Bacterial effector-involved temporal and spatial regulation by hijack of the host ubiquitin pathway

Frontiers in Microbiology

Volumn 2, Issue JULY, 2011, Pages

  Kubori, Tomoko ^a,b   Nagai, Hiroki ^a  

^a OSAKA UNIVERSITY   (Japan)

^b OSAKA UNIVERSITY   (Japan)

Author keywords

Bacterial pathogen; Degradation; Effector; Metaeffector; Proteasome; Secretion system; Temporal regulation; Ubiquitin

Indexed keywords

BACTERIA (MICROORGANISMS); EUKARYOTA;

EID: 84858067652     PISSN: None     EISSN: 1664302X     Source Type: Journal    
DOI: 10.3389/fmicb.2011.00145     Document Type: Review

References (89)

1. Abramovitch, R. B., Janjusevic, R., Stebbins, C. E., and Martin, G. B. (2006). Type III effector AvrPtoB requires intrinsic E3 ubiquitin ligase activity to suppress plant cell death and immunity. Proc. Natl. Acad. Sci. U.S.A. 103, 2851-2856.
2. Abramovitch, R. B., Kim, Y. J., Chen, S., Dickman, M. B., and Martin, G. B. (2003). Pseudomonas type III effector AvrPtoB induces plant disease susceptibility by inhibition of host programmed cell death. EMBO J. 22, 60-69.
3. Angot, A., Vergunst, A., Genin, S., and Peeters, N. (2007). Exploitation of eukaryotic ubiquitin signaling pathways by effectors translocated by bacterial type III and type IV secretion systems. PLoS Pathog. 3, e3. doi: 10.1371/journal.ppat. 0030003
4. Ardley, H. C., and Robinson, P. A. (2005). E3 ubiquitin ligases. Essays Biochem. 41, 15-30.
5. Ashida, H., Kim, M., SchmidtSupprian, M., Ma, A., Ogawa, M., and Sasakawa, C. (2010). A bacterial E3 ubiquitin ligase IpaH9.8 targets NEMO/IKKgamma to dampen the host NF-kappaBmediated inflammatory response. Nat. Cell Biol. 12, 66-73; sup. 61-69.
6. Backert, S., and Meyer, T. F. (2006). Type IV secretion systems and their effectors in bacterial pathogenesis. Curr. Opin. Microbiol. 9, 207-217.
7. Bakshi, C. S., Singh, V. P., Wood, M. W., Jones, P. W., Wallis, T. S., and Galyov, E. E. (2000). Identification of SopE2, a Salmonella secreted protein which is highly homologous to SopE and involved in bacterial invasion of epithelial cells. J. Bacteriol. 182, 2341-2344.
8. Buchwald, G., Friebel, A., Galan, J. E., Hardt, W. D., Wittinghofer, A., and Scheffzek, K. (2002). Structural basis for the reversible activation of a Rho protein by the bacterial toxin SopE. EMBO J. 21, 3286-3295.
9. Chen, C., Banga, S., Mertens, K., Weber, M. M.,Gorbaslieva,I.,Tan,Y.,Luo,Z. Q., and Samuel, J. E. (2010). Largescale identification and translocation of type IV secretion substrates by Coxiella burnetii. Proc. Natl. Acad. Sci. U.S.A. 107, 21755-21760.
10. Chen, L. M., Hobbie, S., and Galan, J. E. (1996). Requirement of CDC42 for Salmonella-induced cytoskeletal and nuclear responses. Science 274, 2115-2118.
11. Christie, P. J., Atmakuri, K., Krishnamoorthy, V., Jakubowski, S., and Cascales, E. (2005). Biogenesis, architecture, and function of bacterial type IV secretion systems. Annu. Rev. Microbiol. 59, 451-485.
12. Dai, S., Sarmiere, P. D., Wiggan, O., Bamburg, J. R., and Zhou, D. (2004). Efficient Salmonella entry requires activity cycles of host ADF and cofilin. Cell. Microbiol. 6, 459-471.
13. Diao, J., Zhang, Y., Huibregtse, J. M., Zhou, D., and Chen, J. (2008). Crystal structure of SopA, a Salmonella effector protein mimicking a eukaryotic ubiquitin ligase. Nat. Struct. Mol. Biol. 15, 65-70.
14. Ensminger, A. W., and Isberg, R. R. (2009). Legionella pneumophila Dot/Icm translocated substrates: a sum of parts. Curr. Opin. Microbiol. 12, 67-73.
15. Fields, B. S. (1996). The molecular ecology of Legionellae. Trends Microbiol. 4, 286-290.
16. Fields, B. S., Benson, R. F., and Besser, R. E. (2002). Legionella and Legionnaires' disease: 25 years of investigation. Clin. Microbiol. Rev. 15, 506-526.
17. Filloux, A., Hachani, A., and Bleves, S. (2008). The bacterial type VI secretion machine: yet another player for protein transport across membranes. Microbiology 154, 1570-1583.
18. Finlay, B. B., Ruschkowski, S., and Dedhar, S. (1991). Cytoskeletal rearrangements accompanying Salmonella entry into epithelial cells. J. Cell Sci. 99(Pt 2), 283-296.
19. Francis, C. L., Ryan, T. A., Jones, B. D., Smith, S. J., and Falkow, S. (1993). Ruffles induced by Salmonella and other stimuli direct macropinocytosis of bacteria. Nature 364, 639-642.
20. Franco, I. S., Shuman, H. A., and Charpentier, X. (2009). The perplexing functions and surprising origins of Legionella pneumophila type IV secretion effectors. Cell. Microbiol. 11, 1435-1443.
21. Fu, Y., and Galan, J. E. (1998). The Salmonella typhimurium tyrosine phosphatase SptP is translocated into host cells and disrupts the actin cytoskeleton. Mol. Microbiol. 27, 359-368.
22. Fu, Y., and Galan, J. E. (1999). A Salmonella protein antagonizes Rac-1 and Cdc42 to mediate host-cell recovery after bacterial invasion. Nature 401, 293-297.
23. Galan, J. E. (2001). Salmonella interactions with host cells: type III secretion at work. Annu.Rev.CellDev. Biol. 17, 53-86.
24. Galan, J. E., and Wolf-Watz, H. (2006). Protein delivery into eukaryotic cells by type III secretion machines. Nature 444, 567-573.
25. Gimenez-Ibanez, S., Hann, D. R., Ntoukakis,V., Petutschnig, E., Lipka, V., and Rathjen, J. P. (2009). AvrPtoB targets the LysM receptor kinase CERK1 to promote bacterial virulence on plants. Curr. Biol. 19, 423-429.
26. Ginocchio, C., Pace, J., and Galan, J. E. (1992). Identification and molecular characterization of a Salmonella typhimurium gene involved in triggering the internalization of Salmonellae into cultured epithelial cells. Proc. Natl. Acad. Sci. U.S.A. 89, 5976-5980.
27. Gohre, V., Spallek, T., Haweker, H., Mersmann, S., Mentzel, T., Boller, T., de Torres, M., Mansfield, J. W., and Robatzek, S. (2008). Plant patternrecognition receptor FLS2 is directed for degradation by the bacterial ubiquitin ligase AvrPtoB. Curr. Biol. 18, 1824-1832.
28. Goldstein, G., Scheid, M., Hammerling, U., Schlesinger, D. H., Niall, H. D., and Boyse, E. A. (1975). Isolation of a polypeptide that has lymphocyte-differentiating properties and is probably represented universally in living cells. Proc. Natl. Acad. Sci. U.S.A. 72, 11-15.
29. Haglund, K., and Dikic, I. (2005). Ubiquitylation and cell signaling. EMBO J. 24, 3353-3359.
30. Hardt, W. D., Chen, L. M., Schuebel, K. E., Bustelo, X. R., and Galan, J. E. (1998). S. typhimurium encodes an activator of Rho GTPases that induces membrane ruffling and nuclear responses in host cells. Cell 93, 815-826.
31. Hayward, R. D., and Koronakis, V. (1999). Direct nucleation and bundling of actin by the SipC protein of invasive Salmonella. EMBO J. 18, 4926-4934.
32. Hernandez, L. D., Hueffer, K., Wenk, M. R., and Galan, J. E. (2004). Salmonella modulates vesicular traffic by altering phosphoinositide metabolism. Science 304, 1805-1807.
33. Hershko, A., and Ciechanover, A. (1998). The ubiquitin system. Annu. Rev. Biochem. 67, 425-479.
34. Hershko, A., Heller, H., Elias, S., and Ciechanover, A. (1983). Components of ubiquitin-protein ligase system. Resolution, affinity purification, and role in protein breakdown. J. Biol. Chem. 258, 8206-8214.
35. Hicks, S. W., and Galan, J. E. (2010). Hijacking the host ubiquitin pathway: structural strategies of bacterial E3 ubiquitin ligases. Curr. Opin. Microbiol. 13, 41-46.
36. Higashide, W., Dai, S., Hombs, V. P., and Zhou, D. (2002). Involvement of SipA in modulating actin dynamics during Salmonella invasion into cultured epithelial cells. Cell. Microbiol. 4, 357-365.
37. Horwitz, M. A. (1983). Formation of a novel phagosome by the Legionnaires' disease bacterium (Legionella pneumophila) in human monocytes. J. Exp. Med. 158, 1319-1331.
38. Hubber, A., and Roy, C. R. (2010). Modulation of host cell function by Legionella pneumophila type IV effectors. Annu.Rev.CellDev.Biol. 26, 261-283.
39. Ingmundson, A., Delprato, A., Lambright, D. G., and Roy, C. R. (2007). Legionella pneumophila proteins that regulate Rab1 membrane cycling. Nature 450, 365-369.
40. Isberg, R. R., O'Connor, T. J., and Heidtman, M. (2009). The Legionella pneumophila replication vacuole: making a cosy niche inside host cells. Nat. Rev. Microbiol. 7, 13-24.
41. Janjusevic, R., Abramovitch, R. B., Martin, G. B., and Stebbins, C. E. (2006). A bacterial inhibitor of host programmed cell death defenses is an E3 ubiquitin ligase. Science 311, 222-226.
42. Knodler, L. A., Winfree, S., Drecktrah, D., Ireland, R., and Steele-Mortimer, O. (2009). Ubiquitination of the bacterial inositol phosphatase, SopB, regulates its biological activity at the plasma membrane. Cell. Microbiol. 11, 1652-1670.
43. Kubori, T., and Galan, J. E. (2003). Temporal regulation of Salmonella virulence effector function by proteasome-dependent protein degradation. Cell 115, 333-342.
44. Kubori, T., Hyakutake, A., and Nagai, H. (2008). Legionella translocates an E3 ubiquitin ligase that has multiple U-boxes with distinct functions. Mol. Microbiol. 67, 1307-1319.
45. Kubori, T., Shinzawa, N., Kanuka, H., and Nagai, H. (2010). Legionella metaeffector exploits host proteasome to temporally regulate cognate effector. PLoS Pathog. 6, e1001216. doi: 10.1371/journal.ppat.1001216
46. Laguna, R. K., Creasey, E. A., Li, Z., Valtz, N., and Isberg, R. R. (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.
47. Levin, I., Eakin, C., Blanc, M. P., Klevit, R. E., Miller, S. I., and Brzovic, P. S. (2010). Identification of an unconventional E3 binding surface on the UbcH5 ~ Ub conjugate recognized by a pathogenic bacterial E3 ligase. Proc. Natl. Acad. Sci. U.S.A. 107, 2848-2853.
48. Lilic, M., Galkin, V. E., Orlova, A., VanLoock, M. S., Egelman, E. H., and Stebbins, C. E. (2003). Salmonella SipA polymerizes actin by stapling filaments with nonglobular protein arms. Science 301, 1918-1921.
49. Lin, D. Y., Diao, J., Zhou, D., and Chen, J. (2011). Biochemical and structural studies of a HECT-like ubiquitin ligase from Escherichia coli O157:H7. J. Biol. Chem. 286, 441-449.
50. Luo, Z. Q., and Isberg, R. R. (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.
51. 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.
52. Machner, M. P., and Isberg, R. R. (2007). A bifunctional bacterial protein links GDI displacement to Rab1 activation. Science 318, 974-977.
53. McGhie, E. J., Hayward, R. D., and Koronakis, V. (2004). Control of actin turnover by a Salmonella invasion protein. Mol. Cell 13, 497-510.
54. 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.
55. Ninio, S., and Roy, C. R. (2007). Effector proteins translocated by Legionella pneumophila: strength in numbers. Trends Microbiol. 15, 372-380.
56. Nomura, K., Debroy, S., Lee, Y. H., Pumplin, N., Jones, J., and He, S. Y. (2006). A bacterial virulence protein suppresses host innate immunity to cause plant disease. Science 313, 220-223.
57. Patel, J. C., and Galan, J. E. (2006). Differential activation and function of Rho GTPases during Salmonellahost cell interactions. J. Cell Biol. 175, 453-463.
58. Patel, J. C., Hueffer, K., Lam, T. T., and Galan, J. E. (2009). Diversification of a Salmonella virulence protein function by ubiquitin-dependent differential localization. Cell 137, 283294.
59. Patel, J. C., Rossanese, O. W., and Galan, J. E. (2005). The functional interface between Salmonella and its host cell: opportunities for therapeutic intervention. Trends Pharmacol. Sci. 26, 564-570.
60. Pavletich, N. P. (2002). Structural biology of ubiquitin-protein ligases. Harvey Lect. 98, 65-102.
61. Price, C. T., and Abu Kwaik, Y. (2010). Exploitation of host polyubiquitination machinery through molecular mimicry by eukaryotic-like bacterial F-box effectors. Front. Microbio. 1:122. doi: 10.3389/fmicb.2010.00122
62. Pukatzki, S., McAuley, S. B., and Miyata, S. T. (2009). The type VI secretion system: translocation of effectors and effector-domains. Curr. Opin. Microbiol. 12, 11-17.
63. Quezada,C. M.,Hicks,S.W.,Galan,J. E., and Stebbins, C. E. (2009). A family of Salmonella virulence factors functions as a distinct class of autoregulated E3 ubiquitin ligases. Proc. Natl. Acad. Sci. U.S.A. 106, 4864-4869.
64. Rohde, J. R., Breitkreutz, A., Chenal, A., Sansonetti, P. J., and Parsot, C. (2007). Type III secretion effectors of the IpaH family are E3 ubiquitin ligases. Cell Host Microbe 1, 77-83.
65. Rosebrock, T. R., Zeng, L., Brady, J. J., Abramovitch, R. B., Xiao, F., and Martin, G. B. (2007). A bacterial E3 ubiquitin ligase targets a host protein kinase to disrupt plant immunity. Nature 448, 370-374.
66. Rudolph, M. G., Weise, C., Mirold, S., Hillenbrand, B., Bader, B., Wittinghofer, A., and Hardt, W. D. (1999). Biochemical analysis of SopE from Salmonella typhimurium, a highly efficient guanosine nucleotide exchange factor for RhoGTPases. J. Biol. Chem. 274, 30501-30509.
67. Rytkonen,A.,and Holden,D. W. (2007). Bacterial interference of ubiquitination and deubiquitination. Cell Host Microbe 1, 13-22.
68. Scherer, C. A., Cooper, E., and Miller, S. I. (2000). The Salmonella type III secretion translocon protein SspC is inserted into the epithelial cell plasma membrane upon infection. Mol. Microbiol. 37, 1133-1145.
69. Schulman, B. A., Carrano, A. C., Jeffrey, P. D., Bowen, Z., Kinnucan, E. R., Finnin, M. S., Elledge, S. J., Harper, J. W., Pagano, M., and Pavletich, N. P. (2000). Insights into SCF ubiquitin ligases from the structure of the Skp1-Skp2 complex. Nature 408, 381-386.
70. Segal, G., Purcell, M., and Shuman, H. A. (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.
71. Shin, S., and Roy, C. R. (2008). Host cell processes that influence the intracellular survival of Legionella pneumophila. Cell. Microbiol. 10, 12091220.
72. Singer, A. U., Rohde, J. R., Lam, R., Skarina, T., Kagan, O., Dileo, R., Chirgadze, N. Y., Cuff, M. E., Joachimiak, A., Tyers, M., Sansonetti, P. J., Parsot, C., and Savchenko, A. (2008). Structure of the Shigella T3SS effector IpaH defines a new class of E3 ubiquitin ligases. Nat. Struct. Mol. Biol. 15, 1293-1301.
73. Stebbins, C. E., and Galan, J. E. (2000). Modulation of host signaling by a bacterial mimic: structure of the Salmonella effector SptP bound to Rac1. Mol. Cell 6, 1449-1460.
74. Stebbins, C. E., and Galan, J. E. (2001). Maintenance of an unfolded polypeptide by a cognate chaperone in bacterial type III secretion. Nature 414, 77-81.
75. Steele-Mortimer, O., Knodler, L. A., Marcus, S. L., Scheid, M. P., Goh, B., Pfeifer, C. G., Duronio, V., and Finlay, B. B. (2000). Activation of Akt/protein kinase B in epithelial cellsbytheSalmonella typhimurium effector sigD. J. Biol. Chem. 275, 37718-37724.
76. Stender, S., Friebel,A., Linder, S., Rohde, M., Mirold, S., and Hardt, W. D. (2000). Identification of SopE2 from Salmonella typhimurium,aconserved guanine nucleotide exchange factor for Cdc42 of the host cell. Mol. Microbiol. 36, 1206-1221.
77. Swanson,M. S.,and Isberg,R. R. (1995). Association of Legionella pneumophila with the macrophage endoplasmic reticulum. Infect. Immun. 63, 3609-3620.
78. Takeuchi, A. (1967). Electron microscope studies of experimental Salmonella infection. I. Penetration into the intestinal epithelium by Salmonella typhimurium. Am. J. Pathol. 50, 109-136.
79. Thrower, J. S., Hoffman, L., Rechsteiner, M., and Pickart, C. M. (2000). Recognition of the polyubiquitin proteolytic signal. EMBO J. 19, 94-102.
80. Tilney, L. G., Harb, O. S., Connelly, P. S., Robinson, C. G., and Roy, C. R. (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.
81. Vogel, J. P., Andrews, H. L., Wong, S. K., and Isberg,R. R. (1998). Conjugative transfer by the virulence system of Legionella pneumophila. Science 279, 873-876.
82. Waterman, S. R., and Holden, D. W. (2003). Functions and effectors of the Salmonella pathogenicity island 2 type III secretion system. Cell. Microbiol. 5, 501-511.
83. Wu, B., Skarina, T., Yee, A., Jobin, M. C., Dileo, R., Semesi, A., Fares, C., Lemak, A., Coombes, B. K., Arrowsmith, C. H., Singer, A. U., Savchenko, A. (2010). NleG Type 3 effectors from enterohaemorrhagic Escherichia coli are U-box E3 ubiquitin ligases. PLoS Pathog. 6, e1000960. doi: 10.1371/journal.ppat. 1000960
84. Zhang, M., Windheim, M., Roe, S. M., Peggie, M., Cohen, P., Prodromou, C., and Pearl, L. H. (2005). Chaperoned ubiquitylation crystal structures of the CHIP U box E3 ubiquitin ligase and a CHIPUbc13-Uev1a complex. Mol. Cell 20, 525-538.
85. Zhang, Y., Higashide, W. M., McCormick, B. A., Chen, J., and Zhou, D. (2006). The inflammationassociated Salmonella SopA is a HECT-like E3 ubiquitin ligase. Mol. Microbiol. 62, 786-793.
86. Zhou, D., Chen, L. M., Hernandez, L., Shears, S. B., and Galan, J. E. (2001). A Salmonella inositol polyphosphatase acts in conjunction with other bacterial effectors to promote host cell actin cytoskeleton rearrangements and bacterial internalization. Mol. Microbiol. 39, 248259.
87. Zhou, D., Mooseker, M. S., and Galan, J. E. (1999). Role of the S. typhimurium actin-binding protein SipA in bacterial internalization. Science 283, 2092-2095.
88. Zhu, W., Banga, S., Tan, Y., Zheng, C., Stephenson, R., Gately, J., and Luo, Z. Q. (2011). Comprehensive identification of protein substrates of the Dot/Icm type IV transporter of Legionella pneumophila. PLoS ONE 6, e17638. doi: 10.1371/journal.pone.0017638
89. Zhu, Y., Li, H., Hu, L., Wang, J., Zhou, Y., Pang, Z., Liu, L., and Shao, F. (2008). Structure of a Shigella effector reveals a new class of ubiquitin ligases. Nat. Struct. Mol. Biol. 15, 1302-1308.