Legionella eukaryotic-like type IV substrates interfere with organelle trafficking

PLoS Pathogens

Volumn 4, Issue 8, 2008, Pages

  De Felipe, Karim Suwwan ^a   Glover, Robert T ^a   Charpentier, Xavier ^a   Anderson, O Roger ^b   Reyes, Moraima ^a   Pericone, Christopher D ^a   Shuman, Howard A ^a  

^a NewYork Presbyterian Hospital   (United States)

^b Department of Earth and Environmental Sciences   (United States)

Author keywords

[No Author keywords available]

Indexed keywords

BACTERIAL PROTEIN; LEGC2 YLFA PROTEIN; LEGC3 PROTEIN; LEGC7 YLFB PROTEIN; LYSOSOME ASSOCIATED MEMBRANE PROTEIN 1; UNCLASSIFIED DRUG; CARRIER PROTEIN; HYBRID PROTEIN; LAMP1 PROTEIN, MOUSE; LYSOSOME ASSOCIATED MEMBRANE PROTEIN;

ANIMAL CELL; ARTICLE; BACTERIAL GENE; CELL MEMBRANE; CELL MIGRATION; CELL ORGANELLE; CELL STRUCTURE; CELL VACUOLE; CONTROLLED STUDY; DICTYOSTELIUM DISCOIDEUM; ENDOSOME; FLUORESCENCE; GENE EXPRESSION; GENE LOCATION; GENE STRUCTURE; GENE TRANSLOCATION; HOST CELL; INTRACELLULAR TRANSPORT; LEGIONELLA PNEUMOPHILA; MAMMAL CELL; MOLECULAR INTERACTION; MOUSE; NONHUMAN; PHENOTYPE; PROTEIN ANALYSIS; PROTEIN DETERMINATION; PROTEIN DOMAIN; PROTEIN EXPRESSION; PROTEIN FUNCTION; PROTEIN LOCALIZATION; PROTEIN TARGETING; PROTEIN TRANSPORT; SEQUENCE HOMOLOGY; YEAST; ANIMAL; CELL LINE; DICTYOSTELIUM; GENETICS; LEGIONNAIRE DISEASE; METABOLISM; SACCHAROMYCES CEREVISIAE;

DICTYOSTELIUM DISCOIDEUM; EUKARYOTA; LEGIONELLA; LEGIONELLA PNEUMOPHILA; MAMMALIA; PHAGO; PROTOZOA;

ANIMALS; BACTERIAL PROTEINS; CARRIER PROTEINS; CELL LINE; DICTYOSTELIUM; ENDOSOMES; GENE EXPRESSION; LEGIONELLA PNEUMOPHILA; LEGIONNAIRES' DISEASE; LYSOSOME-ASSOCIATED MEMBRANE GLYCOPROTEINS; MICE; RECOMBINANT FUSION PROTEINS; SACCHAROMYCES CEREVISIAE; VACUOLES;

EID: 50849115482     PISSN: 15537366     EISSN: 15537374     Source Type: Journal    
DOI: 10.1371/journal.ppat.1000117     Document Type: Article

References (74)

1. Fraser DW, Tsai TR, Orenstein W, Parkin WE, Beecham HJ, et al. (1977) Legionnaires' disease: description of an epidemic of pneumonia. N Engl J Med 297: 1189-1197.
2. McDade JE, Shepard CC, Fraser DW, Tsai TR, Redus MA, et al. (1977) Legionnaires' disease: isolation of a bacterium and demonstration of its role in other respiratory disease. N Engl J Med 297: 1197-1203.
3. Horwitz MA, Silverstein SC (1980) Legionnaires' disease bacterium (Legionella pneumophila) multiples intracellularly in human monocytes. J Clin Invest 66: 441-450.
4. Garcia-Vidal C, Carratala J (2006) Current clinical management of Legionnaires' disease. Expert Rev Anti Infect Ther 4: 995-1004.
5. Greenberg D, Chiou CC, Famigilleti R, Lee TC, Yu VL (2006) Problem pathogens: paediatric legionellosis-implications for improved diagnosis. Lancet Infect Dis 6: 529-535.
6. Breiman RF, Fields BS, Sanden GN, Volmer L, Meier A, et al. (1990) Association of shower use with Legionnaires' disease. Possible role of amoebae. Jama 263: 2924-2926.
7. Philippe C, Blech MF, Hartemann P (2006) [Intra-amoebal development of Legionella pneumophila and the potential role of amoebae in the transmission of Legionnaires' disease]. Med Mal Infect 36: 196-200.
8. Molmeret M, Horn M, Wagner M, Santic M, Abu Kwaik Y (2005) Amoebae as training grounds for intracellular bacterial pathogens. Appl Environ Microbiol 71: 20-28.
9. Adeleke A, Pruckler J, Benson R, Rowbotham T, Halablab M, et al. (1996) Legionella-like amebal pathogens-phylogenetic status and possible role in respiratory disease. Emerg Infect Dis 2: 225-230.
10. Rowbotham TJ (1980) Preliminary report on the pathogenicity of Legionella pneumophila for freshwater and soil amoebae. J Clin Pathol 33: 1179-1183.
11. Fields BS, Barbaree JM, Shotts EB, Jr, Feeley JC, Morrill WE, et al. (1986) Comparison of guinea pig and protozoan models for determining virulence of Legionella species. Infect Immun 53: 553-559.
12. Hales LM, Shuman HA (1999) The Legionella pneumophila rpoS gene is required for growth within Acanthamoeba castellanii. J Bacteriol 181: 4879-4889.
13. Segal G, Purcell M, Shuman HA (1998) Host cell killing and bacterial conjugation require overlapping sets of genes within a 22-kb region of the Legionella pneumophila genome. Proc Natl Acad Sci U S A 95: 1669-1674.
14. Hilbi H, Segal G, Shuman HA (2001) Icm/dot-dependent upregulation of phagocytosis by Legionella pneumophila. Mol Microbiol 42: 603-617.
15. Newton HJ, Sansom FM, Bennett-Wood V, Hartland EL (2006) Identification of Legionella pneumophila-specific genes by genomic subtractive hybridization with Legionella micdadei and identification of lpnE, a gene required for efficient host cell entry. Infect Immun 74: 1683-1691.
16. Cirillo SL, Lum J, Cirillo JD (2000) Identification of novel loci involved in entry by Legionella pneumophila. Microbiology 146 ( Pt 6): 1345-1359.
17. Horwitz MA, Maxfield FR (1984) Legionella pneumophila inhibits acidification of its phagosome in human monocytes. J Cell Biol 99: 1936-1943. 18. Wiater LA, Dunn K, Maxfield FR, Shuman HA (1998) Early events in phagosome establishment are required for intracellular survival of Legionella pneumophila. Infect Immun 66: 4450-4460.
18. 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.
19. Horwitz MA (1983) Formation of a novel phagosome by the Legionnaires' disease bacterium (Legionella pneumophila) in human monocytes. J Exp Med 158: 1319-1331.
20. Kagan JC, Roy CR (2002) Legionella phagosomes intercept vesicular traffic from endoplasmic reticulum exit sites. Nat Cell Biol 4: 945-954.
21. Derre I, Isberg RR (2005) LidA, a translocated substrate of the Legionella pneumophila type IV secretion system, interferes with the early secretory pathway. Infect Immun 73: 4370-4380.
22. 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.
23. Robinson CG, Roy CR (2006) Attachment and fusion of endoplasmic reticulum with vacuoles containing Legionella pneumophila. Cell Microbiol 8: 793-805.
24. Vogel JP, Andrews HL, Wong SK, Isberg RR (1998) Conjugative transfer by the virulence system of Legionella pneumophila. Science 279: 873-876.
25. 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.
26. Ingmundson A, Delprato A, Lambright DG, Roy CR (2007) Legionella pneumophila proteins that regulate Rab1 membrane cycling. Nature 450: 365-369.
27. Machner MP, Isberg RR (2006) Targeting of host Rab GTPase function by the intravacuolar pathogen Legionella pneumophila. Dev Cell 11: 47-56.
28. Machner MP, Isberg RR (2007) A bifunctional bacterial protein links GDI displacement to Rab1 activation. Science 318: 974-977.
29. 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. doi:10.1371/journal.ppat.0020046.
30. Kubori T, Hyakutake A, Nagai H (2008) Legionella translocates an E3 ubiquitin ligase that has multiple U-boxes with distinct functions. Mol Microbiol 67: 1307-1319.
31. 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.
32. 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.
33. 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.
34. 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.
35. 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.
36. 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.
37. 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.
38. Laguna RK, Creasey EA, Li Z, Valtz N, Isberg RR (2006) A Legionella pneumophila-translocated substrate that is required for growth within macrophages and protection from host cell death. Proc Natl Acad Sci U S A 103: 18745-18750.
39. 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.
40. 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.
41. 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.
42. 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.
43. 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.
44. Cazalet C, Rusniok C, Bruggemann H, Zidane N, Magnier A, et al. (2004) Evidence in the Legionella pneumophila genome for exploitation of host cell functions and high genome plasticity. Nat Genet 36: 1165-1173.
45. Sansom FM, Newton HJ, Crikis S, Cianciotto NP, Cowan PJ, et al. (2007) A bacterial ecto-triphosphate diphosphohydrolase similar to human CD39 is essential for intracellular multiplication of Legionella pneumophila. Cell Microbiol.
46. 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.
47. 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.
48. Hurley JH, Emr SD (2006) The ESCRT complexes: structure and mechanism of a membrane-trafficking network. Annu Rev Biophys Biomol Struct 35: 277-298.
49. Katzmann DJ, Odorizzi G, Emr SD (2002) Receptor downregulation and multivesicular-body sorting. Nat Rev Mol Cell Biol 3: 893-905.
50. Sisko JL, Spaeth K, Kumar Y, Valdivia RH (2006) Multifunctional analysis of Chlamydia-specific genes in a yeast expression system. Mol Microbiol 60: 51-66.
51. Kramer RW, Slagowski NL, Eze NA, Giddings KS, Morrison MF, et al. (2007) Yeast Functional Genomic Screens Lead to Identification of a Role for a Bacterial Effector in Innate Immunity Regulation. PLoS Pathog 3: e21. doi:10.1371/journal.ppat.0030021.
52. Lesser CF, Miller SI (2001) Expression of microbial virulence proteins in Saccharomyces cerevisiae models mammalian infection. Embo J 20: 1840-1849.
53. 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.
54. Charpentier X, Oswald E (2004) Identification of the secretion and translocation domain of the enteropathogenic and enterohemorrhagic Escherichia coli effector Cif, using TEM-1 beta-lactamase as a new fluorescence-based reporter. J Bacteriol 186: 5486-5495.
55. Bankaitis VA, Johnson LM, Emr SD (1986) Isolation of yeast mutants defective in protein targeting to the vacuole. Proc Natl Acad Sci U S A 83: 9075-9079.
56. Robinson JS, Klionsky DJ, Banta LM, Emr SD (1988) Protein sorting in Saccharomyces cerevisiae: isolation of mutants defective in the delivery and processing of multiple vacuolar hydrolases. Mol Cell Biol 8: 4936-4948.
57. Bryant NJ, Stevens TH (1998) Vacuole biogenesis in Saccharomyces cerevisiae: protein transport pathways to the yeast vacuole. Microbiol Mol Biol Rev 62: 230-247.
58. Darsow T, Odorizzi G, Emr SD (2000) Invertase fusion proteins for analysis of protein trafficking in yeast. Methods Enzymol 327: 95-106.
59. Rose MD, Novick P, Thomas JH, Botstein D, Fink GR (1987) A Saccharomyces cerevisiae genomic plasmid bank based on a centromere-containing shuttle vector. Gene 60: 237-243.
60. Babst M, Sato TK, Banta LM, Emr SD (1997) Endosomal transport function in yeast requires a novel AAA-type ATPase, Vps4p. Embo J 16: 1820-1831.
61. Vida TA, Emr SD (1995) A new vital stain for visualizing vacuolar membrane dynamics and endocytosis in yeast. J Cell Biol 128: 779-792.
62. Raymond CK, Howald-Stevenson I, Vater CA, Stevens TH (1992) Morphological classification of the yeast vacuolar protein sorting mutants: evidence for a prevacuolar compartment in class E vps mutants. Mol Biol Cell 3: 1389-1402.
63. Horwitz MA (1983) The Legionnaires' disease bacterium (Legionella pneumophila) inhibits phagosome-lysosome fusion in human monocytes. J Exp Med 158: 2108-2126.
64. Joiner KA, Fuhrman SA, Miettinen HM, Kasper LH, Mellman I (1990) Toxoplasma gondii: fusion competence of parasitophorous vacuoles in Fc receptor-transfected fibroblasts. Science 249: 641-646.
65. Cowles CR, Snyder WB, Burd CG, Emr SD (1997) Novel Golgi to vacuole delivery pathway in yeast: identification of a sorting determinant and required transport component. Embo J 16: 2769-2782.
66. Osterberg M, Kim H, Warringer J, Melen K, Blomberg A, et al. (2006) Phenotypic effects of membrane protein overexpression in Saccharomyces cerevisiae. Proc Natl Acad Sci U S A 103: 11148-11153.
67. Snapp EL, Hegde RS, Francolini M, Lombardo F, Colombo S, et al. (2003) Formation of stacked ER cisternae by low affinity protein interactions. J Cell Biol 163: 257-269.
68. Sherman F, Fink G, Hicks J (1986) Methods in yeast genetics: a laboratory manual. Cold Spring HarborN.Y: Cold Spring Harbor Laboratory Press. pp 163-169.
69. Cristea IM, Williams R, Chait BT, Rout MP (2005) Fluorescent proteins as proteomic probes. Mol Cell Proteomics 4: 1933-1941.
70. Watts DJ, Ashworth JM (1970) Growth of myxameobae of the cellular slime mould Dictyostelium discoideum in axenic culture. Biochem J 119: 171-174.
71. Moran DM, Anderson OR, Dennett MR, Caron DA, Gast RJ (2007) A Description of Seven Antarctic Marine Gymnamoebae Including a New Subspecies, Two New Species and a New Genus: Neoparamoeba aestuarina antarctica n. subsp., Platyamoeba oblongata n. sp., Platyamoeba contorta n. sp. and Vermistella antarctica n. gen. n. sp. J Eukaryot Microbiol 54: 169-183.
72. Sadosky AB, Wiater LA, Shuman HA (1993) Identification of Legionella pneumophila genes required for growth within and killing of human macrophages. Infect Immun 61: 5361-5373.
73. Sussman M (1987) Cultivation and synchronous morphogenesis of Dictyostelium under controlled experimental conditions. Methods Cell Biol 28: 9-29.
74. Blaauw M, Linskens MH, van Haastert PJ (2000) Efficient control of gene expression by a tetracycline-dependent transactivator in single Dictyostelium discoideum cells. Gene 252: 71-82.