Modulation of NF-κB signalling by microbial pathogens

Nature Reviews Microbiology

Volumn 9, Issue 4, 2011, Pages 291-306

  Rahman, Masmudur M ^a   McFadden, Grant ^a  

^a UNIVERSITY OF FLORIDA COLLEGE OF MEDICINE   (United States)

Author keywords

[No Author keywords available]

Indexed keywords

CELL RECEPTOR; GLYCINE DEHYDROGENASE (DECARBOXYLATING); I KAPPA B; IMMUNOGLOBULIN ENHANCER BINDING PROTEIN; M PROTEIN; MICRORNA; NONSTRUCTURAL PROTEIN 5A; PROTEIN P100; PROTEIN P105; SYNAPTOTAGMIN I; TRANSCRIPTION FACTOR REL; TRANSCRIPTION FACTOR RELA; TRANSCRIPTION FACTOR RELB;

BACTERIAL VIRULENCE; IMMUNE RESPONSE; IMMUNOMODULATION; NONHUMAN; PRIORITY JOURNAL; PROTEIN MODIFICATION; REVIEW; SIGNAL TRANSDUCTION; VIRUS VIRULENCE;

ADAPTIVE IMMUNITY; ANIMALS; BACTERIA; BACTERIAL INFECTIONS; IMMUNITY, INNATE; MICE; NF-KAPPA B; SIGNAL TRANSDUCTION; VIRUS DISEASES; VIRUSES;

EID: 79952773453     PISSN: 17401526     EISSN: None     Source Type: Journal    
DOI: 10.1038/nrmicro2539     Document Type: Review

References (167)

1. Hoffmann, A. & Baltimore, D. Circuitry of nuclear factor κB signaling. Immunol. Rev. 210, 171-186 (2006).
2. Vallabhapurapu, S. & Karin, M. Regulation and function of NF κB transcription factors in the immune system. Annu. Rev. Immunol. 27, 693-733 (2009).
3. Hayden, M.S. & Ghosh, S. Shared principles in NF κB signaling. Cell 132, 344-362 (2008).
4. Finlay, B.B. & McFadden, G. Anti-immunology: evasion of the host immune system by bacterial and viral pathogens. Cell 124, 767-782 (2006). (Pubitemid 43261451)
5. Bowie, A.G. & Unterholzner, L. Viral evasion and subversion of pattern-recognition receptor signalling. Nature Rev. Immunol. 8, 911-922 (2008).
6. Ghosh, S. & Hayden, M.S. New regulators of NF κB in inflammation. Nature Rev. Immunol. 8, 837-848 (2008).
7. Wan, F. & Lenardo, M.J. The nuclear signaling of NF κB: current knowledge, new insights, and future perspectives. Cell Res. 20, 24-33 (2010).
8. Solt, L.A. & May, M.J. The IκB kinase complex: master regulator of NF κB signaling. Immunol. Res. 42, 3-18 (2008).
9. Hacker, H. & Karin, M. Regulation and function of IKK and IKK-related kinases. Sci. STKE 2006, re13 (2006).
10. Chen, Z.J. Ubiquitin signalling in the NF κB pathway. Nature Cell Biol. 7, 758-765 (2005).
11. Pham, A.M. & tenOever, B.R. The IKK kinases: operators of antiviral signaling. Viruses 2, 55-72 (2010).
12. Peters, R.T. & Maniatis, T. A new family of IKK-related kinases may function as IκB kinase kinases. Biochim. Biophys. Acta 1471, M57-M62 (2001). (Pubitemid 32146545)
13. Gilmore, T.D. Introduction to NF κB: players, pathways, perspectives. Oncogene 25, 6680-6684 (2006).
14. Basak, S. & Hoffmann, A. Crosstalk via the NF κB signaling system. Cytokine Growth Factor Rev. 19, 187-197 (2008).
15. Wang, X.W., Tan, N.S., Ho, B. & Ding, J.L. Evidence for the ancient origin of the NF κB/IκB cascade: its archaic role in pathogen infection and immunity. Proc. Natl Acad. Sci. USA 103, 4204-4209 (2006).
16. Kawai, T. & Akira, S. The roles of TLRs, RLRs and NLRs in pathogen recognition. Int. Immunol. 21, 317-337 (2009).
17. Tato, C.M. & Hunter, C.A. Host-pathogen interactions: subversion and utilization of the NF κ B pathway during infection. Infect. Immun. 70, 3311-3317 (2002). (Pubitemid 34665964)
18. Wang, J. et al. NF κB RelA subunit is crucial for early IFN- β expression and resistance to RNA virus replication. J.Immunol. 185, 1720-1729 (2010).
19. Hiscott, J., Nguyen, T.L., Arguello, M., Nakhaei, P. & Paz, S. Manipulation of the nuclear factor- κB pathway and the innate immune response by viruses. Oncogene 25, 6844-6867 (2006). (Pubitemid 44657856)
20. de Oliveira, D.E., Ballon, G. & Cesarman, E. NF κB signaling modulation by EBV and KSHV. Trends Microbiol. 18, 248-257 (2010).
21. Santoro, M.G., Rossi, A. & Amici C. NF κB and virus infection: who controls whom. EMBO J 22, 2552-2560 (2003). (Pubitemid 36712353)
22. Mulhern, O., Harrington, B. & Bowie, A.G. Modulation of innate immune signalling pathways by viral proteins. Adv. Exp. Med. Biol. 666, 49-63 (2009).
23. Rahman, M.M. & McFadden, G. Modulation of tumor necrosis factor by microbial pathogens. PLoS Pathog. 2, e4 (2006).
24. Unterholzner, L. & Bowie, A.G. The interplay between viruses and innate immune signaling: recent insights and therapeutic opportunities. Biochem. Pharmacol. 75, 589-602 (2008).
25. Sugrue, R.J. Interactions between respiratory syncytial virus and the host cell: opportunities for antivirus strategies? Expert Rev. Mol. Med. 8, 1-17 (2006). (Pubitemid 44336391)
26. Yoboua, F., Martel, A., Duval, A., Mukawera, E. & Grandvaux, N. Respiratory syncytial virus-mediated NF κB p65 phosphorylation at serine 536 is dependent on RIGI, TRAF6, and IKKβ. J.Virol. 84, 7267-7277 (2010).
27. Choudhary, S., Boldogh, S., Garofalo, R., Jamaluddin,M. & Brasier, A.R. Respiratory syncytial virus influences NF κB dependent gene expression through a novel pathway involving MAP3K14/NIK expression and nuclear complex formation with NF κB2. J.Virol. 79, 8948-8959 (2005). (Pubitemid 40934806)
28. Kurt-Jones, E.A. et al. Pattern recognition receptors TLR4 and CD14 mediate response to respiratory syncytial virus. Nature Immunol. 1, 398-401 (2000).
29. Reimers, K., Buchholz, K. & Werchau, H. Respiratory syncytial virus M2-1 protein induces the activation of nuclear factor kappa B. Virology 331, 260-268 (2005). (Pubitemid 40075454)
30. Demarchi, F., Gutierrez, M.I. & Giacca, M. Human immunodeficiency virus type1 Tat protein activates transcription factor NF κB through the cellular interferon-inducible, double-stranded RNA-dependent protein kinase, PKR. J.Virol. 73, 7080-7086 (1999). (Pubitemid 29327899)
31. Furia, B. et al. Enhancement of nuclear factor- κB acetylation by coactivator p300 and HIV-1 Tat proteins. J.Biol. Chem. 277, 4973-4980 (2002). (Pubitemid 34968536)
32. Varin, A. et al. Exogenous Nef protein activates NF κB, AP-1, and c-Jun N-terminal kinase and stimulates HIV transcription in promonocytic cells. Role in AIDS pathogenesis. J.Biol. Chem. 278, 2219-2227 (2003). (Pubitemid 36801289)
33. Varin, A. et al. Synthetic Vpr protein activates activator protein-1, c-Jun N-terminal kinase, and NF κB and stimulates HIV-1 transcription in promonocytic cells and primary macrophages. J.Biol. Chem. 280, 42557-42567 (2005). (Pubitemid 43049213)
34. Higuchi, M. & Fujii, M. Distinct functions of HTLV-1 Tax1 from HTLV-2 Tax2 contribute key roles to viral pathogenesis. Retrovirology 6, 117 (2009).
35. Sun, S.C. & Yamaoka, S. Activation of NF κB by HTLVI and implications for cell transformation. Oncogene 24, 5952-5964 (2005). (Pubitemid 43086113)
36. Harhaj, E.W. et al. Somatic mutagenesis studies of NF κB signaling in human Tcells: evidence for an essential role of IKKγ in NF κB activation by T-cell costimulatory signals and HTLV-I Tax protein. Oncogene 19, 1448-1456 (2000). (Pubitemid 30171176)
37. Wu, X. & Sun, S.C. Retroviral oncoprotein Tax deregulates NF κB by activating Tak1 and mediating the physical association of Tak1-IKK. EMBO Rep. 8, 510-515 (2007). (Pubitemid 46696523)
38. Huang, J., Ren, T., Guan, H., Jiang, Y. & Cheng, H. HTLV-1 Tax is a critical lipid raft modulator that hijacks IκB kinases to the microdomains for persistent activation of NF κB. J.Biol. Chem. 284, 6208-6217 (2009).
39. Xiao, G. et al. Retroviral oncoprotein Tax induces processing of NF κB2/p100 in Tcells: evidence for the involvement of IKKα. EMBO J. 20, 6805-6815 (2001). (Pubitemid 33134210)
40. Wang, J. et al. BFV activates the NF κB pathway through its transactivator (BTas) to enhance viral transcription. Virology 400, 215-223 (2010).
41. Gaudreault, E., Fiola, S., Olivier, M. & Gosselin, J. Epstein-Barr virus induces MCP-1 secretion by human monocytes via TLR2. J.Virol. 81, 8016-8024 (2007). (Pubitemid 47101487)
42. Mosialos, G. et al. The Epstein-Barr virus transforming protein LMP1 engages signaling proteins for the tumor necrosis factor receptor family. Cell 80, 389-399 (1995).
43. Paine, E., Scheinman, R.I., Baldwin, A.S. Jr & Raab-Traub, N. Expression of LMP1 in epithelial cells leads to the activation of a select subset of NF κB/Rel family proteins. J.Virol. 69, 4572-4576 (1995).
44. Huen, D.S., Henderson, S.A., Croom-Carter, D. & Rowe, M. The Epstein-Barr virus latent membrane protein-1 (LMP1) mediates activation of NF κB and cell surface phenotype via two effector regions in its carboxy-terminal cytoplasmic domain. Oncogene 10, 549-560 (1995).
45. Wu, L., Nakano, H. & Wu, Z. The C-terminal activating region 2 of the Epstein-Barr virus-encoded latent membrane protein 1 activates NF κB through TRAF6 and TAK1. J.Biol. Chem. 281, 2162-2169 (2006). (Pubitemid 43845806)
46. Luftig, M. et al. Epstein-Barr virus latent infection membrane protein 1 TRAF-binding site induces NIK/IKKα-dependent noncanonical NF κB activation. Proc. Natl Acad. Sci. USA 101, 141-146 (2004). (Pubitemid 38084217)
47. Kung, C.P. & Raab-Traub, N. Epstein-Barr virus latent membrane protein 1 modulates distinctive NF-κB pathways through C-terminus-activating region 1 to regulate epidermal growth factor receptor expression. J.Virol. 84, 6605-6614 (2010).
48. Bagneris, C. et al. Crystal structure of a vFlip-IKKγ complex: insights into viral activation of the IKK signalosome. Mol. Cell 30, 620-631 (2008). (Pubitemid 351755065)
49. Matta, H. et al. A nuclear role for Kaposi's sarcoma-associated herpesvirus-encoded K13 protein in gene regulation. Oncogene 27, 5243-5253 (2008).
50. Ye, F.C. et al. Kaposi's sarcoma-associated herpesvirus latent gene vFLIP inhibits viral lytic replication through NF κB-mediated suppression of the AP-1 pathway: a novel mechanism of virus control of latency. J.Virol. 82, 4235-4249 (2008).
51. Punj, V. et al. Kaposi's sarcoma-associated herpesvirus-encoded viral FLICE inhibitory protein (vFLIP) K13 suppresses CXCR4 expression by upregulating miR-146a. Oncogene 29, 1835-1844 (2010).
52. Chung, Y.H. et al. STP-C, an oncoprotein of herpesvirus saimiri augments the activation of NF κB through ubiquitination of TRAF6. J.Biochem. Mol. Biol. 40, 341-348 (2007).
53. Cho, I.R. et al. Activation of non-canonical NF κB pathway mediated by STP-A11, an oncoprotein of Herpesvirus saimiri. Virology 359, 37-45 (2007).
54. de Jong, S.J., Albrecht, J.C., Schmidt, M., Muller-Fleckenstein, I. & Biesinger, B. Activation of noncanonical NF κB signaling by the oncoprotein Tio. J.Biol. Chem. 285, 16495-16503 (2010).
55. Dong, X. et al. Murine gamma-herpesvirus 68 hijacks MAVS and IKKβ to initiate lytic replication. PLoS Pathog. 6, e1001001 (2010).
56. Brown, H.J. et al. NF κB inhibits gammaherpesvirus lytic replication. J.Virol. 77, 8532-8540 (2003).
57. Zhang, X., Zhang, H. & Ye, L. Effects of hepatitis B virus X protein on the development of liver cancer. J.Lab. Clin. Med. 147, 58-66 (2006). (Pubitemid 43188997)
58. Bouchard, M.J. & Schneider, R.J. The enigmatic X gene of hepatitis B virus. J.Virol. 78, 12725-12734 (2004). (Pubitemid 39507781)
59. Bui-Nguyen, T.M. et al. NF κB signaling mediates the induction of MTA1 by hepatitis B virus transactivator protein HBx. Oncogene 29, 1179-1189 (2010).
60. Chang, S., Dolganiuc, A. & Szabo, G. Toll-like receptors 1 and 6 are involved in TLR2mediated macrophage activation by hepatitis C virus core and NS3 proteins. J.Leukoc. Biol. 82, 479-487 (2007). (Pubitemid 47367138)
61. Rodriguez, C.I. et al. African swine fever virus IAP-like protein induces the activation of nuclear factor κB. J.Virol. 76, 3936-3942 (2002). (Pubitemid 34250558)
62. Sciortino, M.T. et al. Involvement of HVEM receptor in activation of nuclear factor κB by herpes simplex virus1 glycoprotein D. Cell. Microbiol. 10, 2297-2311 (2008).
63. Liu, X., Fitzgerald, K., Kurt-Jones, E., Finberg, R. & Knipe, D.M. Herpesvirus tegument protein activates NF κB signaling through the TRAF6 adaptor protein. Proc. Natl Acad. Sci. USA 105, 11335-11339 (2008).
64. Hargett, D., Rice, S. & Bachenheimer, S.L. Herpes simplex virus type1 ICP27dependent activation of NF κB. J.Virol. 80, 10565-10578 (2006). (Pubitemid 44628903)
65. van Lint, A.L. et al. Herpes simplex virus immediate-early ICP0 protein inhibits Toll-like receptor 2dependent inflammatory responses and NF κB signaling. J.Virol. 84, 10802-10811 (2010).
66. Kim, J.C. et al. HSV-1 ICP27 suppresses NF κB activity by stabilizing IκBα. FEBS Lett. 582, 2371-2376 (2008).
67. Li, K. et al. Immune evasion by hepatitis C virus NS3/4A protease-mediated cleavage of the Toll-like receptor 3 adaptor protein TRIF. Proc. Natl Acad. Sci. USA 102, 2992-2997 (2005). (Pubitemid 40299904)
68. Li, X.D., Sun, L., Seth, R.B., Pineda, G. & Chen, Z.J. Hepatitis C virus protease NS3/4A cleaves mitochondrial antiviral signaling protein off the mitochondria to evade innate immunity. Proc. Natl Acad. Sci. USA 102, 17717-17722 (2005). (Pubitemid 41803563)
69. Abe, T. et al. Hepatitis C virus nonstructural protein5A modulates the Toll-like receptor-MyD88-dependent signaling pathway in macrophage cell lines. J.Virol. 81, 8953-8966 (2007). (Pubitemid 47311439)
70. Zahoor, M.A. et al. Bovine viral diarrhea virus non-structural protein 5A interacts with NIK- and IKKβ-binding protein. J.Gen. Virol. 91, 1939-1948 (2010).
71. Choi, S.H. et al. Hepatitis C virus nonstructural 5B protein regulates tumor necrosis factor alpha signaling through effects on cellular IκB kinase. Mol. Cell Biol. 26, 3048-3059 (2006).
72. Joo, M. et al. Hepatitis C virus core protein suppresses NF κB activation and cyclooxygenase-2 expression by direct interaction with IκB kinase β. J.Virol. 79, 7648-7657 (2005). (Pubitemid 40756798)
73. Fang, X. et al. The membrane protein of SARS-CoV suppresses NF κB activation. J.Med. Virol. 79, 1431-1439 (2007). (Pubitemid 47328730)
74. Valentine, R. et al. Epstein-Barr virus-encoded EBNA1 inhibits the canonical NF κB pathway in carcinoma cells by inhibiting IKK phosphorylation. Mol. Cancer 9, 1 (2010).
75. Mohamed, M.R. & McFadden, G. NFκB inhibitors: strategies from poxviruses. Cell Cycle 8, 3125-3132 (2009).
76. Harte, M.T. et al. The poxvirus protein A52R targets Toll-like receptor signaling complexes to suppress host defense. J.Exp. Med. 197, 343-351 (2003). (Pubitemid 36184241)
77. Stack, J. et al. Vaccinia virus protein A46R targets multiple TolLlike-interleukin-1 receptor adaptors and contributes to virulence. J.Exp. Med. 201, 1007-1018 (2005). (Pubitemid 40524469)
78. Graham, S.C. et al. Vaccinia virus proteins A52 and B14 Share a BcL2like fold but have evolved to inhibit NF κB rather than apoptosis. PLoS Pathog. 4, e1000128 (2008).
79. DiPerna, G. et al. Poxvirus protein N1L targets the I κB kinase complex, inhibits signaling to NF κB by the tumor necrosis factor superfamily of receptors, and inhibits NF κB and IRF3 signaling by Toll-like receptors. J.Biol. Chem. 279, 36570-36578 (2004).
80. Chen, R.A., Ryzhakov, G., Cooray, S., Randow, F. & Smith, G.L. Inhibition of IκB kinase by vaccinia virus virulence factor B14. PLoS Pathog. 4, e22 (2008).
81. McCoy, L.E., Fahy, A.S., Chen, R.A. & Smith, G.L. Mutations in modified virus Ankara protein 183 render it a non-functional counterpart of B14, an inhibitor of nuclear factor κB activation. J.Gen. Virol. 91, 2216-2220 (2010).
82. Meng, X. et al. Vaccinia virus K1L and C7L inhibit antiviral activities induced by typeI interferons. J.Virol. 83, 10627-10636 (2009).
83. Myskiw, C., Arsenio, J., van Bruggen, R., Deschambault, Y. & Cao, J. Vaccinia virus E3 suppresses expression of diverse cytokines through inhibition of the PKR, NF κB, and IRF3 pathways. J.Virol. 83, 6757-6768 (2009).
84. Murao, L.E. & Shisler, J.L The MCV MC159 protein inhibits late, but not early, events of TNF α-induced NF κB activation. Virology 340, 255-264 (2005). (Pubitemid 41317499)
85. Challa, S., Woelfel, M., Guildford, M., Moquin, D. & Chan, F.K. Viral cell death inhibitor MC159 enhances innate immunity against vaccinia virus infection. J.Virol. 84, 10467-10476 (2010).
86. Nichols, D.B. & Shisler, J.L. Poxvirus MC160 protein utilizes multiple mechanisms to inhibit NF κB activation mediated via components of the tumor necrosis factor receptor 1 signal transduction pathway. J.Virol. 83, 3162-3174 (2009).
87. Diel, D.G., Delhon, G., Luo, S., Flores, E.F. & Rock, D.L. A novel inhibitor of the NF κB signaling pathway encoded by the parapoxvirus orf virus. J.Virol. 84, 3962-3973 (2010).
88. Tait, S.W., Reid, E.B., Greaves, D.R., Wileman, T.E. & Powell, P.P. Mechanism of inactivation of NF κB by a viral homologue of IκBα. Signal-induced release of IκBα results in binding of the viral homologue to NF κB. J.Biol. Chem. 275, 34656-34664 (2000).
89. Zaragoza, C. et al. Viral protease cleavage of inhibitor of κBα triggers host cell apoptosis. Proc. Natl Acad. Sci. USA 103, 19051-19056 (2006). (Pubitemid 350002826)
90. Doceul, V. et al. The Npro product of classical swine fever virus interacts with IκBα, the NF κB inhibitor. J.Gen. Virol. 89, 1881-1889 (2008).
91. Bour, S., Perrin, C., Akari, H. & Strebel, K. The human immunodeficiency virus type1 Vpu protein inhibits NF κB activation by interfering with βTrCP-mediated degradation of IκB. J.Biol. Chem. 276, 15920-15928 (2001).
92. Akari, H., Bour, S., Kao, S., Adachi, A. & Strebel, K. The human immunodeficiency virus type1 accessory protein Vpu induces apoptosis by suppressing the nuclear factor κB-dependent expression of antiapoptotic factors. J.Exp. Med. 194, 1299-1311 (2001). (Pubitemid 33055048)
93. Graff, J.W., Ettayebi, K. & Hardy, M.E. Rotavirus NSP1 inhibits NFκB activation by inducing proteasome-dependent degradation of β-TrCP: a novel mechanism of IFN antagonism. PLoS Pathog. 5, e1000280 (2009).
94. Yim, H.C., Li, J.C., Lau, J.S. & Lau, A.S. HIV-1 Tat dysregulation of lipopolysaccharide-induced cytokine responses: microbial interactions in HIV infection. AIDS 23, 1473-1484 (2009).
95. Neznanov, N. et al. Proteolytic cleavage of the p65-RelA subunit of NF κB during poliovirus infection. J.Biol. Chem. 280, 24153-24158 (2005). (Pubitemid 40884903)
96. Chang, S.J. et al. Poxvirus host range protein CP77 contains an F-box-like domain that is necessary to suppress NF κB activation by tumor necrosis factor alpha but is independent of its host range function. J.Virol. 83, 4140-4152 (2009).
97. Mohamed, M.R. et al. Proteomic screening of variola virus reveals a unique NF κB inhibitor that is highly conserved among pathogenic orthopoxviruses. Proc. Natl Acad. Sci. USA 106, 9045-9050 (2009).
98. Rahman, M.M., Mohamed, M.R., Kim, M., Smallwood, S. & McFadden, G. Co-regulation of NF κB and inflammasome-mediated inflammatory responses by myxoma virus pyrin domain-containing protein M013. PLoS Pathog. 5, e1000635 (2009).
99. Taylor, S.L., Frias-Staheli, N., Garcia-Sastre, A. & Schmaljohn, C.S. Hantaan virus nucleocapsid protein binds to importin α proteins and inhibits tumor necrosis factor α-induced activation of nuclear factorκB. J.Virol. 83, 1271-1279 (2009).
100. Jiao, J., Guan, H., Lippa, A.M. & Ricciardi, R.P. The N terminus of adenovirus type12 E1A inhibits major histocompatibility complex class I expression by preventing phosphorylation of NF κB p65 Ser276 through direct binding. J.Virol. 84, 7668-7674 (2010).
101. Guan, H., Jiao, J. & Ricciardi, R.P. Tumorigenic adenovirus type12 E1A inhibits phosphorylation of NF κB by PKAc, causing loss of DNA binding and transactivation. J.Virol. 82, 40-48 (2008). (Pubitemid 350309121)
102. Taylor, R.T. & Bresnahan, W.A. Human cytomegalovirus IE86 attenuates virus- and tumor necrosis factor α-induced NFκB-dependent gene expression. J.Virol. 80, 10763-10771 (2006). (Pubitemid 44628922)
103. Jarvis, M.A. et al. Human cytomegalovirus attenuates interleukin-1β and tumor necrosis factor α proinflammatory signaling by inhibition of NF κB activation. J.Virol. 80, 5588-5598 (2006).
104. Montag, C., Wagner, J., Gruska, I. & Hagemeier, C. Human cytomegalovirus blocks tumor necrosis factorα- and interleukin-1β- mediated NF κB signaling. J.Virol. 80, 11686-11698 (2006). (Pubitemid 44788882)
105. Nachtwey, J. & Spencer, J.V. HCMV IL10 suppresses cytokine expression in monocytes through inhibition of nuclear factor- κB. Viral Immunol. 21, 477-482 (2008).
106. Hansberger, M.W. et al. IκB kinase subunits α and γ are required for activation of NF κB and induction of apoptosis by mammalian reovirus. J.Virol. 81, 1360-1371 (2007). (Pubitemid 46167857)
107. Clarke, P., Debiasi, R.L., Meintzer, S.M., Robinson, B.A. & Tyler, K.L. Inhibition of NF κB activity and cFLIP expression contribute to viral-induced apoptosis. Apoptosis 10, 513-524 (2005). (Pubitemid 40896658)
108. Wilson, J.R., de Sessions, P.F., Leon, M.A. & Scholle,F. West Nile virus nonstructural protein 1 inhibits TLR3 signal transduction. J.Virol. 82, 8262-8271 (2008).
109. Lei, X. et al. Regulation of NF κB inhibitor IκBα and viral replication by a KSHV microRNA. Nature Cell Biol. 12, 193-199 (2010).
110. Bhavsar, A.P., Guttman, J.A. & Finlay, B.B. Manipulation of host-cell pathways by bacterial pathogens. Nature 449, 827-834 (2007). (Pubitemid 47598623)
111. Naumann, M. Control of the NF κB inhibitor IκBα in pathogen infection. Biochem. Soc. Trans. 35, 267-269 (2007).
112. Kvitko, B.H. et al. Deletions in the repertoire of Pseudomonas syringae pv. tomato DC3000 typeIII secretion effector genes reveal functional overlap among effectors. PLoS Pathog. 5, e1000388 (2009).
113. Tseng, T.T., Tyler, B.M. & Setubal, J.C. Protein secretion systems in bacterial-host associations, and their description in the Gene Ontology. BMC Microbiol. 9 (Suppl. 1), S2 (2009).
114. Viboud, G.I. & Bliska, J.B. Yersinia outer proteins: role in modulation of host cell signaling responses and pathogenesis. Annu. Rev. Microbiol. 59, 69-89 (2005). (Pubitemid 41507424)
115. Zhou, H. et al. Yersinia virulence factor YopJ acts as a deubiquitinase to inhibit NF κB activation. J.Exp. Med. 202, 1327-1332 (2005). (Pubitemid 41668735)
116. Sweet, C.R., Conlon, J., Golenbock, D.T., Goguen, J. & Silverman, N. YopJ targets TRAF proteins to inhibit TLR-mediated NF κB, MAPK and IRF3 signal transduction. Cell. Microbiol. 9, 2700-2715 (2007). (Pubitemid 47500520)
117. Mukherjee, S. et al. Yersinia YopJ acetylates and inhibits kinase activation by blocking phosphorylation. Science 312, 1211-1214 (2006). (Pubitemid 43801146)
118. Mittal, R., Peak-Chew, S.Y. & McMahon, H.T. Acetylation of MEK2 and IκB kinase (IKK) activation loop residues by YopJ inhibits signaling. Proc. Natl Acad. Sci. USA 103, 18574-18579 (2006). (Pubitemid 44913452)
119. Fehr, D. et al. AopP, a typeIII effector protein of Aeromonas salmonicida, inhibits the NF κB signalling pathway. Microbiology 152, 2809-2818 (2006). (Pubitemid 44405105)
120. Brummelkamp, T.R., Nijman, S.M., Dirac, A.M. & Bernards, R. Loss of the cylindromatosis tumour suppressor inhibits apoptosis by activating NF κB. Nature 424, 797-801 (2003). (Pubitemid 37021711)
121. Wertz, I.E. et al. De-ubiquitination and ubiquitin ligase domains of A20 downregulate NF κB signalling. Nature 430, 694-699 (2004).
122. Ye, Z., Petrof, E.O., Boone, D., Claud, E.C. & Sun, J. Salmonella effector AvrA regulation of colonic epithelial cell inflammation by deubiquitination. Am. J.Pathol. 171, 882-892 (2007). (Pubitemid 47440987)
123. Collier-Hyams, L.S. et al. Cutting edge: Salmonella AvrA effector inhibits the key proinflammatory, anti-apoptotic NF κB pathway. J.Immunol. 169, 2846-2850 (2002). (Pubitemid 35013124)
124. Rytkonen, A. et al. SseL, a Salmonella deubiquitinase required for macrophage killing and virulence. Proc. Natl Acad. Sci. USA 104, 3502-3507 (2007). (Pubitemid 46364188)
125. Le Negrate, G. et al. Salmonella secreted factor L deubiquitinase of Salmonella typhimurium inhibits NF κB, suppresses IκBα ubiquitination and modulates innate immune responses. J.Immunol. 180, 5045-5056 (2008).
126. Kim, D.W. et al. The Shigella flexneri effector OspG interferes with innate immune responses by targeting ubiquitin-conjugating enzymes. Proc. Natl Acad. Sci. USA 102, 14046-14051 (2005). (Pubitemid 41377700)
127. Gao, X. et al. Bacterial effector binding to ribosomal protein s3 subverts NF κB function. PLoS Pathog. 5, e1000708 (2009).
128. Nobe, R. et al. Enterohaemorrhagic Escherichia coli serogroup O111 inhibits NF κB-dependent innate responses in a manner independent of a typeIII secreted OspG orthologue. Microbiology 155, 3214-3225 (2009).
129. Malladi, V., Puthenedam, M., Williams, P.H. & Balakrishnan, A. Enteropathogenic Escherichia coli outer membrane proteins induce iNOS by activation of NF κB and MAP kinases. Inflammation 28, 345-353 (2004). (Pubitemid 41504278)
130. Nadler, C. et al. The typeIII secretion effector NleE inhibits NF κB activation. PLoS Pathog. 6, e1000743 (2010).
131. Newton, H.J. et al. The typeIII effectors NleE and NleB from enteropathogenic E.coli and OspZ from Shigella block nuclear translocation of NF κB p65. PLoS Pathog. 6, e1000898 (2010).
132. Ashida, H. et al. A bacterial E3 ubiquitin ligase IpaH9.8 targets NEMO/IKKγ to dampen the host NF κB-mediated inflammatory response. Nature Cell Biol. 12, 66-73 (2010).
133. Selvaraj, S.K. & Prasadarao, N.V. Escherichia coli K1 inhibits proinflammatory cytokine induction in monocytes by preventing NF κB activation. J.Leukoc. Biol. 78, 544-554 (2005). (Pubitemid 41061326)
134. Kravchenko, V.V. et al. Modulation of gene expression via disruption of NF κB signaling by a bacterial small molecule. Science 321, 259-263 (2008). (Pubitemid 351989099)
135. Bhattacharjee, R.N. et al. VP1686, a Vibrio typeIII secretion protein, induces Toll-like receptor-independent apoptosis in macrophage through NF κB inhibition. J.Biol. Chem. 281, 36897-36904 (2006). (Pubitemid 46042158)
136. Betts, H.J., Wolf, K. & Fields, K.A. Effector protein modulation of host cells: examples in the Chlamydiaspp. arsenal. Curr. Opin. Microbiol. 12, 81-87 (2009).
137. Lad, S.P. et al. Cleavage of p65/RelA of the NF κB pathway by Chlamydia. Proc. Natl Acad. Sci. USA 104, 2933-2938 (2007).
138. Le Negrate G., et al. ChlaDub1 of Chlamydia trachomatis suppresses NF κB activation and inhibits IκBα ubiquitination and degradation. Cell. Microbiol. 10, 1879-1892 (2008).
139. Wolf, K., Plano, G.V. & Fields, K.A. A protein secreted by the respiratory pathogen Chlamydia pneumoniae impairs IL17 signaling via interaction with human Act1. Cell. Microbiol. 11, 769-779 (2009).
140. Ge, J. et al. A Legionella typeIV effector activates the NF κB pathway by phosphorylating the IκB family of inhibitors. Proc. Natl Acad. Sci. USA 106, 13725-13730 (2009).
141. Clifton, D.R., Rydkina, E., Freeman, R.S. & Sahni, S.K. NF κB activation during Rickettsia rickettsii infection of endothelial cells involves the activation of catalytic IκB kinases IKKα and IKKβ and phosphorylation-proteolysis of the inhibitor protein IκBα. Infect. Immun. 73, 155-165 (2005). (Pubitemid 40041105)
142. Abramson, T., Kedem, H. & Relman, D.A. Modulation of the NF κB pathway by Bordetella pertussis filamentous hemagglutinin. PLoS ONE 3, e3825 (2008).
143. Carneiro, L.A. et al. Shigella induces mitochondrial dysfunction and cell death in nonmyleoid cells. Cell Host Microbe 5, 123-136 (2009).
144. Wells, J.M., Loonen, L.M. & Karczewski, J.M. The role of innate signaling in the homeostasis of tolerance and immunity in the intestine. Int. J.Med. Microbiol. 300, 41-48 (2010).
145. Iyer, C. et al. Probiotic Lactobacillus reuteri promotes TNF-induced apoptosis in human myeloid leukemia-derived cells by modulation of NF κB and MAPK signalling. Cell. Microbiol. 10, 1442-1452 (2008). (Pubitemid 351837265)
146. Van Baarlen P. et al. Differential NF kappa B pathways induction by Lactobacillus plantarum in the duodenum of healthy humans correlating with immune tolerance. Proc. Natl Acad. Sci. USA 106, 2371-2376 (2009).
147. Guarino, A., Lo Vecchio, A. & Canani, R.B. Probiotics as prevention and treatment for diarrhea. Curr. Opin. Gastroenterol. 25, 18-23 (2009).
148. Nagamatsu, K. et al. Bordetella evades the host immune system by inducing IL10 through a typeIII effector, BopN. J.Exp. Med. 206, 3073-3088 (2009).
149. Legarda, D., Klein-Patel, M.E., Yim, S., Yuk, M.H. & Diamond, G. Suppression of NF κB-mediated β-defensin gene expression in the mammalian airway by the Bordetella typeIII secretion system. Cell. Microbiol. 7, 489-497 (2005). (Pubitemid 40439448)
150. Depaolo, R.W. et al. Toll-like receptor 6 drives differentiation of tolerogenic dendritic cells and contributes to LcrV-mediated plague pathogenesis. Cell Host Microbe 4, 350-361 (2008).
151. Molestina, R.E. & Sinai, A.P. Detection of a novel parasite kinase activity at the Toxoplasma gondii parasitophorous vacuole membrane capable of phosphorylating host IκBα. Cell. Microbiol. 7, 351-362 (2005). (Pubitemid 40277915)
152. Molestina, R.E. & Sinai, A.P. Host and parasite-derived IKK activities direct distinct temporal phases of NF κB activation and target gene expression following Toxoplasma gondii infection. J.Cell Sci. 118, 5785-5796 (2005). (Pubitemid 43079272)
153. Van Waes, C. Nuclear factor- κB in development, prevention, and therapy of cancer. Clin. Cancer Res. 13, 1076-1082 (2007). (Pubitemid 46424045)
154. Song, Y.J. & Kang, M.S. Roles of TRAF2 and TRAF3 in Epstein-Barr virus latent membrane protein 1induced alternative NF κB activation. Virus Genes 41, 174-180 (2010).
155. Brinkmann, M.M. et al. Activation of mitogen-activated protein kinase and NF κB pathways by a Kaposi's sarcoma-associated herpesvirus K15 membrane protein. J.Virol. 77, 9346-9358 (2003). (Pubitemid 37011031)
156. Friedman, J.M. & Horwitz, M.S. Inhibition of tumor necrosis factor α-induced NF κB activation by the adenovirus E3-104/14.5K complex. J.Virol. 76, 5515-5521 (2002). (Pubitemid 34517901)
157. Unterstab, G. et al. Viral targeting of the interferon- β-inducing Traf family member-associated NF κB activator (TANK)-binding kinase-1. Proc. Natl Acad. Sci. USA 102, 13640-13645 (2005). (Pubitemid 41420901)
158. Mohamed, M.R. et al. Cowpox virus expresses a novel ankyrin repeat NF κB inhibitor that controls inflammatory cell influx into virus-infected tissues and is critical for virus pathogenesis. J.Virol. 83, 9223-9236 (2009).
159. Park, K.J. et al. Hepatitis C virus NS5A protein modulates c-Jun N-terminal kinase through interaction with tumor necrosis factor receptor-associated factor2. J.Biol. Chem. 278, 30711-30718 (2003).
160. Mack, C., Sickmann, A., Lembo, D. & Brune, W. Inhibition of proinflammatory and innate immune signaling pathways by a cytomegalovirus RIP1interacting protein. Proc. Natl Acad. Sci. USA 105, 3094-3099 (2008). (Pubitemid 351723673)
161. Spitkovsky, D., Hehner, S.P., Hofmann, T.G., Moller,A. & Schmitz, M.L. The human papillomavirus oncoprotein E7 attenuates NF κB activation by targeting the IκB kinase complex. J.Biol. Chem. 277, 25576-25582 (2002). (Pubitemid 34951874)
162. Nichols, D.B. & Shisler, J.L. The MC160 protein expressed by the dermatotropic poxvirus molluscum contagiosum virus prevents tumor necrosis factor α- induced NF κB activation via inhibition of Iκ kinase complex formation. J.Virol. 80, 578-586 (2006). (Pubitemid 43062870)
163. Shisler, J.L. & Jin, X.L. The vaccinia virus K1L gene product inhibits host NF κB activation by preventing IκBα degradation. J.Virol. 78, 3553-3560 (2004). (Pubitemid 38568297)
164. Gedey, R., Jin, X.L., Hinthong, O. & Shisler, J.L. Poxviral regulation of the host NF κB response: the vaccinia virus M2L protein inhibits induction of NF κB activation via an ERK2 pathway in virus-infected human embryonic kidney cells. J.Virol. 80, 8676-8685 (2006). (Pubitemid 44384877)
165. Jones, J.O. & Arvin, A.M. Inhibition of the NF κB pathway by varicella-zoster virus invitro and in human epidermal cells invivo. J.Virol. 80, 5113-5124 (2006).
166. Heussler, V.T. et al. Hijacking of host cell IKK signalosomes by the transforming parasite Theileria. Science 298, 1033-1036 (2002). (Pubitemid 35247312)
167. Trosky, J.E. et al. Inhibition of MAPK signaling pathways by VopA from Vibrio parahaemolyticus. J.Biol. Chem. 279, 51953-51957 (2004). (Pubitemid 39656564)