Rotavirus antagonism of the innate immune response

Viruses

Volumn 1, Issue 3, 2009, Pages 1035-1056

  Arnold, Michelle M ^a   Patton, John T ^a  

^a NATIONAL INSTITUTE OF ALLERGY AND INFECTIOUS DISEASES   (United States)

Author keywords

Interferon regulatory factor; IRF; NSP1; Rotavirus

Indexed keywords

EID: 84877989213     PISSN: 19994915     EISSN: None     Source Type: Journal    
DOI: 10.3390/v1031035     Document Type: Review

References (112)

1. Bonjardim, C.A.; Ferreira, P.C.; Kroon, E.G. Interferons: signaling, antiviral and viral evasion. Immunol. Lett. 2009, 122, 1-11.
2. Der, S.D.; Zhou, A.; Williams, B.R.; Silverman, R.H. Identification of genes differentially regulated by interferon alpha, beta, or gamma using oligonucleotide arrays. Proc. Natl. Acad. Sci. U S A 1998, 95, 15623-15628.
3. Akira, S.; Uematsu, S.; Takeuchi, O. Pathogen recognition and innate immunity. Cell 2006, 124, 783-801.
4. Paun, A.; Pitha, P.M. The IRF family, revisited. Biochimie 2007, 89, 744-753.
5. Takaoka, A.; Wang, Z.; Choi, M.K.; Yanai, H.; Negishi, H.; Ban, T.; Lu, Y.; Miyagishi, M.; Kodama, T.; Honda, K.; Ohba, Y.; Taniguchi, T. DAI (DLM-1/ZBP1) is a cytosolic DNA sensor and an activator of innate immune response. Nature 2007, 448, 501-505.
6. Maniatis, T.; Falvo, J.V.; Kim, T.H.; Kim, T.K.; Lin, C.H.; Parekh, B.S.; Wathelet, M.G. Structure and function of the interferon-beta enhanceosome. Cold Spring Harb. Symp. Quant. Biol. 1998, 63, 609-620.
7. Honda, K.; Taniguchi, T. IRFs: master regulators of signalling by Toll-like receptors and cytosolic pattern-recognition receptors. Nat. Rev. Immunol. 2006, 6, 644-658.
8. Zhang, L.; Pagano, J.S. IRF-7, a new interferon regulatory factor associated with Epstein-Barr virus latency. Mol. Cell. Biol. 1997, 17, 5748-5757.
9. Fitzgerald, K.A.; McWhirter, S.M.; Faia, K.L.; Rowe, D.C.; Latz, E.; Golenbock, D.T.; Coyle, A. J.; Liao, S.M.; Maniatis, T. IKKepsilon and TBK1 are essential components of the IRF3 signaling pathway. Nat. Immunol. 2003, 4, 491-496.
10. Sharma, S.; tenOever, B.R.; Grandvaux, N.; Zhou, G.P.; Lin, R.; Hiscott, J. Triggering the interferon antiviral response through an IKK-related pathway. Science 2003, 300, 1148-1151.
11. Barnes, B.; Lubyova, B.; Pitha, P.M. On the role of IRF in host defense. J. Interferon Cytokine Res. 2002, 22, 59-71.
12. Lin, R.; Mamane, Y.; Hiscott, J. Multiple regulatory domains control IRF-7 activity in response to virus infection. J. Biol. Chem. 2000, 275, 34320-34327.
13. Marie, I.; Durbin, J.E.; Levy, D.E. Differential viral induction of distinct interferon-alpha genes by positive feedback through interferon regulatory factor-7. EMBO J. 1998, 17, 6660-6669.
14. Sato, M.; Hata, N.; Asagiri, M.; Nakaya, T.; Taniguchi, T.; Tanaka, N. Positive feedback regulation of type I IFN genes by the IFN-inducible transcription factor IRF-7. FEBS Lett. 1998, 441, 106-110.
15. Sato, M.; Suemori, H.; Hata, N.; Asagiri, M.; Ogasawara, K.; Nakao, K.; Nakaya, T.; Katsuki, M.; Noguchi, S.; Tanaka, N.; Taniguchi, T. Distinct and essential roles of transcription factors IRF-3 and IRF-7 in response to viruses for IFN-alpha/beta gene induction. Immunity 2000, 13, 539-548.
16. Colonna, M.; Trinchieri, G.; Liu, Y.J. Plasmacytoid dendritic cells in immunity. Nat. Immunol. 2004, 5, 1219-1226.
17. Honda, K.; Yanai, H.; Negishi, H.; Asagiri, M.; Sato, M.; Mizutani, T.; Shimada, N.; Ohba, Y.; Takaoka, A.; Yoshida, N.; Taniguchi, T. IRF-7 is the master regulator of type-I interferondependent immune responses. Nature 2005, 434, 772-777.
18. Yeow, W.S.; Au, W.C.; Juang, Y.T.; Fields, C.D.; Dent, C.L.; Gewert, D.R.; Pitha, P.M. Reconstitution of virus-mediated expression of interferon alpha genes in human fibroblast cells by ectopic interferon regulatory factor-7. J. Biol. Chem. 2000, 275, 6313-6320.
19. Kroll, M.; Margottin, F.; Kohl, A.; Renard, P.; Durand, H.; Concordet, J.P.; Bachelerie, F.; Arenzana-Seisdedos, F.; Benarous, R. Inducible degradation of IkappaBalpha by the proteasome requires interaction with the F-box protein h-betaTrCP. J. Biol. Chem. 1999, 274, 7941-7945.
20. Parashar, U.D.; Gibson, C.J.; Bresse, J.S.; Glass, R.I. Rotavirus and severe childhood diarrhea. Emerg. Infect. Dis. 2006, 12, 304-306.
21. Greenberg, H.B.; Estes, M.K. Rotaviruses: from pathogenesis to vaccination. Gastroenterology 2009, 136, 1939-1951.
22. Prasad, B.V.; Wang, G.J.; Clerx, J.P.; Chiu, W. Three-dimensional structure of rotavirus. J. Mol. Biol. 1988, 199, 269-275.
23. Yeager, M.; Dryden, K.A.; Olson, N.H.; Greenberg, H.B.; Baker, T.S. Three-dimensional structure of rhesus rotavirus by cryoelectron microscopy and image reconstruction. J. Cell Biol. 1990, 110, 2133-2144.
24. Chen, D.; Luongo, C.L.; Nibert, M.L.; Patton, J.T. Rotavirus open cores catalyze 5'-capping and methylation of exogenous RNA: evidence that VP3 is a methyltransferase. Virology 1999, 265, 120-130.
25. Lawton, J.A.; Estes, M.K.; Prasad, B.V. Three-dimensional visualization of mRNA release from actively transcribing rotavirus particles. Nat. Struct. Biol. 1997, 4, 118-121.
26. Patton, J.T.; Jones, M.T.; Kalbach, A.N.; He, Y.W.; Xiaobo, J. Rotavirus RNA polymerase requires the core shell protein to synthesize the double-stranded RNA genome. J. Virol. 1997, 71, 9618-9626.
27. Bican, P.; Cohen, J.; Charpilienne, A.; Scherrer, R. Purification and characterization of bovine rotavirus cores. J. Virol. 1982, 43, 1113-1117.
28. Spencer, E.; Arias, M.L. In vitro transcription catalyzed by heat-treated human rotavirus. J. Virol. 1981, 40, 1-10.
29. Santos, N.; Hoshino, Y. Global distribution of rotavirus serotypes/genotypes and its implication for the development and implementation of an effective rotavirus vaccine. Rev. Med. Virol. 2005, 15, 29-56.
30. Prasad, B.V.; Rothnagel, R.; Zeng, C.Q.; Jakana, J.; Lawton, J.A.; Chiu, W.; Estes, M.K. Visualization of ordered genomic RNA and localization of transcriptional complexes in rotavirus. Nature 1996, 382, 471-473.
31. Imai, M.; Akatani, K.; Ikegami, N.; Furuichi, Y. Capped and conserved terminal structures in human rotavirus genome double-stranded RNA segments. J. Virol. 1983, 47, 125-136.
32. McCrae, M.A.; McCorquodale, J.G. Molecular biology of rotaviruses. V. Terminal structure of viral RNA species. Virology 1983, 126, 204-212.
33. Chen, D.; Zeng, C.Q.; Wentz, M.J.; Gorziglia, M.; Estes, M.K.; Ramig, R.F. Template-dependent, in vitro replication of rotavirus RNA. J. Virol. 1994, 68, 7030-7039.
34. Patton, J.T.; Spencer, E. Genome replication and packaging of segmented double-stranded RNA viruses. Virology 2000, 277, 217-225.
35. Silvestri, L.S.; Taraporewala, Z.F.; Patton, J.T. Rotavirus replication: plus-sense templates for double-stranded RNA synthesis are made in viroplasms. J. Virol. 2004, 78, 7763-7774.
36. Estes, M.K.; Kang, G.; Zeng, C.Q.; Crawford, S.E.; Ciarlet, M. Pathogenesis of rotavirus gastroenteritis. Novartis Found. Symp. 2001, 238, 82-96; discussion 96-100.
37. Delmas, O.; Durand-Schneider, A.M.; Cohen, J.; Colard, O.; Trugnan, G. Spike protein VP4 assembly with maturing rotavirus requires a postendoplasmic reticulum event in polarized caco-2 cells. J. Virol. 2004, 78, 10987-10994.
38. Jourdan, N.; Maurice, M.; Delautier, D.; Quero, A.M.; Servin, A.L.; Trugnan, G. Rotavirus is released from the apical surface of cultured human intestinal cells through nonconventional vesicular transport that bypasses the Golgi apparatus. J. Virol. 1997, 71, 8268-8278.
39. Taniguchi, K.; Urasawa, S. Diversity in rotavirus genomes. Seminars in Virology 1995, 6, 123-131.
40. Nakagomi, O.; Nakagomi, T. Genomic relationships among rotaviruses recovered from various animal species as revealed by RNA-RNA hybridization assays. Res. Vet. Sci. 2002, 73, 207-214.
41. Matthijnssens, J.; Ciarlet, M.; Heiman, E.; Arijs, I.; Delbeke, T.; McDonald, S.M.; Palombo, E.A.; Iturriza-Gomara, M.; Maes, P.; Patton, J.T.; Rahman, M.; Van Ranst, M. Full genome-based classification of rotaviruses reveals a common origin between human Wa-Like and porcine rotavirus strains and human DS-1-like and bovine rotavirus strains. J. Virol. 2008, 82, 3204-3219.
42. Nakagomi, O.; Nakagomi, T. Genetic diversity and similarity among mammalian rotaviruses in relation to interspecies transmission of rotavirus. Arch. Virol. 1991, 120, 43-55.
43. Hoshino, Y.; Kapikian, A.Z. Classification of rotavirus VP4 and VP7 serotypes. Arch. Virol. Suppl. 1996, 12, 99-111.
44. Matthijnssens, J.; Potgieter, C.A.; Ciarlet, M.; Parreno, V.; Martella, V.; Banyai, K.; Garaicoechea, L.; Palombo, E.A.; Novo, L.; Zeller, M.; Arista, S.; Gerna, G.; Rahman, M.; Van Ranst, M. Are human P[14] rotavirus strains the result of interspecies transmissions from sheep or other ungulates that belong to the mammalian order Artiodactyla? J. Virol. 2009, 83, 2917-2929.
45. Schumann, T.; Hotzel, H.; Otto, P.; Johne, R. Evidence of interspecies transmission and reassortment among avian group A rotaviruses. Virology 2009, 386, 334-343.
46. Solberg, O.D.; Hasing, M.E.; Trueba, G.; Eisenberg, J.N. Characterization of novel VP7, VP4, and VP6 genotypes of a previously untypeable group A rotavirus. Virology 2009, 385, 58-67.
47. Trojnar, E.; Otto, P.; Johne, R. The first complete genome sequence of a chicken group A rotavirus indicates independent evolution of mammalian and avian strains. Virology 2009, 386, 325-333.
48. Bass, E.S.; Pappano, D.A.; Humiston, S.G. Rotavirus. Pediatr. Rev. 2007, 28, 183-191.
49. Ramig, R.F. Systemic rotavirus infection. Expert Rev. Anti. Infect. Ther. 2007, 5, 591-612.
50. Crawford, S.E.; Patel, D.G.; Cheng, E.; Berkova, Z.; Hyser, J.M.; Ciarlet, M.; Finegold, M.J.; Conner, M.E.; Estes, M.K. Rotavirus viremia and extraintestinal viral infection in the neonatal rat model. J. Virol. 2006, 80, 4820-4832.
51. Blutt, S.E.; Conner, M.E. Rotavirus: to the gut and beyond! Curr. Opin. Gastroenterol. 2007, 23, 39-43.
52. Fenaux, M.; Cuadras, M.A.; Feng, N.; Jaimes, M.; Greenberg, H.B. Extraintestinal spread and replication of a homologous EC rotavirus strain and a heterologous rhesus rotavirus in BALB/c mice. J. Virol. 2006, 80, 5219-5232.
53. Mossel, E.C.; Ramig, R.F. Rotavirus genome segment 7 (NSP3) is a determinant of extraintestinal spread in the neonatal mouse. J. Virol. 2002, 76, 6502-6509.
54. Mossel, E.C.; Ramig, R.F. A lymphatic mechanism of rotavirus extraintestinal spread in the neonatal mouse. J. Virol. 2003, 77, 12352-12356.
55. Broome, R.L.; Vo, P.T.; Ward, R.L.; Clark, H.F.; Greenberg, H.B. Murine rotavirus genes encoding outer capsid proteins VP4 and VP7 are not major determinants of host range restriction and virulence. J. Virol. 1993, 67, 2448-2455.
56. Ciarlet, M.; Estes, M.K.; Barone, C.; Ramig, R.F.; Conner, M.E. Analysis of host range restriction determinants in the rabbit model: comparison of homologous and heterologous rotavirus infections. J. Virol. 1998, 72, 2341-2351.
57. Hoshino, Y.; Saif, L.J.; Kang, S.Y.; Sereno, M.M.; Chen, W.K.; Kapikian, A.Z. Identification of group A rotavirus genes associated with virulence of a porcine rotavirus and host range restriction of a human rotavirus in the gnotobiotic piglet model. Virology 1995, 209, 274-280.
58. Azim, T.; Ahmad, S.M.; Sefat, E.K.; Sarker, M.S.; Unicomb, L.E.; De, S.; Hamadani, J.D.; Salam, M.A.; Wahed, M.A.; Albert, M.J. Immune response of children who develop persistent diarrhea following rotavirus infection. Clin. Diagn. Lab. Immunol. 1999, 6, 690-695.
59. De Boissieu, D.; Lebon, P.; Badoual, J.; Bompard, Y.; Dupont, C. Rotavirus induces alphainterferon release in children with gastroenteritis. J. Pediatr. Gastroenterol. Nutr. 1993, 16, 29-32.
60. Wang, Y.; Dennehy, P.H.; Keyserling, H.L.; Tang, K.; Gentsch, J.R.; Glass, R.I.; Jiang, B. Rotavirus infection alters peripheral T-cell homeostasis in children with acute diarrhea. J. Virol. 2007, 81, 3904-3912.
61. Chaplin, P.J.; Entrican, G.; Gelder, K.I.; Collins, R.A. Cloning and biologic activities of a bovine interferon-alpha isolated from the epithelium of a rotavirus-infected calf. J. Interferon Cytokine Res. 1996, 16, 25-30.
62. La Bonnardiere, C.; Cohen, J.; Contrepois, M. Interferon activity in rotavirus infected newborn calves. Ann. Rech. Vet. 1981, 12, 85-91.
63. Lecce, J.G.; Cummins, J.M.; Richards, A.B. Treatment of rotavirus infection in neonate and weanling pigs using natural human interferon alpha. Mol. Biother. 1990, 2, 211-216.
64. Schwers, A.; Vanden Broecke, C.; Maenhoudt, M.; Beduin, J.M.; Werenne, J.; Pastoret, P.P. Experimental rotavirus diarrhoea in colostrum-deprived newborn calves: assay of treatment by administration of bacterially produced human interferon (Hu-IFN alpha 2). Ann. Rech. Vet. 1985, 16, 213-218.
65. Angel, J.; Franco, M.A.; Greenberg, H.B.; Bass, D. Lack of a role for type I and type II interferons in the resolution of rotavirus-induced diarrhea and infection in mice. J. Interferon Cytokine Res. 1999, 19, 655-659.
66. Feng, N.; Kim, B.; Fenaux, M.; Nguyen, H.; Vo, P.; Omary, M.B.; Greenberg, H.B. Role of interferon in homologous and heterologous rotavirus infection in the intestines and extraintestinal organs of suckling mice. J. Virol. 2008, 82, 7578-7590.
67. Dagenais, L.; Pastoret, P.P.; Van den Broecke, C.; Werenne, J. Susceptibility of bovine rotavirus to interferon. Brief report. Arch. Virol. 1981, 70, 377-379.
68. La Bonnardiere, C.; de Vaureix, C.; L'Haridon, R.; Scherrer, R. Weak susceptibility of rotavirus to bovine interferon in calf kidney cells. Arch. Virol. 1980, 64, 167-170.
69. Bass, D.M. Interferon gamma and interleukin 1, but not interferon alfa, inhibit rotavirus entry into human intestinal cell lines. Gastroenterology 1997, 113, 81-89.
70. Casola, A.; Estes, M.K.; Crawford, S.E.; Ogra, P.L.; Ernst, P.B.; Garofalo, R.P.; Crowe, S.E. Rotavirus infection of cultured intestinal epithelial cells induces secretion of CXC and CC chemokines. Gastroenterology 1998, 114, 947-955.
71. Casola, A.; Garofalo, R.P.; Crawford, S.E.; Estes, M.K.; Mercurio, F.; Crowe, S.E.; Brasier, A.R. Interleukin-8 gene regulation in intestinal epithelial cells infected with rotavirus: role of viralinduced IkappaB kinase activation. Virology 2002, 298, 8-19.
72. Rollo, E.E.; Kumar, K.P.; Reich, N.C.; Cohen, J.; Angel, J.; Greenberg, H.B.; Sheth, R.; Anderson, J.; Oh, B.; Hempson, S.J.; Mackow, E.R.; Shaw, R.D. The epithelial cell response to rotavirus infection. J. Immunol. 1999, 163, 4442-4452.
73. Johnson, M.A.; McCrae, M.A. Molecular biology of rotaviruses. VIII. Quantitative analysis of regulation of gene expression during virus replication. J. Virol. 1989, 63, 2048-2055.
74. Hua, J.; Chen, X.; Patton, J.T. Deletion mapping of the rotavirus metalloprotein NS53 (NSP1): the conserved cysteine-rich region is essential for virus-specific RNA binding. J. Virol. 1994, 68, 3990-4000.
75. Hua, J.; Mansell, E.A.; Patton, J.T. Comparative analysis of the rotavirus NS53 gene: conservation of basic and cysteine-rich regions in the protein and possible stem-loop structures in the RNA. Virology 1993, 196, 372-378.
76. Dunn, S.J.; Cross, T.L.; Greenberg, H.B. Comparison of the rotavirus nonstructural protein NSP1 (NS53) from different species by sequence analysis and northern blot hybridization. Virology 1994, 203, 178-183.
77. Kojima, K.; Taniguchi, K.; Kobayashi, N. Species-specific and interspecies relatedness of NSP1 sequences in human, porcine, bovine, feline, and equine rotavirus strains. Arch. Virol. 1996, 141, 1-12.
78. Xu, L.; Tian, Y.; Tarlow, O.; Harbour, D.; McCrae, M.A. Molecular biology of rotaviruses. IX. Conservation and divergence in genome segment 5. J. Gen. Virol. 1994, 75, 3413-3421.
79. Mitchell, D.B.; Both, G.W. Conservation of a potential metal binding motif despite extensive sequence diversity in the rotavirus nonstructural protein NS53. Virology 1990, 174, 618-621.
80. Pina-Vazquez, C.; De Nova-Ocampo, M.; Guzman-Leon, S.; Padilla-Noriega, L. Posttranslational regulation of rotavirus protein NSP1 expression in mammalian cells. Arch. Virol. 2007, 152, 345-368.
81. Brottier, P.; Nandi, P.; Bremont, M.; Cohen, J. Bovine rotavirus segment 5 protein expressed in the baculovirus system interacts with zinc and RNA. J. Gen. Virol. 1992, 73 (Pt 8), 1931-1938.
82. Hua, J.; Patton, J.T. The carboxyl-half of the rotavirus nonstructural protein NS53 (NSP1) is not required for virus replication. Virology 1994, 198, 567-576.
83. Okada, J.; Kobayashi, N.; Taniguchi, K.; Shiomi, H. Functional analysis of the heterologous NSP1 genes in the genetic background of simian rotavirus SA11. Arch. Virol. 1999, 144, 1439-1449.
84. Patton, J.T.; Taraporewala, Z.; Chen, D.; Chizhikov, V.; Jones, M.; Elhelu, A.; Collins, M.; Kearney, K.; Wagner, M.; Hoshino, Y.; Gouvea, V. Effect of intragenic rearrangement and changes in the 3' consensus sequence on NSP1 expression and rotavirus replication. J. Virol. 2001, 75, 2076-2086.
85. Taniguchi, K.; Kojima, K.; Urasawa, S. Nondefective rotavirus mutants with an NSP1 gene which has a deletion of 500 nucleotides, including a cysteine-rich zinc finger motif-encoding region (nucleotides 156 to 248), or which has a nonsense codon at nucleotides 153-155. J. Virol. 1996, 70, 4125-4130.
86. Barro, M.; Patton, J.T. Rotavirus NSP1 inhibits expression of type I interferon by antagonizing the function of interferon regulatory factors IRF3, IRF5, and IRF7. J. Virol. 2007, 81, 4473-4481.
87. Tian, Y.; Tarlow, O.; Ballard, A.; Desselberger, U.; McCrae, M.A. Genomic concatemerization/deletion in rotaviruses: a new mechanism for generating rapid genetic change of potential epidemiological importance. J. Virol. 1993, 67, 6625-6632.
88. Graff, J.W.; Mitzel, D.N.; Weisend, C.M.; Flenniken, M.L.; Hardy, M.E. Interferon regulatory factor 3 is a cellular partner of rotavirus NSP1. J. Virol. 2002, 76, 9545-9550.
89. Barro, M.; Patton, J.T. Rotavirus nonstructural protein 1 subverts innate immune response by inducing degradation of IFN regulatory factor 3. Proc. Natl. Acad. Sci. U S A 2005, 102, 4114-4119.
90. Graff, J.W.; Ewen, J.; Ettayebi, K.; Hardy, M.E. Zinc-binding domain of rotavirus NSP1 is required for proteasome-dependent degradation of IRF3 and autoregulatory NSP1 stability. J. Gen. Virol. 2007, 88, 613-620.
91. Feng, N.; Sen, A.; Nguyen, H.; Vo, P.; Hoshino, Y.; Deal, E.M.; Greenberg, H.B. Variation in antagonism of the interferon response to rotavirus NSP1 results in differential infectivity in mouse embryonic fibroblasts. J. Virol. 2009, 83, 6987-6994.
92. Sen, A.; Feng, N.; Ettayebi, K.; Hardy, M.E.; Greenberg, H.B. IRF3 Inhibition by Rotavirus NSP1 is Host cell and Viral Strain Dependent but Independent of NSP1 Proteasomal Degradation. J. Virol. 2009.
93. Mesa, M.C.; Rodriguez, L.S.; Franco, M.A.; Angel, J. Interaction of rotavirus with human peripheral blood mononuclear cells: plasmacytoid dendritic cells play a role in stimulating memory rotavirus specific T cells in vitro. Virology 2007, 366, 174-184.
94. Barnes, B.J.; Moore, P.A.; Pitha, P.M. Virus-specific activation of a novel interferon regulatory factor, IRF-5, results in the induction of distinct interferon alpha genes. J. Biol. Chem. 2001, 276, 23382-23390.
95. Douagi, I.; McInerney, G.M.; Hidmark, A.S.; Miriallis, V.; Johansen, K.; Svensson, L.; Karlsson Hedestam, G.B. Role of interferon regulatory factor 3 in type I interferon responses in rotavirusinfected dendritic cells and fibroblasts. J. Virol. 2007, 81, 2758-2768.
96. Graff, J.W.; Ettayebi, K.; Hardy, M.E. Rotavirus NSP1 inhibits NFkappaB activation by inducing proteasome-dependent degradation of beta-TrCP: a novel mechanism of IFN antagonism. PLoS Pathog. 2009, 5, e1000280.
97. Holloway, G.; Truong, T.T.; Coulson, B.S. Rotavirus antagonizes cellular antiviral responses by inhibiting the nuclear accumulation of STAT1, STAT2, and NF-kappaB. J. Virol. 2009, 83, 4942-4951.
98. Vancott, J.L.; McNeal, M.M.; Choi, A.H.; Ward, R.L. The role of interferons in rotavirus infections and protection. J. Interferon Cytokine Res. 2003, 23, 163-170.
99. Aravind, L.; Iyer, L.M.; Koonin, E.V. Scores of RINGS but no PHDs in ubiquitin signaling. Cell Cycle 2003, 2, 123-126.
100. Dodd, R.B.; Allen, M.D.; Brown, S.E.; Sanderson, C.M.; Duncan, L.M.; Lehner, P.J.; Bycroft, M.; Read, R.J. Solution structure of the Kaposi's sarcoma-associated herpesvirus K3 N-terminal domain reveals a Novel E2-binding C4HC3-type RING domain. J. Biol. Chem. 2004, 279, 53840-53847.
101. Weber, F.; Kochs, G.; Haller, O. Inverse interference: how viruses fight the interferon system. Viral Immunol. 2004, 17, 498-515.
102. Katze, M.G.; He, Y.; Gale, M., Jr. Viruses and interferon: a fight for supremacy. Nat. Rev. Immunol. 2002, 2, 675-687.
103. Ronco, L.V.; Karpova, A.Y.; Vidal, M.; Howley, P.M. Human papillomavirus 16 E6 oncoprotein binds to interferon regulatory factor-3 and inhibits its transcriptional activity. Genes Dev. 1998, 12, 2061-2072.
104. La Rocca, S.A.; Herbert, R.J.; Crooke, H.; Drew, T.W.; Wileman, T.E.; Powell, P.P. Loss of interferon regulatory factor 3 in cells infected with classical swine fever virus involves the N-terminal protease, Npro. J. Virol. 2005, 79, 7239-7247.
105. Bauhofer, O.; Summerfield, A.; Sakoda, Y.; Tratschin, J.D.; Hofmann, M.A.; Ruggli, N. Classical swine fever virus Npro interacts with interferon regulatory factor 3 and induces its proteasomal degradation. J. Virol. 2007, 81, 3087-3096.
106. Chen, Z.; Rijnbrand, R.; Jangra, R.K.; Devaraj, S.G.; Qu, L.; Ma, Y.; Lemon, S.M.; Li, K. Ubiquitination and proteasomal degradation of interferon regulatory factor-3 induced by Npro from a cytopathic bovine viral diarrhea virus. Virology 2007, 366, 277-292.
107. Hilton, L.; Moganeradj, K.; Zhang, G.; Chen, Y.H.; Randall, R.E.; McCauley, J.W.; Goodbourn, S. The NPro product of bovine viral diarrhea virus inhibits DNA binding by interferon regulatory factor 3 and targets it for proteasomal degradation. J. Virol. 2006, 80, 11723-11732.
108. Szymanski, M.R.; Fiebach, A.R.; Tratschin, J.D.; Gut, M.; Ramanujam, V.M.; Gottipati, K.; Patel, P.; Ye, M.; Ruggli, N.; Choi, K.H. Zinc binding in pestivirus N(pro) is required for interferon regulatory factor 3 interaction and degradation. J. Mol. Biol. 2009, 391, 438-449.
109. Guo, Z.; Chen, L.M.; Zeng, H.; Gomez, J.A.; Plowden, J.; Fujita, T.; Katz, J.M.; Donis, R.O.; Sambhara, S. NS1 protein of influenza A virus inhibits the function of intracytoplasmic pathogen sensor, RIG-I. Am. J. Respir. Cell. Mol. Biol. 2007, 36, 263-269.
110. Mibayashi, M.; Martinez-Sobrido, L.; Loo, Y.M.; Cardenas, W.B.; Gale, M., Jr.; Garcia-Sastre, A. Inhibition of retinoic acid-inducible gene I-mediated induction of beta interferon by the NS1 protein of influenza A virus. J. Virol. 2007, 81, 514-524.
111. Pichlmair, A.; Schulz, O.; Tan, C.P.; Naslund, T.I.; Liljestrom, P.; Weber, F.; Reis e Sousa, C. RIG-I-mediated antiviral responses to single-stranded RNA bearing 5'-phosphates. Science 2006, 314, 997-1001.
112. Hirata, Y.; Broquet, A.H.; Menchen, L.; Kagnoff, M.F. Activation of innate immune defense mechanisms by signaling through RIG-I/IPS-1 in intestinal epithelial cells. J. Immunol. 2007, 179, 5425-5432.