Structural basis for the molecular evolution of SRP-GTPase activation by protein

Nature Structural and Molecular Biology

Volumn 18, Issue 12, 2011, Pages 1376-1380

  Bange, Gert ^a   Kümmerer, Nico ^a   Grudnik, Przemyslaw ^a   Lindner, Robert ^a   Petzold, Georg ^a,b   Kressler, Dieter ^a,b,c   Hurt, Ed ^a   Wild, Klemens ^a   Sinning, Irmgard ^a  

^a UNIVERSITY OF HEIDELBERG   (Germany)

^b RESEARCH INSTITUTE OF MOLECULAR PATHOLOGY   (Austria)

^c UNIVERSITY OF FRIBOURG   (Switzerland)

Author keywords

[No Author keywords available]

Indexed keywords

GUANINE NUCLEOTIDE BINDING PROTEIN; GUANOSINE TRIPHOSPHATASE; GUANOSINE TRIPHOSPHATE; HETERODIMER; HOMODIMER; PROTEIN FFH; PROTEIN FLHF; PROTEIN FTSY; RNA; SIGNAL RECOGNITION PARTICLE; UNCLASSIFIED DRUG;

ARTICLE; BACILLUS SUBTILIS; COMPLEX FORMATION; CRYSTAL STRUCTURE; ENZYME ACTIVATION; ENZYME MECHANISM; ENZYME STRUCTURE; MOLECULAR EVOLUTION; NONHUMAN; PRIORITY JOURNAL; PROTEIN PROTEIN INTERACTION; PROTEIN TARGETING;

AMINO ACID SEQUENCE; BACILLUS SUBTILIS; BACTERIAL PROTEINS; CRYSTALLOGRAPHY, X-RAY; ENZYME ACTIVATION; EVOLUTION, MOLECULAR; MODELS, MOLECULAR; MOLECULAR SEQUENCE DATA; MONOMERIC GTP-BINDING PROTEINS; PROTEIN STRUCTURE, TERTIARY; SEQUENCE ALIGNMENT; SIGNAL TRANSDUCTION;

BACILLUS SUBTILIS;

EID: 82955232389     PISSN: 15459993     EISSN: 15459985     Source Type: Journal    
DOI: 10.1038/nsmb.2141     Document Type: Article

References (49)

1. Leipe, D.D., Wolf, Y.I., Koonin, E.V. & Aravind, L. Classification and evolution of P-loop GTPases and related ATPases. J. Mol. Biol. 317, 41-72 (2002). (Pubitemid 34722199)
2. Lutkenhaus, J. Assembly dynamics of the bacterial MinCDE system and spatial regulation of the Z ring. Annu. Rev. Biochem. 76, 539-562 (2007).
3. Montoya, G., Svensson, C., Luirink, J. & Sinning, I. Crystal structure of the NG domain from the signal-recognition particle receptor FtsY. Nature 385, 365-368 (1997). (Pubitemid 27053110)
4. Freymann, D.M., Keenan, R.J., Stroud, R.M. & Walter, P. Structure of the conserved GTPase domain of the signal recognition particle. Nature 385, 361-364 (1997). (Pubitemid 27053109)
5. Bange, G., Petzold, G., Wild, K., Parlitz, R.O. & Sinning, I. The crystal structure of the third signal-recognition particle GTPase FlhF reveals a homodimer with bound GTP. Proc. Natl. Acad. Sci. USA 104, 13621-13625 (2007). (Pubitemid 350003370)
6. Grudnik, P., Bange, G. & Sinning, I. Protein targeting by the signal recognition particle. Biol. Chem. 390, 775-782 (2009).
7. Cross, B.C., Sinning, I., Luirink, J. & High, S. Delivering proteins for export from the cytosol. Nat. Rev. Mol. Cell Biol. 10, 255-264 (2009).
8. Egea, P.F. et al. Substrate twinning activates the signal recognition particle and its receptor. Nature 427, 215-221 (2004). (Pubitemid 38112032)
9. Focia, P.J., Shepotinovskaya, I.V., Seidler, J.A. & Freymann, D.M. Heterodimeric GTPase core of the SRP targeting complex. Science 303, 373-377 (2004). (Pubitemid 38095777)
10. Zhang, X., Schaffitzel, C., Ban, N. & Shan, S.O. Multiple conformational switches in a GTPase complex control co-translational protein targeting. Proc. Natl. Acad. Sci. USA 106, 1754-1759 (2009).
11. Wild, K., Halic, M., Sinning, I. & Beckmann, R. SRP meets the ribosome. Nat. Struct. Mol. Biol. 11, 1049-1053 (2004). (Pubitemid 39453332)
12. Powers, T. & Walter, P. Reciprocal stimulation of GTP hydrolysis by two directly interacting GTPases. Science 269, 1422-1424 (1995).
13. Peluso, P., Shan, S.O., Nock, S., Herschlag, D. & Walter, P. Role of SRP RNA in the GTPase cycles of Ffh and FtsY. Biochemistry 40, 15224-15233 (2001). (Pubitemid 33151937)
14. Siu, F.Y., Spanggord, R.J. & Doudna, J.A. SRP RNA provides the physiologically essential GTPase activation function in cotranslational protein targeting. RNA 13, 240-250 (2007). (Pubitemid 46147899)
15. Bradshaw, N., Neher, S.B., Booth, D.S. & Walter, P. Signal sequences activate the catalytic switch of SRP RNA. Science 323, 127-130 (2009).
16. De Leeuw, E. et al. Anionic phospholipids are involved in membrane association of FtsY and stimulate its GTPase activity. EMBO J. 19, 531-541 (2000). (Pubitemid 30093726)
17. Stjepanovic, G. et al. Lipids trigger a conformational switch that regulates signal recognition particle (SRP)-mediated protein targeting. J. Biol. Chem. 286, 23489-23497 (2011).
18. Ataide, S.F. et al. The crystal structure of the signal recognition particle in complex with its receptor. Science 331, 881-886 (2011).
19. Kirkpatrick, C.L. & Viollier, P.H. Poles apart: prokaryotic polar organelles and their spatial regulation. Cold Spring Harb. Perspect. Biol. 3 (2011).
20. Murray, T.S. & Kazmierczak, B.I. FlhF is required for swimming and swarming in Pseudomonas aeruginosa. J. Bacteriol. 188, 6995-7004 (2006). (Pubitemid 44497912)
21. Carpenter, P.B., Hanlon, D.W. & Ordal, G.W. flhF, a Bacillus subtilis flagellar gene that encodes a putative GTP-binding protein. Mol. Microbiol. 6, 2705-2713 (1992).
22. Pandza, S. et al. The G-protein FlhF has a role in polar flagellar placement and general stress response induction in Pseudomonas putida. Mol. Microbiol. 36, 414-423 (2000). (Pubitemid 30229486)
23. Correa, N.E., Peng, F. & Klose, K.E. Roles of the regulatory proteins FlhF and FlhG in the Vibrio cholerae flagellar transcription hierarchy. J. Bacteriol. 187, 6324-6332 (2005). (Pubitemid 41318391)
24. Kusumoto, A. et al. Regulation of polar flagellar number by the flhF and flhG genes in Vibrio alginolyticus. J. Biochem. 139, 113-121 (2006). (Pubitemid 43258853)
25. Green, J.C. et al. Recruitment of the earliest component of the bacterial flagellum to the old cell division pole by a membrane-associated signal recognition particle family GTP-binding protein. J. Mol. Biol. 391, 679-690 (2009).
26. Nowalk, A.J., Gilmore, R.D. Jr. & Carroll, J.A. Serologic proteome analysis of Borrelia burgdorferi membrane-associated proteins. Infect. Immun. 74, 3864-3873 (2006). (Pubitemid 43993317)
27. Kusumoto, A. et al. Collaboration of FlhF and FlhG to regulate polar-flagella number and localization in Vibrio alginolyticus. Microbiology 154, 1390-1399 (2008).
28. Scheffzek, K. et al. The Ras-RasGAP complex: structural basis for GTPase activation and its loss in oncogenic Ras mutants. Science 277, 333-338 (1997). (Pubitemid 27450699)
29. Wittinghofer, A. Signaling mechanistics: aluminum fluoride for molecule of the year. Curr. Biol. 7, R682-R685 (1997). (Pubitemid 27493106)
30. Gasper, R., Meyer, S., Gotthardt, K., Sirajuddin, M. & Wittinghofer, A. It takes two to tango: regulation of G proteins by dimerization. Nat. Rev. Mol. Cell Biol. 10, 423-429 (2009).
31. Focia, P.J., Gawronski-Salerno, J., Coon, J.S.T. & Freymann, D.M. Structure of a GDP:AlF4 complex of the SRP GTPases Ffh and FtsY, and identification of a peripheral nucleotide interaction site. J. Mol. Biol. 360, 631-643 (2006). (Pubitemid 43975112)
32. Fersht, A. Enzyme Structure and Mechanism (W.H. Freeman, San Francisco, 1977).
33. Bourne, H.R., Sanders, D.A. & McCormick, F. The GTPase superfamily: a conserved switch for diverse cell functions. Nature 348, 125-132 (1990).
34. Vetter, I.R. & Wittinghofer, A. The guanine nucleotide-binding switch in three dimensions. Science 294, 1299-1304 (2001). (Pubitemid 33063089)
35. Daumke, O., Weyand, M., Chakrabarti, P.P., Vetter, I.R. & Wittinghofer, A. The GTPase-activating protein Rap1GAP uses a catalytic asparagine. Nature 429, 197-201 (2004). (Pubitemid 38656197)
36. Kimple, A.J., Bosch, D.E., Giguere, P.M. & Siderovski, D.P. Regulators of G-protein signaling and their Gα substrates: promises and challenges in their use as drug discovery targets. Pharmacol. Rev. 63, 728-749 (2011).
37. Liu, R. & Ochman, H. Origins of flagellar gene operons and secondary flagellar systems. J. Bacteriol. 189, 7098-7104 (2007). (Pubitemid 47525455)
38. del Campo, A.M. et al. Chemotactic control of the two flagellar systems of Rhodobacter sphaeroides is mediated by different sets of CheY and FliM proteins. J. Bacteriol. 189, 8397-8401 (2007). (Pubitemid 350178957)
39. Bohnsack, M.T. & Schleiff, E. The evolution of protein targeting and translocation systems. Biochim. Biophys. Acta 1803, 1115-1130 (2010).
40. Walter, P., Keenan, R. & Schmitz, U. Perspectives: structural biology. SRP-where the RNA and membrane worlds meet. Science 287, 1212-1213 (2000). (Pubitemid 30112132)
41. James, P., Halladay, J. & Craig, E.A. Genomic libraries and a host strain designed for highly efficient two-hybrid selection in yeast. Genetics 144, 1425-1436 (1996).
42. Collaborative Computational Project. N. The CCP4 suite: programs for protein crystallography. Acta Crystallogr. D Biol. Crystallogr. 50, 760-763 (1994).
43. Emsley, P. & Cowtan, K. Coot: model-building tools for molecular graphics. Acta Crystallogr. D Biol. Crystallogr. 60, 2126-2132 (2004). (Pubitemid 41742764)
44. Adams, P.D. et al. PHENIX: a comprehensive Python-based system for macromolecular structure solution. Acta Crystallogr. D Biol. Crystallogr. 66, 213-221 (2010).
45. Kanehisa, M., Goto, S., Furumichi, M., Tanabe, M. & Hirakawa, M. KEGG for representation and analysis of molecular networks involving diseases and drugs. Nucleic Acids Res. 38, D355-D360 (2010).
46. Bailey, T.L., Boden, M., Whitington, T. & Machanick, P. The value of position-specific priors in motif discovery using MEME. BMC Bioinformatics 11, 179 (2010).
47. Bailey, T.L. & Gribskov, M. Combining evidence using p-values: application to sequence homology searches. Bioinformatics 14, 48-54 (1998). (Pubitemid 28395676)
48. Larkin, M.A. et al. Clustal W and Clustal X version 2.0. Bioinformatics 23, 2947-2948 (2007). (Pubitemid 350162903)
49. Paradis, E., Claude, J. & Strimmer, K. APE: Analyses of phylogenetics and evolution in R language. Bioinformatics 20, 289-290 (2004). (Pubitemid 38195693)