NSP-Cas protein structures reveal a promiscuous interaction module in cell signaling

Nature Structural and Molecular Biology

Volumn 18, Issue 12, 2011, Pages 1381-1387

  MacE, Peter D ^a   Wallez, Yann ^a   Dobaczewska, Małgorzata K ^a   Lee, Jeongeun J ^a   Robinson, Howard ^b   Pasquale, Elena B ^a,c   Riedl, Stefan J ^a  

^a BURNHAM INSTITUTE   (United States)

^b BROOKHAVEN NATIONAL LABORATORY   (United States)

^c UNIVERSITY OF CALIFORNIA   (United States)

Author keywords

[No Author keywords available]

Indexed keywords

CELLULAR APOPTOSIS SUSCEPTIBILITY PROTEIN; CRK ASSOCIATED SUBSTRATE PROTEIN; GUANINE NUCLEOTIDE BINDING PROTEIN; PROTEIN CDC25; PROTEIN NSP; PROTEIN SH2; RAS PROTEIN; UNCLASSIFIED DRUG;

ARTICLE; BINDING AFFINITY; CARBOXY TERMINAL SEQUENCE; CELL INVASION; CELL MIGRATION; COMPLEX FORMATION; CRYSTAL STRUCTURE; ENZYME ACTIVITY; FOCAL ADHESION; PRIORITY JOURNAL; PROTEIN CONFORMATION; PROTEIN DOMAIN; PROTEIN FAMILY; PROTEIN MOTIF; PROTEIN PROTEIN INTERACTION; PROTEIN STRUCTURE; SIGNAL TRANSDUCTION;

ADAPTOR PROTEINS, SIGNAL TRANSDUCING; BINDING SITES; CONSERVED SEQUENCE; CRK-ASSOCIATED SUBSTRATE PROTEIN; HUMANS; MODELS, MOLECULAR; PROTEIN STRUCTURE, TERTIARY; SIGNAL TRANSDUCTION;

EID: 82955167894     PISSN: 15459993     EISSN: 15459985     Source Type: Journal    
DOI: 10.1038/nsmb.2152     Document Type: Article

References (51)

1. Brinkman, A., van der Flier, S., Kok, E.M. & Dorssers, L.C. BCAR1, a human homologue of the adapter protein p130Cas, and antiestrogen resistance in breast cancer cells. J. Natl. Cancer Inst. 92, 112-120 (2000). (Pubitemid 30089867)
2. Van Agthoven, T. et al. Identification of BCAR3 by a random search for genes involved in antiestrogen resistance of human breast cancer cells. EMBO J. 17, 2799-2808 (1998). (Pubitemid 28227126)
3. Cabodi, S., Del Pilar Camacho-Leal, M., Di Stefano, P. & Defilippi, P. Integrin signalling adaptors: not only figurants in the cancer story. Nat. Rev. Cancer 10, 858-870 (2010).
4. Felekkis, K., Quilliam, L.A. & Lerner, A. Characterization of AND-34 function and signaling. Methods Enzymol. 407, 55-63 (2006). (Pubitemid 43815938)
5. Gotoh, T., Cai, D., Tian, X., Feig, L.A. & Lerner, A. p130Cas regulates the activity of AND-34, a novel Ral, Rap1, and R-Ras guanine nucleotide exchange factor. J. Biol. Chem. 275, 30118-30123 (2000).
6. Lu, Y., Brush, J. & Stewart, T.A. NSP1 defines a novel family of adaptor proteins linking integrin and tyrosine kinase receptors to the c-Jun N-terminal kinase/stress-activated protein kinase signaling pathway. J. Biol. Chem. 274, 10047-10052 (1999).
7. Sakakibara, A. & Hattori, S. Chat, a Cas/HEF1-associated adaptor protein that integrates multiple signaling pathways. J. Biol. Chem. 275, 6404-6410 (2000). (Pubitemid 30129936)
8. Cai, D. et al. The GDP exchange factor AND-34 is expressed in B cells, associates with HEF1, and activates Cdc42. J. Immunol. 170, 969-978 (2003). (Pubitemid 36070551)
9. Al-Shami, A. et al. The adaptor protein Sh2d3c is critical for marginal zone B cell development and function. J. Immunol. 185, 327-334 (2010).
10. Alexandropoulos, K. & Regelmann, A.G. Regulation of T-lymphocyte physiology by the Chat-H/CasL adapter complex. Immunol. Rev. 232, 160-174 (2009).
11. Browne, C.D. et al. SHEP1 partners with CasL to promote marginal zone B-cell maturation. Proc. Natl. Acad. Sci. USA 107, 18944-18949 (2010).
12. Schrecengost, R.S., Riggins, R.B., Thomas, K.S., Guerrero, M.S. & Bouton, A.H. Breast cancer antiestrogen resistance-3 expression regulates breast cancer cell migration through promotion of p130Cas membrane localization and membrane ruffling. Cancer Res. 67, 6174-6182 (2007). (Pubitemid 47037498)
13. Schuh, N.R., Guerrero, M.S., Schrecengost, R.S. & Bouton, A.H. BCAR3 regulates Src/p130 Cas association, Src kinase activity, and breast cancer adhesion signaling. J. Biol. Chem. 285, 2309-2317 (2010).
14. Wang, L. et al. The SRC homology 2 domain protein Shep1 plays an important role in the penetration of olfactory sensory axons into the forebrain. J. Neurosci. 30, 13201-13210 (2010).
15. Cai, D., Clayton, L.K., Smolyar, A. & Lerner, A. AND-34, a novel p130Cas-binding thymic stromal cell protein regulated by adhesion and inflammatory cytokines. J. Immunol. 163, 2104-2112 (1999). (Pubitemid 29382216)
16. Garron, M.-L. et al. Structural insights into the association between BCAR3 and Cas family members, an atypical complex implicated in anti-oestrogen resistance. J. Mol. Biol. 386, 190-203 (2009).
17. Boriack-Sjodin, P.A., Margarit, S.M., Bar-Sagi, D. & Kuriyan, J. The structural basis of the activation of Ras by Sos. Nature 394, 337-343 (1998). (Pubitemid 28373822)
18. Rehmann, H., Das, J., Knipscheer, P., Wittinghofer, A. & Bos, J.L. Structure of the cyclic-AMP-responsive exchange factor Epac2 in its auto-inhibited state. Nature 439, 625-628 (2006). (Pubitemid 43185390)
19. Freedman, T.S. et al. A Ras-induced conformational switch in the Ras activator Son of sevenless. Proc. Natl. Acad. Sci. USA 103, 16692-16697 (2006). (Pubitemid 44737315)
20. Rehmann, H. et al. Structure of Epac2 in complex with a cyclic AMP analogue and RAP1B. Nature 455, 124-127 (2008).
21. Freedman, T.S. et al. Differences in flexibility underlie functional differences in the Ras activators son of sevenless and Ras guanine nucleotide releasing factor 1. Structure 17, 41-53 (2009).
22. Bos, J.L., de Rooij, J. & Reedquist, K.A. Rap1 signalling: adhering to new models. Nat. Rev. Mol. Cell Biol. 2, 369-377 (2001). (Pubitemid 33674049)
23. Dodelet, V.C., Pazzagli, C., Zisch, A.H., Hauser, C.A. & Pasquale, E.B. A novel signaling intermediate, SHEP1, directly couples Eph receptors to R-Ras and Rap1A. J. Biol. Chem. 274, 31941-31946 (1999).
24. Sakakibara, A., Ohba, Y., Kurokawa, K., Matsuda, M. & Hattori, S. Novel function of Chat in controlling cell adhesion via Cas-Crk-C3G-pathway- mediated Rap1 activation. J. Cell Sci. 115, 4915-4924 (2002). (Pubitemid 36054643)
25. Riggins, R.B., Quilliam, L.A. & Bouton, A.H. Synergistic promotion of c-Src activation and cell migration by Cas and AND-34/BCAR3. J. Biol. Chem. 278, 28264-28273 (2003). (Pubitemid 36900028)
26. van den Berghe, N., Cool, R.H., Horn, G. & Wittinghofer, A. Biochemical characterization of C3G: an exchange factor that discriminates between Rap1 and Rap2 and is not inhibited by Rap1A(S17N). Oncogene 15, 845-850 (1997). (Pubitemid 27390137)
27. Dail, M. et al. SHEP1 function in cell migration is impaired by a single amino acid mutation that disrupts association with the scaffolding protein cas but not with Ras GTPases. J. Biol. Chem. 279, 41892-41902 (2004). (Pubitemid 39313638)
28. Deakin, N.O. & Turner, C.E. Paxillin comes of age. J. Cell Sci. 121, 2435-2444 (2008).
29. Bertolucci, C.M., Guibao, C.D. & Zheng, J. Structural features of the focal adhesion kinase-paxillin complex give insight into the dynamics of focal adhesion assembly. Protein Sci. 14, 644-652 (2005). (Pubitemid 40283902)
30. Hoellerer, M.K. et al. Molecular recognition of paxillin LD motifs by the focal adhesion targeting domain. Structure 11, 1207-1217 (2003). (Pubitemid 37214883)
31. Lulo, J., Yuzawa, S. & Schlessinger, J. Crystal structures of free and ligand-bound focal adhesion targeting domain of Pyk2. Biochem. Biophys. Res. Commun. 383, 347-352 (2009).
32. Thomas, J.W. et al. The role of focal adhesion kinase binding in the regulation of tyrosine phosphorylation of paxillin. J. Biol. Chem. 274, 36684-36692 (1999).
33. Vanden Borre, P., Near, R.I., Makkinje, A., Mostoslavsky, G. & Lerner, A. BCAR3/AND-34 can signal independent of complex formation with CAS family members or the presence of p130Cas. Cell. Signal. 23, 1030-1040 (2011).
34. van Agthoven, T. et al. Functional identification of genes causing estrogen independence of human breast cancer cells. Breast Cancer Res. Treat. 114, 23-30 (2009).
35. Ji, H. et al. LKB1 modulates lung cancer differentiation and metastasis. Nature 448, 807-810 (2007). (Pubitemid 47266337)
36. Kim, M. et al. Comparative oncogenomics identifies NEDD9 as a melanoma metastasis gene. Cell 125, 1269-1281 (2006). (Pubitemid 43949521)
37. Sondermann, H. et al. Structural analysis of autoinhibition in the Ras activator Son of sevenless. Cell 119, 393-405 (2004). (Pubitemid 39423841)
38. Margarit, S.M. et al. Structural evidence for feedback activation by Ras.GTP of the Ras-specific nucleotide exchange factor SOS. Cell 112, 685-695 (2003). (Pubitemid 36331780)
39. Roselli, S., Wallez, Y., Wang, L., Vervoort, V. & Pasquale, E.B. The SH2 domain protein Shep1 regulates the in vivo signaling function of the scaffolding protein Cas. Cell. Signal. 22, 1745-1752 (2010).
40. Kabsch, W. XDS. Acta Crystallogr. D Biol. Crystallogr. 66, 125-132 (2010).
41. CCP4. The CCP4 suite: programs for protein crystallography. Acta Crystallogr. D Biol. Crystallogr. 50, 760-763 (1994).
42. Storoni, L., McCoy, A. & Read, R. Likelihood-enhanced fast rotation functions. Acta Crystallogr. D Biol. Crystallogr. 60, 432-438 (2004). (Pubitemid 41087570)
43. Adams, P.D. et al. PHENIX: a comprehensive Python-based system for macromolecular structure solution. Acta Crystallogr. D Biol. Crystallogr. 66, 213-221 (2010).
44. Emsley, P. & Cowtan, K. Coot: model-building tools for molecular graphics. Acta Crystallogr. D Biol. Crystallogr. 60, 2126-2132 (2004). (Pubitemid 41742764)
45. Otwinowski, Z. & Minor, W. Processing of X-ray diffraction data collected in oscillation mode. Methods Enzymol. 276, 307-326 (1997). (Pubitemid 27085611)
46. Vonrhein, C., Blanc, E., Roversi, P. & Bricogne, G. Automated structure solution with autoSHARP. Methods Mol. Biol. 364, 215-230 (2006 (Pubitemid 350183137)
47. Rychlewski, L., Jaroszewski, L., Li, W. & Godzik, A. Comparison of sequence profiles. Strategies for structural predictions using sequence information. Protein Sci. 9, 232-241 (2000). (Pubitemid 30126996)
48. Eswar, N., Eramian, D., Webb, B., Shen, M.Y. & Sali, A. Protein structure modeling with MODELLER. Methods Mol. Biol. 426, 145-159 (2008).
49. Nassar, N. et al. The 2.2 A crystal structure of the Ras-binding domain of the serine/threonine kinase c-Raf1 in complex with Rap1A and a GTP analogue. Nature 375, 554-560 (1995).
50. Cherfils, J. et al. Crystal structures of the small G protein Rap2A in complex with its substrate GTP, with GDP and with GTPgammaS. EMBO J. 16, 5582-5591 (1997). (Pubitemid 27399850)
51. Lenzen, C.U., Cool, R.H. & Wittinghofer, A. Analysis of intrinsic and CDC25-stimulated guanine nucleotide exchange of p21ras-nucleotide complexes by fluorescence measurements. Methods Enzymol. 255, 95-109 (1995).