Common Themes in the Design and Function of Bacterial Effectors

Cell Host and Microbe

Volumn 5, Issue 6, 2009, Pages 571-579

  Galán, Jorge E ^a  

^a YALE UNIVERSITY SCHOOL OF MEDICINE   (United States)

Author keywords

CELLBIO; MICROBIO

Indexed keywords

BACTERIAL EFFECTOR PROTEIN; BACTERIAL PROTEIN; CELL MEMBRANE PROTEIN; RHO GUANINE NUCLEOTIDE BINDING PROTEIN; UNCLASSIFIED DRUG;

BACTERIAL INFECTION; BACTERIAL VIRULENCE; CELL FUNCTION; EVOLUTIONARY HOMOLOGY; HOST CELL; NONHUMAN; PATHOGENESIS; PRIORITY JOURNAL; PROTEIN FUNCTION; PROTEIN LOCALIZATION; PROTEIN MODIFICATION; PROTEIN SECRETION; PROTEIN TARGETING; REGULATORY MECHANISM; REVIEW; SIGNAL TRANSDUCTION; SPECIES DIFFERENCE; TYPE III SECRETION SYSTEM;

BACTERIA; BACTERIAL PHYSIOLOGICAL PHENOMENA; BACTERIAL PROTEINS; HOST-PATHOGEN INTERACTIONS; MODELS, MOLECULAR; VIRULENCE FACTORS;

BACTERIA (MICROORGANISMS);

EID: 67649400561     PISSN: 19313128     EISSN: None     Source Type: Journal    
DOI: 10.1016/j.chom.2009.04.008     Document Type: Review

References (67)

1. Alouf J.E. Bacterial protein toxins: an overview. Methods Mol. Biol. 145 (2000) 1-26
2. Alto N.M., Shao F., Lazar C.S., Brost R.L., Chua G., Mattoo S., McMahon S.A., Ghosh P., Hughes T.R., Boone C., and Dixon J.E. Identification of a bacterial type III effector family with G protein mimicry functions. Cell 124 (2006) 133-145
3. Angot A., Peeters N., Lechner E., Vailleau F., Baud C., Gentzbittel L., Sartorel E., Genschik P., Boucher C., and Genin S. Ralstonia solanacearum requires F-box-like domain-containing type III effectors to promote disease on several host plants. Proc. Natl. Acad. Sci. USA 103 (2006) 14620-14625
4. Angot A., Vergunst A., Genin S., and Peeters N. Exploitation of eukaryotic ubiquitin signaling pathways by effectors translocated by bacterial type III and type IV secretion systems. PLoS Pathog. 3 (2007) e3
5. Barbieri J.T. Pseudomonas aeruginosa exoenzyme S, a bifunctional type-III secreted cytotoxin. Int. J. Med. Microbiol. 290 (2000) 381-387
6. Benabdillah R., Mota L.J., Lützelschwab S., Demoinet E., and Cornelis G.R. Identification of a nuclear targeting signal in YopM from Yersinia spp. Microb. Pathog. 36 (2004) 247-261
7. Bliska J.B., and Black D.S. Inhibition of the Fc receptor-mediated oxidative burst in macrophages by the Yersinia pseudotuberculosis tyrosine phosphatase. Infect. Immun. 63 (1995) 681-685
8. Buchwald G., Friebel A., Galán J.E., Hardt W.D., Wittinghofer A., and Scheffzek K. Structural basis for the reversible activation of a Rho protein by the bacterial toxin SopE. EMBO J. 21 (2002) 3286-3295
9. Cheng H.C., Skehan B.M., Campellone K.G., Leong J.M., and Rosen M.K. Structural mechanism of WASP activation by the enterohaemorrhagic E. coli effector EspF(U). Nature 454 (2008) 1009-1013
10. Christie P.J., Atmakuri K., Krishnamoorthy V., Jakubowski S., and Cascales E. Biogenesis, architecture, and function of bacterial type IV secretion systems. Annu. Rev. Microbiol. 59 (2005) 451-485
11. Collazo C.M., and Galán J.E. Requirement of exported proteins for secretion through the invasion-associated Type III system in Salmonella typhimurium. Infect. Immun. 64 (1996) 3524-3531
12. Deng W., Li Y., Hardwidge P.R., Frey E.A., Pfuetzner R.A., Lee S., Gruenheid S., Strynakda N.C., Puente J.L., and Finlay B.B. Regulation of type III secretion hierarchy of translocators and effectors in attaching and effacing bacterial pathogens. Infect. Immun. 73 (2005) 2135-2146
13. Diao J., Zhang Y., Huibregtse J.M., Zhou D., and Chen J. Crystal structure of SopA, a Salmonella effector protein mimicking a eukaryotic ubiquitin ligase. Nat. Struct. Mol. Biol. 15 (2008) 65-70
14. Drecktrah D., Knodler L.A., Galbraith K., and Steele-Mortimer O. The Salmonella SPI1 effector SopB stimulates nitric oxide production long after invasion. Cell. Microbiol. 7 (2005) 105-113
15. Filloux A., Hachani A., and Bleves S. The bacterial type VI secretion machine: yet another player for protein transport across membranes. Microbiology 154 (2008) 1570-1583
16. Fu Y., and Galán J.E. The Salmonella spp. protein tyrosine phosphatase SptP is translocated into host cells and disrupts the host-cell cytoskeleton. Mol. Microbiol. 27 (1998) 359-368
17. Fu Y., and Galán J.E. A salmonella protein antagonizes Rac-1 and Cdc42 to mediate host-cell recovery after bacterial invasion. Nature 401 (1999) 293-297
18. Galán J.E. Salmonella interaction with host cells: type III secretion at work. Annu. Rev. Cell Dev. Biol. 17 (2001) 53-86
19. Galán J.E., and Wolf-Watz H. Protein delivery into eukaryotic cells by type III secretion machines. Nature 444 (2006) 567-573
20. Galyov E.E., Hakansson S., Forsberg A., and Wolf-Watz H. A secreted protein kinase of Yersinia pseudotuberculosis is an indispensable virulence determinant. Nature 361 (1993) 730-732
21. Glickman M.H., and Ciechanover A. The ubiquitin-proteasome proteolytic pathway: destruction for the sake of construction. Physiol. Rev. 82 (2002) 373-428
22. Goehring U.M., Schmidt G., Pederson K.J., Aktories K., and Barbieri J.T. The N-terminal domain of Pseudomonas aeruginosa exoenzyme S is a GTPase-activating protein for Rho GTPases. J. Biol. Chem. 274 (1999) 36369-36372
23. Guan K.L., and Dixon J.E. Protein tyrosine phosphatase activity of an essential virulence determinant in Yersinia. Science 249 (1990) 553-556
24. Hardt W.-D., Chen L.-M., Schuebel K.E., Bustelo X.R., and Galán J.E. Salmonella typhimurium encodes an activator of Rho GTPases that induces membrane ruffling and nuclear responses in host cells. Cell 93 (1998) 815-826
25. Hardt W.-D., Urlaub H., and Galán J.E. A substrate of the centisome 63 type III protein secretion system of Salmonella typhimurium is encoded by a cryptic bacteriophage. Proc. Natl. Acad. Sci. USA 95 (1998) 2574-2579
26. Hernandez L.D., Hueffer K., Wenk M.R., and Galán J.E. Salmonella modulates vesicular traffic by altering phosphoinositide metabolism. Science 18 (2004) 1805-1807
27. Hotson A., Chosed R., Shu H., Orth K., and Mudgett M.B. Xanthomonas type III effector XopD targets SUMO-conjugated proteins in planta. Mol. Microbiol. 50 (2003) 377-389
28. Izard T., Tran Van Nhieu G., and Bois P.R. Shigella applies molecular mimicry to subvert vinculin and invade host cells. J. Cell Biol. 175 (2006) 465-475
29. Janjusevic R., Abramovitch R.B., Martin G.B., and Stebbins C.E. A bacterial inhibitor of host programmed cell death defenses is an E3 ubiquitin ligase. Science 311 (2006) 222-226
30. Jones R.M., Wu H., Wentworth C., Luo C., Collier-Hyams L., and Neish A.S. Salmonella AvrA coordinates suppression of host immune and apoptotic defenses via JNK pathway blockade. Cell Host Microbe 3 (2008) 233-244
31. Kaniga K., Uralil J., Bliska J.B., and Galán J.E. A secreted protein tyrosine phosphatase with modular effector domains in the bacterial pathogen Salmonella typhimurium. Mol. Microbiol. 21 (1996) 633-641
32. Kim D.W., Lenzen G., Page A.L., Legrain P., Sansonetti P.J., and Parsot C. The Shigella flexneri effector OspG interferes with innate immune responses by targeting ubiquitin-conjugating enzymes. Proc. Natl. Acad. Sci. USA 102 (2005) 14046-14051
33. Kubori T., and Galán J.E. Temporal regulation of salmonella virulence effector function by proteasome-dependent protein degradation. Cell 115 (2003) 333-342
34. Li H., Xu H., Zhou Y., Zhang J., Long C., Li S., Chen S., Zhou J.M., and Shao F. The phosphothreonine lyase activity of a bacterial type III effector family. Science 315 (2007) 1000-1003
35. Mallo G.V., Espina M., Smith A.C., Terebiznik M.R., Alemán A., Finlay B.B., Rameh L.E., Grinstein S., and Brumell J.H. SopB promotes phosphatidylinositol 3-phosphate formation on Salmonella vacuoles by recruiting Rab5 and Vps34. J. Cell Biol. 182 (2008) 741-752
36. Marcus S.L., Knodler L.A., and Finlay B.B. Salmonella enterica serovar Typhimurium effector SigD/SopB is membrane-associated and ubiquitinated inside host cells. Cell. Microbiol. 4 (2002) 435-446
37. Miao E.A., Scherer C.A., Tsolis R.M., Kingsley R.A., Adams L.G., Baumler A.J., and Miller S.I. Salmonella typhimurium leucine-rich repeat proteins are targeted to the SPI1 and SPI2 type III secretion systems. Mol. Microbiol. 34 (1999) 850-864
38. Montagna L.G., Ivanov M.I., and Bliska J.B. Identification of residues in the N-terminal domain of the Yersinia tyrosine phosphatase that are critical for substrate recognition. J. Biol. Chem. 276 (2001) 5005-5011
39. Mukherjee S., Keitany G., Li Y., Wang Y., Ball H.L., Goldsmith E.J., and Orth K. Yersinia YopJ acetylates and inhibits kinase activation by blocking phosphorylation. Science 312 (2006) 1211-1214
40. Murli S., Watson R.O., and Galán J.E. Role of tyrosine kinases and the tyrosine phosphatase SptP in the interaction of Salmonella with host cells. Cell. Microbiol. 3 (2001) 795-810
41. Navarro L., Koller A., Nordfelth R., Wolf-Watz H., Taylor S., and Dixon J.E. Identification of a molecular target for the Yersinia protein kinase A. Mol. Cell 26 (2007) 465-477
42. Nimchuk Z., Marois E., Kjemtrup S., Leister R.T., Katagiri F., and Dangl J.L. Eukaryotic fatty acylation drives plasma membrane targeting and enhances function of several type III effector proteins from Pseudomonas syringae. Cell 101 (2000) 353-363
43. Ohlson M.B., Huang Z., Alto N.M., Blanc M.P., Dixon J.E., Chai J., and Miller S.I. Structure and function of Salmonella SifA indicate that its interactions with SKIP, SseJ, and RhoA family GTPases induce endosomal tubulation. Cell Host Microbe 4 (2008) 434-446
44. Orth K. Function of the Yersinia effector YopJ. Curr. Opin. Microbiol. 5 (2002) 38-43
45. Patel J.C., and Galán J.E. Differential activation and function of Rho GTPases during Salmonella-host cell interactions. J. Cell Biol. 175 (2006) 453-463
46. Patel J.C., Hueffer K., Lam T.T., and Galán J.E. Diversification of a Salmonella effector function by ubiquitin-dependent differential localization. Cell (2009) in press
47. Quezada C.M., Hicks S.W., Galán J.E., and Stebbins C.E. A family of Salmonella virulence factors functions as a distinct class of autoregulated E3 ubiquitin ligases. Proc. Natl. Acad. Sci. USA 106 (2009) 4864-4869
48. Rabin S.D., Veesenmeyer J.L., Bieging K.T., and Hauser A.R. A C-terminal domain targets the Pseudomonas aeruginosa cytotoxin ExoU to the plasma membrane of host cells. Infect. Immun. 74 (2006) 2552-2561
49. Rohde J.R., Breitkreutz A., Chenal A., Sansonetti P.J., and Parsot C. Type III secretion effectors of the IpaH family are E3 ubiquitin ligases. Cell Host Microbe 1 (2007) 77-83
50. Rytkönen A., Poh J., Garmendia J., Boyle C., Thompson A., Liu M., Freemont P., Hinton J.C., and Holden D.W. SseL, a Salmonella deubiquitinase required for macrophage killing and virulence. Proc. Natl. Acad. Sci. USA 104 (2007) 3502-3507
51. Schlumberger M.C., Käppeli R., Wetter M., Müller A.J., Misselwitz B., Dilling S., Kremer M., and Hardt W.D. Two newly identified SipA domains (F1, F2) steer effector protein localization and contribute to Salmonella host cell manipulation. Mol. Microbiol. 65 (2007) 741-760
52. Singer A.U., Rohde J.R., Lam R., Skarina T., Kagan O., Dileo R., Chirgadze N.Y., Cuff M.E., Joachimiak A., Tyers M., et al. Structure of the Shigella T3SS effector IpaH defines a new class of E3 ubiquitin ligases. Nat. Struct. Mol. Biol. 15 (2008) 1293-1301
53. Sorg J.A., Blaylock B., and Schneewind O. Secretion signal recognition by YscN, the Yersinia type III secretion ATPase. Proc. Natl. Acad. Sci. USA 103 (2006) 16490-16495
54. Stebbins C.E., and Galán J.E. Modulation of host signaling by a bacterial mimic: structure of the Salmonella effector SptP bound to Rac1. Mol. Cell 6 (2000) 1449-1460
55. Stebbins C.E., and Galán J.E. Structural mimicry in bacterial virulence. Nature 412 (2001) 701-705
56. Steele-Mortimer O., Knodler L.A., Marcus S.L., Scheid M.P., Goh B., Pfeifer C.G., Duronio V., and Finlay B.B. Activation of Akt/protein kinase B in epithelial cells by the Salmonella typhimurium effector sigD. J. Biol. Chem. 275 (2000) 37718-37724
57. Steele-Mortimer O., Brumell J.H., Knodler L.A., Meresse S., Lopez A., and Finlay B.B. The invasion-associated type III secretion system of Salmonella enterica serovar Typhimurium is necessary for intracellular proliferation and vacuole biogenesis in epithelial cells. Cell. Microbiol. 4 (2002) 43-54
58. Stender S., Friebel A., Linder S., Rohde M., Mirold S., and Hardt W.D. Identification of SopE2 from Salmonella typhimurium, a conserved guanine nucleotide exchange factor for Cdc42 of the host cell. Mol. Microbiol. 36 (2000) 1206-1211
59. Szurek B., Rossier O., Hause G., and Bonas U. Type III-dependent translocation of the Xanthomonas AvrBs3 protein into the plant cell. Mol. Microbiol. 46 (2002) 13-23
60. Tam V.C., Serruto D., Dziejman M., Brieher W., and Mekalanos J.J. A type III secretion system in Vibrio cholerae translocates a formin/spire hybrid-like actin nucleator to promote intestinal colonization. Cell Host Microbe 1 (2007) 95-107
61. Trosky J.E., Liverman A.D., and Orth K. Yersinia outer proteins: Yops. Cell Microbiol. 10 (2008) 557-565
62. Von Pawel-Rammingen U., Telepnev M.V., Schmidt G., Aktories K., Wolf-Watz H., and Rosqvist R. GAP activity of the Yersinia YopE cytotoxin specifically targets the Rho pathway: a mechanism for disruption of actin microfilament structure. Mol. Microbiol. 36 (2000) 737-748
63. Wang D., Roe A.J., McAteer S., Shipston M.J., and Gally D.L. Hierarchal type III secretion of translocators and effectors from Escherichia coli O157:H7 requires the carboxy terminus of SepL that binds to Tir. Mol. Microbiol. 69 (2008) 1499-1512
64. Yarbrough M.L., Li Y., Kinch L.N., Grishin N.V., Ball H.L., and Orth K. AMPylation of Rho GTPases by Vibrio VopS disrupts effector binding and downstream signaling. Science 323 (2009) 269-272
65. Zhang Y., and Barbieri J.T. A leucine-rich motif targets Pseudomonas aeruginosa ExoS within mammalian cells. Infect. Immun. 73 (2005) 7938-7945
66. Zhou D., Chen L.M., Hernandez L., Shears S.B., and Galán J.E. A Salmonella inositol polyphosphatase acts in conjunction with other bacterial effectors to promote host cell actin cytoskeleton rearrangements and bacterial internalization. Mol. Microbiol. 39 (2001) 248-259
67. Zhu Y., Li H., Hu L., Wang J., Zhou Y., Pang Z., Liu L., and Shao F. Structure of a Shigella effector reveals a new class of ubiquitin ligases. Nat. Struct. Mol. Biol. 15 (2008) 1302-1308