Bacterial effector interplay: A new way to view effector function

Trends in Microbiology

Volumn 20, Issue 5, 2012, Pages 214-219

  Shames, Stephanie R ^a,b,c   Finlay, B Brett ^a,b  

^a UNIVERSITY OF BRITISH COLUMBIA   (Canada)

^b UNIVERSITY OF BRITISH COLUMBIA   (Canada)

^c YALE UNIVERSITY SCHOOL OF MEDICINE   (United States)

Author keywords

Bacterial pathogen; Effector; Effector interplay; Regulation; Type III secretion system; Type IV secretion system

Indexed keywords

BACTERIAL EFFECTOR PROTEIN; BACTERIAL PROTEIN; UNCLASSIFIED DRUG; VIRULENCE FACTOR;

BACTERIAL COLONIZATION; BACTERIAL SECRETION SYSTEM; BACTERIAL VIRULENCE; GRAM NEGATIVE BACTERIUM; HOST; HOST CELL; NONHUMAN; PRIORITY JOURNAL; PROTEIN FUNCTION; REVIEW;

BACTERIA; BACTERIAL INFECTIONS; BACTERIAL PROTEINS; HOST-PATHOGEN INTERACTIONS; HUMANS; VIRULENCE FACTORS;

BACTERIA (MICROORGANISMS); NEGIBACTERIA;

EID: 84860587543     PISSN: 0966842X     EISSN: 18784380     Source Type: Journal    
DOI: 10.1016/j.tim.2012.02.007     Document Type: Review

References (62)

1. Cambronne E.D., Roy C.R. Recognition and delivery of effector proteins into eukaryotic cells by bacterial secretion systems. Traffic 2006, 7:929-939.
2. Backert S., Meyer T.F. Type IV secretion systems and their effectors in bacterial pathogenesis. Curr. Opin. Microbiol. 2006, 9:207-217.
3. Coburn B., et al. Type III secretion systems and disease. Clin. Microbiol. Rev. 2007, 20:535-549.
4. Kumar Y., Valdivia R.H. Leading a sheltered life: intracellular pathogens and maintenance of vacuolar compartments. Cell Host Microbe 2009, 5:593-601.
5. Ernst J.D. Bacterial inhibition of phagocytosis. Cell Microbiol. 2000, 2:379-386.
6. Dean P., et al. Potent diarrheagenic mechanism mediated by the cooperative action of three enteropathogenic Escherichia coli-injected effector proteins. Proc. Natl. Acad. Sci. U.S.A. 2006, 103:1876-1881.
7. Nougayrede J.P., Donnenberg M.S. Enteropathogenic Escherichia coli EspF is targeted to mitochondria and is required to initiate the mitochondrial death pathway. Cell. Microbiol. 2004, 6:1097-1111.
8. Quitard S., et al. The enteropathogenic Escherichia coli EspF effector molecule inhibits PI-3 kinase-mediated uptake independently of mitochondrial targeting. Cell. Microbiol. 2006, 8:972-981.
9. Holmes A., et al. The EspF effector, a bacterial pathogen's Swiss army knife. Infect. Immun. 2010, 78:4445-4453.
10. Kenny B., et al. Enteropathogenic E. coli (EPEC) transfers its receptor for intimate adherence into mammalian cells. Cell 1997, 91:511-520.
11. Jorgensen I., et al. The Chlamydia protease CPAF regulates host and bacterial proteins to maintain pathogen vacuole integrity and promote virulence. Cell Host Microbe 2011, 10:21-32.
12. Chen D., et al. Secretion of the chlamydial virulence factor CPAF requires the Sec-dependent pathway. Microbiology 2010, 156:3031-3040.
13. Hicks S.W., Galan J.E. Hijacking the host ubiquitin pathway: structural strategies of bacterial E3 ubiquitin ligases. Curr. Opin. Microbiol. 2010, 13:41-46.
14. Tzfira T., et al. Involvement of targeted proteolysis in plant genetic transformation by Agrobacterium. Nature 2004, 431:87-92.
15. Magori S., Citovsky V. Agrobacterium counteracts host-induced degradation of its effector F-box protein. Sci. Signal. 2011, 4. pii:ra69.
16. Ninio S., Roy C.R. Effector proteins translocated by Legionella pneumophila: strength in numbers. Trends Microbiol. 2007, 15:372-380.
17. Kubori T., et al. Legionella metaeffector exploits host proteasome to temporally regulate cognate effector. PLoS Pathog. 2010, 6:e1001216.
18. Muller M.P., et al. The Legionella effector protein DrrA AMPylates the membrane traffic regulator Rab1b. Science 2010, 329:946-949.
19. Tan Y., Luo Z.Q. Legionella pneumophila SidD is a deAMPylase that modifies Rab1. Nature 2011, 475:506-509.
20. Mukherjee S., et al. Modulation of Rab GTPase function by a protein phosphocholine transferase. Nature 2011, 477:103-106.
21. Neunuebel M.R., et al. De-AMPylation of the small GTPase Rab1 by the pathogen Legionella pneumophila. Science 2011, 333:453-456.
22. Fu Y., Galan J.E. A salmonella protein antagonizes Rac-1 and Cdc42 to mediate host-cell recovery after bacterial invasion. Nature 1999, 401:293-297.
23. Cain R.J., et al. Deciphering interplay between Salmonella invasion effectors. PLoS Pathog. 2008, 4:e1000037.
24. Ohlson M.B., et al. Structure and function of Salmonella SifA indicate that its interactions with SKIP, SseJ, and RhoA family GTPases induce endosomal tubulation. Cell Host Microbe 2008, 4:434-446.
25. Pulliainen A.T., Dehio C. Bartonella henselae: subversion of vascular endothelial cell functions by translocated bacterial effector proteins. Int. J. Biochem. Cell Biol. 2009, 41:507-510.
26. Truttmann M.C., et al. Combined action of the type IV secretion effector proteins BepC and BepF promotes invasome formation of Bartonella henselae on endothelial and epithelial cells. Cell. Microbiol. 2010, 13:284-299.
27. Crane J.K., et al. Host cell death due to enteropathogenic Escherichia coli has features of apoptosis. Infect. Immun. 1999, 67:2575-2584.
28. Ma C., et al. Citrobacter rodentium infection causes both mitochondrial dysfunction and intestinal epithelial barrier disruption in vivo: role of mitochondrial associated protein (Map). Cell. Microbiol. 2006, 8:1669-1686.
29. Shames S.R., et al. The type III system-secreted effector EspZ localizes to host mitochondria and interacts with the translocase of inner mitochondrial membrane 17B. Infect. Immun. 2011, 79:4784-4790.
30. Hemrajani C., et al. NleH effectors interact with Bax inhibitor-1 to block apoptosis during enteropathogenic Escherichia coli infection. Proc. Natl. Acad. Sci. U.S.A. 2010, 107:3129-3134.
31. Kurushima J., et al. EspJ effector in enterohemorrhagic E. coli translocates into host mitochondria via an atypical mitochondrial targeting signal. Microbiol. Immunol. 2010, 54:371-379.
32. Shames S.R., Finlay B.B. Breaking the stereotype: virulence factor-mediated protection of host cells in bacterial pathogenesis. PLoS Pathog. 2010, 6:e1001057.
33. Dean P., et al. The bacterial effectors EspG and EspG2 induce a destructive calpain activity that is kept in check by the co-delivered Tir effector. Cell. Microbiol. 2010, 12:1308-1321.
34. Mills E., et al. Real-time analysis of effector translocation by the type III secretion system of enteropathogenic Escherichia coli. Cell Host Microbe 2008, 3:104-113.
35. Selyunin A.S., et al. The assembly of a GTPase-kinase signalling complex by a bacterial catalytic scaffold. Nature 2011, 469:107-111.
36. Shaw R.K., et al. Enteropathogenic Escherichia coli type III effectors EspG and EspG2 disrupt the microtubule network of intestinal epithelial cells. Infect. Immun. 2005, 73:4385-4390.
37. Christian J., et al. Cleavage of the NF-κB family protein p65/RelA by the chlamydial protease-like activity factor (CPAF) impairs proinflammatory signaling in cells infected with Chlamydiae. J. Biol. Chem. 2010, 285:41320-41327.
38. Dong F., et al. Cleavage of host keratin 8 by a Chlamydia-secreted protease. Infect. Immun. 2004, 72:3863-3868.
39. Pirbhai M., et al. The secreted protease factor CPAF is responsible for degrading pro-apoptotic BH3-only proteins in Chlamydia trachomatis-infected cells. J. Biol. Chem. 2006, 281:31495-31501.
40. Savijoki K., et al. Proteomic analysis of Chlamydia pneumoniae-infected HL cells reveals extensive degradation of cytoskeletal proteins. FEMS Immunol. Med. Microbiol. 2008, 54:375-384.
41. Sun J., Schoborg R.V. The host adherens junction molecule nectin-1 is degraded by chlamydial protease-like activity factor (CPAF) in Chlamydia trachomatis-infected genital epithelial cells. Microbes Infect. 2009, 11:12-19.
42. Shames S.R., et al. The pathogenic Escherichia coli type III secreted protease NleC degrades the host acetyltransferase p300. Cell. Microbiol. 2011, 13:1542-1557.
43. Sham H.P., et al. The attaching/effacing bacterial effector NleC suppresses epithelial inflammatory responses by inhibiting NF-κB and p38-MAP Kinase activation. Infect. Immun. 2011, 79:3552-3562.
44. Pearson J.S., et al. A type III effector protease NleC from enteropathogenic Escherichia coli targets NF-κB for degradation. Mol. Microbiol. 2011, 80:219-230.
45. Muehlen S., et al. Proteasome-independent degradation of canonical NFkappaB complex components by the NleC protein of pathogenic E.coli. J. Biol. Chem. 2011, 286:5100-5107.
46. Yen H., et al. NleC, a type III secretion protease, compromises NF-κB activation by targeting p65/RelA. PLoS Pathog. 2010, 6:e1001231.
47. Baruch K., et al. Metalloprotease type III effectors that specifically cleave JNK and NF-κB. EMBO J. 2011, 30:221-231.
48. Samba-Louaka A., et al. Bacterial cyclomodulin Cif blocks the host cell cycle by stabilizing the cyclin-dependent kinase inhibitors p21 and p27. Cell. Microbiol. 2008, 10:2496-2508.
49. Shao F., et al. Biochemical characterization of the Yersinia YopT protease: cleavage site and recognition elements in Rho GTPases. Proc. Natl. Acad. Sci. U.S.A. 2003, 100:904-909.
50. Arena E.T., et al. The deubiquitinase activity of the Salmonella Pathogenicity Island 2 effector, SseL, prevents accumulation of cellular lipid droplets. Infect. Immun. 2011, 79:4392-4400.
51. Rytkonen A., et al. SseL, a Salmonella deubiquitinase required for macrophage killing and virulence. Proc. Natl. Acad. Sci. U.S.A. 2007, 104:3502-3507.
52. Kim J.G., et al. XopD SUMO protease affects host transcription, promotes pathogen growth, and delays symptom development in Xanthomonas-infected tomato leaves. Plant Cell 2008, 20:1915-1929.
53. Canonne J., et al. The Xanthomonas type III effector XopD targets the Arabidopsis transcription factor MYB30 to suppress plant defense. Plant Cell 2011, 23:3498-3511.
54. Lopez-Solanilla E., et al. HopPtoN is a Pseudomonas syringae Hrp (type III secretion system) cysteine protease effector that suppresses pathogen-induced necrosis associated with both compatible and incompatible plant interactions. Mol. Microbiol. 2004, 54:353-365.
55. Coux O., et al. Structure and functions of the 20S and 26S proteasomes. Annu. Rev. Biochem. 1996, 65:801-847.
56. Collins C.A., Brown E.J. Cytosol as battleground: ubiquitin as a weapon for both host and pathogen. Trends Cell Biol. 2010, 20:205-213.
57. Zhang Y., et al. The inflammation-associated Salmonella SopA is a HECT-like E3 ubiquitin ligase. Mol. Microbiol. 2006, 62:786-793.
58. Piscatelli H., et al. The EHEC type III effector NleL is an E3 ubiquitin ligase that modulates pedestal formation. PLoS ONE 2011, 6:e19331.
59. Ashida H., et al. A bacterial E3 ubiquitin ligase IpaH9.8 targets NEMO/IKKγ to dampen the host NF-κB-mediated inflammatory response. Nat. Cell Biol. 2010, 12:66-69.
60. Gohre V., et al. Plant pattern-recognition receptor FLS2 is directed for degradation by the bacterial ubiquitin ligase AvrPtoB. Curr. Biol. 2008, 18:1824-1832.
61. Zaltsman A., et al. Agrobacterium induces expression of a host F-box protein required for tumorigenicity. Cell Host Microbe 2010, 7:197-209.
62. Nagai T., et al. Targeting of enteropathogenic Escherichia coli EspF to host mitochondria is essential for bacterial pathogenesis: critical role of the 16th leucine residue in EspF. J. Biol. Chem. 2005, 280:2998-3011.