Soluble NSF attachment protein receptor molecular mimicry by a Legionella pneumophilaDot/Icm effector

Cellular Microbiology

Volumn 17, Issue 6, 2015, Pages 767-784

  King, Nathan P ^a   Newton, Patrice ^b   Schuelein, Ralf ^b   Brown, Darren L ^a   Petru, Marketa ^c   Zarsky, Vojtech ^c   Dolezal, Pavel ^c   Luo, Lin ^a   Bugarcic, Andrea ^a   Stanley, Amanda C ^a   Murray, Rachael Z ^d   Collins, Brett M ^a   Teasdale, Rohan D ^a   Hartland, Elizabeth L ^b   Stow, Jennifer L ^a  

^a UNIVERSITY OF QUEENSLAND   (Australia)

^b UNIVERSITY OF MELBOURNE   (Australia)

^c CHARLES UNIVERSITY   (Czech Republic)

^d QUEENSLAND UNIVERSITY OF TECHNOLOGY   (Australia)

Author keywords

[No Author keywords available]

Indexed keywords

BACTERIAL PROTEIN; SNARE PROTEIN; SOLUBLE N ETHYLMALEIMIDE SENSITIVE FACTOR ATTACHMENT PROTEIN; VIRULENCE FACTOR;

ACANTHAMOEBA CASTELLANII; ACANTHAMOEBA POLYPHAGA; ACIDIFICATION; AMINO ACID SEQUENCE; ARTICLE; BACTERIAL STRAIN; BACTERIUM ISOLATE; CELL DIVISION; CELL STRUCTURE; FARNESYLATION; FEMALE; GOLGI COMPLEX; GOLGI MEMBRANE; HIDDEN MARKOV MODEL; HOST CELL; HUMAN; HUMAN CELL; LEGIONELLA PNEUMOPHILA; LYSOSOME; MACROPHAGE; MAMMAL CELL; MEMBRANE FUSION; MICROBIOLOGICAL EXAMINATION; MOLECULAR MIMICRY; MOLECULAR WEIGHT; PHYLOGENY; POLYMERASE CHAIN REACTION; PRIORITY JOURNAL; PROTEIN ANALYSIS; PROTEIN INTERACTION; PROTEIN MOTIF; TRANSMISSION ELECTRON MICROSCOPY; TYPE IV SECRETION SYSTEM; WESTERN BLOTTING; ANIMAL; CELL LINE; EPITHELIUM CELL; HOST PATHOGEN INTERACTION; METABOLISM; MICROBIOLOGY; MOUSE; PHYSIOLOGY; SEQUENCE HOMOLOGY;

BACTERIA (MICROORGANISMS); EUKARYOTA; LEGIONELLA; LEGIONELLA PNEUMOPHILA; MAMMALIA;

ANIMALS; BACTERIAL PROTEINS; CELL LINE; EPITHELIAL CELLS; HOST-PATHOGEN INTERACTIONS; HUMANS; LEGIONELLA PNEUMOPHILA; MACROPHAGES; MICE; MOLECULAR MIMICRY; SEQUENCE HOMOLOGY, AMINO ACID; SOLUBLE N-ETHYLMALEIMIDE-SENSITIVE FACTOR ATTACHMENT PROTEINS; VIRULENCE FACTORS;

EID: 84929502331     PISSN: 14625814     EISSN: 14625822     Source Type: Journal    
DOI: 10.1111/cmi.12405     Document Type: Article

References (71)

1. Al-Quadan, T., Price, C.T., London, N., Schueler-Furman, O., and AbuKwaik, Y. (2011) Anchoring of bacterial effectors to host membranes through host-mediated lipidation by prenylation: a common paradigm. Trends Microbiol 19: 573-579.
2. Antonin, W., Fasshauer, D., Becker, S., Jahn, R., and Schneider, T.R. (2002) Crystal structure of the endosomal SNARE complex reveals common structural principles of all SNAREs. Nat Struct Biol 9: 107-111.
3. Arasaki, K., Toomre, D.K., and Roy, C.R. (2012) The Legionella pneumophila effector DrrA is sufficient to stimulate SNARE-dependent membrane fusion. Cell Host Microbe 11: 46-57.
4. Bennett, T.L., Kraft, S.M., Reaves, B.J., Mima, J., O'Brien, K.M., and Starai, V.J. (2013) LegC3, an effector protein from Legionella pneumophila, inhibits homotypic yeast vacuole fusion in vivo and in vitro. PLoS ONE 8: e56798. doi:56710.51371/journal.pone.0056798.
5. Brandhorst, D., Zwilling, D., Rizzoli, S.O., Lippert, U., Lang, T., and Jahn, R. (2006) Homotypic fusion of early endosomes: SNAREs do not determine fusion specificity. Proc Natl Acad Sci U S A 103: 2701-2706.
6. Brombacher, E., Urwyler, S., Ragaz, C., Weber, S.S., Kami, K., Overduin, M., and Hilbi, H. (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.
7. Campodonico, E.M., Chesnel, L., and Roy, C.R. (2005) A yeast genetic system for the identification and characterization of substrate proteins transferred into host cells by the Legionella pneumophila Dot/lcm system. Mol Microbiol 56: 918-933.
8. Chen, J., de Felipe, K.S., Clarke, M., Lu, H., Anderson, O.R., Segal, G., and Shuman, H.A. (2004) Legionella effectors that promote nonlytic release from protozoa. Science 303: 1358-1361.
9. D'Auria, G., Jimenez-Hernandez, N., Peris-Bondia, F., Moya, A., and Latorre, A. (2010) Legionella pneumophila pangenome reveals strain-specific virulence factors. BMC Genomics 11: 181. doi:110.1186/1471-2164-1111-1181.
10. Delevoye, C., Nilges, M., Dehoux, P., Paumet, F., Perrinet, S., Dautry-Varsat, A., and Subtil, A. (2008) SNARE protein mimicry by an intracellular bacterium. PLoS Pathog 4: e1000022. doi:1000010.1001371/journal.ppat.1000022.
11. Dolezal, P., Aili, M., Tong, J., Jiang, J.-H., Marobbio, C.M., Lee, S.F., etal. (2012) Legionella pneumophila secretes a mitochondrial carrier protein during infection. PLoS Pathog 8: e1002459. doi:1002410.1001371/journal.ppat.1002459.
12. Eddy, S.R. (2011) Accelerated profile HMM searches. PLoS Comput Biol 7: e1002195. doi:1002110.1001371/journal.pcbi.1002195.
13. Emsley, P., and Cowtan, K. (2004) Coot: model-building tools for molecular graphics. Acta Crystallogr Sect D Biol Crystallogr 60: 2126-2132.
14. de Felipe, K.S., Glover, R.T., Charpentier, X., Anderson, O.R., Reyes, M., Pericone, C.D., and Shuman, H.A. (2008) Legionella eukaryotic-like type IV substrates interfere with organelle trafficking. PLoS Pathog 4: e1000117. doi:1000110.1001371/journal.ppat.1000117.
15. Finsel, I., Ragaz, C., Hoffmann, C., Harrison, C.F., Weber, S., van Rahden, V.A., etal. (2013) The Legionella effector RidL inhibits retrograde trafficking to promote intracellular replication. Cell Host Microbe 14: 38-50.
16. Follett, J., Norwood, S.J., Hamilton, N.A., Mohan, M., Kovtun, O., Tay, S., etal. (2014) The Vps35 D620N mutation linked to Parkinson's disease disrupts the cargo sorting function of retromer. Traffic 15: 230-244.
17. Fukasawa, M., Varlamov, O., Eng, W.S., Sollner, T.H., and Rothman, J.E. (2004) Localization and activity of the SNARE Ykt6 determined by its regulatory domain and palmitoylation. Proc Natl Acad Sci U S A 101: 4815-4820.
18. Ge, J., and Shao, F. (2011) Manipulation of host vesicular trafficking and innate immune defence by Legionella Dot/Icm effectors. Cell Microbiol 13: 1870-1880.
19. Ginevra, C., Forey, F., Campese, C., Reyrolle, M., Che, D., Etienne, J., and Jarraud, S. (2008) Lorraine strain of Legionella pneumophila serogroup 1, France. Emerg Infect Dis 14: 673-675.
20. Gloeckner, G., Albert-Weissenberger, C., Weinmann, E., Jacobi, S., Schunder, E., Steinert, M., etal. (2008) Identification and characterization of a new conjugation/type IVA secretion system (trb/tra) of Legionella pneumophila Corby localized on two mobile genomic islands. Int J Med Microbiol 298: 411-428.
21. Gomez-Valero, L., Rusniok, C., Jarraud, S., Vacherie, B., Rouy, Z., Barbe, V., etal. (2011) Extensive recombination events and horizontal gene transfer shaped the Legionella pneumophila genomes. BMC Genomics 12: 536. doi:510.1186/1471-2164-1112-1536.
22. Goody, R.S., and Itzen, A. (2013) Modulation of small GTPases by Legionella. Curr Top Microbiol Immunol 376: 117-133.
23. Hardiman, C.A., McDonough, J.A., Newton, H.J., and Roy, C.R. (2012) The role of Rab GTPases in the transport of vacuoles containing Legionella pneumophila and Coxiella burnetii. Biochem Soc Trans 40: 1353-1359.
24. Hicks, S.W., and Galan, J.E. (2013) Exploitation of eukaryotic subcellular targeting mechanisms by bacterial effectors. Nat Rev Microbiol 11: 316-326.
25. Hong, W.J. (2005) SNARES and traffic. Biochim Biophys Acta Mol Cell Res 1744: 120-144.
26. Hubber, A., and Roy, C.R. (2010) Modulation of host cell function by Legionella pneumophila type IV effectors. Annu Rev Cell Dev Biol 26: 261-283.
27. Ivanov, S.S., Charron, G., Hang, H.C., and Roy, C.R. (2010) Lipidation by the host prenyltransferase machinery facilitates membrane localization of Legionella pneumophila effector proteins. J Biol Chem 285: 34686-34698.
28. Jahn, R., and Scheller, R.H. (2006) SNAREs - engines for membrane fusion. Nat Rev Mol Cell Biol 7: 631-643.
29. Kelley, L.A., and Sternberg, M.J.E. (2009) Protein structure prediction on the Web: a case study using the Phyre server. Nat Protoc 4: 363-371.
30. Kloepper, T.H., Kienle, C.N., and Fasshauer, D. (2007) An elaborate classification of SNARE proteins sheds light on the conservation of the eukaryotic endomembrane system. Mol Biol Cell 18: 3463-3471.
31. Leonard, J.H., Marks, L.H., Chen, W., Cook, A.L., Boyle, G.M., Smit, D.J., etal. (2003) Screening of human primary melanocytes of defined melanocortin-1 receptor genotype: pigmentation marker, ultrastructural and UV-survival studies. Pigment Cell Res 16: 198-207.
32. Likic, V.A., Dolezal, P., Celik, N., Dagley, M., and Lithgow, T. (2010) Using hidden Markov models to discover new protein transport machines. Methods Mol Biol 619: 271-284.
33. Machner, M.P., and Isberg, R.R. (2006) Targeting of host Rab GTPase function by the intravacuolar pathogen Legionella pneumophila. Dev Cell 11: 47-56.
34. McNicholas, S., Potterton, E., Wilson, K.S., and Noble, M.E.M. (2011) Presenting your structures: the CCP4mg molecular-graphics software. Acta Crystallogr Sect D Biol Crystallogr 67: 386-394.
35. Madan, R., Rastogi, R., Parashuraman, S., and Mukhopadhyay, A. (2012) Salmonella acquires lysosome-associated membrane protein 1 (LAMP1) on phagosomes from Golgi via SipC protein-mediated recruitment of host syntaxin6. J Biol Chem 287: 5574-5587.
36. Mallard, F., Tang, B.L., Galli, T., Tenza, D., Saint-Pol, A., Yue, X., etal. (2002) Early/recycling endosomes-to-TGN transport involves two SNARE complexes and a Rab6 isoform. J Cell Biol 156: 653-664.
37. Manderson, A.P., Kay, J.G., Hammond, L.A., Brown, D.L., and Stow, J.L. (2007) Subcompartments of the macrophage recycling endosome direct the differential secretion of IL-6 and TNFα. J Cell Biol 178: 57-69.
38. Merriam, J.J., Mathur, R., Maxfield-Boumil, R., and Isberg, R.R. (1997) Analysis of the Legionella pneumophila fliI gene: intracellular growth of a defined mutant defective for flagellum biosynthesis. Infect Immun 65: 2497-2501.
39. Moore, E.R., Mead, D.J., Dooley, C.A., Sager, J., and Hackstadt, T. (2011) The trans-Golgi SNARE syntaxin 6 is recruited to the chlamydial inclusion membrane. Microbiology 157: 830-838.
40. Murata, T., Delprato, A., Ingmundson, A., Toomre, D.K., Lambright, D.G., and Roy, C.R. (2006) The Legionella pneumophila effector protein DrrA is a Rab1 guanine nucleotide-exchange factor. Nat Cell Biol 8: 971-977.
41. Murray, R.Z., Wylie, F.G., Khromykh, T., Hume, D.A., and Stow, J.L. (2005) Syntaxin 6 and Vti1b form a novel SNARE complex, which is up-regulated in activated macrophages to facilitate exocytosis of tumor necrosis factor-α. J Biol Chem 280: 10478-10483.
42. Nagai, H., Kagan, J.C., Zhu, X.J., Kahn, R.A., and Roy, C.R. (2002) A bacterial guanine nucleotide exchange factor activates ARF on Legionella phagosomes. Science 295: 679-682.
43. Neunuebel, M.R., and Machner, M.P. (2012a) The taming of a Rab GTPase by Legionella pneumophila. Small GTPases 3: 28-33.
44. Neunuebel, M.R., Mohammadi, S., Jarnik, M., and Machner, M.P. (2012b) Legionella pneumophila LidA affects nucleotide binding and activity of the host GTPase Rab1. J Bacteriol 194: 1389-1400.
45. Newton, H.J., Sansom, F.M., Bennett-Wood, V., and Hartland, E.L. (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.
46. Newton, H.J., Ang, D.K.Y., van Driel, I.R., and Hartland, E.L. (2010) Molecular pathogenesis of infections caused by Legionella pneumophila. Clin Microbiol Rev 23: 274-298.
47. Offenhaeuser, C., Lei, N., Roy, S., Collins, B.M., Stow, J.L., and Murray, R.Z. (2011) Syntaxin 11 binds Vti1b and regulates late endosome to lysosome fusion in macrophages. Traffic 12: 762-773.
48. Paumet, F., Wesolowski, J., Garcia-Diaz, A., Delevoye, C., Aulner, N., Shuman, H.A., etal. (2009) Intracellular bacteria encode inhibitory SNARE-like proteins. PLoS ONE 4: e7375. doi:7310.1371/journal.pone.0007375.
49. Price, C.T.D., Al-Quadan, T., Santic, M., Jones, S.C., and Abu Kwaik, Y. (2010a) Exploitation of conserved eukaryotic host cell farnesylation machinery by an F-box effector of Legionella pneumophila. J Exp Med 207: 1712-1725.
50. Price, C.T.D., Jones, S.C., Amundson, K.E., and Kwaik, Y.A. (2010b) Host-mediated post-translational prenylation of novel Dot/Icm-translocated effectors of Legionella pneumophila. Front Microbiol 1: 131. doi:110.3389/fmicb.2010.00131.
51. Sansom, F.M., Newton, H.J., Crikis, S., Cianciotto, N.P., Cowan, P.J., d'Apice, A.J.F., and Hartland, E.L. (2007) A bacterial ecto-triphosphate diphosphohydrolase similar to human CD39 is essential for intracellular multiplication of Legionella pneumophila. Cell Microbiol 9: 1922-1935.
52. Seaman, M.N.J. (2012) The retromer complex - endosomal protein recycling and beyond. J Cell Sci 125: 4693-4702.
53. Sherwood, R.K., and Roy, C.R. (2013) A Rab-centric perspective of bacterial pathogen-occupied vacuoles. Cell Host Microbe 14: 256-268.
54. Shohdy, N., Efe, J.A., Emr, S.D., and Shuman, H.A. (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.
55. Shurety, W., Merino-Trigo, A., Brown, D., Hume, D.A., and Stow, J.L. (2000) Localization and post-Golgi trafficking of tumor necrosis factor-α in macrophages. J Interferon Cytokine Res 20: 427-438.
56. Sievers, F., Wilm, A., Dineen, D., Gibson, T.J., Karplus, K., Li, W., etal. (2011) Fast, scalable generation of high-quality protein multiple sequence alignments using Clustal Omega. Mol Syst Biol 7: 539. doi:510.1038/msb.2011.1075.
57. Stanley, A.C., Wong, C.X., Micaroni, M., Venturato, J., Khromykh, T., Stow, J.L., and Lacy, P. (2014) The Rho GTPase Rac1 is required for recycling endosome-mediated secretion of TNF in macrophages. Immunol Cell Biol 92: 275-286.
58. Stow, J.L., Manderson, A.P., and Murray, R.Z. (2006) SNAREing immunity: the role of SNAREs in the immune system. Nat Rev Immunol 6: 919-929.
59. Tamura, K., Peterson, D., Peterson, N., Stecher, G., Nei, M., and Kumar, S. (2011) MEGA5: molecular evolutionary genetics analysis using maximum likelihood, evolutionary distance, and maximum parsimony methods. Mol Biol Evol 28: 2731-2739.
60. Varlamov, O., Volchuk, A., Rahimian, V., Doege, C.A., Paumet, F., Eng, W.S., etal. (2004) i-SNAREs: inhibitory SNAREs that fine-tune the specificity of membrane fusion. J Cell Biol 164: 79-88.
61. Vincent, C.D., Friedman, J.R., Jeong, K.C., Buford, E.C., Miller, J.L., and Vogel, J.P. (2006) Identification of the core transmembrane complex of the Legionella Dot/Icm type IV secretion system. Mol Microbiol 62: 1278-1291.
62. Vogel, K., and Roche, P.A. (1999) SNAP-23 and SNAP-25 are palmitoylated in vivo. Biochem Biophys Res Commun 258: 407-410.
63. Wang, Y., Foo, L.Y., Guo, K., Gan, B.Q., Zeng, Q., Hong, W.J., and Tang, B.L. (2006) Syntaxin 9 is enriched in skin hair follicle epithelium and interacts with the epidermal growth factor receptor. Traffic 7: 216-226.
64. Waterhouse, A.M., Procter, J.B., Martin, D.M.A., Clamp, M., and Barton, G.J. (2009) Jalview Version 2 - a multiple sequence alignment editor and analysis workbench. Bioinformatics 25: 1189-1191.
65. Wesolowski, J., and Paumet, F. (2010) SNARE motif: a common motif used by pathogens to manipulate membrane fusion. Virulence 1: 319-324.
66. Wylie, F., Heimann, K., Le, T.L., Brown, D., Rabnott, G., and Stow, J.L. (1999) GAIP, a Gα(i-3)-binding protein, is associated with Golgi-derived vesicles and protein trafficking. Am J Physiol 276: C497-C506.
67. Xu, L., Shen, X.H., Bryan, A., Banga, S., Swanson, M.S., and Luo, Z.Q. (2010) Inhibition of host vacuolar H+-ATPase activity by a Legionella pneumophila effector. PLoS Pathog 6: e1000822. doi:1000810.1001371/journal.ppat.1000822.
68. Xu, Y., Martin, S., James, D.E., and Hong, W.J. (2002) GS15 forms a SNARE complex with syntaxin 5, GS28, and Ykt6 and is implicated in traffic in the early cisternae of the Golgi apparatus. Mol Biol Cell 13: 3493-3507.
69. Zhang, F.L., and Casey, P.J. (1996) Protein prenylation: molecular mechanisms and functional consequences. Annu Rev Biochem 65: 241-269.
70. Zhang, T., and Hong, W.J. (2001) Ykt6 forms a SNARE complex with syntaxin 5, GS28, and Bet1 and participates in a late stage in endoplasmic reticulum-Golgi transport. J Biol Chem 276: 27480-27487.
71. Zwilling, D., Cypionka, A., Pohl, W.H., Fasshauer, D., Walla, P.J., Wahl, M.C., and Jahn, R. (2007) Early endosomal SNAREs form a structurally conserved SNARE complex and fuse liposomes with multiple topologies. EMBO J 26: 9-18.