The Legionella pneumophila IcmSW complex interacts with multiple Dot/Icm effectors to facilitate type IV translocation

PLoS Pathogens

Volumn 3, Issue 12, 2007, Pages 1837-1848

  Cambronne, Eric D ^a   Roy, Craig R ^a  

^a YALE UNIVERSITY SCHOOL OF MEDICINE   (United States)

Author keywords

[No Author keywords available]

Indexed keywords

BACTERIAL PROTEIN; METHYLTRANSFERASE; PROTEIN ICMS; PROTEIN ICMW; PROTEIN SIDG; PROTEINASE; UNCLASSIFIED DRUG; CARRIER PROTEIN; CHAPERONE; DOTA PROTEIN, LEGIONELLA PNEUMOPHILA; ICMS PROTEIN, LEGIONELLA PNEUMOPHILA; MEMBRANE PROTEIN;

AMINO TERMINAL SEQUENCE; ANIMAL CELL; ARTICLE; CELLULAR DISTRIBUTION; EUKARYOTIC CELL; IN VITRO STUDY; LEGIONELLA PNEUMOPHILA; NONHUMAN; PROTEIN BINDING; PROTEIN INTERACTION; PROTEIN STABILITY; PROTEIN TRANSPORT; ANIMAL; BACTERIAL TRANSLOCATION; CHO CELL; CRICETULUS; GENE EXPRESSION REGULATION; GENETICS; HAMSTER; LEGIONNAIRE DISEASE; METABOLISM; PATHOGENICITY;

EUKARYOTA; LEGIONELLA PNEUMOPHILA; NEGIBACTERIA;

ANIMALS; BACTERIAL PROTEINS; BACTERIAL TRANSLOCATION; CARRIER PROTEINS; CHO CELLS; CRICETINAE; CRICETULUS; GENE EXPRESSION REGULATION, BACTERIAL; LEGIONELLA PNEUMOPHILA; LEGIONNAIRES' DISEASE; MEMBRANE PROTEINS; MOLECULAR CHAPERONES;

EID: 37849053708     PISSN: 15537366     EISSN: 15537374     Source Type: Journal    
DOI: 10.1371/journal.ppat.0030188     Document Type: Article

References (50)

1. Cascales E, Christie PJ (2003) The versatile bacterial type IV secretion systems. Nat Rev Microbiol 1: 137-149.
2. 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.
3. Marra A, Blander SJ, Horwitz MA, Shuman HA (1992) Identification of a Legionella pneumophila locus required for intracellular multiplication in human macrophages. Proc Natl Acad Sci U S A 89: 9607-9611.
4. Vogel JP, Andrews HL, Wong SK, Isberg RR (1998) Conjugative transfer by the virulence system of Legionella pneumophila. Science 279: 873-876.
5. Roy CR, Berger KH, Isberg RR (1998) Legionella pneumophila DotA protein is required for early phagosome trafficking decisions that occur within minutes of bacterial uptake. Mol Microbiol 28: 663-674.
6. Horwitz MA, Silverstein SC (1983) Intracellular multiplication of Legionnaires' disease bacteria (Legionella pneumophila) in human monocytes is reversibly inhibited by erythromycin and rifampin. J Clin Invest 71: 15-26.
7. Horwitz MA (1983) Symbiotic interactions between Legionella pneumophila and human leukocytes. Int Rev Cytol Suppl 14: 307-328.
8. Swanson MS, Isberg RR (1995) Association of Legionella pneumophila with the macrophage endoplasmic reticulum. Infect Immun 63: 3609-3620.
9. 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.
10. Kagan JC, Roy CR (2002) Legionella phagosomes intercept vesicular traffic from endoplasmic reticulum exit sites. Nat Cell Biol 4: 945-954.
11. Nagai H, Roy CR (2001) The DotA protein from Legionella pneumophila is secreted by a novel process that requires the Dot/Icm transporter. Embo J 20: 5962-5970.
12. Chen J, de Felipe KS, Clarke M, Lu H, Anderson OR, et al. (2004) Legionella effectors that promote nonlytic release from protozoa. Science 303: 1358-1361.
13. Luo ZQ, Isberg RR (2004) Multiple substrates of the Legionella pneumophila Dot/Icm system identified by interbacterial protein transfer. Proc Natl Acad Sci U S A 101: 841-846.
14. 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.
15. Conover GM, Derre I, Vogel JP, Isberg RR (2003) The Legionella pneumophila LidA protein: a translocated substrate of the Dot/Icm system associated with maintenance of bacterial integrity. Mol Microbiol 48: 305-321.
16. Campodonico EM, Chesnel L, Roy CR (2005) A yeast genetic system for the identification and characterization of substrate proteins transferred into host cells by the Legionella pneumophila Dot/Icm system. Mol Microbiol 56: 918-933.
17. 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.
18. de Felipe KS, Pampou S, Jovanovic OS, Pericone CD, Ye SF, et al. (2005) Evidence for acquisition of Legionella type IV secretion substrates via interdomain horizontal gene transfer. J Bacteriol 187: 7716-7726.
19. Machner MP, Isberg RR (2006) Targeting of host rab GTPase function by the intravacuolar pathogen Legionella pneumophila. Dev Cell 11: 47-56.
20. 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.
21. Ninio S, Zuckman-Cholon DM, Cambronne ED, Roy CR (2005) The Legionella IcmS-IcmW protein complex is important for Dot/Icm-mediated protein translocation. Mol Microbiol 55: 912-926.
22. Banga S, Gao P, Shen X, Fiscus V, Zong WX, et al. (2007) Legionella pneumophila inhibits macrophage apoptosis by targeting pro-death members of the Bcl2 protein family. Proc Natl Acad Sci U S A 104: 5121-5126.
23. Liu Y, Luo ZQ (2007) The Legionella pneumophila effector SidJ is required for efficient recruitment of endoplasmic reticulum proteins to the bacterial phagosome. Infect Immun 75: 592-603.
24. 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.
25. Bardill JP, Miller JL, Vogel JP (2005) IcmS-dependent translocation of SdeA into macrophages by the Legionella pneumophila type IV secretion system. Mol Microbiol 56: 90-103.
26. Zusman T, Aloni G, Halperin E, Kotzer H, Degtyar E, et al. (2007) The response regulator PmrA is a major regulator of the icm/dot type IV secretion system in Legionella pneumophila and Coxiella burnetii. Mol Microbiol 63: 1508-1523.
27. Vergunst AC, Schrammeijer B, den Dulk-Ras A, de Vlaam CM, Regensburg-Tuink TJ, et al. (2000) VirB/D4-dependent protein translocation from Agrobacterium into plant cells. Science 290: 979-982.
28. Simone M, McCullen CA, Stahl LE, Binns AN (2001) The carboxy-terminus of VirE2 from Agrobacterium tumefaciens is required for its transport to host cells by the virB-encoded type IV transport system. Mol Microbiol 41: 1283-1293.
29. Vergunst AC, van Lier MC, den Dulk-Ras A, Stuve TA, Ouwehand A, et al. (2005) Positive charge is an important feature of the C-terminal transport signal of the VirB/D4-translocated proteins of Agrobacterium. Proc Natl Acad Sci U S A 102: 832-837.
30. Hohlfeld S, Pattis I, Puls J, Plano GV, Haas R, et al. (2006) A C-terminal translocation signal is necessary, but not sufficient for type IV secretion of the Helicobacter pylori CagA protein. Mol Microbiol 59: 1624-1637.
31. Schulein R, Guye P, Rhomberg TA, Schmid MC, Schroder G, et al. (2005) A bipartite signal mediates the transfer of type IV secretion substrates of Bartonella henselae into human cells. Proc Natl Acad Sci U S A 102: 856-861.
32. Nagai H, Cambronne ED, Kagan JC, Amor JC, Kahn RA, et al. (2005) A Cterminal 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.
33. Chen J, Reyes M, Clarke M, Shuman HA (2007) Host cell-dependent secretion and translocation of the LepA and LepB effectors of Legionella pneumophila. Cell Microbiol 9: 1660-1671.
34. Schmid MC, Scheidegger F, Dehio M, Balmelle-Devaux N, Schulein R, et al. (2006) A translocated bacterial protein protects vascular endothelial cells from apoptosis. PLoS Pathog 2: e115. doi:10.1371/journal.ppat.0020115
35. 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.
36. Coers J, Kagan JC, Matthews M, Nagai H, Zuckman DM, et al. (2000) Identification of Icm protein complexes that play distinct roles in the biogenesis of an organelle permissive for Legionella pneumophila intracellular growth. Mol Microbiol 38: 719-736.
37. Ghosh P (2004) Process of protein transport by the type III secretion system. Microbiol Mol Biol Rev 68: 771-795.
38. Zuckman DM, Hung JB, Roy CR (1999) Pore-forming activity is not sufficient for Legionella pneumophila phagosome trafficking and intracellular growth. Mol Microbiol 32: 990-1001.
39. Vincent CD, Friedman JR, Jeong KC, Buford EC, Miller JL, et al. (2006) Identification of the core transmembrane complex of the Legionella Dot/Icm type IV secretion system. Mol Microbiol 62: 1278-1291.
40. Vincent CD, Vogel JP (2006) The Legionella pneumophila IcmS-LvgA protein complex is important for Dot/Icm-dependent intracellular growth. Mol Microbiol 61: 596-613.
41. Sory MP, Cornelis GR (1994) Translocation of a hybrid YopE-adenylate cyclase from Yersinia enterocolitica into HeLa cells. Mol Microbiol 14: 583-594.
42. Lilic M, Vujanac M, Stebbins CE (2006) A common structural motif in the binding of virulence factors to bacterial secretion chaperones. Mol Cell 21: 653-664.
43. Birtalan SC, Phillips RM, Ghosh P (2002) Three-dimensional secretion signals in chaperone-effector complexes of bacterial pathogens. Mol Cell 9: 971-980.
44. Akeda Y, Galan JE (2005) Chaperone release and unfolding of substrates in type III secretion. Nature 437: 911-915.
45. Stebbins CE, Galan JE (2001) Maintenance of an unfolded polypeptide by a cognate chaperone in bacterial type III secretion. Nature 414: 77-81.
46. Phan J, Tropea JE, Waugh DS (2004) Structure of the Yersinia pestis type III secretion chaperone SycH in complex with a stable fragment of YscM2. Acta Crystallogr D Biol Crystallogr 60: 1591-1599.
47. Sorg JA, Blaylock B, Schneewind O (2006) Secretion signal recognition by YscN, the Yersinia type III secretion ATPase. Proc Natl Acad Sci U S A 103: 16490-16495.
48. Sexton JA, Yeo HJ, Vogel JP (2005) Genetic analysis of the Legionella pneumophila DotB ATPase reveals a role in type IV secretion system protein export. Mol Microbiol 57: 70-84.
49. Feldman M, Segal G (2007) A pair of highly conserved two-component systems participates in the regulation of the hypervariable FIR proteins in different Legionella species. J Bacteriol 189: 3382-3391.
50. Bruggemann H, Hagman A, Jules M, Sismeiro O, Dillies MA, et al. (2006) Virulence strategies for infecting phagocytes deduced from the in vivo transcriptional program of Legionella pneumophila. Cell Microbiol 8: 1228-1240.