIC REGULATION CRG   (Spain)

^b UNIVERSITAT POMPEU FABRA   (Spain)

^c INSTITUCIÓ CATALANA DE RECERCA I ESTUDIS AVANÇATS ICREA   (Spain)

Author keywords

[No Author keywords available]

Indexed keywords

CELL PROTEIN; EPIDERMAL GROWTH FACTOR RECEPTOR; RAF PROTEIN; RAS AND RAB INTERACTOR 1 PROTEIN; RAS PROTEIN; UNCLASSIFIED DRUG;

ARTICLE; CELL CULTURE; HUMAN; HUMAN CELL; PRIORITY JOURNAL; PROTEIN BINDING; PROTEIN DOMAIN; PROTEIN INTERACTION; PROTEIN MOTIF; PROTEIN PHOSPHORYLATION; PROTEIN STRUCTURE; SIGNAL TRANSDUCTION;

MODELS, MOLECULAR; ONCOGENE PROTEINS V-ERBB; PROTEIN CONFORMATION; SIGNAL TRANSDUCTION;

EID: 84891845335     PISSN: 19450877     EISSN: 19379145     Source Type: Journal    
DOI: 10.1126/scisignal.2004560     Document Type: Article

References (61)

1. C. J. Marshall, Specificity of receptor tyrosine kinase signaling: Transient versus sustained extracellular signal-regulated kinase activation. Cell 80, 179-185 (1995).
2. M. R. Birtwistle,M. Hatakeyama, N. Yumoto, B. A. Ogunnaike, J. B. Hoek, B. N. Kholodenko, Ligand-dependent responses of the ErbB signaling network: Experimental and modeling analyses. Mol. Syst. Biol. 3, 144 (2007).
3. C. Kiel, L. Serrano, Cell type-specific importance of ras-c-raf complex association rate constants for MAPK signaling. Sci. Signal. 2, ra38 (2009).
4. E. Aksamitiene, B. N. Kholodenko, W. Kolch, J. B. Hoek, A. Kiyatkin, PI3K/Akt-sensitive MEK-independent compensatory circuit of ERK activation in ER-positive PI3K-mutant T47D breast cancer cells. Cell. Signal. 22, 1369-1378 (2010).
5. B. N. Kholodenko, J. F. Hancock, W. Kolch, Signalling ballet in space and time. Nat. Rev. Mol. Cell Biol. 11, 414-426 (2010).
6. S. Yang, M. A. Raymond-Stintz, W. Ying, J. Zhang, D. S. Lidke, S. L. Steinberg, L. Williams, J. M. Oliver, B. S. Wilson, Mapping ErbB receptors on breast cancer cell membranes during signal transduction. J. Cell Sci. 120, 2763-2773 (2007).
7. A. Abulrob, Z. Lu, E. Baumann, D. Vobornik, R. Taylor, D. Stanimirovic, L. J. Johnston, Nanoscale imaging of epidermal growth factor receptor clustering: Effects of inhibitors. J. Biol. Chem. 285, 3145-3156 (2010).
8. M. C. Good, J. G. Zalatan, W. A. Lim, Scaffold proteins: Hubs for controlling the flow of cellular information. Science 332, 680-686 (2011).
9. O. Rocks, A. Peyker, M. Kahms, P. J. Verveer, C. Koerner, M. Lumbierres, J. Kuhlmann, H. Waldmann, A. Wittinghofer, P. I. Bastiaens, An acylation cycle regulates localization and activity of palmitoylated Ras isoforms. Science 307, 1746-1752 (2005).
10. C. I. Maeder, M. A. Hink, A. Kinkhabwala, R. Mayr, P. I. Bastiaens, M. Knop, Spatial regulation of Fus3 MAP kinase activity through a reaction-diffusion mechanism in yeast pheromone signalling. Nat. Cell Biol. 9, 1319-1326 (2007).
11. J. R. James, R. D. Vale, Biophysical mechanism of T-cell receptor triggering in a reconstituted system. Nature 487, 64-69 (2012).
12. D. Emig, M. Albrecht, Tissue-specific proteins and functional implications. J. Proteome Res. 10, 1893-1903 (2011).
13. J. Rauch, K. Moran-Jones, V. Albrecht, T. Schwarzl, K. Hunter, O. Gires, W. Kolch, c-Myc regulates RNA splicing of the A-Raf kinase and its activation of the ERK pathway. Cancer Res. 71, 4664-4674 (2011).
14. M. Sundvall, V. Veikkolainen, K. Kurppa, Z. Salah, D. Tvorogov, E. J. van Zoelen, R. Aqeilan, K. Elenius, Cell death or survival promoted by alternative isoforms of ErbB4. Mol. Biol. Cell 21, 4275-4286 (2010).
15. R. Avraham, Y. Yarden, Feedback regulation of EGFR signalling: Decision making by early and delayed loops. Nat. Rev. Mol. Cell Biol. 12, 104-117 (2011).
16. P. M. Kim, L. J. Lu, Y. Xia, M. B. Gerstein, Relating three-dimensional structures to protein networks provides evolutionary insights. Science 314, 1938-1941 (2006).
17. C. Kiel, A. Vogt, A. Campagna, A. Chatr-aryamontri, M. Swiatek-de Lange, M. Beer, S. Bolz, A. F. Mack, N. Kinkl, G. Cesareni, L. Serrano, M. Ueffing, Structural and functional protein network analyses predict novel signaling functions for rhodopsin. Mol. Syst. Biol. 7, 551 (2011).
18. D.Heitzler, G. Durand, N. Gallay, A. Rizk, S. Ahn, J.Kim, J. D. Violin, L. Dupuy,C. Gauthier, V. Piketty, P. Crepieux, A. Poupon, F. Clement, F. Fages, R. J. Lefkowitz, E. Reiter, Competing G protein-coupled receptor kinases balance G protein and β-arrestin signaling. Mol. Syst. Biol. 8, 590 (2012).
19. E. A. Franzosa, Y. Xia, Structural principles within the human-virus protein-protein interaction network. Proc. Natl. Acad. Sci. U.S.A. 108, 10538-10543 (2011).
20. K. Oda, Y. Matsuoka, A. Funahashi, H. Kitano, A comprehensive pathway map of epidermal growth factor receptor signaling. Mol. Syst. Biol. 1, 2005.0010 (2005).
21. J. Schlessinger, Cell signaling by receptor tyrosine kinases. Cell 103, 211-225 (2000).
22. A. Citri, Y. Yarden, EGF-ERBB signalling: Towards the systems level. Nat. Rev. Mol. Cell Biol. 7, 505-516 (2006).
23. K. Kandasamy, S. S. Mohan, R. Raju, S. Keerthikumar, G. S. Kumar, A. K. Venugopal, D. Telikicherla, J. D. Navarro, S. Mathivanan, C. Pecquet, S. K. Gollapudi, S. G. Tattikota, S. Mohan, H. Padhukasahasram, Y. Subbannayya, R. Goel, H. K. Jacob, J. Zhong, R. Sekhar, V. Nanjappa, L. Balakrishnan, R. Subbaiah, Y. L. Ramachandra, B. A. Rahiman, T. S. Prasad, J. X. Lin, J. C. Houtman, S. Desiderio, J. C. Renauld, S. N. Constantinescu, O. Ohara, T. Hirano, M. Kubo, S. Singh, P. Khatri, S. Draghici, G. D. Bader, C. Sander, W. J. Leonard, A. Pandey, NetPath: A public resource of curated signal transduction pathways. Genome Biol. 11, R3 (2010).
24. D. Croft, G. O'Kelly, G. Wu, R. Haw, M. Gillespie, L. Matthews, M. Caudy, P. Garapati, G.Gopinath, B. Jassal, S. Jupe, I. Kalatskaya, S. Mahajan, B. May, N. Ndegwa, E. Schmidt, V. Shamovsky, C. Yung, E. Birney, H. Hermjakob, P. D'Eustachio, L. Stein, Reactome: A database of reactions, pathways and biological processes. Nucleic Acids Res. 39, D691-D697 (2011).
25. L. J. Jensen, M. Kuhn, M. Stark, S. Chaffron, C. Creevey, J. Muller, T. Doerks, P. Julien, A. Roth, M. Simonovic, P. Bork, C. von Mering, STRING 8 - A global view on proteins and their functional interactions in 630 organisms. Nucleic Acids Res. 37, D412-D416 (2009).
26. S. Morandell, T. Stasyk, S. Skvortsov, S. Ascher, L. A. Huber, Quantitative proteomics and phosphoproteomics reveal novel insights into complexity and dynamics of the EGFR signaling network. Proteomics 8, 4383-4401 (2008).
27. Y. Yarden, M. X. Sliwkowski, Untangling the ErbB signalling network. Nat. Rev. Mol. Cell Biol. 2, 127-137 (2001).
28. M. Punta, P. C. Coggill, R. Y. Eberhardt, J. Mistry, J. Tate, C. Boursnell, N. Pang, K. Forslund, G. Ceric, J. Clements, A. Heger, L. Holm, E. L. Sonnhammer, S. R. Eddy, A. Bateman, R. D. Finn, The Pfam protein families database. Nucleic Acids Res. 40, D290-D301 (2012).
29. F. C. Bernstein, T. F. Koetzle, G. J. Williams, E. F. Meyer Jr., M. D. Brice, J. R. Rodgers, O. Kennard, T. Shimanouchi, M. Tasumi, The Protein Data Bank: A computer-based archival file for macromolecular structures. Arch. Biochem. Biophys. 185, 584-591 (1978).
30. P. Aloy, R. B. Russell, Interrogating protein interaction networks through structural biology. Proc. Natl. Acad. Sci. U.S.A. 99, 5896-5901 (2002).
31. A. Stein, R. Mosca, P. Aloy, Three-dimensional modeling of protein interactions and complexes is going "omics". Curr. Opin. Struct. Biol. 21, 200-208 (2011).
32. J. Gureasko, W. J. Galush, S. Boykevisch, H. Sondermann, D. Bar-Sagi, J. T. Groves, J. Kuriyan, Membrane-dependent signal integration by the Ras activator Son of sevenless. Nat. Struct. Mol. Biol. 15, 452-461 (2008).
33. B. Schwanhäusser, D. Busse, N. Li, G. Dittmar, J. Schuchhardt, J. Wolf, W. Chen, M. Selbach, Global quantification of mammalian gene expression control. Nature 473, 337-342 (2011).
34. M. Beck, A. Schmidt, J. Malmstroem, M. Claassen, A. Ori, A. Szymborska, F. Herzog, O. Rinner, J. Ellenberg, R. Aebersold, The quantitative proteome of a human cell line. Mol. Syst. Biol. 7, 549 (2011).
35. N. Nagaraj, J. R.Wisniewski, T. Geiger, J. Cox, M. Kircher, J. Kelso, S. Paabo, M. Mann, Deep proteome and transcriptome mapping of a human cancer cell line. Mol. Syst. Biol. 7, 548 (2011).
36. C. Wu, C. Orozco, J. Boyer, M. Leglise, J. Goodale, S. Batalov, C. L. Hodge, J. Haase, J. Janes, J. W. Huss III, A. I. Su, BioGPS: An extensible and customizable portal for querying and organizing gene annotation resources. Genome Biol. 10, R130 (2009).
37. A. S. Dhillon, S. Hagan, O. Rath, W. Kolch, MAP kinase signalling pathways in cancer. Oncogene 26, 3279-3290 (2007).
38. Y. Wang, R. T. Waldron, A. Dhaka, A. Patel, M. M. Riley, E. Rozengurt, J. Colicelli, The RAS effector RIN1 directly competes with RAF and is regulated by 14-3-3 proteins. Mol. Cell. Biol. 22, 916-926 (2002).
39. S. Wohlgemuth, C. Kiel, A. Krämer, L. Serrano, F. Wittinghofer, C. Herrmann, Recognizing and defining true Ras binding domains I: Biochemical analysis. J. Mol. Biol. 348, 741-758 (2005).
40. A. Dhaka, R. M. Costa, H. Hu, D.K. Irvin, A. Patel, H. I. Kornblum, A. J. Silva, T. J. O'Dell, J. Colicelli, The RAS effector RIN1 modulates the formation of aversive memories. J. Neurosci. 23, 748- 757 (2003).
41. J. F. Hancock, K. Cadwallader, H. Paterson, C. J. Marshall, A CAAX or a CAAL motif and a second signal are sufficient for plasma membrane targeting of ras proteins. EMBO J. 10, 4033-4039 (1991).
42. J. E. Smotrys, M. E. Linder, Palmitoylation of intracellular signaling proteins: Regulation and function. Annu. Rev. Biochem. 73, 559-587 (2004).
43. J. H. Hurley, S. Misra, Signaling and subcellular targeting by membrane-binding domains. Annu. Rev. Biophys. Biomol. Struct. 29, 49-79 (2000).
44. R. Hosur, J. Peng, A. Vinayagam, U. Stelzl, J. Xu, N. Perrimon, J. Bienkowska, B. Berger, A computational framework for boosting confidence in high-throughput protein-protein interaction datasets. Genome Biol. 13, R76 (2012).
45. H. T. McMahon, E. Boucrot, Molecular mechanism and physiological functions of clathrinmediated endocytosis. Nat. Rev. Mol. Cell Biol. 12, 517-533 (2011).
46. B. Goldstein, J. R. Faeder, W. S. Hlavacek, Mathematical and computational models of immune-receptor signalling. Nat. Rev. Immunol. 4, 445-456 (2004).
47. J. R. Faeder, M. L. Blinov, W. S. Hlavacek, Rule-based modeling of biochemical systems with BioNetGen. Methods Mol. Biol. 500, 113-167 (2009).
48. E. J. Deeds, J. Krivine, J. Feret, V. Danos, W. Fontana, Combinatorial complexity and compositional drift in protein interaction networks. PLOS One 7, e32032 (2012).
49. E. C. O'Shaughnessy, S. Palani, J. J. Collins, C. A. Sarkar, Tunable signal processing in synthetic MAP kinase cascades. Cell 144, 119-131 (2011).
50. F. Lluis, E. Pedone, S. Pepe, M. P. Cosma, Periodic activation of Wnt/β-catenin signaling enhances somatic cell reprogramming mediated by cell fusion. Cell Stem Cell 3, 493-507 (2008).
51. K. Yamauchi, J. E. Pessin, Insulin receptor substrate-1 (IRS1) and Shc compete for a limited pool of Grb2 in mediating insulin downstream signaling. J. Biol. Chem. 269, 31107- 31114 (1994).
52. S. L. Spencer, S. Gaudet, J. G. Albeck, J. M. Burke, P. K. Sorger, Non-genetic origins of cell-to-cell variability in TRAIL-induced apoptosis. Nature 459, 428-432 (2009).
53. H. He, G. Wu, H. Liu, Y. Cheng, Y. Yu, Y. Wang, Y. Liu, Low RIN1 expression in HCC is associated with tumor invasion and unfavorable prognosis. Am. J. Clin. Pathol. 140, 73-81 (2013).
54. N. Omidvar, L. Pearn, A. K. Burnett, R. L. Darley, Ral is both necessary and sufficient for the inhibition of myeloid differentiation mediated by Ras. Mol. Cell. Biol. 26, 3966-3975 (2006).
55. J. Domen, S. H. Cheshier, I. L. Weissman, The role of apoptosis in the regulation of hematopoietic stem cells: Overexpression of BCL-2 increases both their number and repopulation potential. J. Exp. Med. 191, 253-264 (2000).
56. A. Vinayagam, U. Stelzl, R. Foulle, S. Plassmann, M. Zenkner, J. Timm, H. E. Assmus, M. A. Andrade-Navarro, E. E. Wanker, A directed protein interaction network for investigating intracellular signal transduction. Sci. Signal. 4, rs8 (2011).
57. R. B. Jones, A. Gordus, J. A. Krall, G. MacBeath, A quantitative protein interaction network for the ErbB receptors using protein microarrays. Nature 439, 168-174 (2006).
58. P. Thomas, H. Matuschek, R. Grima, Intrinsic noise analyzer: A software package for the exploration of stochastic biochemical kinetics using the system size expansion. PLOS One 7, e38518 (2012).
59. B. N. Kholodenko, O. V. Demin, G. Moehren, J. B. Hoek, Quantification of short term signaling by the epidermal growth factor receptor. J. Biol. Chem. 274, 30169-30181 (1999).
60. S. Yamada, T. Taketomi, A. Yoshimura, Model analysis of difference between EGF pathway and FGF pathway. Biochem. Biophys. Res. Commun. 314, 1113-1120 (2004).
61. D. G. Gibson, L. Young, R. Y. Chuang, J. C. Venter, C. A. Hutchison III, H. O. Smith, Enzymatic assembly of DNA molecules up to several hundred kilobases. Nat. Methods 6, 343-345 (2009).