A Novel Membrane Sensor Controls the Localization and ArfGEF Activity of Bacterial RalF

PLoS Pathogens

Volumn 9, Issue 11, 2013, Pages

  Folly Klan, Marcia ^a   Alix, Eric ^b   Stalder, Danièle ^c   Ray, Pampa ^a   Duarte, Lionel V ^a   Delprato, Anna ^a   Zeghouf, Mahel ^a   Antonny, Bruno ^c   Campanacci, Valérie ^a   Roy, Craig R ^b   Cherfils, Jacqueline ^a  

^a LABORATOIRE D ENZYMOLOGIE ET BIOCHIMIE STRUCTURALES   (France)

^b YALE UNIVERSITY SCHOOL OF MEDICINE   (United States)

^c INSTITUT DE PHARMACOLOGIE MOLÉCULAIRE ET CELLULAIRE   (France)

Author keywords

[No Author keywords available]

Indexed keywords

AMINO ACID; ARF PROTEIN; BACTERIAL PROTEIN; GUANINE NUCLEOTIDE EXCHANGE FACTOR; PROTEIN RALF; UNCLASSIFIED DRUG;

ARTICLE; BINDING SITE; CELL VACUOLE; CELLULAR DISTRIBUTION; CONTROLLED STUDY; ENZYME ACTIVITY; FEEDBACK SYSTEM; HUMAN; HUMAN CELL; IMMUNOGOLD ELECTRON MICROSCOPY; INTRACELLULAR MEMBRANE; LEGIONELLA PNEUMOPHILA; NONHUMAN; PROTEIN CONFORMATION; PROTEIN DOMAIN; PROTEIN STRUCTURE; TYPE IV SECRETION SYSTEM;

BACTERIAL PROTEINS; BINDING SITES; GUANINE NUCLEOTIDE EXCHANGE FACTORS; HEK293 CELLS; HUMANS; LEGIONELLA PNEUMOPHILA; LEGIONNAIRES' DISEASE; PROTEIN STRUCTURE, TERTIARY; RICKETTSIA PROWAZEKII; VACUOLES;

EID: 84888249699     PISSN: 15537366     EISSN: 15537374     Source Type: Journal    
DOI: 10.1371/journal.ppat.1003747     Document Type: Article

References (39)

1. Aktories K, (2011) Bacterial protein toxins that modify host regulatory GTPases. Nat Rev Microbiol 9: 487-498.
2. Hubber A, Roy CR, (2010) Modulation of host cell function by Legionella pneumophila type IV effectors. Annu Rev Cell Dev Biol 26: 261-283.
3. Isberg RR, O'Connor TJ, Heidtman M, (2009) The Legionella pneumophila replication vacuole: making a cosy niche inside host cells. Nat Rev Microbiol 7: 13-24.
4. Nagai H, Kagan JC, Zhu X, Kahn RA, Roy CR, (2002) A bacterial guanine nucleotide exchange factor activates ARF on Legionella phagosomes. Science 295: 679-682.
5. Nagai H, Cambronne ED, Kagan JC, Amor JC, Kahn RA, et al. (2005) A C-terminal translocation signal required for Dot/Icm-dependent delivery of the Legionella RalF protein to host cells. Proc Natl Acad Sci U S A 102: 826-831.
6. Tilney LG, Harb OS, Connelly PS, Robinson CG, Roy CR, (2001) How the parasitic bacterium Legionella pneumophila modifies its phagosome and transforms it into rough ER: implications for conversion of plasma membrane to the ER membrane. J Cell Sci 114: 4637-4650.
7. Kagan JC, Roy CR, (2002) Legionella phagosomes intercept vesicular traffic from endoplasmic reticulum exit sites. Nat Cell Biol 4: 945-954.
8. Hardiman CA, McDonough JA, Newton HJ, Roy CR, (2012) The role of Rab GTPases in the transport of vacuoles containing Legionella pneumophila and Coxiella burnetii. Biochem Soc Trans 40: 1353-1359.
9. D'Souza-Schorey C, Chavrier P, (2006) ARF proteins: roles in membrane traffic and beyond. Nat Rev Mol Cell Biol 7: 347-358.
10. Hutagalung AH, Novick PJ, (2011) Role of Rab GTPases in membrane traffic and cell physiology. Physiol Rev 91: 119-149.
11. Casanova JE, (2007) Regulation of Arf activation: the Sec7 family of guanine nucleotide exchange factors. Traffic 8: 1476-1485.
12. Balraj P, Renesto P, Raoult D, (2009) Advances in rickettsia pathogenicity. Ann N Y Acad Sci 1166: 94-105.
13. Amor JC, Swails J, Zhu X, Roy CR, Nagai H, et al. (2005) The structure of RalF, an ADP-ribosylation factor guanine nucleotide exchange factor from Legionella pneumophila, reveals the presence of a cap over the active site. J Biol Chem 280: 1392-1400.
14. Alix E, Chesnel L, Bowzard BJ, Tucker AM, Delprato A, et al. (2012) The Capping Domain in RalF Regulates Effector Functions. PLoS Pathog 8: e1003012.
15. Cherfils J, Zeghouf M, (2013) Regulation of Small GTPases by GEFs, GAPs, and GDIs. Physiol Rev 93: 269-309.
16. Pasqualato S, Renault L, Cherfils J (2004) The GDP/GTP cycle of Arf proteins. Structural and biochemical aspects. In: Richard A Kahn, editor. The ARF Book. Kluwer Academic Publishers. pp. 23-48.
17. Zeeh JC, Zeghouf M, Grauffel C, Guibert B, Martin E, et al. (2006) Dual specificity of the interfacial inhibitor brefeldin a for arf proteins and sec7 domains. J Biol Chem 281: 11805-11814.
18. Margarit SM, Sondermann H, Hall BE, Nagar B, Hoelz A, et al. (2003) Structural evidence for feedback activation by Ras.GTP of the Ras-specific nucleotide exchange factor SOS. Cell 112: 685-695.
19. Stalder D, Barelli H, Gautier R, Macia E, Jackson CL, et al. (2011) Kinetic studies of the Arf activator Arno on model membranes in the presence of Arf effectors suggest control by a positive feedback loop. J Biol Chem 286: 3873-3883.
20. Richardson BC, McDonold CM, Fromme JC, (2012) The Sec7 Arf-GEF is recruited to the trans-Golgi network by positive feedback. Dev Cell 22: 799-810.
21. Lomize AL, Pogozheva ID, Lomize MA, Mosberg HI, (2007) The role of hydrophobic interactions in positioning of peripheral proteins in membranes. BMC Struct Biol 7: 44.
22. Goldberg J, (1998) Structural basis for activation of ARF GTPase: mechanisms of guanine nucleotide exchange and GTP-myristoyl switching. Cell 95: 237-248.
23. Renault L, Guibert B, Cherfils J, (2003) Structural snapshots of the mechanism and inhibition of a guanine nucleotide exchange factor. Nature 426: 525-530.
24. DiNitto JP, Delprato A, Gabe Lee MT, Cronin TC, Huang S, et al. (2007) Structural basis and mechanism of autoregulation in 3-phosphoinositide-dependent Grp1 family Arf GTPase exchange factors. Mol Cell 28: 569-583.
25. Lemmon MA, (2008) Membrane recognition by phospholipid-binding domains. Nat Rev Mol Cell Biol 9: 99-111.
26. Antonny B, (2011) Mechanisms of membrane curvature sensing. Annu Rev Biochem 80: 101-123.
27. Aizel K, Biou V, Navaza J, Duarte LV, Campanacci V, et al. (2013) Integrated Conformational and Lipid-Sensing Regulation of Endosomal ArfGEF BRAG2. PLoS Biol 11: e1001652.
28. Berger KH, Isberg RR, (1993) Two distinct defects in intracellular growth complemented by a single genetic locus in Legionella pneumophila. Mol Microbiol 7: 7-19.
29. Feeley JC, Gibson RJ, Gorman GW, Langford NC, Rasheed JK, et al. (1979) Charcoal-yeast extract agar: primary isolation medium for Legionella pneumophila. J Clin Microbiol 10: 437-441.
30. Franco M, Chardin P, Chabre M, Paris S, (1995) Myristoylation of ADP-ribosylation factor 1 facilitates nucleotide exchange at physiological Mg2+ levels. J Biol Chem 270: 1337-1341.
31. Béraud-Dufour S, Robineau S, Chardin P, Paris S, Chabre M, et al. (1998) A glutamic finger in the guanine nucleotide exchange factor ARNO displaces Mg2+ and the beta-phosphate to destabilize GDP on ARF1. Embo J 17: 3651-3659.
32. Antonny B, Beraud-Dufour S, Chardin P, Chabre M, (1997) N-terminal hydrophobic residues of the G-protein ADP-ribosylation factor-1 insert into membrane phospholipids upon GDP to GTP exchange. Biochemistry 36: 4675-4684.
33. Kabsch W, (2010) Xds. Acta Crystallogr D Biol Crystallogr 66: 125-132.
34. McCoy AJ, Grosse-Kunstleve RW, Adams PD, Winn MD, Storoni LC, et al. (2007) Phaser crystallographic software. J Appl Crystallogr 40: 658-674.
35. Blanc E, Roversi P, Vonrhein C, Flensburg C, Lea SM, et al. (2004) Refinement of severely incomplete structures with maximum likelihood in BUSTER-TNT. Acta Crystallogr D Biol Crystallogr 60: 2210-2221.
36. Emsley P, Cowtan K, (2004) Coot: model-building tools for molecular graphics. Acta Crystallogr D Biol Crystallogr 60: 2126-2132.
37. Biou V, Aizel K, Roblin P, Thureau A, Jacquet E, et al. (2010) SAXS and X-ray crystallography suggest an unfolding model for the GDP/GTP conformational switch of the small GTPase Arf6. J Mol Biol 402: 696-707.
38. Lomize MA, Pogozheva ID, Joo H, Mosberg HI, Lomize AL, (2012) OPM database and PPM web server: resources for positioning of proteins in membranes. Nucleic Acids Res 40: D370-376.
39. Arasaki K, Roy CR, (2010) Legionella pneumophila promotes functional interactions between plasma membrane syntaxins and Sec22b. Traffic 11: 587-600.