Interplay between coronavirus, a cytoplasmic RNA virus, and nonsense-mediated mRNA decay pathway

Proceedings of the National Academy of Sciences of the United States of America

Volumn 115, Issue 43, 2018, Pages E10157-E10166

  Wada, Masami ^a   Lokugamage, Kumari G ^a   Nakagawa, Keisuke ^a   Narayanan, Krishna ^a   Makino, Shinji ^a,b  

^a University of Texas Medical Branch School of Medicine   (United States)

^b UNIVERSITY OF TEXAS MEDICAL BRANCH   (United States)

Author keywords

Coronavirus; Cytoplasmic RNA virus; Inhibition of NMD; Long 3' UTR; Nonsense mediated mRNA decay

Indexed keywords

GENOMIC RNA; GUANINE NUCLEOTIDE BINDING PROTEIN; MESSENGER RNA;

ANIMAL CELL; ARTICLE; BIOACCUMULATION; CONTROLLED STUDY; FIBROBLAST; MOUSE; MURINE HEPATITIS VIRUS; NONHUMAN; NONSENSE MEDIATED MRNA DECAY; PRIORITY JOURNAL; RNA DEGRADATION; RNA SYNTHESIS; VIRUS REPLICATION; 3' UNTRANSLATED REGION; ANIMAL; CORONAVIRINAE; CYTOPLASM; GENETICS; OPEN READING FRAME; RNA STABILITY; RNA VIRUS;

3' UNTRANSLATED REGIONS; ANIMALS; CORONAVIRUS; CYTOPLASM; MICE; NONSENSE MEDIATED MRNA DECAY; OPEN READING FRAMES; RNA STABILITY; RNA VIRUSES; RNA, MESSENGER; VIRUS REPLICATION;

EID: 85055601012     PISSN: 00278424     EISSN: 10916490     Source Type: Journal    
DOI: 10.1073/pnas.1811675115     Document Type: Article

References (56)

1. Memish ZA, et al. (2013) Middle East respiratory syndrome coronavirus in bats, Saudi Arabia. Emerg Infect Dis 19: 1819-1823.
2. Lau SK, et al. (2005) Severe acute respiratory syndrome coronavirus-like virus in Chinese horseshoe bats. Proc Natl Acad Sci USA 102: 14040-14045.
3. Li W, et al. (2005) Bats are natural reservoirs of SARS-like coronaviruses. Science 310: 676-679.
4. Fendrick AM, Monto AS, Nightengale B, Sarnes M (2003) The economic burden of non-influenza-related viral respiratory tract infection in the United States. Arch Intern Med 163: 487-494.
5. Keogh-Brown MR, Smith RD (2008) The economic impact of SARS: How does the reality match the predictions? Health Policy 88: 110-120.
6. Masters PS (2006) The molecular biology of coronaviruses. Adv Virus Res 66: 193-292.
7. Neuman BW, Chamberlain P, Bowden F, Joseph J (2014) Atlas of coronavirus replicase structure. Virus Res 194: 49-66.
8. Narayanan K, Huang C, Makino S (2008) SARS coronavirus accessory proteins. Virus Res 133: 113-121.
9. Menachery VD, et al. (2017) MERS-CoV accessory ORFs play key role for infection and pathogenesis. MBio 8: e00665-17.
10. Schweingruber C, Rufener SC, Zünd D, Yamashita A, Mühlemann O (2013) Nonsensemediated mRNA decay-Mechanisms of substrate mRNA recognition and degradation in mammalian cells. Biochim Biophys Acta 1829: 612-623.
11. Isken O, Maquat LE (2008) The multiple lives of NMD factors: Balancing roles in gene and genome regulation. Nat Rev Genet 9: 699-712.
12. Durand S, Lykke-Andersen J (2013) Nonsense-mediated mRNA decay occurs during eIF4F-dependent translation in human cells. Nat Struct Mol Biol 20: 702-709.
13. Garcia D, Garcia S, Voinnet O (2014) Nonsense-mediated decay serves as a general viral restriction mechanism in plants. Cell Host Microbe 16: 391-402.
14. Withers JB, Beemon KL (2011) The structure and function of the Rous sarcoma virus RNA stability element. J Cell Biochem 112: 3085-3092.
15. Hurt JA, Robertson AD, Burge CB (2013) Global analyses of UPF1 binding and function reveal expanded scope of nonsense-mediated mRNA decay. Genome Res 23: 1636-1650.
16. Balistreri G, et al. (2014) The host nonsense-mediated mRNA decay pathway restricts mammalian RNA virus replication. Cell Host Microbe 16: 403-411.
17. Ramage HR, et al. (2015) A combined proteomics/genomics approach links hepatitis C virus infection with nonsense-mediated mRNA decay. Mol Cell 57: 329-340.
18. Sturman LS, Takemoto KK (1972) Enhanced growth of a murine coronavirus in transformed mouse cells. Infect Immun 6: 501-507.
19. Boelz S, Neu-Yilik G, Gehring NH, Hentze MW, Kulozik AE (2006) A chemiluminescencebased reporter system to monitor nonsense-mediated mRNA decay. Biochem Biophys Res Commun 349: 186-191.
20. Hug N, Longman D, Cáceres JF (2016) Mechanism and regulation of the nonsensemediated decay pathway. Nucleic Acids Res 44: 1483-1495.
21. Popp MW, Maquat LE (2013) Organizing principles of mammalian nonsensemediated mRNA decay. Annu Rev Genet 47: 139-165.
22. Yamashita A, Ohnishi T, Kashima I, Taya Y, Ohno S (2001) Human SMG-1, a novel phosphatidylinositol 3-kinase-related protein kinase, associates with components of the mRNA surveillance complex and is involved in the regulation of nonsensemediated mRNA decay. Genes Dev 15: 2215-2228.
23. Brumbaugh KM, et al. (2004) The mRNA surveillance protein hSMG-1 functions in genotoxic stress response pathways in mammalian cells. Mol Cell 14: 585-598.
24. Beaty SM, et al. (2017) Efficient and robust Paramyxoviridae reverse genetics systems. MSphere 2: e00376-16.
25. Kanai Y, et al. (2017) Entirely plasmid-based reverse genetics system for rotaviruses. Proc Natl Acad Sci USA 114: 2349-2354.
26. Morgan JR, Cohen LK, Roberts BE (1984) Identification of the DNA sequences encoding the large subunit of the mRNA-capping enzyme of vaccinia virus. J Virol 52: 206-214.
27. Niles EG, Lee-Chen GJ, Shuman S, Moss B, Broyles SS (1989) Vaccinia virus gene D12L encodes the small subunit of the viral mRNA capping enzyme. Virology 172: 513-522.
28. Ensinger MJ, Martin SA, Paoletti E, Moss B (1975) Modification of the 5'-terminus of mRNA by soluble guanylyl and methyl transferases from vaccinia virus. Proc Natl Acad Sci USA 72: 2525-2529.
29. Elroy-Stein O, Moss B (1990) Cytoplasmic expression system based on constitutive synthesis of bacteriophage T7 RNA polymerase in mammalian cells. Proc Natl Acad Sci USA 87: 6743-6747.
30. Karam R, et al. (2015) The unfolded protein response is shaped by the NMD pathway. EMBO Rep 16: 599-609.
31. Cuccurese M, Russo G, Russo A, Pietropaolo C (2005) Alternative splicing and nonsense-mediated mRNA decay regulate mammalian ribosomal gene expression. Nucleic Acids Res 33: 5965-5977.
32. Maquat LE, Tarn WY, Isken O (2010) The pioneer round of translation: Features and functions. Cell 142: 368-374.
33. Carter MS, et al. (1995) A regulatory mechanism that detects premature nonsense codons in T-cell receptor transcripts in vivo is reversed by protein synthesis inhibitors in vitro. J Biol Chem 270: 28995-29003.
34. Noensie EN, Dietz HC (2001) A strategy for disease gene identification through nonsense-mediated mRNA decay inhibition. Nat Biotechnol 19: 434-439.
35. Banerjee S, An S, Zhou A, Silverman RH, Makino S (2000) RNase L-independent specific 28S rRNA cleavage in murine coronavirus-infected cells. J Virol 74: 8793-8802.
36. Siddell S, Wege H, Barthel A, ter Meulen V (1981) Coronavirus JHM: Intracellular protein synthesis. J Gen Virol 53: 145-155.
37. Huang C, et al. (2011) Alphacoronavirus transmissible gastroenteritis virus nsp1 protein suppresses protein translation in mammalian cells and in cell-free HeLa cell extracts but not in rabbit reticulocyte lysate. J Virol 85: 638-643.
38. Kim JC, Spence RA, Currier PF, Lu X, Denison MR (1995) Coronavirus protein processing and RNA synthesis is inhibited by the cysteine proteinase inhibitor E64d. Virology 208: 1-8.
39. Balistreri G, Bognanni C, Mühlemann O (2017) Virus escape and manipulation of cellular nonsense-mediated mRNA decay. Viruses 9: E24.
40. Weil JE, Beemon KL (2006) A 3' UTR sequence stabilizes termination codons in the unspliced RNA of Rous sarcoma virus. RNA 12: 102-110.
41. Nakano K, et al. (2013) Viral interference with host mRNA surveillance, the nonsensemediated mRNA decay (NMD) pathway, through a new function of HTLV-1 Rex: Implications for retroviral replication. Microbes Infect 15: 491-505.
42. Mocquet V, et al. (2012) The human T-lymphotropic virus type 1 tax protein inhibits nonsense-mediated mRNA decay by interacting with INT6/EIF3E and UPF1. J Virol 86: 7530-7543.
43. Serquiña AK, et al. (2013) UPF1 is crucial for the infectivity of human immunodeficiency virus type 1 progeny virions. J Virol 87: 8853-8861.
44. Ajamian L, et al. (2015) HIV-1 recruits UPF1 but excludes UPF2 to promote nucleocytoplasmic export of the genomic RNA. Biomolecules 5: 2808-2839.
45. Ajamian L, et al. (2008) Unexpected roles for UPF1 in HIV-1 RNA metabolism and translation. RNA 14: 914-927.
46. Matsuda D, Hosoda N, Kim YK, Maquat LE (2007) Failsafe nonsense-mediated mRNA decay does not detectably target eIF4E-bound mRNA. Nat Struct Mol Biol 14: 974-979.
47. Li Y, Masaki T, Yamane D, McGivern DR, Lemon SM (2013) Competing and noncompeting activities of miR-122 and the 5' exonuclease Xrn1 in regulation of hepatitis C virus replication. Proc Natl Acad Sci USA 110: 1881-1886.
48. Yount B, et al. (2003) Reverse genetics with a full-length infectious cDNA of severe acute respiratory syndrome coronavirus. Proc Natl Acad Sci USA 100: 12995-13000.
49. Casais R, Thiel V, Siddell SG, Cavanagh D, Britton P (2001) Reverse genetics system for the avian coronavirus infectious bronchitis virus. J Virol 75: 12359-12369.
50. Yount B, Denison MR, Weiss SR, Baric RS (2002) Systematic assembly of a full-length infectious cDNA of mouse hepatitis virus strain A59. J Virol 76: 11065-11078.
51. Curtis KM, Yount B, Baric RS (2002) Heterologous gene expression from transmissible gastroenteritis virus replicon particles. J Virol 76: 1422-1434.
52. Emmott E, et al. (2013) The cellular interactome of the coronavirus infectious bronchitis virus nucleocapsid protein and functional implications for virus biology. J Virol 87: 9486-9500.
53. Jourdan SS, Osorio F, Hiscox JA (2012) An interactome map of the nucleocapsid protein from a highly pathogenic North American porcine reproductive and respiratory syndrome virus strain generated using SILAC-based quantitative proteomics. Proteomics 12: 1015-1023.
54. Hirano N, Fujiwara K, Hino S, Matumoto M (1974) Replication and plaque formation of mouse hepatitis virus (MHV-2) in mouse cell line DBT culture. Arch Gesamte Virusforsch 44: 298-302.
55. Huang C, et al. (2011) SARS coronavirus nsp1 protein induces template-dependent endonucleolytic cleavage of mRNAs: Viral mRNAs are resistant to nsp1-induced RNA cleavage. PLoS Pathog 7: e1002433.
56. Makino S, Taguchi F, Fujiwara K (1984) Defective interfering particles of mouse hepatitis virus. Virology 133: 9-17.