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Abstract

The matrix protein of many enveloped RNA viruses regulates multiple stages of viral life cycle and has the characteristics of nucleocytoplasmic shuttling. We have previously demonstrated that matrix protein 1 (M1) of an RNA virus, influenza virus, blocks host cell cycle progression by interacting with SLD5, a member of the GINS complex, which is required for normal cell cycle progression. In this study, we found that M protein of several other RNA viruses, including VSV, SeV and HIV, interacted with SLD5. Furthermore, VSV/SeV infection and M protein of VSV/SeV/HIV induced cell cycle arrest at G0/G1 phase. Importantly, overexpression of SLD5 partially rescued the cell cycle arrest by VSV/SeV infection and VSV M protein. In addition, SLD5 suppressed VSV replication and , and enhanced type Ⅰ interferon signalling. Taken together, our results suggest that targeting SLD5 by M protein might be a common strategy used by multiple enveloped RNA viruses to block host cell cycle. Our findings provide new mechanistic insights for virus to manipulate cell cycle progression by hijacking host replication factor SLD5 during infection.

Funding
This study was supported by the:
  • National Natural Science Foundation of China (Award 91749112)
    • Principle Award Recipient: MinFang
  • National Natural Science Foundation of China (Award 31970164)
    • Principle Award Recipient: MinFang
  • State Key Laboratory of veterinary biotechnology (Award SKLVBF201901)
    • Principle Award Recipient: MinFang
  • This is an open-access article distributed under the terms of the Creative Commons Attribution License.
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2021-12-09
2024-03-29
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References

  1. Liljeroos L, Butcher SJ. Matrix proteins as centralized organizers of negative-sense RNA virions. Front Biosci 2013; 18:696 [View Article]
    [Google Scholar]
  2. Kordyukova LV, Shtykova EV, Baratova LA, Svergun DI, Batishchev OV. Matrix proteins of enveloped viruses: a case study of Influenza A virus M1 protein. J Biomol Struct Dyn 2019; 37:671–690 [View Article] [PubMed]
    [Google Scholar]
  3. Justice PA, Sun W, Li Y, Ye Z, Grigera PR et al. Membrane vesiculation function and exocytosis of wild-type and mutant matrix proteins of vesicular stomatitis virus. J Virol 1995; 69:3156–3160 [View Article] [PubMed]
    [Google Scholar]
  4. Gómez-Puertas P, Albo C, Pérez-Pastrana E, Vivo A, Portela A. Influenza virus matrix protein is the major driving force in virus budding. J Virol 2000; 74:11538–11547 [View Article] [PubMed]
    [Google Scholar]
  5. Pohl C, Duprex WP, Krohne G, Rima BK, Schneider-Schaulies S. Measles virus M and F proteins associate with detergent-resistant membrane fractions and promote formation of virus-like particles. J Gen Virol 2007; 88:1243–1250 [View Article] [PubMed]
    [Google Scholar]
  6. Hamard-Peron E, Muriaux D. Retroviral matrix and lipids, the intimate interaction. Retrovirology 2011; 8:15 [View Article] [PubMed]
    [Google Scholar]
  7. Dancho B, McKenzie MO, Connor JH, Lyles DS. Vesicular stomatitis virus matrix protein mutations that affect association with host membranes and viral nucleocapsids. J Biol Chem 2009; 284:4500–4509 [View Article] [PubMed]
    [Google Scholar]
  8. Hoenen T, Biedenkopf N, Zielecki F, Jung S, Groseth A et al. Oligomerization of Ebola Virus VP40 Is Essential for Particle Morphogenesis and Regulation of Viral Transcription. J Virol 2010; 84:7053–7063 [View Article] [PubMed]
    [Google Scholar]
  9. Wijesinghe KJ, Urata S, Bhattarai N, Kooijman EE, Gerstman BS et al. Detection of lipid-induced structural changes of the Marburg virus matrix protein VP40 using hydrogen/deuterium exchange-mass spectrometry. J Biol Chem 2017; 292:6108–6122 [View Article] [PubMed]
    [Google Scholar]
  10. Bui M, Wills EG, Helenius A, Whittaker GR. Role of the influenza virus M1 protein in nuclear export of viral ribonucleoproteins. J Virol 2000; 74:1781–1786 [View Article] [PubMed]
    [Google Scholar]
  11. Yoshida T, Nagai Y’Yoshii S, Maeno K, Matsumoto T. Membrane (M) protein of HVJ (Sendai virus): its role in virus assembly. Virology 1976; 71:143–161 [View Article] [PubMed]
    [Google Scholar]
  12. Lyles DS, Puddington L, McCreedy BJ. Vesicular stomatitis virus M protein in the nuclei of infected cells. J Virol 1988; 62:4387–4392 [View Article] [PubMed]
    [Google Scholar]
  13. Nascimento R, Costa H, Parkhouse RME. Virus manipulation of cell cycle. Protoplasma 2012; 249:519–528 [View Article] [PubMed]
    [Google Scholar]
  14. He Y, Xu K, Keiner B, Zhou J, Czudai V et al. Influenza A virus replication induces cell cycle arrest in G0/G1 phase. J Virol 2010; 84:12832–12840 [View Article] [PubMed]
    [Google Scholar]
  15. Jiang W, Wang Q, Chen S, Gao S, Song L et al. Influenza A virus NS1 induces G0/G1 cell cycle arrest by inhibiting the expression and activity of RhoA protein. J Virol 2013; 87:3039–3052 [View Article] [PubMed]
    [Google Scholar]
  16. Zhu L, Zhao W, Lu J, Li S, Zhou K et al. Influenza virus matrix protein M1 interacts with SLD5 to block host cell cycle. Cell Microbiol 2019; 21:e13038. [View Article] [PubMed]
    [Google Scholar]
  17. Moran E. DNA tumor virus transforming proteins and the cell cycle. Curr Opin Genet Dev 1993; 3:63–70 [View Article] [PubMed]
    [Google Scholar]
  18. Helt AM, Galloway DA. Mechanisms by which DNA tumor virus oncoproteins target the Rb family of pocket proteins. Carcinogenesis 2003; 24:159–169 [View Article] [PubMed]
    [Google Scholar]
  19. Paladino P, Marcon E, Greenblatt J, Frappier L. Identification of herpesvirus proteins that contribute to G1/S arrest. J Virol 2014; 88:4480–4492 [View Article] [PubMed]
    [Google Scholar]
  20. Yuan X, Shan Y, Zhao Z, Chen J, Cong Y. G0/G1 arrest and apoptosis induced by SARS-CoV 3b protein in transfected cells. Virol J 2005; 2:66. [View Article] [PubMed]
    [Google Scholar]
  21. Yuan X, Wu J, Shan Y, Yao Z, Dong B et al. SARS coronavirus 7a protein blocks cell cycle progression at G0/G1 phase via the cyclin D3/pRb pathway. Virology 2006; 346:74–85 [View Article] [PubMed]
    [Google Scholar]
  22. Gibbs JD, Ornoff DM, Igo HA, Zeng JY, Imani F. Cell cycle arrest by transforming growth factor beta1 enhances replication of respiratory syncytial virus in lung epithelial cells. J Virol 2009; 83:12424–12431 [View Article] [PubMed]
    [Google Scholar]
  23. Bian T, Gibbs JD, Örvell C, Imani F. Respiratory syncytial virus matrix protein induces lung epithelial cell cycle arrest through a p53 dependent pathway. PLoS One 2012; 7:e38052 [View Article] [PubMed]
    [Google Scholar]
  24. Yu J, Zhang L, Ren P, Zhong T, Li Z et al. Enterovirus 71 mediates cell cycle arrest in S phase through non-structural protein 3D. Cell Cycle 2015; 14:425–436 [View Article] [PubMed]
    [Google Scholar]
  25. Salamango DJ, Ikeda T, Moghadasi SA, Wang J, McCann JL et al. HIV-1 Vif Triggers Cell Cycle Arrest by Degrading Cellular PPP2R5 Phospho-regulators. Cell Reports 2019; 29:1057–1065 [View Article]
    [Google Scholar]
  26. Davy C, Doorbar J. G2/M cell cycle arrest in the life cycle of viruses. Virology 2007; 368:219–226 [View Article] [PubMed]
    [Google Scholar]
  27. Chang YP, Wang G, Bermudez V, Hurwitz J, Chen XS. Crystal structure of the GINS complex and functional insights into its role in DNA replication. Proc Natl Acad Sci U S A 2007; 104:12685–12690 [View Article] [PubMed]
    [Google Scholar]
  28. MacNeill SA. Structure and function of the GINS complex, a key component of the eukaryotic replisome. Biochem J 2010; 425:489–500 [View Article] [PubMed]
    [Google Scholar]
  29. Gouge CA, Christensen TW. Drosophila Sld5 is essential for normal cell cycle progression and maintenance of genomic integrity. Biochem Biophys Res Commun 2010; 400:145–150 [View Article] [PubMed]
    [Google Scholar]
  30. Yamane K, Naito H, Wakabayashi T, Yoshida H, Muramatsu F et al. Regulation of SLD5 gene expression by miR-370 during acute growth of cancer cells. Sci Rep 2016; 6:30941. [View Article] [PubMed]
    [Google Scholar]
  31. Reimers K, Buchholz K, Werchau H. Respiratory syncytial virus M2-1 protein induces the activation of nuclear factor kappa B. Virology 2005; 331:260–268 [View Article] [PubMed]
    [Google Scholar]
  32. Gaudier M, Gaudin Y, Knossow M. Crystal structure of vesicular stomatitis virus matrix protein. EMBO J 2002; 21:2886–2892 [View Article] [PubMed]
    [Google Scholar]
  33. Pan W, Song D, He W, Lu H, Lan Y et al. EIF3i affects vesicular stomatitis virus growth by interacting with matrix protein. Vet Microbiol 2017; 212:59–66 [View Article] [PubMed]
    [Google Scholar]
  34. Luo M. The nucleocapsid of vesicular stomatitis virus. Sci China Life Sci 2012; 55:291–300 [View Article] [PubMed]
    [Google Scholar]
  35. Petersen JM, Her LS, Varvel V, Lund E, Dahlberg JE. The matrix protein of vesicular stomatitis virus inhibits nucleocytoplasmic transport when it is in the nucleus and associated with nuclear pore complexes. Mol Cell Biol 2000; 20:8590–8601 [View Article] [PubMed]
    [Google Scholar]
  36. Glodowski DR, Petersen JM, Dahlberg JE. Complex nuclear localization signals in the matrix protein of vesicular stomatitis virus. J Biol Chem 2002; 277:46864–46870 [View Article] [PubMed]
    [Google Scholar]
  37. Bressy C, Droby GN, Maldonado BD, Steuerwald N, Grdzelishvili VZ. Cell Cycle Arrest in G2/M Phase Enhances Replication of Interferon-Sensitive Cytoplasmic RNA Viruses via Inhibition of Antiviral Gene Expression. J Virol 2019; 93:e01885-18. [View Article] [PubMed]
    [Google Scholar]
  38. Liu SY, Sanchez DJ, Aliyari R, Lu S, Cheng G. Systematic identification of type I and type II interferon-induced antiviral factors. Proc Natl Acad Sci U S A 2012; 109:4239–4244 [View Article] [PubMed]
    [Google Scholar]
  39. Zhang K, Zhang Y, Xue J, Meng Q, Liu H et al. DDX19 Inhibits Type I Interferon Production by Disrupting TBK1-IKKε-IRF3 Interactions and Promoting TBK1 and IKKε Degradation. Cell Reports 2019; 26:1258–1272 [View Article]
    [Google Scholar]
  40. Zheng W, Tao YJ. Structure and assembly of the influenza A virus ribonucleoprotein complex. FEBS Lett 2013; 587:1206–1214 [View Article] [PubMed]
    [Google Scholar]
  41. Aparicio T, Guillou E, Coloma J, Montoya G, Méndez J. The human GINS complex associates with Cdc45 and MCM and is essential for DNA replication. Nucleic Acids Res 2009; 37:2087–2095 [View Article] [PubMed]
    [Google Scholar]
  42. Sha B, Luo M. Structure of a bifunctional membrane-RNA binding protein, influenza virus matrix protein M1. Nat Struct Biol 1997; 4:239–244 [View Article] [PubMed]
    [Google Scholar]
  43. Oliere S, Arguello M, Mesplede T, Tumilasci V, Nakhaei P et al. Vesicular stomatitis virus oncolysis of T lymphocytes requires cell cycle entry and translation initiation. J Virol 2008; 82:5735–5749 [View Article] [PubMed]
    [Google Scholar]
  44. Marozin S, De Toni EN, Rizzani A, Altomonte J, Junger A et al. Cell cycle progression or translation control is not essential for vesicular stomatitis virus oncolysis of hepatocellular carcinoma. PLoS One 2010; 5:e10988 [View Article] [PubMed]
    [Google Scholar]
  45. Chakraborty P, Seemann J, Mishra RK, Wei J-H, Weil L et al. Vesicular stomatitis virus inhibits mitotic progression and triggers cell death. EMBO Rep 2009; 10:1154–1160 [View Article] [PubMed]
    [Google Scholar]
  46. Letchworth GJ, Rodriguez LL, Del cbarrera J. Vesicular stomatitis. Vet J 1999; 157:239–260 [View Article] [PubMed]
    [Google Scholar]
  47. Kim MY, Ma Y, Zhang Y, Li J, Shu Y et al. hsp70-dependent antiviral immunity against cytopathic neuronal infection by vesicular stomatitis virus. J Virol 2013; 87:10668–10678 [View Article] [PubMed]
    [Google Scholar]
  48. Malilas W, Koh SS, Srisuttee R, Boonying W, Cho I-R et al. Cancer upregulated gene 2, a novel oncogene, confers resistance to oncolytic vesicular stomatitis virus through STAT1-OASL2 signaling. Cancer Gene Ther 2013; 20:125–132 [View Article] [PubMed]
    [Google Scholar]
  49. Samuel CE. Antiviral actions of interferons. Clin Microbiol Rev 2001; 14:778–809 [View Article] [PubMed]
    [Google Scholar]
  50. Teijaro JR. Type I interferons in viral control and immune regulation. Curr Opin Virol 2016; 16:31–40 [View Article] [PubMed]
    [Google Scholar]
  51. You F, Sun H, Zhou X, Sun W, Liang S et al. PCBP2 mediates degradation of the adaptor MAVS via the HECT ubiquitin ligase AIP4. Nat Immunol 2009; 10:1300–1308 [View Article] [PubMed]
    [Google Scholar]
  52. Elster C, Larsen K, Gagnon J, Ruigrok RW, Baudin F. Influenza virus M1 protein binds to RNA through its nuclear localization signal. J Gen Virol 1997; 78 (Pt 7):1589–1596 [View Article] [PubMed]
    [Google Scholar]
  53. Ye Z, Robinson D, Wagner RR. Nucleus-targeting domain of the matrix protein (M1) of influenza virus. J Virol 1995; 69:1964–1970 [View Article] [PubMed]
    [Google Scholar]
  54. Gao S, Wang S, Cao S, Sun L, Li J et al. Characteristics of nucleocytoplasmic transport of H1N1 influenza A virus nuclear export protein. J Virol 2014; 88:7455–7463 [View Article] [PubMed]
    [Google Scholar]
  55. Chaimayo C, Hayashi T, Underwood A, Hodges E, Takimoto T. Selective incorporation of vRNP into influenza A virions determined by its specific interaction with M1 protein. Virology 2017; 505:23–32 [View Article] [PubMed]
    [Google Scholar]
  56. Kumar S, Yeo D, Harur Muralidharan N, Lai SK, Tong C et al. Impaired nuclear export of the ribonucleoprotein complex and virus-induced cytotoxicity combine to restrict propagation of the A/Duck/Malaysia/02/2001 (H9N2) virus in human airway cells. Cells 2020; 9:355 [View Article]
    [Google Scholar]
  57. Zhang J, Yu XL, Xu L, Li FZ, Li YG. Sequence Characterization of matrix protein (M1) in influenza A viruses (H1, H3 and H5). Microbiol Res (Pavia) 2011; 2:16 [View Article]
    [Google Scholar]
  58. Terrier O, Carron C, Cartet G, Traversier A, Julien T et al. Ultrastructural fingerprints of avian influenza A (H7N9) virus in infected human lung cells. Virology 2014; 456–457:39–42 [View Article] [PubMed]
    [Google Scholar]
  59. Wang S, Zhao Z, Bi Y, Sun L, Liu X et al. Tyrosine 132 phosphorylation of influenza A virus M1 protein is crucial for virus replication by controlling the nuclear import of M1. J Virol 2013; 87:6182–6191 [View Article] [PubMed]
    [Google Scholar]
  60. Cao S, Jiang J, Li J, Li Y, Yang L et al. Characterization of the nucleocytoplasmic shuttle of the matrix protein of influenza B virus. J Virol 2014; 88:7464–7473 [View Article] [PubMed]
    [Google Scholar]
  61. Zheng W, Fan W, Zhang S, Jiao P, Shang Y et al. Naproxen exhibits broad anti-influenza virus activity in mice by impeding viral nucleoprotein nuclear export. Cell Reports 2019; 27:1875–1885 [View Article]
    [Google Scholar]
  62. Kochs G, Weber F, Gruber S, Delvendahl A, Leitz C et al. Thogoto virus matrix protein is encoded by a spliced mRNA. J Virol 2000; 74:10785–10789 [View Article] [PubMed]
    [Google Scholar]
  63. Coleman NA, Peeples ME. The matrix protein of Newcastle disease virus localizes to the nucleus via a bipartite nuclear localization signal. Virology 1993; 195:596–607 [View Article] [PubMed]
    [Google Scholar]
  64. Duan Z, Xu H, Ji X, Zhao J, Xu H et al. Importin α5 negatively regulates importin β1-mediated nuclear import of Newcastle disease virus matrix protein and viral replication and pathogenicity in chicken fibroblasts. Virulence 2018; 9:783–803 [View Article] [PubMed]
    [Google Scholar]
  65. Duan Z, Deng S, Ji X, Zhao J, Yuan C et al. Nuclear localization of Newcastle disease virus matrix protein promotes virus replication by affecting viral RNA synthesis and transcription and inhibiting host cell transcription. Vet Res 2019; 50:22. [View Article] [PubMed]
    [Google Scholar]
  66. Bauer A, Neumann S, Karger A, Henning A-K, Maisner A et al. ANP32B is a nuclear target of henipavirus M proteins. PLoS One 2014; 9:e97233 [View Article] [PubMed]
    [Google Scholar]
  67. Pentecost M, Vashisht AA, Lester T, Voros T, Beaty SM et al. Evidence for ubiquitin-regulated nuclear and subnuclear trafficking among Paramyxovirinae matrix proteins. PLoS Pathog 2015; 11:e1004739. [View Article] [PubMed]
    [Google Scholar]
  68. McLinton EC, Wagstaff KM, Lee A, Moseley GW, Marsh GA et al. Nuclear localization and secretion competence are conserved among henipavirus matrix proteins. J Gen Virol 2017; 98:563–576 [View Article] [PubMed]
    [Google Scholar]
  69. Wang YE, Park A, Lake M, Pentecost M, Torres B et al. Ubiquitin-regulated nuclear-cytoplasmic trafficking of the Nipah virus matrix protein is important for viral budding. PLoS Pathog 2010; 6:e1001186. [View Article] [PubMed]
    [Google Scholar]
  70. Günther M, Bauer A, Müller M, Zaeck L, Finke S. Interaction of host cellular factor ANP32B with matrix proteins of different paramyxoviruses. J Gen Virol 2020; 101:44–58 [View Article] [PubMed]
    [Google Scholar]
  71. Yu X, Shahriari S, Li H-M, Ghildyal R, Palazzo AF. Measles virus matrix protein inhibits host cell transcription. PLoS One 2016; 11:e0161360 [View Article]
    [Google Scholar]
  72. Sabo Y, Ehrlich M, Bacharach E. The conserved YAGL motif in human metapneumovirus is required for higher-order cellular assemblies of the matrix protein and for virion production. J Virol 2011; 85:6594–6609 [View Article] [PubMed]
    [Google Scholar]
  73. Ghildyal R, Ho A, Wagstaff KM, Dias MM, Barton CL et al. Nuclear import of the respiratory syncytial virus matrix protein is mediated by importin beta1 independent of importin alpha. Biochemistry 2005; 44:12887–12895 [View Article] [PubMed]
    [Google Scholar]
  74. Ghildyal R, Ho A, Jans DA. Central role of the respiratory syncytial virus matrix protein in infection. FEMS Microbiol Rev 2006; 30:692–705 [View Article] [PubMed]
    [Google Scholar]
  75. Ghildyal R, Ho A, Dias M, Soegiyono L, Bardin PG et al. The respiratory syncytial virus matrix protein possesses a Crm1-mediated nuclear export mechanism. J Virol 2009; 83:5353–5362 [View Article] [PubMed]
    [Google Scholar]
  76. Nakahara K, Ohnuma H, Sugita S, Yasuoka K, Nakahara T et al. Intracellular behavior of rabies virus matrix protein (M) is determined by the viral glycoprotein (G). Microbiol Immunol 1999; 43:259–270 [View Article] [PubMed]
    [Google Scholar]
  77. Zan J, Liu S, Sun D-N, Mo K-K, Yan Y et al. Rabies virus infection induces microtubule depolymerization to facilitate viral RNA synthesis by upregulating HDAC6. Front Cell Infect Microbiol 2017; 7:146. [View Article] [PubMed]
    [Google Scholar]
  78. Cheng CY, Shih WL, Huang WR, Chi PI, Wu MH et al. Bovine ephemeral fever virus uses a clathrin-mediated and dynamin 2-dependent endocytosis pathway that requires Rab5 and Rab7 as well as microtubules. J Virol 2012; 86:13653–13661 [View Article] [PubMed]
    [Google Scholar]
  79. Valmas C, Grosch MN, Schümann M, Olejnik J, Martinez O et al. Marburg virus evades interferon responses by a mechanism distinct from ebola virus. PLoS Pathog 2010; 6:e1000721. [View Article] [PubMed]
    [Google Scholar]
  80. Nanbo A, Watanabe S, Halfmann P, Kawaoka Y. The spatio-temporal distribution dynamics of Ebola virus proteins and RNA in infected cells. Sci Rep 2013; 3:1206. [View Article] [PubMed]
    [Google Scholar]
  81. Kolesnikova L, Bugany H, Klenk HD, Becker S. VP40, the matrix protein of Marburg virus, is associated with membranes of the late endosomal compartment. J Virol 2002; 76:1825–1838 [View Article] [PubMed]
    [Google Scholar]
  82. Honda T, Tomonaga K. Nucleocytoplasmic shuttling of viral proteins in borna disease virus infection. Viruses 2013; 5:1978–1990 [View Article] [PubMed]
    [Google Scholar]
  83. Bukrinsky MI, Haggerty S, Dempsey MP, Sharova N, Adzhubel A et al. A nuclear localization signal within HIV-1 matrix protein that governs infection of non-dividing cells. Nature 1993; 365:666–669 [View Article] [PubMed]
    [Google Scholar]
  84. Haffar OK, Popov S, Dubrovsky L, Agostini I, Tang H et al. Two nuclear localization signals in the HIV-1 matrix protein regulate nuclear import of the HIV-1 pre-integration complex. J Mol Biol 2000; 299:359–368 [View Article] [PubMed]
    [Google Scholar]
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