Dimeric plant RhoGAPs are regulated by its CRIB effector motif to stimulate a sequential GTP hydrolysis

Journal of Molecular Biology

Volumn 411, Issue 4, 2011, Pages 808-822

  Schaefer, Antje ^a,b   Miertzschke, Mandy ^a   Berken, Antje ^a,c   Wittinghofer, Alfred ^a  

^a MAX PLANCK INSTITUTE OF MOLECULAR PHYSIOLOGY   (Germany)

^b UNIVERSITY OF AMSTERDAM   (Netherlands)

^c MAX PLANCK INSTITUTE FOR BRAIN RESEARCH   (Germany)

Author keywords

CRIB effector; G protein; GTPase activating protein; RopGAP

Indexed keywords

DIMER; GUANOSINE TRIPHOSPHATASE ACTIVATING PROTEIN; GUANOSINE TRIPHOSPHATE; PROTEIN CDC42; PROTEIN ROP4; PROTEIN ROP7; RAC PROTEIN; UNCLASSIFIED DRUG; VEGETABLE PROTEIN;

ARABIDOPSIS; ARTICLE; BINDING AFFINITY; CATALYSIS; ENZYME ACTIVE SITE; ENZYME ACTIVITY; NONHUMAN; PRIORITY JOURNAL; PROTEIN DOMAIN; PROTEIN EXPRESSION; PROTEIN HYDROLYSIS; PROTEIN MOTIF; PROTEIN PROTEIN INTERACTION; PROTEIN PURIFICATION; PROTEIN SECRETION; PROTEIN STRUCTURE; REGULATORY MECHANISM; SITE DIRECTED MUTAGENESIS; STRUCTURE ANALYSIS; WILD TYPE;

ANIMALIA; ARABIDOPSIS THALIANA; FUNGI;

EID: 80051665477     PISSN: 00222836     EISSN: 10898638     Source Type: Journal    
DOI: 10.1016/j.jmb.2011.06.033     Document Type: Article

References (50)

1. Bos J.L., Rehmann H., and Wittinghofer A. GEFs and GAPs: critical elements in the control of small G proteins Cell 129 2007 865 877 (Pubitemid 46802708)
2. Vetter I.R., and Wittinghofer A. The guanine nucleotide-binding switch in three dimensions Science 294 2001 1299 1304 (Pubitemid 33063089)
3. Gasper R., Meyer S., Gotthardt K., Sirajuddin M., and Wittinghofer A. It takes two to tango: regulation of G proteins by dimerization Nat. Rev., Mol. Cell Biol. 10 2009 423 429
4. Scheffzek K., Ahmadian M.R., Kabsch W., Wiesmuller L., Lautwein A., Schmitz F., and Wittinghofer A. The Ras-RasGAP complex: structural basis for GTPase activation and its loss in oncogenic Ras mutants Science 277 1997 333 338 (Pubitemid 27450699)
5. Rittinger K., Walker P.A., Eccleston J.F., Smerdon S.J., and Gamblin S.J. Structure at 1.65 Å of RhoA and its GTPase-activating protein in complex with a transition-state analogue Nature 389 1997 758 762 (Pubitemid 27458966)
6. Pan X., Eathiraj S., Munson M., and Lambright D.G. TBC-domain GAPs for Rab GTPases accelerate GTP hydrolysis by a dual-finger mechanism Nature 442 2006 303 306 (Pubitemid 44114905)
7. 2+ regulatory mechanism Cell 141 2010 812 821
8. Veltel S., Gasper R., Eisenacher E., and Wittinghofer A. The retinitis pigmentosa 2 gene product is a GTPase-activating protein for Arf-like 3 Nat. Struct. Mol. Biol. 15 2008 373 380 (Pubitemid 351483389)
9. Scrima A., Thomas C., Deaconescu D., and Wittinghofer A. The Rap-RapGAP complex: GTP hydrolysis without catalytic glutamine and arginine residues EMBO J. 27 2008 1145 1153 (Pubitemid 351508140)
10. Daumke O., Weyand M., Chakrabarti P.P., Vetter I.R., and Wittinghofer A. The GTPase-activating protein Rap1GAP uses a catalytic asparagine Nature 429 2004 197 201 (Pubitemid 38656197)
11. Burbelo P.D., Drechsel D., and Hall A. A conserved binding motif defines numerous candidate target proteins for both Cdc42 and Rac GTPases J. Biol. Chem. 270 1995 29071 29074
12. Bishop A.L., and Hall A. Rho GTPases and their effector proteins Biochem. J. 348 2000 241 255 (Pubitemid 30345195)
13. Rudolph M.G., Bayer P., Abo A., Kuhlmann J., Vetter I.R., and Wittinghofer A. The Cdc42/Rac interactive binding region motif of the Wiskott Aldrich syndrome protein (WASP) is necessary but not sufficient for tight binding to Cdc42 and structure formation J. Biol. Chem. 273 1998 18067 18076 (Pubitemid 28334722)
14. Thompson G., Owen D., Chalk P.A., and Lowe P.N. Delineation of the Cdc42/Rac-binding domain of p21-activated kinase Biochemistry 37 1998 7885 7891 (Pubitemid 28248649)
15. Morreale A., Venkatesan M., Mott H.R., Owen D., Nietlispach D., Lowe P.N., and Laue E.D. Structure of Cdc42 bound to the GTPase binding domain of PAK Nat. Struct. Biol. 7 2000 384 388 (Pubitemid 30250001)
16. Kim A.S., Kakalis L.T., Abdul-Manan N., Liu G.A., and Rosen M.K. Autoinhibition and activation mechanisms of the Wiskott-Aldrich syndrome protein Nature 404 2000 151 158 (Pubitemid 30154475)
17. Mott H.R., Owen D., Nietlispach D., Lowe P.N., Manser E., Lim L., and Laue E.D. Structure of the small G protein Cdc42 bound to the GTPase-binding domain of ACK Nature 399 1999 384 388 (Pubitemid 29318139)
18. Zheng Z.L., and Yang Z. The Rop GTPase: an emerging signaling switch in plants Plant Mol. Biol. 44 2000 1 9
19. Berken A. ROPs in the spotlight of plant signal transduction Cell. Mol. Life Sci. 63 2006 2446 2459 (Pubitemid 44722377)
20. Berken A., and Wittinghofer A. Structure and function of Rho-type molecular switches in plants Plant Physiol. Biochem. 46 2008 380 393
21. Lee Y.J., and Yang Z. Tip growth: signaling in the apical dome Curr. Opin. Plant Biol. 11 2008 662 671
22. Mucha E., Fricke I., Schaefer A., Wittinghofer A., and Berken A. Rho proteins of plants-functional cycle and regulation of cytoskeletal dynamics Eur. J. Cell Biol. 2011 10.1016/j.ejcb.2010.11.009
23. Christensen T.M., Vejlupkova Z., Sharma Y.K., Arthur K.M., Spatafora J.W., and Albright C.A. Conserved subgroups and developmental regulation in the monocot rop gene family Plant Physiol. 133 2003 1791 1808 (Pubitemid 38047309)
24. Hwang J.U., Vernoud V., Szumlanski A., Nielsen E., and Yang Z. A tip-localized RhoGAP controls cell polarity by globally inhibiting Rho GTPase at the cell apex Curr. Biol. 18 2008 1907 1916 (Pubitemid 352841665)
25. Schaefer A., Hoehner K., Berken A., and Wittinghofer A. The unique plant RhoGAPs are dimeric and contain a CRIB motif required for affinity and specificity towards cognate small G proteins Biopolymers 95 2011 420 433
26. Wu G., Li H., and Yang Z. Arabidopsis RopGAPs are a novel family of rho GTPase-activating proteins that require the Cdc42/Rac-interactive binding motif for rop-specific GTPase stimulation Plant Physiol. 124 2000 1625 1636 (Pubitemid 32053497)
27. Klahre U., and Kost B. Tobacco RhoGTPase ACTIVATING PROTEIN1 spatially restricts signaling of RAC/Rop to the apex of pollen tubes Plant Cell 18 2006 3033 3046 (Pubitemid 46013274)
28. Borg S., Podenphant L., Jensen T.J., and Poulsen C. Plant cell growth and differentiation may involve GAP regulation of Rac activity FEBS Lett. 453 1999 341 345 (Pubitemid 29326675)
29. Abbal P., and Tesniere C. Putative Vitis vinifera Rop- and Rab-GAP-, GEF-, and GDI-interacting proteins uncovered with novel methods for public genomic and EST database analysis J. Exp. Bot. 61 2010 65 74
30. Baxter-Burrell A., Yang Z., Springer P.S., and Bailey-Serres J. RopGAP4-dependent Rop GTPase rheostat control of Arabidopsis oxygen deprivation tolerance Science 296 2002 2026 2028 (Pubitemid 34627525)
31. Fu Y., Wu G., and Yang Z. Rop GTPase-dependent dynamics of tip-localized F-actin controls tip growth in pollen tubes J. Cell Biol. 152 2001 1019 1032 (Pubitemid 34286077)
32. Brune M., Hunter J.L., Corrie J.E., and Webb M.R. Direct, real-time measurement of rapid inorganic phosphate release using a novel fluorescent probe and its application to actomyosin subfragment 1 ATPase Biochemistry 33 1994 8262 8271 (Pubitemid 24241060)
33. Brune M., Hunter J.L., Howell S.A., Martin S.R., Hazlett T.L., Corrie J.E., and Webb M.R. Mechanism of inorganic phosphate interaction with phosphate binding protein from Escherichia coli Biochemistry 37 1998 10370 10380 (Pubitemid 28357558)
34. Graham D.L., Eccleston J.F., and Lowe P.N. The conserved arginine in rho-GTPase-activating protein is essential for efficient catalysis but not for complex formation with Rho•GDP and aluminum fluoride Biochemistry 38 1999 985 991
35. Mazhab-Jafari M.T., Marshall C.B., Smith M., Gasmi-Seabrook G.M., Stambolic V., and Rottapel R. Real-time NMR study of three small GTPases reveals that fluorescent 2′(3′)-O-(N-methylanthraniloyl)-tagged nucleotides alter hydrolysis and exchange kinetics J. Biol. Chem. 285 2010 5132 5136
36. Ahmadian M.R., Stege P., Scheffzek K., and Wittinghofer A. Confirmation of the arginine-finger hypothesis for the GAP-stimulated GTP-hydrolysis reaction of Ras Nat. Struct. Biol. 4 1997 686 689
37. Eberth A., Dvorsky R., Becker C.F., Beste A., Goody R.S., and Ahmadian M.R. Monitoring the real-time kinetics of the hydrolysis reaction of guanine nucleotide-binding proteins Biol. Chem. 386 2005 1105 1114 (Pubitemid 41705365)
38. Hemsath L., Dvorsky R., Fiegen D., Carlier M.F., and Ahmadian M.R. An electrostatic steering mechanism of Cdc42 recognition by Wiskott-Aldrich syndrome proteins Mol. Cell 20 2005 313 324 (Pubitemid 41484175)
39. Kraemer A., Brinkmann T., Plettner I., Goody R., and Wittinghofer A. Fluorescently labelled guanine nucleotide binding proteins to analyse elementary steps of GAP-catalysed reactions J. Mol. Biol. 324 2002 763 774 (Pubitemid 36044111)
40. Kötting C., Blessenohl M., Suveyzdis Y., Goody R.S., Wittinghofer A., and Gerwert K. A phosphoryl transfer intermediate in the GTPase reaction of Ras in complex with its GTPase-activating protein Proc. Natl Acad. Sci. USA 103 2006 13911 13916 (Pubitemid 44452956)
41. Chakrabarti P.P., Daumke O., Suveyzdis Y., Kötting C., Gerwert K., and Wittinghofer A. Insight into catalysis of a unique GTPase reaction by a combined biochemical and FTIR approach J. Mol. Biol. 367 2007 983 995 (Pubitemid 46389620)
42. Phillips R.A., Hunter J.L., Eccleston J.F., and Webb M.R. The mechanism of Ras GTPase activation by neurofibromin Biochemistry 42 2003 3956 3965 (Pubitemid 36402689)
43. Lamson R.E., Winters M.J., and Pryciak P.M. Cdc42 regulation of kinase activity and signaling by the yeast p21-activated kinase Ste20 Mol. Cell. Biol. 22 2002 2939 2951 (Pubitemid 34437453)
44. Abdul-Manan N., Aghazadeh B., Liu G.A., Majumdar A., Ouerfelli O., Siminovitch K.A., and Rosen M.K. Structure of Cdc42 in complex with the GTPase-binding domain of the 'Wiskott-Aldrich syndrome' protein Nature 399 1999 379 383 (Pubitemid 29318138)
45. Scheffzek K., and Ahmadian M.R. GTPase activating proteins: structural and functional insights 18 years after discovery Cell. Mol. Life Sci. 62 2005 3014 3038 (Pubitemid 43004752)
46. Kötting C., Kallenbach A., Suveyzdis Y., Wittinghofer A., and Gerwert K. The GAP arginine finger movement into the catalytic site of Ras increases the activation entropy Proc. Natl Acad. Sci. USA 105 2008 6260 6265 (Pubitemid 351758334)
47. Rittinger K., Walker P.A., Eccleston J.F., Nurmahomed K., Owen D., and Laue E. Crystal structure of a small G protein in complex with the GTPase-activating protein rhoGAP Nature 388 1997 693 697 (Pubitemid 27366443)
48. Zutz A., Gompf S., Schagger H., and Tampe R. Mitochondrial ABC proteins in health and disease Biochim. Biophys. Acta 1787 2009 681 690
49. Procko E., Ferrin-O'Connell I., Ng S.L., and Gaudet R. Distinct structural and functional properties of the ATPase sites in an asymmetric ABC transporter Mol. Cell 24 2006 51 62 (Pubitemid 44466678)
50. Zaitseva J., Oswald C., Jumpertz T., Jenewein S., Wiedenmann A., Holland I.B., and Schmitt L. A structural analysis of asymmetry required for catalytic activity of an ABC-ATPase domain dimer EMBO J. 25 2006 3432 3443 (Pubitemid 44141799)