Structural Basis for Rab1 De-AMPylation by the Legionella pneumophila Effector SidD

PLoS Pathogens

Volumn 9, Issue 5, 2013, Pages

  Chen, Yang ^a,f   Tascón, Igor ^b   Neunuebel, M Ramona ^a   Pallara, Chiara ^c   Brady, Jacqueline ^a   Kinch, Lisa N ^d   Fernández Recio, Juan ^c   Rojas, Adriana L ^b   Machner, Matthias P ^a   Hierro, Aitor ^b,e  

^a EUNICE KENNEDY SHRIVER NATIONAL INSTITUTE OF CHILD HEALTH AND HUMAN DEVELOPMENT   (United States)

^b CIC BIOGUNE   (Spain)

^c BARCELONA SUPERCOMPUTING CENTER   (Spain)

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

^e BASQUE FOUNDATION FOR SCIENCE   (Spain)

^f PEKING UNIVERSITY HEALTH SCIENCE CENTER   (China)

Author keywords

[No Author keywords available]

Indexed keywords

ADENOSINE PHOSPHATE; DOCKING PROTEIN; RAB PROTEIN;

ANIMAL CELL; ARTICLE; CELL STRAIN COS1; CONTROLLED STUDY; CRYSTALLIZATION; CYTOTOXICITY; ENZYME ACTIVE SITE; IMMUNOFLUORESCENCE MICROSCOPY; LEGIONELLA PNEUMOPHILA; MOLECULAR DYNAMICS; NONHUMAN; POLYACRYLAMIDE GEL ELECTROPHORESIS; PROTEIN DOMAIN; PROTEIN HYDROLYSIS; PROTEIN STRUCTURE; RADIOACTIVITY;

ADENOSINE MONOPHOSPHATE; BACTERIAL PROTEINS; CRYSTALLOGRAPHY, X-RAY; HUMANS; LEGIONELLA PNEUMOPHILA; MOLECULAR DOCKING SIMULATION; PHOSPHOPROTEIN PHOSPHATASES; PROTEIN STRUCTURE, QUATERNARY; RAB1 GTP-BINDING PROTEINS; STRUCTURE-ACTIVITY RELATIONSHIP;

LEGIONELLA PNEUMOPHILA; MAMMALIA;

EID: 84878488505     PISSN: 15537366     EISSN: 15537374     Source Type: Journal    
DOI: 10.1371/journal.ppat.1003382     Document Type: Article

References (48)

1. Mantel M, Holzer H, (1970) Reversibility of the ATP:glutamine synthetase adenylyltransferase reaction. Proc Natl Acad Sci U S A 65: 660-667.
2. Yarbrough ML, Li Y, Kinch LN, Grishin NV, Ball HL, et al. (2009) AMPylation of Rho GTPases by Vibrio VopS disrupts effector binding and downstream signaling. Science 323: 269-272.
3. Worby CA, Mattoo S, Kruger RP, Corbeil LB, Koller A, et al. (2009) The fic domain: regulation of cell signaling by adenylylation. Mol Cell 34: 93-103.
4. Muller MP, Peters H, Blumer J, Blankenfeldt W, Goody RS, et al. (2010) The Legionella effector protein DrrA AMPylates the membrane traffic regulator Rab1b. Science 329: 946-949.
5. Hutagalung AH, Novick PJ, (2011) Role of Rab GTPases in membrane traffic and cell physiology. Physiol Rev 91: 119-149.
6. Stenmark H, (2009) Rab GTPases as coordinators of vesicle traffic. Nat Rev Mol Cell Biol 10: 513-525.
7. Andres DA, Seabra MC, Brown MS, Armstrong SA, Smeland TE, et al. (1993) cDNA cloning of component A of Rab geranylgeranyl transferase and demonstration of its role as a Rab escort protein. Cell 73: 1091-1099.
8. Desnoyers L, Anant JS, Seabra MC, (1996) Geranylgeranylation of Rab proteins. Biochem Soc Trans 24: 699-703.
9. Collins RN, (2003) "Getting it on"-GDI displacement and small GTPase membrane recruitment. Mol Cell 12: 1064-1066.
10. Machner MP, Isberg RR, (2006) Targeting of host Rab GTPase function by the intravacuolar pathogen Legionella pneumophila. Dev Cell 11: 47-56.
11. Kagan JC, Stein MP, Pypaert M, Roy CR, (2004) Legionella subvert the functions of Rab1 and Sec22b to create a replicative organelle. J Exp Med 199: 1201-1211.
12. Derre I, Isberg RR, (2004) Legionella pneumophila replication vacuole formation involves rapid recruitment of proteins of the early secretory system. Infect Immun 72: 3048-3053.
13. Murata T, Delprato A, Ingmundson A, Toomre DK, Lambright DG, et al. (2006) The Legionella pneumophila effector protein DrrA is a Rab1 guanine nucleotide-exchange factor. Nat Cell Biol 8: 971-977.
14. Ensminger AW, Isberg RR, (2009) Legionella pneumophila Dot/Icm translocated substrates: a sum of parts. Curr Opin Microbiol 12: 67-73.
15. Brombacher E, Urwyler S, Ragaz C, Weber SS, Kami K, et al. (2009) Rab1 guanine nucleotide exchange factor SidM is a major phosphatidylinositol 4-phosphate-binding effector protein of Legionella pneumophila. J Biol Chem 284: 4846-4856.
16. Machner MP, Isberg RR, (2007) A bifunctional bacterial protein links GDI displacement to Rab1 activation. Science 318: 974-977.
17. Ingmundson A, Delprato A, Lambright DG, Roy CR, (2007) Legionella pneumophila proteins that regulate Rab1 membrane cycling. Nature 450: 365-369.
18. Neunuebel MR, Chen Y, Gaspar AH, Backlund PS Jr, Yergey A, et al. (2011) De-AMPylation of the small GTPase Rab1 by the pathogen Legionella pneumophila. Science 333: 453-456.
19. Tan Y, Luo ZQ, (2011) Legionella pneumophila SidD is a deAMPylase that modifies Rab1. Nature 475: 506-509.
20. Anderson WB, Stadtman ER, (1970) Glutamine synthetase deadenylation: a phosphorolytic reaction yielding ADP as nucleotide product. Biochem Biophys Res Commun 41: 704-709.
21. Holm L, Rosenstrom P, (2010) Dali server: conservation mapping in 3D. Nucleic Acids Res 38: W545-549.
22. Das AK, Helps NR, Cohen PT, Barford D, (1996) Crystal structure of the protein serine/threonine phosphatase 2C at 2.0 A resolution. EMBO J 15: 6798-6809.
23. Pullen KE, Ng HL, Sung PY, Good MC, Smith SM, et al. (2004) An alternate conformation and a third metal in PstP/Ppp, the M. tuberculosis PP2C-Family Ser/Thr protein phosphatase. Structure 12: 1947-1954.
24. Shi Y, (2009) Serine/threonine phosphatases: mechanism through structure. Cell 139: 468-484.
25. Sugiura T, Noguchi Y, (2009) Substrate-dependent metal preference of PPM1H, a cancer-associated protein phosphatase 2C: comparison with other family members. Biometals 22: 469-477.
26. Romani A, Scarpa A, (1992) Regulation of cell magnesium. Arch Biochem Biophys 298: 1-12.
27. Jackson MD, Fjeld CC, Denu JM, (2003) Probing the function of conserved residues in the serine/threonine phosphatase PP2Calpha. Biochemistry 42: 8513-8521.
28. Fjeld CC, Denu JM, (1999) Kinetic analysis of human serine/threonine protein phosphatase 2Calpha. J Biol Chem 274: 20336-20343.
29. Bellinzoni M, Wehenkel A, Shepard W, Alzari PM, (2007) Insights into the catalytic mechanism of PPM Ser/Thr phosphatases from the atomic resolution structures of a mycobacterial enzyme. Structure 15: 863-872.
30. Mukherjee S, Liu X, Arasaki K, McDonough J, Galan JE, et al. (2011) Modulation of Rab GTPase function by a protein phosphocholine transferase. Nature 477: 103-106.
31. Goody PR, Heller K, Oesterlin LK, Muller MP, Itzen A, et al. (2012) Reversible phosphocholination of Rab proteins by Legionella pneumophila effector proteins. EMBO J 31: 1774-1784.
32. Neunuebel MR, Mohammadi S, Jarnik M, Machner MP, (2012) Legionella pneumophila LidA affects nucleotide binding and activity of the host GTPase Rab1. J Bacteriol 194: 1389-1400.
33. Tan Y, Arnold RJ, Luo ZQ, (2011) Legionella pneumophila regulates the small GTPase Rab1 activity by reversible phosphorylcholination. Proc Natl Acad Sci U S A 108: 21212-21217.
34. Wehenkel A, Bellinzoni M, Schaeffer F, Villarino A, Alzari PM, (2007) Structural and binding studies of the three-metal center in two mycobacterial PPM Ser/Thr protein phosphatases. J Mol Biol 374: 890-898.
35. Su J, Schlicker C, Forchhammer K, (2011) A third metal is required for catalytic activity of the signal-transducing protein phosphatase M tPphA. J Biol Chem 286: 13481-13488.
36. Weber SS, Ragaz C, Reus K, Nyfeler Y, Hilbi H, (2006) Legionella pneumophila exploits PI(4)P to anchor secreted effector proteins to the replicative vacuole. PLoS Pathog 2: e46.
37. Nagem RA, Ambrosio AL, Rojas AL, Navarro MV, Golubev AM, et al. (2005) Getting the most out of X-ray home sources. Acta Crystallogr D Biol Crystallogr 61: 1022-1030.
38. Sheldrick GM, (2008) A short history of SHELX. Acta Crystallogr A 64: 112-122.
39. Adams PD, Afonine PV, Bunkoczi G, Chen VB, Davis IW, et al. (2010) PHENIX: a comprehensive Python-based system for macromolecular structure solution. Acta Crystallogr D Biol Crystallogr 66: 213-221.
40. Emsley P, Cowtan K, (2004) Coot: model-building tools for molecular graphics. Acta Crystallogr D Biol Crystallogr 60: 2126-2132.
41. Collaborative Computational Project N, (1994) The CCP4 suite: programs for protein crystallography. Acta Crystallogr D Biol Crystallogr 50: 760-763.
42. Murshudov GN, Vagin AA, Dodson EJ, (1997) Refinement of macromolecular structures by the maximum-likelihood method. Acta Crystallogr D Biol Crystallogr 53: 240-255.
43. Chen R, Weng Z, (2003) A novel shape complementarity scoring function for protein-protein docking. Proteins 51: 397-408.
44. Cheng TM, Blundell TL, Fernandez-Recio J, (2007) pyDock: electrostatics and desolvation for effective scoring of rigid-body protein-protein docking. Proteins 68: 503-515.
45. Case DA, Cheatham TE 3rd, Darden T, Gohlke H, Luo R, et al. (2005) The Amber biomolecular simulation programs. J Comput Chem 26: 1668-1688.
46. Wang J, Cieplak P, Kollman PA, (2000) How well does a restrained electrostatic potential (RESP) model perform in calculating conformational energies of organic and biological molecules? J Comput Chem 21: 1049-1074.
47. Case DA, Darden TA, Cheatham TEI, LSimmerling C, Wang J, et al. (2012) AMBER 12.
48. Ellis KJ, Morrison JF, (1982) Buffers of constant ionic strength for studying pH-dependent processes. Methods Enzymol 87: 405-426.