Structural basis for activation and non-canonical catalysis of the Rap GTPase activating protein domain of plexin

eLife

Volumn 2013, Issue 2, 2013, Pages

  Wang, Yuxiao ^a   Pascoe, Heath G ^a   Brautigam, Chad A ^b   He, Huawei ^a,c   Zhang, Xuewu ^a,b  

^a UNIVERSITY OF TEXAS SOUTHWESTERN MEDICAL CENTER   (United States)

^b UNIVERSITY OF TEXAS SOUTHWESTERN MEDICAL CENTER   (United States)

^c SOUTHWEST UNIVERSITY   (China)

Author keywords

[No Author keywords available]

Indexed keywords

CELL ADHESION MOLECULE; GUANOSINE TRIPHOSPHATE; NERVE PROTEIN; PLEXIN; PROTEIN BINDING; RAP PROTEIN; ZEBRAFISH PROTEIN;

AMINO ACID SEQUENCE; ANIMAL; CHEMICAL STRUCTURE; CHEMISTRY; ENZYME ACTIVE SITE; GENE EXPRESSION REGULATION; GENETICS; HUMAN; METABOLISM; MOLECULAR GENETICS; MOUSE; PROTEIN MULTIMERIZATION; PROTEIN SECONDARY STRUCTURE; PROTEIN TERTIARY STRUCTURE; SEQUENCE ALIGNMENT; SEQUENCE HOMOLOGY; SIGNAL TRANSDUCTION; X RAY CRYSTALLOGRAPHY; ZEBRA FISH;

AMINO ACID SEQUENCE; ANIMALS; CATALYTIC DOMAIN; CELL ADHESION MOLECULES; CHEMISTRY; CRYSTALLOGRAPHY, X-RAY; GENE EXPRESSION REGULATION; GENETICS; GUANOSINE TRIPHOSPHATE; HUMANS; METABOLISM; MICE; MODELS, MOLECULAR; MOLECULAR SEQUENCE DATA; NERVE TISSUE PROTEINS; PROTEIN BINDING; PROTEIN MULTIMERIZATION; PROTEIN STRUCTURE, SECONDARY; PROTEIN STRUCTURE, TERTIARY; RAP GTP-BINDING PROTEINS; SEQUENCE ALIGNMENT; SEQUENCE HOMOLOGY, AMINO ACID; SIGNAL TRANSDUCTION; ZEBRAFISH; ZEBRAFISH PROTEINS;

DANIO RERIO;

EID: 84885158575     PISSN: None     EISSN: 2050084X     Source Type: Journal    
DOI: 10.7554/eLife.01279.001     Document Type: Article

References (74)

1. Adams PD, Grosse-Kunstleve RW, Hung LW, Ioerger TR, McCoy AJ, Moriarty NW, et al. 2002. PHENIX: building new software for automated crystallographic structure determination. Acta Crystallogr 58:1948-54. doi: 10.1107/S0907444902016657.
2. Antipenko A, Himanen JP, van Leyen K, Nardi-Dei V, Lesniak J, Barton WA, et al. 2003. Structure of the semaphorin-3A receptor binding module. Neuron 39:589-98. doi: 10.1016/S0896-6273(03)00502-6.
3. Bell CH, Aricescu AR, Jones EY, Siebold C. 2011. A dual binding mode for RhoGTPases in plexin signalling. PLOS Biol 9:e1001134. doi: 10.1371/journal.pbio.1001134.
4. Bos JL, Rehmann H, Wittinghofer A. 2007. GEFs and GAPs: critical elements in the control of small G proteins. Cell 129:865-77. doi: 10.1016/j.cell.2007.05.018.
5. Cancer Genome Atlas Research Network. 2012. Comprehensive molecular characterization of human colon and rectal cancer. Nature 487:330-7. doi: 10.1038/nature11252.
6. Cancer Genome Atlas Research Network. 2012. Comprehensive genomic characterization of squamous cell lung cancers. Nature 489:519-25. doi: 10.1038/nature11404.
7. Chen VB, Arendall WB III, Headd JJ, Keedy DA, Immormino RM, Kapral GJ, et al. 2010. MolProbity: all-atom structure validation for macromolecular crystallography. Acta Crystallogr 66:12-21. doi: 10.1107/S0907444909042073.
8. Dai Y, Walker SA, de Vet E, Cook S, Welch HC, Lockyer PJ. 2011. Ca2+-dependent monomer and dimer formation switches CAPRI protein between ras GTPase-activating protein (GAP) and RapGAP activities. J Biol Chem 286:19905-16. doi: 10.1074/jbc.M110.201301.
9. Driessens MH, Hu H, Nobes CD, Self A, Jordens I, Goodman CS, et al. 2001. Plexin-B semaphorin receptors interact directly with active Rac and regulate the actin cytoskeleton by activating Rho. Curr Biol 11:339-44. doi: 10.1016/S0960-9822(01)00092-6.
10. Emsley P, Cowtan K. 2004. Coot: model-building tools for molecular graphics. Acta Crystallogr 60:2126-32. doi: 10.1107/S0907444904019158.
11. Frech M, John J, Pizon V, Chardin P, Tavitian A, Clark R, et al. 1990. Inhibition of GTPase activating protein stimulation of Ras-p21 GTPase by the Krev-1 gene product. Science 249:169-71. doi: 10.1126/science.2164710.
12. Gloerich M, Bos JL. 2011. Regulating Rap small G-proteins in time and space. Trends Cell Biol 21:615-23. doi: 10.1016/j.tcb.2011.07.001.
13. Gouet P, Courcelle E, Stuart DI, Metoz F. 1999. ESPript: analysis of multiple sequence alignments in PostScript. Bioinformatics 15:305-8.
14. Gu C, Giraudo E. 2013. The role of semaphorins and their receptors in vascular development and cancer. Exp Cell Res 319:1306-16. doi: 10.1016/j.yexcr.2013.02.003.
15. Gui Y, Guo G, Huang Y, Hu X, Tang A, Gao S, et al. 2011. Frequent mutations of chromatin remodeling genes in transitional cell carcinoma of the bladder. Nat Genet 43:875-8. doi: 10.1038/ng.907.
16. Hata Y, Kikuchi A, Sasaki T, Schaber MD, Gibbs JB, Takai Y. 1990. Inhibition of the ras p21 GTPase-activating protein-stimulated GTPase activity of c-Ha-ras p21 by smg p21 having the same putative effector domain as ras p21s. J Biol Chem 265:7104-7.
17. He H, Yang T, Terman JR, Zhang X. 2009. Crystal structure of the plexin A3 intracellular region reveals an autoinhibited conformation through active site sequestration. Proc Natl Acad Sci USA 106:15610-5. doi: 10.1073/pnas.0906923106.
18. Hu H, Marton TF, Goodman CS. 2001. Plexin B mediates axon guidance in Drosophila by simultaneously inhibiting active Rac and enhancing RhoA signaling. Neuron 32:39-51. doi: 10.1016/S0896-6273(01)00453-6.
19. Huse M, Kuriyan J. 2002. The conformational plasticity of protein kinases. Cell 109:275-82. doi: 10.1016/S0092-8674(02)00741-9.
20. Janssen BJ, Malinauskas T, Weir GA, Cader MZ, Siebold C, Jones EY. 2012. Neuropilins lock secreted semaphorins onto plexins in a ternary signaling complex. Nat Struct Mol Biol 19:1293-9. doi: 10.1038/nsmb.2416.
21. Janssen BJ, Robinson RA, Perez-Branguli F, Bell CH, Mitchell KJ, Siebold C, et al. 2010. Structural basis of semaphorin-plexin signalling. Nature 467:1118-22. doi: 10.1038/nature09468.
22. Klostermann A, Lohrum M, Adams RH, Puschel AW. 1998. The chemorepulsive activity of the axonal guidance signal semaphorin D requires dimerization. J Biol Chem 273:7326-31. doi: 10.1074/jbc.273.13.7326.
23. Koppel AM, Raper JA. 1998. Collapsin-1 covalently dimerizes, and dimerization is necessary for collapsing activity. J Biol Chem 273:15708-13. doi: 10.1074/jbc.273.25.15708.
24. Krebs WG, Gerstein M. 2000. The morph server: a standardized system for analyzing and visualizing macromolecular motions in a database framework. Nucleic Acids Res 28:1665-75. doi: 10.1093/nar/28.8.1665.
25. Kupzig S, Bouyoucef-Cherchalli D, Yarwood S, Sessions R, Cullen PJ. 2009. The ability of GAP1IP4BP to function as a Rap1 GTPase-activating protein (GAP) requires its Ras GAP-related domain and an arginine finger rather than an asparagine thumb. Mol Cell Biol 29:3929-40. doi: 10.1128/MCB.00427-09.
26. Kupzig S, Deaconescu D, Bouyoucef D, Walker SA, Liu Q, Polte CL, et al. 2006. GAP1 family members constitute bifunctional Ras and Rap GTPase-activating proteins. J Biol Chem 281:9891-900. doi: 10.1074/jbc.M512802200.
27. Laue TM, Shah BD, Ridgeway TM, Pelletier SL. 1992. Computer-aided interpretation of analytical sedimentation data for proteins. In: Harding SE, Rowe AJ, Horton JC, editors. Analytical ultracentrifugation in biochemistry and polymer science. Cambridge, United Kingdom: Royal Society of Chemistry. p. 90-125.
28. Li S, Nakamura S, Hattori S. 1997. Activation of R-Ras GTPase by GTPase-activating proteins for Ras, Gap1(m), and p120GAP. J Biol Chem 272:19328-32. doi: 10.1074/jbc.272.31.19328.
29. Liu H, Juo ZS, Shim AH, Focia PJ, Chen X, Garcia KC, et al. 2010. Structural basis of semaphorin-plexin recognition and viral mimicry from Sema7A and A39R complexes with PlexinC1. Cell 142:749-61. doi: 10.1016/j.cell.2010.07.040.
30. Love CA, Harlos K, Mavaddat N, Davis SJ, Stuart DI, Jones EY, et al. 2003. The ligand-binding face of the semaphorins revealed by the high-resolution crystal structure of SEMA4D. Nat Struct Biol 10:843-8. doi: 10.1038/nsb977.
31. Mccoy AJ, Grosse-Kunstleve RW, Adams PD, Winn MD, Storoni LC, Read RJ. 2007. Phaser crystallographic software. J Appl Crystallogr 40:658-74. doi: 10.1107/S0021889807021206.
32. Nassar N, Horn G, Herrmann C, Block C, Janknecht R, Wittinghofer A. 1996. Ras/Rap effector specificity determined by charge reversal. Nat Struct Biol 3:723-9. doi: 10.1038/nsb0896-723.
33. Nogi T, Yasui N, Mihara E, Matsunaga Y, Noda M, Yamashita N, et al. 2010. Structural basis for semaphorin signalling through the plexin receptor. Nature 467:1123-7. doi: 10.1038/nature09473.
34. Notredame C, Higgins DG, Heringa J. 2000. T-Coffee: a novel method for fast and accurate multiple sequence alignment. J Mol Biol 302:205-17. doi: 10.1006/jmbi.2000.4042.
35. Ohba Y, Mochizuki N, Yamashita S, Chan AM, Schrader JW, Hattori S, et al. 2000. Regulatory proteins of r-ras, TC21/R-Ras2, and m-Ras/R-Ras3. J Biol Chem 275:20020-6. doi: 10.1074/jbc.M000981200.
36. Oinuma I, Ishikawa Y, Katoh H, Negishi M. 2004. The Semaphorin 4D receptor Plexin-B1 is a GTPase activating protein for R-Ras. Science 305:862-5. doi: 10.1126/science.1097545.
37. O'Shea EK, Klemm JD, Kim PS, Alber T. 1991. X-ray structure of the GCN4 leucine zipper, a two-stranded, parallel coiled coil. Science 254:539-44. doi: 10.1126/science.1948029.
38. Otwinowski Z, Minor W. 1997. Processing of x-ray diffraction data collected in oscillation mode. Methods Enzymol 276:307-26. doi: 10.1016/S0076-6879(97)76066-X.
39. Padilla JE, Yeates TO. 2003. A statistic for local intensity differences: robustness to anisotropy and pseudo-centering and utility for detecting twinning. Acta Crystallogr D Biol Crystallogr 59:1124-30. doi: 10.1107/S0907444903007947.
40. Pena V, Hothorn M, Eberth A, Kaschau N, Parret A, Gremer L, et al. 2008. The C2 domain of SynGAP is essential for stimulation of the Rap GTPase reaction. EMBO Rep 9:350-5. doi: 10.1038/embor.2008.20.
41. Perrot V, Vazquez-Prado J, Gutkind JS. 2002. Plexin B regulates Rho through the guanine nucleotide exchange factors leukemia-associated Rho GEF (LARG) and PDZ-RhoGEF. J Biol Chem 277:43115-20. doi: 10.1074/jbc.M206005200.
42. Popp MW, Antos JM, Ploegh HL. 2009. Site-specific protein labeling via sortase-mediated transpeptidation. Curr Protoc Protein Sci Chapter 15:Unit 15 13. doi: 10.1002/0471140864.ps1503s56.
43. Quilliam LA, Castro AF, Rogers-Graham KS, Martin CB, Der CJ, Bi C. 1999. M-Ras/R-Ras3, a transforming ras protein regulated by Sos1, GRF1, and p120 Ras GTPase-activating protein, interacts with the putative Ras effector AF6. J Biol Chem 274:23850-7. doi: 10.1074/jbc.274.34.23850.
44. Rohm B, Rahim B, Kleiber B, Hovatta I, Püschel AW. 2000. The semaphorin 3A receptor may directly regulate the activity of small GTPases. FEBS Lett 486:68-72. doi: 10.1016/S0014-5793(00)02240-7.
45. Saito Y, Oinuma I, Fujimoto S, Negishi M. 2009. Plexin-B1 is a GTPase activating protein for M-Ras, remodelling dendrite morphology. EMBO Rep 10:614-21. doi: 10.1038/embor.2009.63.
46. Sakurai A, Doci C, Gutkind JS. 2012. Semaphorin signaling in angiogenesis, lymphangiogenesis and cancer. Cell Res 22:23-32. doi: 10.1038/cr.2011.198.
47. Scheffzek K, Ahmadian MR, Kabsch W, Wiesmuller L, Lautwein A, et al. 1997. The Ras-RasGAP complex: structural basis for GTPase activation and its loss in oncogenic Ras mutants. Science 277:333-8. doi: 10.1126/science.277.5324.333.
48. Scheffzek K, Ahmadian MR, Wiesmuller L, Kabsch W, Stege P, Schmitz F, et al. 1998. Structural analysis of the GAP-related domain from neurofibromin and its implications. EMBO J 17:4313-27. doi: 10.1093/emboj/17.15.4313.
49. Schmidt EF, Shim SO, Strittmatter SM. 2008. Release of MICAL autoinhibition by semaphorin-plexin signaling promotes interaction with collapsin response mediator protein. J Neurosci 28:2287-97. doi: 10.1523/JNEUROSCI.5646-07.2008.
50. Schuck P. 2000. Size-distribution analysis of macromolecules by sedimentation velocity ultracentrifugation and lamm equation modeling. Biophys J 78:1606-19. doi: 10.1016/S0006-3495(00)76713-0.
51. Schuck P, Demeler B. 1999. Direct sedimentation analysis of interference optical data in analytical ultracentrifugation. Biophys J 76:2288-96. doi: 10.1016/S0006-3495(99)77384-4.
52. Scrima A, Thomas C, Deaconescu D, Wittinghofer A. 2008. The Rap-RapGAP complex: GTP hydrolysis without catalytic glutamine and arginine residues. EMBO J 27:1145-53. doi: 10.1038/emboj.2008.30.
53. Seshagiri S, Stawiski EW, Durinck S, Modrusan Z, Storm EE, Conboy CB, et al. 2012. Recurrent R-spondin fusions in colon cancer. Nature 488:660-4. doi: 10.1038/nature11282.
54. Siebold C, Jones EY. 2013. Structural insights into semaphorins and their receptors. Semin Cell Dev Biol 24:139-45. doi: 10.1016/j.semcdb.2012.11.003.
55. Snyder JT, Worthylake DK, Rossman KL, Betts L, Pruitt WM, Siderovski DP, et al. 2002. Structural basis for the selective activation of Rho GTPases by Dbl exchange factors. Nat Struct Biol 9:468-75. doi: 10.1038/nsb796.
56. Sot B, Kötting C, Deaconescu D, Suveyzdis Y, Gerwert K, Wittinghofer A. 2010. Unravelling the mechanism of dual-specificity GAPs. EMBO J 29:1205-14. doi: 10.1038/emboj.2010.20.
57. Takahashi T, Fournier A, Nakamura F, Wang LH, Murakami Y, Kalb RG, et al. 1999. Plexin-neuropilin-1 complexes form functional semaphorin-3A receptors. Cell 99:59-69. doi: 10.1016/S0092-8674(00)80062-8.
58. Takamatsu H, Kumanogoh A. 2012. Diverse roles for semaphorin-plexin signaling in the immune system. Trends Immunol 33:127-35. doi: 10.1016/j.it.2012.01.008.
59. Tamagnone L. 2012. Emerging role of semaphorins as major regulatory signals and potential therapeutic targets in cancer. Cancer Cell 22:145-52. doi: 10.1016/j.ccr.2012.06.031.
60. Tong Y, Chugha P, Hota PK, Alviani RS, Li M, Tempel W, et al. 2007. Binding of Rac1, Rnd1, and RhoD to a novel Rho GTPase interaction motif destabilizes dimerization of the plexin-B1 effector domain. J Biol Chem 282:37215-24. doi: 10.1074/jbc.M703800200.
61. Tong Y, Hota PK, Penachioni JY, Hamaneh MB, Kim S, Alviani RS, et al. 2009. Structure and function of the intracellular region of the plexin-b1 transmembrane receptor. J Biol Chem 284:35962-72. doi: 10.1074/jbc.M109.056275.
62. Toyofuku T, Yoshida J, Sugimoto T, Zhang H, Kumanogoh A, Hori M, et al. 2005. FARP2 triggers signals for Sema3A-mediated axonal repulsion. Nat Neurosci 8:1712-9. doi: 10.1038/nn1596.
63. Tran TS, Kolodkin AL, Bharadwaj R. 2007. Semaphorin regulation of cellular morphology. Ann Rev Cell Dev Biol 23:263-92. doi: 10.1146/annurev.cellbio.22.010605.093554.
64. Turner LJ, Nicholls S, Hall A. 2004. The activity of the plexin-A1 receptor is regulated by Rac. J Biol Chem 279:33199-205. doi: 10.1074/jbc.M402943200.
65. Vetter IR, Wittinghofer A. 2001. The guanine nucleotide-binding switch in three dimensions. Science 294:1299-304. doi: 10.1126/science.1062023.
66. Vikis HG, Li W, He Z, Guan KL. 2000. The semaphorin receptor plexin-B1 specifically interacts with active Rac in a ligand-dependent manner. Proc Natl Acad Sci USA 97:12457-62. doi: 10.1073/pnas.220421797.
67. Wang Y, He H, Srivastava N, Vikarunnessa S, Chen YB, Jiang J, et al. 2012. Plexins are GTPase-activating proteins for Rap and are activated by induced dimerization. Sci Signal 5:ra6. doi: 10.1126/scisignal.2002636.
68. Webb MR, Hunter JL. 1992. Interaction of GTPase-activating protein with p21ras, measured using a continuous assay for inorganic phosphate release. Biochem J 287(Pt 2):555-9.
69. Winn MD, Ballard CC, Cowtan KD, Dodson EJ, Emsley P, Evans PR, et al. 2011. Overview of the CCP4 suite and current developments. Acta Crystallogr 67:235-42. doi: 10.1107/S0907444910045749.
70. Yaron A, Zheng B. 2007. Navigating their way to the clinic: emerging roles for axon guidance molecules in neurological disorders and injury. Dev Neurobiol 67:1216-31. doi: 10.1002/dneu.20512.
71. Yatani A, Quilliam LA, Brown AM, Bokoch GM. 1991. Rap1A antagonizes the ability of Ras and Ras-Gap to inhibit muscarinic K+ channels. J Biol Chem 266:22222-6.
72. Yazdani U, Terman JR. 2006. The semaphorins. Genome Biol 7:211. doi: 10.1186/gb-2006-7-3-211.
73. Zanata SM, Hovatta I, Rohm B, Püschel AW. 2002. Antagonistic effects of Rnd1 and RhoD GTPases regulate receptor activity in Semaphorin 3A-induced cytoskeletal collapse. J Neurosci 22:471-7.
74. Zhao H, Ghirlando R, Piszczek G, Curth U, Brautigam CA, Schuck P. 2013. Recorded scan times can limit the accuracy of sedimentation coefficients in analytical ultracentrifugation. Anal Biochem 437:104-8. doi: 10.1016/j.ab.2013.02.011.