Rotavirus-host cell interactions: An arms race

Current Opinion in Virology

Volumn 2, Issue 4, 2012, Pages 389-398

  López, Susana ^a   Arias, Carlos F ^a  

^a INSTITUTO DE BIOTECNOLOGÍA   (Mexico)

Author keywords

[No Author keywords available]

Indexed keywords

ACTIVATING TRANSCRIPTION FACTOR 4; ACTIVATING TRANSCRIPTION FACTOR 6; ALPHA INTERFERON; BETA INTERFERON; DOUBLE STRANDED RNA; INITIATION FACTOR 2ALPHA; INITIATION FACTOR 4A; INITIATION FACTOR 4G; MESSENGER RNA; NONSTRUCTURAL PROTEIN 1; NONSTRUCTURAL PROTEIN 3; POLYA BINDING PROTEIN; PROTEIN; UNCLASSIFIED DRUG;

ARTICLE; CELL STRESS; HUMAN; INNATE IMMUNITY; NONHUMAN; PRIORITY JOURNAL; PROTEIN SYNTHESIS; RNA INTERFERENCE; RNA TRANSLATION; ROTAVIRUS; ROTAVIRUS INFECTION; UNFOLDED PROTEIN RESPONSE; VIRUS CELL INTERACTION; VIRUS REPLICATION;

EID: 84865152204     PISSN: 18796257     EISSN: 18796265     Source Type: Journal    
DOI: 10.1016/j.coviro.2012.05.001     Document Type: Review

References (87)

1. J.A. Lawton, M.K. Estes, and B.V. Prasad Mechanism of genome transcription in segmented dsRNA viruses Advances in Virus Research 55 2000 185 229
2. M.K. Estes, and A.Z. Kapikian Rotaviruses D.N. Knipe, P.M. Howley, Fields Virology edn 5 2007 Wolters Kluwer Health/Lippincott Williams and Wilkins Philadelphia, PA 1917 1974
3. J.T. Patton, R. Vasquez-Del Carpio, M.A. Tortorici, and Z.F. Taraporewala Coupling of rotavirus genome replication and capsid assembly Advances in Virus Research 69 2007 167 201
4. J.T. Patton, and E. Spencer Genome replication and packaging of segmented double-stranded RNA viruses Virology 277 2000 217 225
5. C. Ayala-Breton, M. Arias, R. Espinosa, P. Romero, C.F. Arias, and S. Lopez Analysis of the kinetics of transcription and replication of the rotavirus genome by RNA interference Journal of Virology 83 2009 8819 8831
6. C.Q. Zeng, M.J. Wentz, J. Cohen, M.K. Estes, and R.F. Ramig Characterization and replicase activity of double-layered and single-layered rotavirus-like particles expressed from baculovirus recombinants Journal of Virology 70 1996 2736 2742
7. M. Campagna, C. Eichwald, F. Vascotto, and O.R. Burrone RNA interference of rotavirus segment 11 mRNA reveals the essential role of NSP5 in the virus replicative cycle Journal of General Virology 86 2005 1481 1487 (Pubitemid 40613267)
8. T. Lopez, M. Rojas, C. Ayala-Breton, S. Lopez, and C.F. Arias Reduced expression of the rotavirus NSP5 gene has a pleiotropic effect on virus replication Journal of General Virology 86 2005 1609 1617 (Pubitemid 40766873)
9. L.S. Silvestri, Z.F. Taraporewala, and J.T. Patton Rotavirus replication: plus-sense templates for double-stranded RNA synthesis are made in viroplasms Journal of Virology 78 2004 7763 7774 (Pubitemid 38915922)
10. W. Cheung, M. Gill, A. Esposito, C.F. Kaminski, N. Courousse, S. Chwetzoff, G. Trugnan, N. Keshavan, A. Lever, and U. Desselberger Rotaviruses associate with cellular lipid droplet components to replicate in viroplasms, and compounds disrupting or blocking lipid droplets inhibit viroplasm formation and viral replication Journal of Virology 84 2010 6782 6798 This manuscript describes for the first time that lipid droplet components have an effect on rotavirus replication.
11. R. Contin, F. Arnoldi, M. Mano, and O.R. Burrone Rotavirus replication requires a functional proteasome for effective assembly of viroplasms Journal of Virology 85 2011 2781 2792
12. T. Lopez, D. Silva-Ayala, S. Lopez, and C.F. Arias Replication of the rotavirus genome requires an active ubiquitin-proteasome system Journal of Virology 85 2011 11964 11971
13. T.E. Dever Gene-specific regulation by general translation factors Cell 108 2002 545 556 (Pubitemid 34260879)
14. M. Bushell, and P. Sarnow Hijacking the translation apparatus by RNA viruses Journal of Cell Biology 158 2002 395 399 (Pubitemid 34851696)
15. R.J. Schneider, and I. Mohr Translation initiation and viral tricks Trends in Biochemical Sciences 28 2003 130 136 (Pubitemid 36293850)
16. D. Walsh, and I. Mohr Viral subversion of the host protein synthesis machinery Nature Reviews Microbiology 9 2011 860 875 An excellent review of viral strategies to control cell protein synthesis.
17. D. Poncet Translation of rotavirus mRNAs in the infected cell U. Desselberger, J. Gray, Viral Gastroenteritis 2003 Elsevier Science Amsterdam 185 205 (Pubitemid 137641017)
18. M. Piron, P. Vende, J. Cohen, and D. Poncet Rotavirus RNA-binding protein NSP3 interacts with eIF4GI and evicts the poly(A) binding protein from eIF4F EMBO Journal 17 1998 5811 5821 (Pubitemid 28445992)
19. H. Montero, C.F. Arias, and S. Lopez Rotavirus Nonstructural Protein NSP3 is not required for viral protein synthesis Journal of Virology 80 2006 9031 9038 This manuscript challenges the previously assigned function of NSP3 in the translation of rotavirus mRNAs. (Pubitemid 44359977)
20. R.C. Deo, C.M. Groft, K.R. Rajashankar, and S.K. Burley Recognition of the rotavirus mRNA 3′ consensus by an asymmetric NSP3 homodimer Cell 108 2002 71 81 (Pubitemid 34137013)
21. C.M. Groft, and S.K. Burley Recognition of eIF4G by rotavirus NSP3 reveals a basis for mRNA circularization Molecular Cell 9 2002 1273 1283 (Pubitemid 34722306)
22. M. Harb, M.M. Becker, D. Vitour, C.H. Baron, P. Vende, S.C. Brown, S. Bolte, S.T. Arold, and D. Poncet Nuclear localization of cytoplasmic poly(A)-binding protein upon rotavirus infection involves the interaction of NSP3 with eIF4G and RoXaN Journal of Virology 82 2008 11283 11293
23. H. Montero, M. Rojas, C.F. Arias, and S. Lopez Rotavirus infection induces the phosphorylation of eIF2alpha but prevents the formation of stress granules Journal of Virology 82 2008 1496 1504
24. D. Vitour, P. Lindenbaum, P. Vende, M.M. Becker, and D. Poncet RoXaN, a novel cellular protein containing TPR, LD, and zinc finger motifs, forms a ternary complex with eukaryotic initiation factor 4G and rotavirus NSP3 Journal of Virology 78 2004 3851 3862 (Pubitemid 38437191)
25. M. Rojas, C.F. Arias, and S. Lopez Protein kinase R is responsible for the phosphorylation of eIF2alpha in rotavirus infection Journal of Virology 84 2010 10457 10466
26. M. Vijay-Kumar, J.R. Gentsch, W.J. Kaiser, N. Borregaard, M.K. Offermann, A.S. Neish, and A.T. Gewirtz Protein kinase R mediates intestinal epithelial gene remodeling in response to double-stranded RNA and live rotavirus Journal of Immunology 174 2005 6322 6331 (Pubitemid 40663825)
27. J. Wu, and R.J. Kaufman From acute ER stress to physiological roles of the Unfolded Protein Response Cell Death and Differentiation 13 2006 374 384
28. P. Anderson, and N. Kedersha Stressful initiations Journal of Cell Science 115 2002 3227 3234 (Pubitemid 34960175)
29. N. Kedersha, and P. Anderson Stress granules: sites of mRNA triage that regulate mRNA stability and translatability Biochemical Society Transactions 30 2002 963 969 (Pubitemid 36002389)
30. C.J. Beckham, and R. Parker P bodies, stress granules, and viral life cycles Cell Host Microbe 3 2008 206 212 An excellent review of viral strategies to interact with RNA granules. (Pubitemid 351494719)
31. H.P. Harding, M. Calfon, F. Urano, I. Novoa, and D. Ron Transcriptional and translational control in the Mammalian unfolded protein response Annual Review of Cell and Developmental Biology 18 2002 575 599 (Pubitemid 35387362)
32. R.J. Kaufman Stress signaling from the lumen of the endoplasmic reticulum: coordination of gene transcriptional and translational controls Genes and Development 13 1999 1211 1233 (Pubitemid 29250189)
33. D.T. Rutkowski, and R.J. Kaufman A trip to the ER: coping with stress Trends in Cell Biology 14 2004 20 28 (Pubitemid 38076857)
34. R.J. Kaufman Regulation of mRNA translation by protein folding in the endoplasmic reticulum Trends in Biochemical Sciences 29 2004 152 158 (Pubitemid 38314861)
35. V. Trujillo-Alonso, L. Maruri-Avidal, C.F. Arias, and S. Lopez Rotavirus infection induces the unfolded protein response of the cell and controls it through the nonstructural protein NSP3 Journal of Virology 85 2011 12594 12604
36. J.L. Zambrano, K. Ettayebi, W.S. Maaty, N.R. Faunce, B. Bothner, and M.E. Hardy Rotavirus infection activates the UPR but modulates its activity Virology Journal 8 2011 359
37. C. Wilkins, and M. Gale Jr. Recognition of viruses by cytoplasmic sensors Current Opinion in Immunology 22 2010 41 47
38. R.E. Randall, and S. Goodbourn Interferons and viruses: an interplay between induction, signalling, antiviral responses and virus countermeasures Journal of General Virology 89 2008 1 47 A comprehensive and interesting review of viruses and the innate immune response of the cell.
39. A.H. Broquet, Y. Hirata, C.S. McAllister, and M.F. Kagnoff RIG-I/MDA5/MAVS are required to signal a protective IFN response in rotavirus-infected intestinal epithelium Journal of Immunology 186 2011 1618 1626
40. A. Sen, A.J. Pruijssers, T.S. Dermody, A. Garcia-Sastre, and H.B. Greenberg The early interferon response to rotavirus is regulated by PKR and depends on MAVS/IPS-1, RIG-I, MDA-5, and IRF3 Journal of Virology 85 2011 3717 3732
41. M. Barro, and J.T. Patton Rotavirus nonstructural protein 1 subverts innate immune response by inducing degradation of IFN regulatory factor 3 Proceedings of the National Academy of Sciences of the United States of America 102 2005 4114 4119 This work shows that one of the functions of rotavirus NSP1 is to induce the degradation of IRF3 to rotaviruses subvert the innate immune response of the cell. (Pubitemid 40388564)
42. M. Barro, and J.T. Patton Rotavirus NSP1 inhibits expression of type I interferon by antagonizing the function of interferon regulatory factors IRF3, IRF5, and IRF7 Journal of Virology 81 2007 4473 4481 (Pubitemid 46668645)
43. N. Feng, A. Sen, H. Nguyen, P. Vo, Y. Hoshino, E.M. Deal, and H.B. Greenberg Variation in antagonism of the interferon response to rotavirus NSP1 results in differential infectivity in mouse embryonic fibroblasts Journal of Virology 83 2009 6987 6994
44. J.W. Graff, D.N. Mitzel, C.M. Weisend, M.L. Flenniken, and M.E. Hardy Interferon regulatory factor 3 is a cellular partner of rotavirus NSP1 Journal of Virology 76 2002 9545 9550 (Pubitemid 34919912)
45. J.W. Graff, K. Ettayebi, and M.E. Hardy Rotavirus NSP1 inhibits NFkappaB activation by inducing proteasome-dependent degradation of beta-TrCP: a novel mechanism of IFN antagonism PLoS Pathogens 5 2009 e1000280 An interesting paper that defines a second strategy of immune evasion used by rotaviruses.
46. G. Holloway, T.T. Truong, and B.S. Coulson Rotavirus antagonizes cellular antiviral responses by inhibiting the nuclear accumulation of STAT1, STAT2, and NF-kappaB Journal of Virology 83 2009 4942 4951
47. J. Rehwinkel, and C. Reis e Sousa RIGorous detection: exposing virus through RNA sensing Science 327 2010 284 286
48. S.M. McDonald, and J.T. Patton Assortment and packaging of the segmented rotavirus genome Trends in Microbiology 19 2011 136 144
49. W. Li, E. Manktelow, J.C. von Kirchbach, J.R. Gog, U. Desselberger, and A.M. Lever Genomic analysis of codon, sequence and structural conservation with selective biochemical-structure mapping reveals highly conserved and dynamic structures in rotavirus RNAs with potential cis-acting functions Nucleic Acids Research 38 2010 7718 7735 An extensive in silico and in vitro characterization of the rotavirus genome that provides evidence of the conservation, complexity and dynamics of rotavirus RNA structures.
50. R.H. Silverman Viral encounters with 2′,5′-oligoadenylate synthetase and RNase L during the interferon antiviral response Journal of Virology 81 2007 12720 12729 (Pubitemid 350156909)
51. J.W.B. Hershey, and W.C. Merrick The pathway and mechanism of initiation of protein synthesis N. Sonenberg, J.W. Hershey, M.B. Mathews, Translational Control of Gene Expression 2000 Cold Spring Harbor Press Cold Spring Harbor, NY 33 88
52. T.V. Pestova, V.G. Kolupaeva, I.B. Lomakin, E.V. Pilipenko, I.N. Shatsky, V.I. Agol, and C.U. Hellen Molecular mechanisms of translation initiation in eukaryotes Proceedings of the National Academy of Sciences of the United States of America 98 2001 7029 7036 (Pubitemid 32567898)
53. C.G. Proud eIF2 and the control of cell physiology Seminars in Cell and Developmental Biology 16 2005 3 12 (Pubitemid 40126871)
54. S.R. Kimball, R.L. Horetsky, D. Ron, L.S. Jefferson, and H.P. Harding Mammalian stress granules represent sites of accumulation of stalled translation initiation complexes American Journal of Physiology - Cell Physiology 284 2003 C273 C284
55. P. Anderson, and N. Kedersha RNA granules Journal of Cell Biology 172 2006 803 808 A very good review that describes the composition of RNA granules.
56. I.E. Gallouzi, C.M. Brennan, M.G. Stenberg, M.S. Swanson, A. Eversole, N. Maizels, and J.A. Steitz HuR binding to cytoplasmic mRNA is perturbed by heat shock Proceedings of the National Academy of Sciences of the United States of America 97 2000 3073 3078 (Pubitemid 30183257)
57. N.L. Kedersha, M. Gupta, W. Li, I. Miller, and P. Anderson RNA-binding proteins TIA-1 and TIAR link the phosphorylation of eIF-2 alpha to the assembly of mammalian stress granules Journal of Cell Biology 147 1999 1431 1442
58. H. Tourriere, K. Chebli, L. Zekri, B. Courselaud, J.M. Blanchard, E. Bertrand, and J. Tazi The RasGAP-associated endoribonuclease G3BP assembles stress granules Journal of Cell Biology 160 2003 823 831 (Pubitemid 36350838)
59. R. Mazroui, R. Sukarieh, M.E. Bordeleau, R.J. Kaufman, P. Northcote, J. Tanaka, I. Gallouzi, and J. Pelletier Inhibition of ribosome recruitment induces stress granule formation independently of eukaryotic initiation factor 2alpha phosphorylation Molecular Biology of the Cell 17 2006 4212 4219 (Pubitemid 44522042)
60. L.G. Abrahamyan, L. Chatel-Chaix, L. Ajamian, M.P. Milev, A. Monette, J.F. Clement, R. Song, M. Lehmann, L. DesGroseillers, and M. Laughrea Novel Staufen1 ribonucleoproteins prevent formation of stress granules but favour encapsidation of HIV-1 genomic RNA Journal of Cell Science 123 2010 369 383
61. Y. Ariumi, M. Kuroki, Y. Kushima, K. Osugi, M. Hijikata, M. Maki, M. Ikeda, and N. Kato Hepatitis C virus hijacks P-body and stress granule components around lipid droplets Journal of Virology 85 2011 6882 6892
62. F. Borghese, and T. Michiels The leader protein of cardioviruses inhibits stress granule assembly Journal of Virology 85 2011 9614 9622
63. M.M. Emara, and M.A. Brinton Interaction of TIA-1/TIAR with West Nile and dengue virus products in infected cells interferes with stress granule formation and processing body assembly Proceedings of the National Academy of Sciences of the United States of America 104 2007 9041 9046 (Pubitemid 47175433)
64. D.A. Khaperskyy, T.F. Hatchette, and C. McCormick Influenza A virus inhibits cytoplasmic stress granule formation FASEB Journal 26 2012 1629 1639
65. G.M. McInerney, N.L. Kedersha, R.J. Kaufman, P. Anderson, and P. Liljestrom Importance of eIF2alpha phosphorylation and stress granule assembly in alphavirus translation regulation Molecular Biology of the Cell 16 2005 3753 3763 (Pubitemid 41077084)
66. Q. Qin, C. Hastings, and C.L. Miller Mammalian orthoreovirus particles induce and are recruited into stress granules at early times postinfection Journal of Virology 83 2009 11090 11101
67. J.P. White, A.M. Cardenas, W.E. Marissen, and R.E. Lloyd Inhibition of cytoplasmic mRNA stress granule formation by a viral proteinase Cell Host Microbe 2 2007 295 305 (Pubitemid 350056396)
68. J.P. White, and R.E. Lloyd Poliovirus unlinks TIA1 aggregation and mRNA stress granule formation Journal of Virology 85 2011 12442 12454
69. D. Ron Translational control in the endoplasmic reticulum stress response Journal of Clinical Investigation 110 2002 1383 1388 (Pubitemid 35396906)
70. P.D. Lu, H.P. Harding, and D. Ron Translation reinitiation at alternative open reading frames regulates gene expression in an integrated stress response Journal of Cell Biology 167 2004 27 33 (Pubitemid 39363411)
71. H.P. Harding, Y. Zhang, A. Bertolotti, H. Zeng, and D. Ron Perk is essential for translational regulation and cell survival during the unfolded protein response Molecular Cell 5 2000 897 904
72. H.P. Harding, Y. Zhang, H. Zeng, I. Novoa, P.D. Lu, M. Calfon, N. Sadri, C. Yun, B. Popko, and R. Paules An integrated stress response regulates amino acid metabolism and resistance to oxidative stress Molecular Cell 11 2003 619 633 (Pubitemid 36385118)
73. C.A. Hetz ER stress signaling and the BCL-2 family of proteins: from adaptation to irreversible cellular damage Antioxidants and Redox Signalling 9 2007 2345 2355 (Pubitemid 350059017)
74. J.D. Malhotra, and R.J. Kaufman The endoplasmic reticulum and the unfolded protein response Seminars in Cell and Developmental Biology 18 2007 716 731 An excellent review of the unfolded protein response. (Pubitemid 350138453)
75. D.T. Rutkowski, S.M. Arnold, C.N. Miller, J. Wu, J. Li, K.M. Gunnison, K. Mori, A.A. Sadighi Akha, D. Raden, and R.J. Kaufman Adaptation to ER stress is mediated by differential stabilities of pro-survival and pro-apoptotic mRNAs and proteins PLoS Biology 4 2006 e374
76. I. Novoa, H. Zeng, H.P. Harding, and D. Ron Feedback inhibition of the unfolded protein response by GADD34-mediated dephosphorylation of eIF2alpha Journal of Cell Biology 153 2001 1011 1022
77. N. Pavio, P.R. Romano, T.M. Graczyk, S.M. Feinstone, and D.R. Taylor Protein synthesis and endoplasmic reticulum stress can be modulated by the hepatitis C virus envelope protein E2 through the eukaryotic initiation factor 2alpha kinase PERK Journal of Virology 77 2003 3578 3585 (Pubitemid 36297277)
78. M. Mulvey, C. Arias, and I. Mohr Maintenance of endoplasmic reticulum (ER) homeostasis in herpes simplex virus type 1-infected cells through the association of a viral glycoprotein with PERK, a cellular ER stress sensor Journal of Virology 81 2007 3377 3390 (Pubitemid 46456647)
79. X. Wang, Y. Liao, P.L. Yap, K.J. Png, J.P. Tam, and D.X. Liu Inhibition of protein kinase R activation and upregulation of GADD34 expression play a synergistic role in facilitating coronavirus replication by maintaining de novo protein synthesis in virus-infected cells Journal of Virology 83 2009 12462 12472
80. J.A. Isler, A.H. Skalet, and J.C. Alwine Human cytomegalovirus infection activates and regulates the unfolded protein response Journal of Virology 79 2005 6890 6899 (Pubitemid 40684492)
81. B. Xuan, Z. Qian, E. Torigoi, and D. Yu Human cytomegalovirus protein pUL38 induces ATF4 expression, inhibits persistent JNK phosphorylation, and suppresses endoplasmic reticulum stress-induced cell death Journal of Virology 83 2009 3463 3474
82. J. Bechill, Z. Chen, J.W. Brewer, and S.C. Baker Coronavirus infection modulates the unfolded protein response and mediates sustained translational repression Journal of Virology 82 2008 4492 4501 (Pubitemid 351563685)
83. J.R. Jheng, K.S. Lau, W.F. Tang, M.S. Wu, and J.T. Horng Endoplasmic reticulum stress is induced and modulated by enterovirus 71 Cellular Microbiology 12 2010 796 813
84. J.A. Smith, S.C. Schmechel, A. Raghavan, M. Abelson, C. Reilly, M.G. Katze, R.J. Kaufman, P.R. Bohjanen, and L.A. Schiff Reovirus induces and benefits from an integrated cellular stress response Journal of Virology 80 2006 2019 2033 (Pubitemid 43228742)
85. T. Kawai, K. Takahashi, S. Sato, C. Coban, H. Kumar, H. Kato, K.J. Ishii, O. Takeuchi, and S. Akira IPS-1, an adaptor triggering RIG-I- and Mda5-mediated type I interferon induction Nature Immunology 6 2005 981 988 (Pubitemid 41486182)
86. R.B. Seth, L. Sun, C.K. Ea, and Z.J. Chen Identification and characterization of MAVS, a mitochondrial antiviral signaling protein that activates NF-kappaB and IRF 3 Cell 122 2005 669 682 (Pubitemid 41242633)
87. L.G. Xu, Y.Y. Wang, K.J. Han, L.Y. Li, Z. Zhai, and H.B. Shu VISA is an adapter protein required for virus-triggered IFN-beta signaling Molecular Cell 19 2005 727 740 (Pubitemid 41316668)