Structural analysis of the Ras-like G protein MglA and its cognate GAP MglB and implications for bacterial polarity

EMBO Journal

Volumn 30, Issue 20, 2011, Pages 4185-4197

  Miertzschke, Mandy ^a   Koerner, Carolin ^a   Vetter, Ingrid R ^a   Keilberg, Daniela ^b   Hot, Edina ^b   Leonardy, Simone ^b,c   Søgaard Andersen, Lotte ^b   Wittinghofer, Alfred ^a  

^a MAX PLANCK INSTITUTE OF MOLECULAR PHYSIOLOGY   (Germany)

^b MAX PLANCK INSTITUTE FOR TERRESTRIAL MICROBIOLOGY   (Germany)

^c Ingenieurbüro Gunter Reimann ^*  (Germany)

Author keywords

bacterial Ras like G protein; cell polarity; GTPase activating protein; intrinsic arginine finger; Roadblock LC7 domain

Indexed keywords

ARGININE; BACTERIAL PROTEIN; GLUTAMINE; GUANINE NUCLEOTIDE BINDING PROTEIN; GUANOSINE DIPHOSPHATE; GUANOSINE TRIPHOSPHATASE ACTIVATING PROTEIN; PROTEIN MG1A; PROTEIN MG1B; UNCLASSIFIED DRUG;

AMINO ACID SEQUENCE; ARTICLE; BETA SHEET; BIOCHEMISTRY; CATALYSIS; CELL POLARITY; COMPLEX FORMATION; CONFORMATIONAL TRANSITION; ENZYME ACTIVE SITE; GAMMAPROTEOBACTERIA; HYDROLYSIS; IN VIVO STUDY; MYXOCOCCUS XANTHUS; NONHUMAN; PRIORITY JOURNAL; PROTEIN EXPRESSION; PROTEIN FUNCTION; PROTEIN LOCALIZATION; PROTEIN STRUCTURE;

AMINO ACID SEQUENCE; ARGININE; BACTERIAL PROTEINS; CATALYSIS; CATALYTIC DOMAIN; CELL POLARITY; GLUTAMINE; GUANOSINE TRIPHOSPHATE; HYDROLYSIS; MOLECULAR SEQUENCE DATA; MYXOCOCCUS XANTHUS; PROTEIN CONFORMATION; RAS PROTEINS;

BACTERIA (MICROORGANISMS); MYXOCOCCUS XANTHUS;

EID: 80054934194     PISSN: 02614189     EISSN: 14602075     Source Type: Journal    
DOI: 10.1038/emboj.2011.291     Document Type: Article

References (64)

1. Ahnn J, March PE, Takiff HE, Inouye M (1986) A GTP-binding protein of Escherichia coli has homology to yeast RAS proteins. PNAS 83: 8849-8853 (Pubitemid 17223498)
2. Alto NM (2008) Mimicking small G-proteins: an emerging theme from the bacterial virulence arsenal. Cell Microbiol 10 : 566-575 (Pubitemid 351194086)
3. Bergfors T (2003) Seeds to crystals. J Struct Biol 142: 66-76 (Pubitemid 36457891)
4. Blackhart BD, Zusman DR (1985) 'Frizzy' genes of Myxococcus xanthus are involved in control of frequency of reversal of gliding motility. PNAS 82: 8767-8770 (Pubitemid 16101125)
5. Bos JL, Rehmann H, Wittinghofer A (2007) GEFs and GAPs: critical elements in the control of small G proteins. Cell 129: 865-877 (Pubitemid 46802708)
6. Brown ED (2005) Conserved P-loop GTPases of unknown function in bacteria: an emerging and vital ensemble in bacterial physiology 1. Cell 746: 738-746 (Pubitemid 43200412)
7. Bulyha I, Schmidt C, Lenz P, Jakovljevic V, Höne A, Maier B, Hoppert M, Søgaard-Andersen L (2009) Regulation of the type IV pili molecular machine by dynamic localization of two motor proteins. Mol Microbiol 74: 691-706
8. Clausen M, Jakovljevic V, Søgaard-Andersen L, Maier B (2009) High-force generation is a conserved property of type IV pilus systems. J Bacteriol 191: 4633-4638
9. Cox AD, Der CJ (2010) Ras history. Small GTPases 1: 2-27
10. Daumke O, Weyand M, Chakrabarti PP, Vetter IR, Wittinghofer A (2004) The GTPase-activating protein Rap1GAP uses a catalytic asparagine. Nature 429: 197-201 (Pubitemid 38656197)
11. Dubouloz F, Deloche O, Wanke V, Cameroni E, De Virgilio C (2005) The TOR and EGO protein complexes orchestrate microautophagy in yeast. Mol Cell 19: 15-26 (Pubitemid 40884654)
12. Emsley P, Cowtan K (2004) Coot: model-building tools for molecular graphics. Acta Crystallogr D Biol Crystallogr 60: 2126-2132 (Pubitemid 41742764)
13. Gao M, Kaiser CA (2006) A conserved GTPase-containing complex is required for intracellular sorting of the general amino-acid permease in yeast. Nat Cell Biol 8: 657-667
14. Gasper R, Meyer S, Gotthardt K, Sirajuddin M, Wittinghofer A (2009) It takes two to tango: regulation of G proteins by dimer-ization. Nat Rev Mol Cell Biol 10: 423-429
15. Gremer L, Gilsbach B, Ahmadian MR, Wittinghofer A (2008) Fluoride complexes of oncogenic Ras mutants to study the Ras-RasGap interaction. Biol Chem 389: 1163-1171
16. Herrmann C (2003) Ras-effector interactions: after one decade. Curr Opin Struct Biol 13: 122-129 (Pubitemid 36170264)
17. Hillig RC, Hanzal-Bayer M, Linari M, Becker J, Wittinghofer A, Renault L (2000) Structural and biochemical properties show ARL3-GDP as a distinct GTP binding protein. Structure 8: 1239-1245 (Pubitemid 32149750)
18. Hwang J, Inouye M (2010) A bacterial GAP-like protein, YihI, regulating the GTPase of Der, an essential GTP-binding protein in Escherichia coli. J Mol Biol 399: 759-772
19. Ilangovan U, Ding W, Zhong Y, Wilson CL, Groppe JC, Trbovich JT, Zúñiga J, Demeler B, Tang Q, Gao G, Mulder KM, Hinck AP (2005) Structure and dynamics of the homodimeric dynein light chain km23. J Mol Biol 352: 338-354 (Pubitemid 41207786)
20. Inoki K, Li Y, Xu T, Guan K-L (2003) Rheb GTPase is a direct target of TSC2 GAP activity and regulates mTOR signaling. Genes Dev 17: 1829-1834 (Pubitemid 36944560)
21. Jelsbak L, Søgaard-Andersen L (2002) Pattern formation by a cell surface-associated morphogen in Myxococcus xanthus. PNAS 99: 2032-2037
22. Kabsch W (1993) Automatic processing of rotation diffraction data from crystals of initially unknown symmetry and cell constants. J Appl Chrystallogr 26: 795-800
23. Kardon JR, Vale RD (2009) Regulators of the cytoplasmic dynein motor. Nat Rev Mol Cell Biol 10 : 854-865
24. Kogan K, Spear ED, Kaiser CA, Fass D (2010) Structural conservation of components in the amino acid sensing branch of the TOR pathway in yeast and mammals. J Mol Biol 402: 388-398
25. Koonin EV, Aravind L (2000) Dynein light chains of the Roadblock/LC7 group belong to an ancient protein superfamily implicated in NTPase regulation. Curr Biol 10 : R774-R776
26. Kurzbauer R, Teis D, Araujo MEGD, Maurer-stroh S, Eisenhaber F, Bourenkov GP, Bartunik HD, Hekman M, Rapp UR, Huber LA, Clausen T (2004) Crystal structure of the p14-MP1 scaffolding complex: how a twin couple attaches mitogen-activated protein kinase signaling to late endosomes. PNAS 101: 10984-10989 (Pubitemid 38989571)
27. Leonardy S, Bulyha I, Søgaard-Andersen L (2008) Reversing cells and oscillating motility proteins. Mol Biosyst 4: 1009-1014
28. Leonardy S, Freymark G, Hebener S, Ellehauge E, Søgaard-Andersen L (2007) Coupling of protein localization and cell movements by a dynamically localized response regulator in Myxococcus xanthus. EMBO J 26: 4433-4444 (Pubitemid 350036633)
29. Leonardy S, Miertzschke M, Bulyha I, Sperling E, Wittinghofer A, Søgaard-Andersen L (2010) Regulation of dynamic polarity switching in bacteria by a Ras-like G-protein and its cognate GAP. EMBO J 29: 2276-2289
30. Lunin VV, Munger C, Wagner J, Ye Z, Cygler M, Sacher M (2004) The structure of the MAPK scaffold, MP1, bound to its partner, p14. A complex with a critical role in endosomal map kinase signaling. J Biol Chem 279: 23422-23430 (Pubitemid 38685652)
31. Mehr IJ, Long CD, Serkin CD, Seifert HS (2000) A homologue of the recombination-dependent growth gene, rdgC, is involved in gonococcal pilin antigenic variation. Genetics 154: 523-532 (Pubitemid 30096577)
32. Merz AJ, So M, Sheetz MP (2000) Pilus retraction powers bacterial twitching motility. Nature 407: 98-102
33. Mignot T, Merlie JP, Zusman DR (2005) Regulated pole-to-pole oscillations of a bacterial gliding motility protein. Science 310: 855-857 (Pubitemid 41567344)
34. Mignot T, Shaevitz JW, Hartzell PL, Zusman DR (2007) Evidence that focal adhesion complexes power bacterial gliding motility. Science 315: 853-856
35. Mittal R, Ahmadian MR, Goody RS, Wittinghofer A (1996) Formation of a transition-state analog of the Ras GTPase reaction by Ras-GDP, tetrafluoroaluminate, and GTPase-activating proteins. Science 273: 115-117 (Pubitemid 26255439)
36. Murshudov GN, Vagin AA, Dodson EJ (1997) Refinement of macromolecular structures by the maximum-likelihood method. Acta Crystallogr D Biol Crystallogr 53: 240-255 (Pubitemid 27235885)
37. Pasqualato S, Renault L, Cherfils J (2002) Arf, Arl, Arp and Sar proteins: a family of GTP-binding proteins with a structural device for 'front-back' communication. EMBO Rep 3: 1035-1041 (Pubitemid 35469894)
38. Patryn J, Allen K, Dziewanowska K, Otto R, Hartzell PL (2010) Localization of MglA, an essential gliding motility protein in Myxococcus xanthus. Cytoskeleton 67: 322-337
39. Rensland H, John J, Linke R, Simon I, Schlichting I, Wittinghofer A, Goody RS (1995) Substrate and product structural requirements for binding of nucleotides to H-ras p21: the mechanism of discrimination between guanosine and adenosine nucleotides. Biochemistry 34: 593-599
40. Sancak Y, Bar-Peled L, Zoncu R, Markhard AL, Nada S, Sabatini DM (2010) Ragulator-Rag complex targets mTORC1 to the lysosomal surface and is necessary for its activation by amino acids. Cell 141: 290-303
41. Schaefer A, Höhner K, Berken A, Wittinghofer A (2011) The unique plant RhoGAPs are dimeric and contain a CRIB motif required for affinity and specificity towards cognate small G proteins. Biopolymers 95: 420-433
42. Scheffzek K, Ahmadian MR (2005) GTPase activating proteins: structural and functional insights 18 years after discovery. Cell Mol Life Sci 62: 3014-3038 (Pubitemid 43004752)
43. Scheffzek K, Ahmadian MR, Kabsch W, Wiesmüller L, Lautwein A, Schmitz F, Wittinghofer A (1997a) The Ras-RasGAP complex: structural basis for GTPase activation and its loss in oncogenic Ras mutants. Science 277: 333-338 (Pubitemid 27450699)
44. Scheffzek K, Lautwein A, Scherer A, Franken S, Wittinghofer A (1997b) Crystallization and preliminary X-ray crystallographic study of the Ras-GTPase-activating domain of human p120GAP. Proteins 27: 315-318 (Pubitemid 27113726)
45. Scrima A, Thomas C, Deaconescu D, Wittinghofer A (2008) The Rap-RapGAP complex: GTP hydrolysis without catalytic glutamine and arginine residues. EMBO J 27: 1145-1153 (Pubitemid 351508140)
46. Shapiro L, McAdams HH, Losick R (2009) Why and how bacteria localize proteins. Science 326: 1225-1228
47. Skerker JM, Berg HC (2001) Direct observation of extension and retraction of type IV pili. PNAS 98: 6901-6904 (Pubitemid 32538314)
48. Song J, Tyler RC, Lee MS, Tyler EM, Markley JL (2005) Solution structure of isoform 1 of Roadblock/LC7, a light chain in the dynein complex. J Mol Biol 354: 1043-1051 (Pubitemid 41698914)
49. Spoerner M, Herrmann C, Vetter IR, Kalbitzer HR, Wittinghofer A (2001) Dynamic properties of the Ras switch I region and its importance for binding to effectors. PNAS 98: 4944-4949 (Pubitemid 32397062)
50. Sprang SR (1997) G protein mechanisms: insights from structural analysis. Annu Rev Biochem 66: 639-678 (Pubitemid 27274670)
51. Sprang SR, Chen Z, Du X (2007) Mechanisms and pathways of heterotrimeric G protein signaling. Adv Protein Chem 74: 1-65
52. Srinivasa SP, Watson N, Overton MC, Blumer KJ (1998) Mechanism of RGS4, a GTPase-activating protein for G protein alpha sub-units. J Biol Chem 273: 1529-1533 (Pubitemid 28133676)
53. Sun H, Zusman DR, Shi W (2000) Type IV pilus of Myxococcus xanthus is a motility apparatus controlled by the frz chemosen-sory system. Curr Biol 10: 1143-1146
54. Tee AR, Manning BD, Roux PP, Cantley LC, Blenis J (2003) Tuberous sclerosis complex gene products, Tuberin and Hamartin, control mTOR signaling by acting as a GTPase-activating protein complex toward Rheb. Curr Biol 13: 1259-1268 (Pubitemid 36953298)
55. Terwilliger TC (2002) Automated structure solution, density modification and model building. Acta Crystallogr D Biol Crystallogr 58: 1937-1940 (Pubitemid 35337291)
56. Tesmer JJ, Berman DM, Gilman AG, Sprang SR (1997) Structure of RGS4 bound to AlF4-activated G(i alpha1): stabilization of the transition state for GTP hydrolysis. Cell 89: 251-261 (Pubitemid 27199897)
57. Veltel S, Gasper R, Eisenacher E, Wittinghofer A (2008a) The retinitis pigmentosa 2 gene product is a GTPase-activating protein for Arf-like 3. Nat Struct Mol Biol 15: 373-380 (Pubitemid 351483389)
58. Veltel S, Kravchenko A, Ismail S, Wittinghofer A (2008b) Specificity of Arl2/Arl3 signaling is mediated by a ternary Arl3-effector-GAP complex. FEBS Lett 582: 2501-2507
59. Vetter IR, Nowak C, Nishimoto T, Kuhlmann J, Wittinghofer A (1999) Structure of a Ran-binding domain complexed with Ran bound to a GTP analogue: implications for nuclear transport. Nature 398: 39-46
60. Vetter IR, Wittinghofer A (2001) The guanine nucleotide-binding switch in three dimensions. Science 294: 1299-1304 (Pubitemid 33063089)
61. Wittinghofer A, Nassar N (1996) How Ras-related proteins talk to their effectors. Trends Biochem Sci 21: 488-491 (Pubitemid 27018818)
62. Wittinghofer A, Vetter IR (2010) Structure-function relationships of the G domain, a canonical switch motif. Annu Rev Biochem 80: 943-971
63. Zhang Y, Franco M, Ducret A, Mignot T (2010) A bacterial Ras-like small GTP-binding protein and its cognate GAP establish a dynamic spatial polarity axis to control directed motility. PLoS Biol 8: e1000430
64. Zurita-Martinez SA, Puria R, Pan X, Boeke JD, Cardenas ME (2007) Efficient Tor signaling requires a functional class C Vps protein complex in Saccharomyces cerevisiae. Genetics 176: 2139-2150 (Pubitemid 47360648)