VipD of Legionella pneumophila Targets Activated Rab5 and Rab22 to Interfere with Endosomal Trafficking in Macrophages

PLoS Pathogens

Volumn 8, Issue 12, 2012, Pages

  Ku, Bonsu ^a   Lee, Kwang Hoon ^a,e   Park, Wei Sun ^a   Yang, Chul Su ^b,f   Ge, Jianning ^b,c   Lee, Seong Gyu ^a   Cha, Sun Shin ^d   Shao, Feng ^c   Heo, Won Do ^a   Jung, Jae U ^b   Oh, Byung Ha ^a  

^a Korea Advanced Institute of Science and Technology (KAIST)   (South Korea)

^b UNIVERSITY OF SOUTHERN CALIFORNIA   (United States)

^c NATIONAL INSTITUTE OF BIOLOGICAL SCIENCES   (China)

^d Korea Research Institute of Ships and Ocean Engineering   (South Korea)

^e Samsung Advanced Institute of Technology (SAIT)   (South Korea)

^f Chungnam National University   (South Korea)

Author keywords

[No Author keywords available]

Indexed keywords

ALANINE; EARLY ENDOSOME ANTIGEN 1; GLUTATHIONE TRANSFERASE; GUANINE NUCLEOTIDE EXCHANGE FACTOR; LIPOPOLYSACCHARIDE; LYSOSOME ASSOCIATED MEMBRANE PROTEIN 1; LYSOSOME ENZYME; PHOSPHOLIPASE A2; RAB PROTEIN; RAB22 PROTEIN; RAB5 PROTEIN; UNCLASSIFIED DRUG; VACUOLAR PROTEIN SORTING INHIBITOR PROTEIN D;

ANIMAL CELL; ARTICLE; CARBOXY TERMINAL SEQUENCE; CELL MIGRATION; CONTROLLED STUDY; CRYSTALLIZATION; ENDOSOME; FLUORESCENCE RESONANCE ENERGY TRANSFER; HANGING DROP VAPOR DIFFUSION METHOD; HELA CELL; HUMAN; HUMAN CELL; INFORMATION PROCESSING; LEGIONELLA PNEUMOPHILA; MACROPHAGE; MOUSE; NONHUMAN; PROTEIN BINDING; PROTEIN EXPRESSION; PROTEIN TARGETING; SIGNAL TRANSDUCTION; X RAY DIFFRACTION;

ANIMALS; BACTERIAL PROTEINS; BIOLOGICAL TRANSPORT; CARRIER PROTEINS; ENDOSOMES; HELA CELLS; HUMANS; LEGIONELLA PNEUMOPHILA; LEGIONELLOSIS; LYSOSOMES; MACROPHAGES; MICE; NUCLEAR PROTEINS; PROTEIN STRUCTURE, TERTIARY; RAB5 GTP-BINDING PROTEINS; VESICULAR TRANSPORT PROTEINS;

BACTERIA (MICROORGANISMS); LEGIONELLA PNEUMOPHILA;

EID: 84872026290     PISSN: 15537366     EISSN: 15537374     Source Type: Journal    
DOI: 10.1371/journal.ppat.1003082     Document Type: Article

References (59)

1. Horwitz MA, (1983) The Legionnaires' disease bacterium (Legionella pneumophila) inhibits phagosome-lysosome fusion in human monocytes. J Exp Med 158: 2108-2126.
2. 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.
3. Horwitz MA, (1983) Formation of a novel phagosome by the Legionnaires' disease bacterium (Legionella pneumophila) in human monocytes. J Exp Med 158: 1319-1331.
4. Hubber A, Roy CR, (2010) Modulation of host cell function by Legionella pneumophila type IV effectors. Annu Rev Cell Dev Biol 26: 261-283.
5. Zhu W, Banga S, Tan Y, Zheng C, Stephenson R, et al. (2011) Comprehensive identification of protein substrates of the Dot/Icm type IV transporter of Legionella pneumophila. PLoS One 6: e17638.
6. Schoebel S, Oesterlin LK, Blankenfeldt W, Goody RS, Itzen A, (2009) RabGDI displacement by DrrA from Legionella is a consequence of its guanine nucleotide exchange activity. Mol Cell 36: 1060-1072.
7. Suh HY, Lee DW, Lee KH, Ku B, Choi SJ, et al. (2010) Structural insights into the dual nucleotide exchange and GDI displacement activity of SidM/DrrA. EMBO J 29: 496-504.
8. Zhu Y, Hu L, Zhou Y, Yao Q, Liu L, et al. (2010) Structural mechanism of host Rab1 activation by the bifunctional Legionella type IV effector SidM/DrrA. Proc Natl Acad Sci U S A 107: 4699-4704.
9. 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.
10. Machner MP, Isberg RR, (2007) A bifunctional bacterial protein links GDI displacement to Rab1 activation. Science 318: 974-977.
11. 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.
12. Ingmundson A, Delprato A, Lambright DG, Roy CR, (2007) Legionella pneumophila proteins that regulate Rab1 membrane cycling. Nature 450: 365-369.
13. Belyi Y, Niggeweg R, Opitz B, Vogelsgesang M, Hippenstiel S, et al. (2006) Legionella pneumophila glucosyltransferase inhibits host elongation factor 1A. Proc Natl Acad Sci U S A 103: 16953-16958.
14. Hurtado-Guerrero R, Zusman T, Pathak S, Ibrahim AF, Shepherd S, et al. (2010) Molecular mechanism of elongation factor 1A inhibition by a Legionella pneumophila glycosyltransferase. Biochem J 426: 281-292.
15. Belyi Y, Stahl M, Sovkova I, Kaden P, Luy B, et al. (2009) Region of elongation factor 1A1 involved in substrate recognition by Legionella pneumophila glucosyltransferase Lgt1: identification of Lgt1 as a retaining glucosyltransferase. J Biol Chem 284: 20167-20174.
16. Pan X, Luhrmann A, Satoh A, Laskowski-Arce MA, Roy CR, (2008) Ankyrin repeat proteins comprise a diverse family of bacterial type IV effectors. Science 320: 1651-1654.
17. 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.
18. 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.
19. Ge J, Shao F, (2011) Manipulation of host vesicular trafficking and innate immune defence by Legionella Dot/Icm effectors. Cell Microbiol 13: 1870-1880.
20. Shohdy N, Efe JA, Emr SD, Shuman HA, (2005) Pathogen effector protein screening in yeast identifies Legionella factors that interfere with membrane trafficking. Proc Natl Acad Sci U S A 102: 4866-4871.
21. Andrews DL, Beames B, Summers MD, Park WD, (1988) Characterization of the lipid acyl hydrolase activity of the major potato (Solanum tuberosum) tuber protein, patatin, by cloning and abundant expression in a baculovirus vector. Biochem J 252: 199-206.
22. VanRheenen SM, Luo ZQ, O'Connor T, Isberg RR, (2006) Members of a Legionella pneumophila family of proteins with ExoU (phospholipase A) active sites are translocated to target cells. Infect Immun 74: 3597-3606.
23. Finck-Barbancon V, Goranson J, Zhu L, Sawa T, Wiener-Kronish JP, et al. (1997) ExoU expression by Pseudomonas aeruginosa correlates with acute cytotoxicity and epithelial injury. Mol Microbiol 25: 547-557.
24. Sato H, Frank DW, Hillard CJ, Feix JB, Pankhaniya RR, et al. (2003) The mechanism of action of the Pseudomonas aeruginosa-encoded type III cytotoxin, ExoU. EMBO J 22: 2959-2969.
25. Holm L, Sander C, (1996) Mapping the protein universe. Science 273: 595-603.
26. Dessen A, Tang J, Schmidt H, Stahl M, Clark JD, et al. (1999) Crystal structure of human cytosolic phospholipase A2 reveals a novel topology and catalytic mechanism. Cell 97: 349-360.
27. Banerji S, Aurass P, Flieger A, (2008) The manifold phospholipases A of Legionella pneumophila- identification, export, regulation, and their link to bacterial virulence. Int J Med Microbiol 298: 169-181.
28. Delprato A, Merithew E, Lambright DG, (2004) Structure, exchange determinants, and family-wide rab specificity of the tandem helical bundle and Vps9 domains of Rabex-5. Cell 118: 607-617.
29. Horiuchi H, Lippe R, McBride HM, Rubino M, Woodman P, et al. (1997) A novel Rab5 GDP/GTP exchange factor complexed to Rabaptin-5 links nucleotide exchange to effector recruitment and function. Cell 90: 1149-1159.
30. Hutagalung AH, Novick PJ, (2011) Role of Rab GTPases in membrane traffic and cell physiology. Physiol Rev 91: 119-149.
31. Weigert R, Yeung AC, Li J, Donaldson JG, (2004) Rab22a regulates the recycling of membrane proteins internalized independently of clathrin. Mol Biol Cell 15: 3758-3770.
32. Shen A, Lupardus PJ, Morell M, Ponder EL, Sadaghiani AM, et al. (2009) Simplified, enhanced protein purification using an inducible, autoprocessing enzyme tag. PLoS One 4: e8119.
33. Ng EL, Wang Y, Tang BL, (2007) Rab22B's role in trans-Golgi network membrane dynamics. Biochem Biophys Res Commun 361: 751-757.
34. Chen PI, Kong C, Su X, Stahl PD, (2009) Rab5 isoforms differentially regulate the trafficking and degradation of epidermal growth factor receptors. J Biol Chem 284: 30328-30338.
35. Huang F, Khvorova A, Marshall W, Sorkin A, (2004) Analysis of clathrin-mediated endocytosis of epidermal growth factor receptor by RNA interference. J Biol Chem 279: 16657-16661.
36. Magadan JG, Barbieri MA, Mesa R, Stahl PD, Mayorga LS, (2006) Rab22a regulates the sorting of transferrin to recycling endosomes. Mol Cell Biol 26: 2595-2614.
37. Haas AK, Fuchs E, Kopajtich R, Barr FA, (2005) A GTPase-activating protein controls Rab5 function in endocytic trafficking. Nat Cell Biol 7: 887-893.
38. Eathiraj S, Pan X, Ritacco C, Lambright DG, (2005) Structural basis of family-wide Rab GTPase recognition by rabenosyn-5. Nature 436: 415-419.
39. Nielsen E, Christoforidis S, Uttenweiler-Joseph S, Miaczynska M, Dewitte F, et al. (2000) Rabenosyn-5, a novel Rab5 effector, is complexed with hVPS45 and recruited to endosomes through a FYVE finger domain. J Cell Biol 151: 601-612.
40. Zhu G, Zhai P, Liu J, Terzyan S, Li G, et al. (2004) Structural basis of Rab5-Rabaptin5 interaction in endocytosis. Nat Struct Mol Biol 11: 975-983.
41. Stenmark H, Vitale G, Ullrich O, Zerial M, (1995) Rabaptin-5 is a direct effector of the small GTPase Rab5 in endocytic membrane fusion. Cell 83: 423-432.
42. Mishra A, Eathiraj S, Corvera S, Lambright DG, (2010) Structural basis for Rab GTPase recognition and endosome tethering by the C2H2 zinc finger of Early Endosomal Autoantigen 1 (EEA1). Proc Natl Acad Sci U S A 107: 10866-10871.
43. Kauppi M, Simonsen A, Bremnes B, Vieira A, Callaghan J, et al. (2002) The small GTPase Rab22 interacts with EEA1 and controls endosomal membrane trafficking. J Cell Sci 115: 899-911.
44. Ostermeier C, Brunger AT, (1999) Structural basis of Rab effector specificity: crystal structure of the small G protein Rab3A complexed with the effector domain of rabphilin-3A. Cell 96: 363-374.
45. Merithew E, Hatherly S, Dumas JJ, Lawe DC, Heller-Harrison R, et al. (2001) Structural plasticity of an invariant hydrophobic triad in the switch regions of Rab GTPases is a determinant of effector recognition. J Biol Chem 276: 13982-13988.
46. Gay NJ, Gangloff M, Weber AN, (2006) Toll-like receptors as molecular switches. Nat Rev Immunol 6: 693-698.
47. Clemens DL, Lee BY, Horwitz MA, (2000) Deviant expression of Rab5 on phagosomes containing the intracellular pathogens Mycobacterium tuberculosis and Legionella pneumophila is associated with altered phagosomal fate. Infect Immun 68: 2671-2684.
48. Tan Y, Luo ZQ, (2011) Legionella pneumophila SidD is a deAMPylase that modifies Rab1. Nature 475: 506-509.
49. 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.
50. Cheng W, Yin K, Lu D, Li B, Zhu D, et al. (2012) Structural insights into a unique Legionella pneumophila effector LidA recognizing both GDP and GTP bound Rab1 in their active state. PLoS Pathog 8: e1002528.
51. Schoebel S, Cichy AL, Goody RS, Itzen A, (2011) Protein LidA from Legionella is a Rab GTPase supereffector. Proc Natl Acad Sci U S A 108: 17945-17950.
52. Zhu H, Liang Z, Li G, (2009) Rabex-5 is a Rab22 effector and mediates a Rab22-Rab5 signaling cascade in endocytosis. Mol Biol Cell 20: 4720-4729.
53. Simonsen A, Lippe R, Christoforidis S, Gaullier JM, Brech A, et al. (1998) EEA1 links PI(3)K function to Rab5 regulation of endosome fusion. Nature 394: 494-498.
54. Rink J, Ghigo E, Kalaidzidis Y, Zerial M, (2005) Rab conversion as a mechanism of progression from early to late endosomes. Cell 122: 735-749.
55. Wang T, Ming Z, Xiaochun W, Hong W, (2011) Rab7: role of its protein interaction cascades in endo-lysosomal traffic. Cell Signal 23: 516-521.
56. Sheldrick GM, (2010) Experimental phasing with SHELXC/D/E: combining chain tracing with density modification. Acta Crystallogr D Biol Crystallogr 66: 479-485.
57. Bricogne G, Vonrhein C, Flensburg C, Schiltz M, Paciorek W, (2003) Generation, representation and flow of phase information in structure determination: recent developments in and around SHARP 2.0. Acta Crystallogr D Biol Crystallogr 59: 2023-2030.
58. Emsley P, Cowtan K, (2004) Coot: model-building tools for molecular graphics. Acta Crystallogr D Biol Crystallogr 60: 2126-2132.
59. Brunger AT, Adams PD, Clore GM, DeLano WL, Gros P, et al. (1998) Crystallography & NMR system: A new software suite for macromolecular structure determination. Acta Crystallogr D Biol Crystallogr 54: 905-921.