Host Cell Restriction Factors of Paramyxoviruses and Pneumoviruses
Abstract
:1. Introduction
2. Infection of Host Cells and Viral Replication
3. Virus Interactions with the Innate Immune System
4. Host Cell Restriction Factors
5. Restriction Factors that Affect Viral Entry and Fusion
5.1. Interferon Inducible Transmembrane Proteins (IFITM)
5.2. Cholesterol-25-Hydroxylase (CH25H)
6. Restriction Factors that Affect Virus Transcription, Translation, or Protein Synthesis
6.1. IFN-Induced Proteins with Tetratricopeptide Repeats (IFIT)
6.2. Myxovirus Resistance (Mx) Proteins and Other GTPases
6.3. 2′-5′ Oligosynthetase Proteins (OAS)
6.4. Apolipoprotein B (apoB) mRNA-Editing Enzyme Catalytic Polypeptide (APOBEC) Proteins
6.5. Indoleamine 2,3-Dioxygenase (IDO)
6.6. Protein Kinase R (PKR)
6.7. Interferon Stimulated Gene 15 (ISG15)
6.8. Other Host Restriction Factors
7. Restriction Factors that Affect Virus Release
7.1. Viperin
7.2. Tetherin
8. Perspective and Conclusions
Author Contributions
Funding
Conflicts of Interest
References
- Audsley, M.D.; Moseley, G.W. Paramyxovirus evasion of innate immunity: Diverse strategies for common targets. World J. Virol. 2013, 2, 57–70. [Google Scholar] [CrossRef] [PubMed]
- Rima, B.; Balkema-Buschmann, A.; Dundon, W.G.; Duprex, P.; Easton, A.; Fouchier, R.; Kurath, G.; Lamb, R.; Lee, B.; Rota, P.; et al. ICTV Virus Taxonomy Profile: Paramyxoviridae. J. Gen. Virol. 2019, 100, 1593–1594. [Google Scholar] [CrossRef] [PubMed]
- Rima, B.; Collins, P.; Easton, A.; Fouchier, R.; Kurath, G.; Lamb, R.A.; Lee, B.; Maisner, A.; Rota, P.; Wang, L.; et al. ICTV Virus Taxonomy Profile: Pneumoviridae. J. Gen. Virol. 2017, 98, 2912–2913. [Google Scholar] [CrossRef] [PubMed]
- Rubin, S.; Eckhaus, M.; Rennick, L.J.; Bamford, C.G.G.; Duprex, W.P. Molecular biology, pathogenesis and pathology of mumps virus. J. Pathol. 2015, 235, 242–252. [Google Scholar] [CrossRef]
- Misin, A.; Antonello, R.M.; Di Bella, S.; Campisciano, G.; Zanotta, N.; Giacobbe, D.R.; Comar, M.; Luzzati, R. Measles: An Overview of a Re-Emerging Disease in Children and Immunocompromised Patients. Microorganisms 2020, 8, 276. [Google Scholar] [CrossRef] [Green Version]
- Jafri, S.K.; Kumar, R.; Ibrahim, S.H. Subacute sclerosing panencephalitis-current perspectives. Pediatric. Health Med. Ther. 2018, 9, 67–71. [Google Scholar] [CrossRef] [Green Version]
- Samal, S.K. Paramyxoviruses of Animals. Encycl. Virol. 2008, 40–47. [Google Scholar] [CrossRef]
- Brown, V.R.; Bevins, S.N. A review of virulent Newcastle disease viruses in the United States and the role of wild birds in viral persistence and spread. Vet. Res. 2017, 48, 68. [Google Scholar] [CrossRef] [Green Version]
- Plemper, R.K.; Snyder, J.P. Measles control--can measles virus inhibitors make a difference? Curr. Opin. Investig. Drugs 2009, 10, 811–820. [Google Scholar]
- Schnorr, J.J.; Schneider-Schaulies, S.; Simon-Jödicke, A.; Pavlovic, J.; Horisberger, M.A.; ter Meulen, V. MxA-dependent inhibition of measles virus glycoprotein synthesis in a stably transfected human monocytic cell line. J. Virol. 1993, 67, 4760–4768. [Google Scholar] [CrossRef] [Green Version]
- Fehrholz, M.; Kendl, S.; Prifert, C.; Weissbrich, B.; Lemon, K.; Rennick, L.; Duprex, P.W.; Rima, B.K.; Koning, F.A.; Holmes, R.K.; et al. The innate antiviral factor APOBEC3G targets replication of measles, mumps and respiratory syncytial viruses. J. Gen. Virol. 2012, 93, 565–576. [Google Scholar] [CrossRef]
- Kurokawa, C.; Iankov, I.D.; Galanis, E. A key anti-viral protein, RSAD2/VIPERIN, restricts the release of measles virus from infected cells. Virus Res. 2019, 263, 145–150. [Google Scholar] [CrossRef]
- Braun, E.; Hotter, D.; Koepke, L.; Zech, F.; Groß, R.; Sparrer, K.M.J.; Müller, J.A.; Pfaller, C.K.; Heusinger, E.; Wombacher, R.; et al. Guanylate-Binding Proteins 2 and 5 Exert Broad Antiviral Activity by Inhibiting Furin-Mediated Processing of Viral Envelope Proteins. Cell Rep. 2019, 27, 2092–2104.e10. [Google Scholar] [CrossRef] [PubMed] [Green Version]
- Obojes, K.; Andres, O.; Kim, K.S.; Däubener, W.; Schneider-Schaulies, J. Indoleamine 2,3-dioxygenase mediates cell type-specific anti-measles virus activity of gamma interferon. J. Virol. 2005, 79, 7768–7776. [Google Scholar] [CrossRef] [Green Version]
- Okonski, K.M.; Samuel, C.E. Stress granule formation induced by measles virus is protein kinase PKR dependent and impaired by RNA adenosine deaminase ADAR1. J. Virol. 2013, 87, 756–766. [Google Scholar] [CrossRef] [Green Version]
- Smith, S.E.; Busse, D.C.; Binter, S.; Weston, S.; Diaz Soria, C.; Laksono, B.M.; Clare, S.; Van Nieuwkoop, S.; Van den Hoogen, B.G.; Clement, M.; et al. Interferon-Induced Transmembrane Protein 1 Restricts Replication of Viruses That Enter Cells via the Plasma Membrane. J. Virol. 2019, 93, e02003-18. [Google Scholar] [CrossRef] [Green Version]
- Hviid, A.; Rubin, S.; Mühlemann, K. Mumps. Lancet (Lond. Engl.) 2008, 371, 932–944. [Google Scholar] [CrossRef]
- Young, D.F.; Andrejeva, J.; Li, X.; Inesta-Vaquera, F.; Dong, C.; Cowling, V.H.; Goodbourn, S.; Randall, R.E. Human IFIT1 Inhibits mRNA Translation of Rubulaviruses but Not Other Members of the Paramyxoviridae Family. J. Virol. 2016, 90, 9446–9456. [Google Scholar] [CrossRef] [Green Version]
- Shahani, L.; Ariza-Heredia, E.J.; Chemaly, R.F. Antiviral therapy for respiratory viral infections in immunocompromised patients. Expert Rev. Anti Infect. Ther. 2017, 15, 401–415. [Google Scholar] [CrossRef]
- Zhao, H.; De, B.P.; Das, T.; Banerjee, A.K. Inhibition of human parainfluenza virus-3 replication by interferon and human MxA. Virology 1996, 220, 330–338. [Google Scholar] [CrossRef] [Green Version]
- Subramanian, G.; Kuzmanovic, T.; Zhang, Y.; Peter, C.B.; Veleeparambil, M.; Chakravarti, R.; Sen, G.C.; Chattopadhyay, S. A new mechanism of interferon’s antiviral action: Induction of autophagy, essential for paramyxovirus replication, is inhibited by the interferon stimulated gene, TDRD7. PLoS Pathog. 2018, 14, e1006877. [Google Scholar] [CrossRef] [PubMed] [Green Version]
- Rabbani, M.A.; Ribaudo, M.; Guo, J.T.; Barik, S. Identification of Interferon-Stimulated Gene Proteins That Inhibit Human Parainfluenza Virus Type 3. J. Virol. 2016, 90, 11145–11156. [Google Scholar] [CrossRef] [PubMed] [Green Version]
- Andrejeva, J.; Norsted, H.; Habjan, M.; Thiel, V.; Goodbourn, S.; Randall, R.E. ISG56/IFIT1 is primarily responsible for interferon-induced changes to patterns of parainfluenza virus type 5 transcription and protein synthesis. J. Gen. Virol. 2013, 94, 59–68. [Google Scholar] [CrossRef] [PubMed] [Green Version]
- Dimitrov, K.M.; Afonso, C.L.; Yu, Q.; Miller, P.J. Newcastle disease vaccines—A solved problem or a continuous challenge? Vet. Microbiol. 2017, 206, 126–136. [Google Scholar] [CrossRef]
- Yang, C.; Liu, F.; Chen, S.; Wang, M.; Jia, R.; Zhu, D.; Liu, M.; Sun, K.; Yang, Q.; Wu, Y.; et al. Identification of 2′-5′-Oligoadenylate Synthetase-Like Gene in Goose: Gene Structure, Expression Patterns, and Antiviral Activity Against Newcastle Disease Virus. J. Interferon Cytokine Res. Off. J. Int. Soc. Interferon Cytokine Res. 2016, 36, 563–572. [Google Scholar] [CrossRef] [Green Version]
- Wang, W.; Chang, X.; Yao, W.; Wei, N.; Huo, N.; Wang, Y.; Wei, Q.; Liu, H.; Wang, X.; Zhang, S.; et al. Host CARD11 Inhibits Newcastle Disease Virus Replication by Suppressing Viral Polymerase Activity in Neurons. J. Virol. 2019, 93, e01499-193. [Google Scholar] [CrossRef]
- Shi, M.; Tan, L.; Zhang, Y.; Meng, C.; Wang, W.; Sun, Y.; Song, C.; Liu, W.; Liao, Y.; Yu, S.; et al. Characterization and functional analysis of chicken APOBEC4. Dev. Comp. Immunol. 2020, 106, 103631. [Google Scholar] [CrossRef]
- Santhakumar, D.; Rohaim, M.; Hussein, H.A.; Hawes, P.; Ferreira, H.L.; Behboudi, S.; Iqbal, M.; Nair, V.; Arns, C.W.; Munir, M. Chicken Interferon-induced Protein with Tetratricopeptide Repeats 5 Antagonizes Replication of RNA Viruses. Sci. Rep. 2018, 8, 6794. [Google Scholar] [CrossRef] [Green Version]
- Hu, Y.; Wang, J.; Yang, B.; Zheng, N.; Qin, M.; Ji, Y.; Lin, G.; Tian, L.; Wu, X.; Wu, L.; et al. Guanylate binding protein 4 negatively regulates virus-induced type I IFN and antiviral response by targeting IFN regulatory factor 7. J. Immunol. 2011, 187, 6456–6462. [Google Scholar] [CrossRef] [Green Version]
- Kong, W.S.; Irie, T.; Yoshida, A.; Kawabata, R.; Kadoi, T.; Sakaguchi, T. Inhibition of virus-like particle release of Sendai virus and Nipah virus, but not that of mumps virus, by tetherin/CD317/BST-2. Hiroshima J. Med Sci. 2012, 61, 59–67. [Google Scholar]
- Liu, S.Y.; Aliyari, R.; Chikere, K.; Li, G.; Marsden, M.D.; Smith, J.K.; Pernet, O.; Guo, H.; Nusbaum, R.; Zack, J.A.; et al. Interferon-inducible cholesterol-25-hydroxylase broadly inhibits viral entry by production of 25-hydroxycholesterol. Immunity 2013, 38, 92–105. [Google Scholar] [CrossRef] [PubMed] [Green Version]
- McMichael, T.M.; Zhang, Y.; Kenney, A.D.; Zhang, L.; Zani, A.; Lu, M.; Chemudupati, M.; Li, J.; Yount, J.S. IFITM3 Restricts Human Metapneumovirus Infection. J. Infect. Dis. 2018, 218, 1582–1591. [Google Scholar] [CrossRef] [PubMed] [Green Version]
- Everitt, A.R.; Clare, S.; McDonald, J.U.; Kane, L.; Harcourt, K.; Ahras, M.; Lall, A.; Hale, C.; Rodgers, A.; Young, D.B.; et al. Defining the range of pathogens susceptible to Ifitm3 restriction using a knockout mouse model. PLoS ONE 2013, 8, e80723. [Google Scholar] [CrossRef] [PubMed] [Green Version]
- Rajan, D.; Chinnadurai, R.; O’Keefe, E.L.; Boyoglu-Barnum, S.; Todd, S.O.; Hartert, T.V.; Galipeau, J.; Anderson, L.J. Protective role of Indoleamine 2,3 dioxygenase in Respiratory Syncytial Virus associated immune response in airway epithelial cells. Virology 2017, 512, 144–150. [Google Scholar] [CrossRef]
- Behera, A.K.; Kumar, M.; Lockey, R.F.; Mohapatra, S.S. 2′-5′ Oligoadenylate synthetase plays a critical role in interferon-gamma inhibition of respiratory syncytial virus infection of human epithelial cells. J. Biol. Chem. 2002, 277, 25601–25608. [Google Scholar] [CrossRef] [Green Version]
- González-Sanz, R.; Mata, M.; Bermejo-Martín, J.; Álvarez, A.; Cortijo, J.; Melero, J.A.; Martínez, I. ISG15 Is Upregulated in Respiratory Syncytial Virus Infection and Reduces Virus Growth through Protein ISGylation. J. Virol. 2016, 90, 3428–3438. [Google Scholar] [CrossRef] [Green Version]
- Lindquist, M.E.; Mainou, B.A.; Dermody, T.S.; Crowe, J.E., Jr. Activation of protein kinase R is required for induction of stress granules by respiratory syncytial virus but dispensable for viral replication. Virology 2011, 413, 103–110. [Google Scholar] [CrossRef] [Green Version]
- McGillivary, G.; Jordan, Z.B.; Peeples, M.E.; Bakaletz, L.O. Replication of respiratory syncytial virus is inhibited by the host defense molecule viperin. J. Innate Immun. 2013, 5, 60–71. [Google Scholar] [CrossRef]
- Di Pietrantonj, C.; Rivetti, A.; Marchione, P.; Debalini, M.G.; Demicheli, V. Vaccines for measles, mumps, rubella, and varicella in children. Cochrane Database Syst. Rev. 2020, 4, Cd004407. [Google Scholar] [CrossRef]
- Parks, G.D.; Alexander-Miller, M.A. Paramyxovirus activation and inhibition of innate immune responses. J. Mol. Biol. 2013, 425, 4872–4892. [Google Scholar] [CrossRef] [Green Version]
- Noton, S.L.; Fearns, R. Initiation and regulation of paramyxovirus transcription and replication. Virology 2015, 479–480, 545–554. [Google Scholar] [CrossRef] [PubMed] [Green Version]
- Smith, E.C.; Popa, A.; Chang, A.; Masante, C.; Dutch, R.E. Viral entry mechanisms: The increasing diversity of paramyxovirus entry. Febs J. 2009, 276, 7217–7227. [Google Scholar] [CrossRef] [PubMed] [Green Version]
- Dou, D.; Revol, R.; Östbye, H.; Wang, H.; Daniels, R. Influenza A Virus Cell Entry, Replication, Virion Assembly and Movement. Front. Immunol. 2018, 9, 1581. [Google Scholar] [CrossRef] [PubMed]
- Harrison, M.S.; Sakaguchi, T.; Schmitt, A.P. Paramyxovirus assembly and budding: Building particles that transmit infections. Int. J. Biochem. Cell Biol. 2010, 42, 1416–1429. [Google Scholar] [CrossRef] [Green Version]
- Takeuchi, O.; Akira, S. Innate immunity to virus infection. Immunol. Rev. 2009, 227, 75–86. [Google Scholar] [CrossRef]
- Tapia, K.; Kim, W.-K.; Sun, Y.; Mercado-López, X.; Dunay, E.; Wise, M.; Adu, M.; López, C.B. Defective viral genomes arising in vivo provide critical danger signals for the triggering of lung antiviral immunity. PLoS Pathog. 2013, 9, e1003703. [Google Scholar] [CrossRef]
- Sun, Y.; Jain, D.; Koziol-White, C.J.; Genoyer, E.; Gilbert, M.; Tapia, K.; Panettieri, R.A., Jr.; Hodinka, R.L.; López, C.B. Immunostimulatory Defective Viral Genomes from Respiratory Syncytial Virus Promote a Strong Innate Antiviral Response during Infection in Mice and Humans. PLoS Pathog. 2015, 11, e1005122. [Google Scholar] [CrossRef] [Green Version]
- Sadler, A.J.; Williams, B.R. Interferon-inducible antiviral effectors. Nat. Rev. Immunol. 2008, 8, 559–568. [Google Scholar] [CrossRef]
- Tau, G.; Rothman, P. Biologic functions of the IFN-gamma receptors. Allergy 1999, 54, 1233–1251. [Google Scholar] [CrossRef]
- Kang, S.; Brown, H.M.; Hwang, S. Direct Antiviral Mechanisms of Interferon-Gamma. Immune Netw. 2018, 18, e33. [Google Scholar] [CrossRef]
- Lazear, H.M.; Schoggins, J.W.; Diamond, M.S. Shared and Distinct Functions of Type I and Type III Interferons. Immunity 2019, 50, 907–923. [Google Scholar] [CrossRef] [PubMed]
- Sedeyn, K.; Schepens, B.; Saelens, X. Respiratory syncytial virus nonstructural proteins 1 and 2: Exceptional disrupters of innate immune responses. PLoS Pathog. 2019, 15, e1007984. [Google Scholar] [CrossRef] [PubMed]
- Chemudupati, M.; Kenney, A.D.; Bonifati, S.; Zani, A.; McMichael, T.M.; Wu, L.; Yount, J.S. From APOBEC to ZAP: Diverse mechanisms used by cellular restriction factors to inhibit virus infections. Biochim. Et Biophys. Acta. Mol. Cell Res. 2019, 1866, 382–394. [Google Scholar] [CrossRef] [PubMed]
- Colomer-Lluch, M.; Ruiz, A.; Moris, A.; Prado, J.G. Restriction Factors: From Intrinsic Viral Restriction to Shaping Cellular Immunity Against HIV-1. Front. Immunol. 2018, 9, 2876. [Google Scholar] [CrossRef] [Green Version]
- Villalón-Letelier, F.; Brooks, A.G.; Saunders, P.M.; Londrigan, S.L.; Reading, P.C. Host Cell Restriction Factors that Limit Influenza A Infection. Viruses 2017, 9, 376. [Google Scholar] [CrossRef] [Green Version]
- Diamond, M.S.; Farzan, M. The broad-spectrum antiviral functions of IFIT and IFITM proteins. Nat. Rev. Immunol. 2013, 13, 46–57. [Google Scholar] [CrossRef]
- Yount, J.S.; Karssemeijer, R.A.; Hang, H.C. S-palmitoylation and ubiquitination differentially regulate interferon-induced transmembrane protein 3 (IFITM3)-mediated resistance to influenza virus. J. Biol. Chem. 2012, 287, 19631–19641. [Google Scholar] [CrossRef] [Green Version]
- Savidis, G.; Perreira, J.M.; Portmann, J.M.; Meraner, P.; Guo, Z.; Green, S.; Brass, A.L. The IFITMs Inhibit Zika Virus Replication. Cell Rep. 2016, 15, 2323–2330. [Google Scholar] [CrossRef] [Green Version]
- Jia, R.; Ding, S.; Pan, Q.; Liu, S.L.; Qiao, W.; Liang, C. The C-terminal sequence of IFITM1 regulates its anti-HIV-1 activity. PLoS ONE 2015, 10, e0118794. [Google Scholar] [CrossRef] [Green Version]
- Brass, A.L.; Huang, I.C.; Benita, Y.; John, S.P.; Krishnan, M.N.; Feeley, E.M.; Ryan, B.J.; Weyer, J.L.; van der Weyden, L.; Fikrig, E.; et al. The IFITM proteins mediate cellular resistance to influenza A H1N1 virus, West Nile virus, and dengue virus. Cell 2009, 139, 1243–1254. [Google Scholar] [CrossRef] [Green Version]
- Zhang, W.; Zhang, L.; Zan, Y.; Du, N.; Yang, Y.; Tien, P. Human respiratory syncytial virus infection is inhibited by IFN-induced transmembrane proteins. J. Gen. Virol. 2015, 96, 170–182. [Google Scholar] [CrossRef] [PubMed]
- Kolokoltsov, A.A.; Deniger, D.; Fleming, E.H.; Roberts, N.J., Jr.; Karpilow, J.M.; Davey, R.A. Small interfering RNA profiling reveals key role of clathrin-mediated endocytosis and early endosome formation for infection by respiratory syncytial virus. J. Virol. 2007, 81, 7786–7800. [Google Scholar] [CrossRef] [Green Version]
- Chesarino, N.M.; Compton, A.A.; McMichael, T.M.; Kenney, A.D.; Zhang, L.; Soewarna, V.; Davis, M.; Schwartz, O.; Yount, J.S. IFITM3 requires an amphipathic helix for antiviral activity. EMBO Rep. 2017, 18, 1740–1751. [Google Scholar] [CrossRef]
- Liu, S.Y.; Sanchez, D.J.; Aliyari, R.; Lu, S.; Cheng, G. Systematic identification of type I and type II interferon-induced antiviral factors. Proc. Natl. Acad. Sci. USA 2012, 109, 4239–4244. [Google Scholar] [CrossRef] [Green Version]
- Lv, L.; Zhao, G.; Wang, H.; He, H. Cholesterol 25-Hydroxylase inhibits bovine parainfluenza virus type 3 replication through enzyme activity-dependent and -independent ways. Vet. Microbiol. 2019, 239, 108456. [Google Scholar] [CrossRef]
- Li, C.; Deng, Y.Q.; Wang, S.; Ma, F.; Aliyari, R.; Huang, X.Y.; Zhang, N.N.; Watanabe, M.; Dong, H.L.; Liu, P.; et al. 25-Hydroxycholesterol Protects Host against Zika Virus Infection and Its Associated Microcephaly in a Mouse Model. Immunity 2017, 46, 446–456. [Google Scholar] [CrossRef] [Green Version]
- Blanc, M.; Hsieh, W.Y.; Robertson, K.A.; Kropp, K.A.; Forster, T.; Shui, G.; Lacaze, P.; Watterson, S.; Griffiths, S.J.; Spann, N.J.; et al. The transcription factor STAT-1 couples macrophage synthesis of 25-hydroxycholesterol to the interferon antiviral response. Immunity 2013, 38, 106–118. [Google Scholar] [CrossRef] [Green Version]
- Xiang, Y.; Tang, J.J.; Tao, W.; Cao, X.; Song, B.L.; Zhong, J. Identification of Cholesterol 25-Hydroxylase as a Novel Host Restriction Factor and a Part of the Primary Innate Immune Responses against Hepatitis C Virus Infection. J. Virol. 2015, 89, 6805–6816. [Google Scholar] [CrossRef] [Green Version]
- Haller, O.; Staeheli, P.; Schwemmle, M.; Kochs, G. Mx GTPases: Dynamin-like antiviral machines of innate immunity. Trends Microbiol. 2015, 23, 154–163. [Google Scholar] [CrossRef]
- Pavlovic, J.; Haller, O.; Staeheli, P. Human and mouse Mx proteins inhibit different steps of the influenza virus multiplication cycle. J. Virol. 1992, 66, 2564–2569. [Google Scholar] [CrossRef] [Green Version]
- Yu, Z.; Wang, Z.; Chen, J.; Li, H.; Lin, Z.; Zhang, F.; Zhou, Y.; Hou, J. GTPase activity is not essential for the interferon-inducible MxA protein to inhibit the replication of hepatitis B virus. Arch. Virol. 2008, 153, 1677–1684. [Google Scholar] [CrossRef] [PubMed]
- Goujon, C.; Moncorgé, O.; Bauby, H.; Doyle, T.; Ward, C.C.; Schaller, T.; Hué, S.; Barclay, W.S.; Schulz, R.; Malim, M.H. Human MX2 is an interferon-induced post-entry inhibitor of HIV-1 infection. Nature 2013, 502, 559–562. [Google Scholar] [CrossRef] [PubMed]
- Schneider-Schaulies, S.; Schneider-Schaulies, J.; Schuster, A.; Bayer, M.; Pavlovic, J.; ter Meulen, V. Cell type-specific MxA-mediated inhibition of measles virus transcription in human brain cells. J. Virol. 1994, 68, 6910–6917. [Google Scholar] [CrossRef] [PubMed] [Green Version]
- Torisu, H.; Kusuhara, K.; Kira, R.; Bassuny, W.M.; Sakai, Y.; Sanefuji, M.; Takemoto, M.; Hara, T. Functional MxA promoter polymorphism associated with subacute sclerosing panencephalitis. Neurology 2004, 62, 457–460. [Google Scholar] [CrossRef] [PubMed]
- Carlos, T.S.; Young, D.; Stertz, S.; Kochs, G.; Randall, R.E. Interferon-induced inhibition of parainfluenza virus type 5; the roles of MxA, PKR and oligo A synthetase/RNase L. Virology 2007, 363, 166–173. [Google Scholar] [CrossRef] [PubMed] [Green Version]
- Atreya, P.L.; Kulkarni, S. Respiratory syncytial virus strain A2 is resistant to the antiviral effects of type I interferons and human MxA. Virology 1999, 261, 227–241. [Google Scholar] [CrossRef] [Green Version]
- Ciencewicki, J.M.; Wang, X.; Marzec, J.; Serra, M.E.; Bell, D.A.; Polack, F.P.; Kleeberger, S.R. A genetic model of differential susceptibility to human respiratory syncytial virus (RSV) infection. Faseb J. Off. Publ. Fed. Am. Soc. Exp. Biol. 2014, 28, 1947–1956. [Google Scholar] [CrossRef] [Green Version]
- Anderson, S.L.; Carton, J.M.; Lou, J.; Xing, L.; Rubin, B.Y. Interferon-induced guanylate binding protein-1 (GBP-1) mediates an antiviral effect against vesicular stomatitis virus and encephalomyocarditis virus. Virology 1999, 256, 8–14. [Google Scholar] [CrossRef] [Green Version]
- Itsui, Y.; Sakamoto, N.; Kakinuma, S.; Nakagawa, M.; Sekine-Osajima, Y.; Tasaka-Fujita, M.; Nishimura-Sakurai, Y.; Suda, G.; Karakama, Y.; Mishima, K.; et al. Antiviral effects of the interferon-induced protein guanylate binding protein 1 and its interaction with the hepatitis C virus NS5B protein. Hepatology 2009, 50, 1727–1737. [Google Scholar] [CrossRef]
- Li, Z.; Qu, X.; Liu, X.; Huan, C.; Wang, H.; Zhao, Z.; Yang, X.; Hua, S.; Zhang, W. GBP5 is an interferon-induced inhibitor of respiratory syncytial virus. J. Virol. 2020, 94, e01407-20. [Google Scholar] [CrossRef]
- Silverman, R.H. Viral encounters with 2′,5′-oligoadenylate synthetase and RNase L during the interferon antiviral response. J. Virol. 2007, 81, 12720–12729. [Google Scholar] [CrossRef] [Green Version]
- Leaman, D.W.; Longano, F.J.; Okicki, J.R.; Soike, K.F.; Torrence, P.F.; Silverman, R.H.; Cramer, H. Targeted therapy of respiratory syncytial virus in African green monkeys by intranasally administered 2-5A antisense. Virology 2002, 292, 70–77. [Google Scholar] [CrossRef] [PubMed] [Green Version]
- Dhar, J.; Cuevas, R.A.; Goswami, R.; Zhu, J.; Sarkar, S.N.; Barik, S. 2’-5’-Oligoadenylate Synthetase-Like Protein Inhibits Respiratory Syncytial Virus Replication and Is Targeted by the Viral Nonstructural Protein 1. J. Virol. 2015, 89, 10115–10119. [Google Scholar] [CrossRef] [PubMed] [Green Version]
- Zhu, J.; Zhang, Y.; Ghosh, A.; Cuevas, R.A.; Forero, A.; Dhar, J.; Ibsen, M.S.; Schmid-Burgk, J.L.; Schmidt, T.; Ganapathiraju, M.K.; et al. Antiviral activity of human OASL protein is mediated by enhancing signaling of the RIG-I RNA sensor. Immunity 2014, 40, 936–948. [Google Scholar] [CrossRef] [PubMed] [Green Version]
- Sheehy, A.M.; Gaddis, N.C.; Choi, J.D.; Malim, M.H. Isolation of a human gene that inhibits HIV-1 infection and is suppressed by the viral Vif protein. Nature 2002, 418, 646–650. [Google Scholar] [CrossRef] [PubMed]
- Zhang, H.; Yang, B.; Pomerantz, R.J.; Zhang, C.; Arunachalam, S.C.; Gao, L. The cytidine deaminase CEM15 induces hypermutation in newly synthesized HIV-1 DNA. Nature 2003, 424, 94–98. [Google Scholar] [CrossRef] [PubMed] [Green Version]
- Bodaghi, B.; Goureau, O.; Zipeto, D.; Laurent, L.; Virelizier, J.L.; Michelson, S. Role of IFN-gamma-induced indoleamine 2,3 dioxygenase and inducible nitric oxide synthase in the replication of human cytomegalovirus in retinal pigment epithelial cells. J. Immunol. 1999, 162, 957–964. [Google Scholar]
- Adams, O.; Besken, K.; Oberdörfer, C.; MacKenzie, C.R.; Takikawa, O.; Däubener, W. Role of indoleamine-2,3-dioxygenase in alpha/beta and gamma interferon-mediated antiviral effects against herpes simplex virus infections. J. Virol. 2004, 78, 2632–2636. [Google Scholar] [CrossRef] [Green Version]
- Cheung, M.B.; Sampayo-Escobar, V.; Green, R.; Moore, M.L.; Mohapatra, S.; Mohapatra, S.S. Respiratory Syncytial Virus-Infected Mesenchymal Stem Cells Regulate Immunity via Interferon Beta and Indoleamine-2,3-Dioxygenase. PLoS ONE 2016, 11, e0163709. [Google Scholar] [CrossRef] [Green Version]
- Munir, M.; Berg, M. The multiple faces of proteinkinase R in antiviral defense. Virulence 2013, 4, 85–89. [Google Scholar] [CrossRef] [Green Version]
- Takeuchi, K.; Komatsu, T.; Kitagawa, Y.; Sada, K.; Gotoh, B. Sendai virus C protein plays a role in restricting PKR activation by limiting the generation of intracellular double-stranded RNA. J. Virol. 2008, 82, 10102–10110. [Google Scholar] [CrossRef] [PubMed] [Green Version]
- Chen, L.; Sun, J.; Meng, L.; Heathcote, J.; Edwards, A.M.; McGilvray, I.D. ISG15, a ubiquitin-like interferon-stimulated gene, promotes hepatitis C virus production in vitro: Implications for chronic infection and response to treatment. J. Gen. Virol. 2010, 91, 382–388. [Google Scholar] [CrossRef] [PubMed]
- Okumura, A.; Pitha, P.M.; Harty, R.N. ISG15 inhibits Ebola VP40 VLP budding in an L-domain-dependent manner by blocking Nedd4 ligase activity. Proc. Natl. Acad. Sci. USA 2008, 105, 3974–3979. [Google Scholar] [CrossRef] [Green Version]
- Zhao, C.; Denison, C.; Huibregtse, J.M.; Gygi, S.; Krug, R.M. Human ISG15 conjugation targets both IFN-induced and constitutively expressed proteins functioning in diverse cellular pathways. Proc. Natl. Acad. Sci. USA 2005, 102, 10200–10205. [Google Scholar] [CrossRef] [Green Version]
- Dastur, A.; Beaudenon, S.; Kelley, M.; Krug, R.M.; Huibregtse, J.M. Herc5, an interferon-induced HECT E3 enzyme, is required for conjugation of ISG15 in human cells. J. Biol. Chem. 2006, 281, 4334–4338. [Google Scholar] [CrossRef] [Green Version]
- Zhao, C.; Beaudenon, S.L.; Kelley, M.L.; Waddell, M.B.; Yuan, W.; Schulman, B.A.; Huibregtse, J.M.; Krug, R.M. The UbcH8 ubiquitin E2 enzyme is also the E2 enzyme for ISG15, an IFN-alpha/beta-induced ubiquitin-like protein. Proc. Natl. Acad. Sci. USA 2004, 101, 7578–7582. [Google Scholar] [CrossRef] [Green Version]
- Martínez, I.; Lombardía, L.; García-Barreno, B.; Domínguez, O.; Melero, J.A. Distinct gene subsets are induced at different time points after human respiratory syncytial virus infection of A549 cells. J. Gen. Virol. 2007, 88, 570–581. [Google Scholar] [CrossRef]
- Holthaus, D.; Vasou, A.; Bamford, C.G.G.; Andrejeva, J.; Paulus, C.; Randall, R.E.; McLauchlan, J.; Hughes, D.J. Direct antiviral activity of interferon stimulated genes is responsible for resistance to paramyxoviruses in ISG15-deficient cells. bioRxiv 2019. [Google Scholar] [CrossRef] [Green Version]
- Speer, S.D.; Li, Z.; Buta, S.; Payelle-Brogard, B.; Qian, L.; Vigant, F.; Rubino, E.; Gardner, T.J.; Wedeking, T.; Hermann, M.; et al. ISG15 deficiency and increased viral resistance in humans but not mice. Nat. Commun. 2016, 7, 11496. [Google Scholar] [CrossRef]
- Thibault, P.A.; Ryan, A.P.; Hung, C.-t.; Daugherty, M.; Lee, B. The long isoform of ZAP widely restricts Paramyxoviruses. Access Microbiol. 2019, 1, 854. [Google Scholar] [CrossRef]
- Schoggins, J.W.; MacDuff, D.A.; Imanaka, N.; Gainey, M.D.; Shrestha, B.; Eitson, J.L.; Mar, K.B.; Richardson, R.B.; Ratushny, A.V.; Litvak, V.; et al. Pan-viral specificity of IFN-induced genes reveals new roles for cGAS in innate immunity. Nature 2014, 505, 691–695. [Google Scholar] [CrossRef]
- Wu, W.; Choi, E.J.; Lee, I.; Lee, Y.S.; Bao, X. Non-Coding RNAs and Their Role in Respiratory Syncytial Virus (RSV) and Human Metapneumovirus (hMPV) Infections. Viruses 2020, 12, 345. [Google Scholar] [CrossRef] [Green Version]
- Wang, X.; Jia, Y.; Ren, J.; Liu, H.; Xiao, S.; Wang, X.; Yang, Z. MicroRNA gga-miR-455-5p suppresses Newcastle disease virus replication via targeting cellular suppressors of cytokine signaling 3. Vet. Microbiol. 2019, 239, 108460. [Google Scholar] [CrossRef] [PubMed]
- Wang, X.; Hinson, E.R.; Cresswell, P. The interferon-inducible protein viperin inhibits influenza virus release by perturbing lipid rafts. Cell Host Microbe 2007, 2, 96–105. [Google Scholar] [CrossRef] [PubMed] [Green Version]
- Helbig, K.J.; Carr, J.M.; Calvert, J.K.; Wati, S.; Clarke, J.N.; Eyre, N.S.; Narayana, S.K.; Fiches, G.N.; McCartney, E.M.; Beard, M.R. Viperin is induced following dengue virus type-2 (DENV-2) infection and has anti-viral actions requiring the C-terminal end of viperin. PLoS Negl. Trop. Dis. 2013, 7, e2178. [Google Scholar] [CrossRef] [PubMed] [Green Version]
- Janssen, R.; Pennings, J.; Hodemaekers, H.; Buisman, A.; van Oosten, M.; de Rond, L.; Oztürk, K.; Dormans, J.; Kimman, T.; Hoebee, B. Host transcription profiles upon primary respiratory syncytial virus infection. J. Virol. 2007, 81, 5958–5967. [Google Scholar] [CrossRef] [Green Version]
- Zaas, A.K.; Chen, M.; Varkey, J.; Veldman, T.; Hero, A.O., 3rd; Lucas, J.; Huang, Y.; Turner, R.; Gilbert, A.; Lambkin-Williams, R.; et al. Gene expression signatures diagnose influenza and other symptomatic respiratory viral infections in humans. Cell Host Microbe 2009, 6, 207–217. [Google Scholar] [CrossRef] [Green Version]
- Neil, S.J.; Zang, T.; Bieniasz, P.D. Tetherin inhibits retrovirus release and is antagonized by HIV-1 Vpu. Nature 2008, 451, 425–430. [Google Scholar] [CrossRef] [PubMed] [Green Version]
- Perez-Caballero, D.; Zang, T.; Ebrahimi, A.; McNatt, M.W.; Gregory, D.A.; Johnson, M.C.; Bieniasz, P.D. Tetherin inhibits HIV-1 release by directly tethering virions to cells. Cell 2009, 139, 499–511. [Google Scholar] [CrossRef] [PubMed] [Green Version]
- Kuhl, B.D.; Cheng, V.; Wainberg, M.A.; Liang, C. Tetherin and its viral antagonists. J. Neuroimmune Pharm. 2011, 6, 188–201. [Google Scholar] [CrossRef] [Green Version]
- Radoshitzky, S.R.; Dong, L.; Chi, X.; Clester, J.C.; Retterer, C.; Spurgers, K.; Kuhn, J.H.; Sandwick, S.; Ruthel, G.; Kota, K.; et al. Infectious Lassa virus, but not filoviruses, is restricted by BST-2/tetherin. J. Virol. 2010, 84, 10569–10580. [Google Scholar] [CrossRef] [Green Version]
- McDonald, J.U.; Kaforou, M.; Clare, S.; Hale, C.; Ivanova, M.; Huntley, D.; Dorner, M.; Wright, V.J.; Levin, M.; Martinon-Torres, F.; et al. A Simple Screening Approach To Prioritize Genes for Functional Analysis Identifies a Role for Interferon Regulatory Factor 7 in the Control of Respiratory Syncytial Virus Disease. mSystems 2016, 1, e00051-16. [Google Scholar] [CrossRef] [PubMed] [Green Version]
- Zilliox, M.J.; Parmigiani, G.; Griffin, D.E. Gene expression patterns in dendritic cells infected with measles virus compared with other pathogens. Proc. Natl. Acad. Sci. USA 2006, 103, 3363–3368. [Google Scholar] [CrossRef] [PubMed] [Green Version]
- OhAinle, M.; Helms, L.; Vermeire, J.; Roesch, F.; Humes, D.; Basom, R.; Delrow, J.J.; Overbaugh, J.; Emerman, M. A virus-packageable CRISPR screen identifies host factors mediating interferon inhibition of HIV. eLife 2018, 7, e39823. [Google Scholar] [CrossRef]
- Yong, H.Y.; Luo, D. RIG-I-Like Receptors as Novel Targets for Pan-Antivirals and Vaccine Adjuvants Against Emerging and Re-Emerging Viral Infections. Front. Immunol. 2018, 9, 1379. [Google Scholar] [CrossRef] [Green Version]
- Pattabhi, S.; Wilkins, C.R.; Dong, R.; Knoll, M.L.; Posakony, J.; Kaiser, S.; Mire, C.E.; Wang, M.L.; Ireton, R.C.; Geisbert, T.W.; et al. Targeting Innate Immunity for Antiviral Therapy through Small Molecule Agonists of the RLR Pathway. J. Virol. 2015, 90, 2372–2387. [Google Scholar] [CrossRef] [Green Version]
- Bam, R.A.; Hansen, D.; Irrinki, A.; Mulato, A.; Jones, G.S.; Hesselgesser, J.; Frey, C.R.; Cihlar, T.; Yant, S.R. TLR7 Agonist GS-9620 Is a Potent Inhibitor of Acute HIV-1 Infection in Human Peripheral Blood Mononuclear Cells. Antimicrob. Agents Chemother. 2017, 61. [Google Scholar] [CrossRef] [Green Version]
- Lanford, R.E.; Guerra, B.; Chavez, D.; Giavedoni, L.; Hodara, V.L.; Brasky, K.M.; Fosdick, A.; Frey, C.R.; Zheng, J.; Wolfgang, G.; et al. GS-9620, an oral agonist of Toll-like receptor-7, induces prolonged suppression of hepatitis B virus in chronically infected chimpanzees. Gastroenterology 2013, 144, 1508–1517. [Google Scholar] [CrossRef] [Green Version]
- Tan, A.C.; Mifsud, E.J.; Zeng, W.; Edenborough, K.; McVernon, J.; Brown, L.E.; Jackson, D.C. Intranasal administration of the TLR2 agonist Pam2Cys provides rapid protection against influenza in mice. Mol. Pharm. 2012, 9, 2710–2718. [Google Scholar] [CrossRef]
Virus | Genus | Species | Disease | Vaccines and Antivirals | Restriction Factors |
---|---|---|---|---|---|
Paramyxoviruses | |||||
MeV | Morbillivirus | Human | Systemic | MMR (measles-mumps-rubella) vaccine, No licensed antiviral [9] | MxA ([10], Apobec3g [11], Viperin [12], GBP2 and 5 [13], IDO1 [14], PKR [15], IFITM1 [16] |
MuV | Orthorubulavirus | Human | Systemic | MMR (measles-mumps-rubella) vaccine, No licensed antiviral [17] | IFITM1 [16], Apobec3g [11], IFIT1 [18] |
PIV-2 | Orthorubulavirus | Human | Respiratory | No licensed vaccine or antiviral [19] | IFIT1 [18] |
PIV-3 | Respirovirus | Human | Respiratory | No licensed vaccine or antiviral [19] | MxA [20], TDRD7 [21], PKR [22], IDO1 [22], IFIT1 [22] |
PIV-5 | Orthorubulavirus | Human | Respiratory | No licensed vaccine or antiviral [19] | IFIT1 [23] |
NDV | Orthoavalovirus | Avian | Systemic | Inactivated or Live vaccine available [24], No licensed antiviral | OASL (avian) [25], CARD11 ([26], Apobec4g (avian) [27], IFIT5 (Avian) [28], IFITM1 [16] |
SeV | Respirovirus | Mouse | Respiratory | No licensed vaccine or antiviral | TDRD7 [21], GBP4 (mouse) [29], Tetherin [30] |
NiV | Henipavirus | Fruit bats/Human (zoonotic) | Systemic | No licensed vaccine or antiviral | Tetherin [30], CH25H [31] |
Pneumoviruses | |||||
HMPV | Metapneumovirus | Human | Respiratory | No licensed vaccine or antiviral [19] | IFITM1 [16], IFITM3 [32] |
HRSV | Orthopneumovirus | Human | Respiratory | No licensed vaccine, Ribavarin approved for severe infections, Palivizumab (monoclonal antibody) approved as prophylaxis for high risk infants and children [19] | IFITM1 [16], IFITM3 [33], IDO1 [34], OAS [35], TDRD7 [21], ISG15 [36], Apobec3g [11], PKR [37], Viperin [38] |
Publisher’s Note: MDPI stays neutral with regard to jurisdictional claims in published maps and institutional affiliations. |
© 2020 by the authors. Licensee MDPI, Basel, Switzerland. This article is an open access article distributed under the terms and conditions of the Creative Commons Attribution (CC BY) license (http://creativecommons.org/licenses/by/4.0/).
Share and Cite
Farrukee, R.; Ait-Goughoulte, M.; Saunders, P.M.; Londrigan, S.L.; Reading, P.C. Host Cell Restriction Factors of Paramyxoviruses and Pneumoviruses. Viruses 2020, 12, 1381. https://doi.org/10.3390/v12121381
Farrukee R, Ait-Goughoulte M, Saunders PM, Londrigan SL, Reading PC. Host Cell Restriction Factors of Paramyxoviruses and Pneumoviruses. Viruses. 2020; 12(12):1381. https://doi.org/10.3390/v12121381
Chicago/Turabian StyleFarrukee, Rubaiyea, Malika Ait-Goughoulte, Philippa M. Saunders, Sarah L. Londrigan, and Patrick C. Reading. 2020. "Host Cell Restriction Factors of Paramyxoviruses and Pneumoviruses" Viruses 12, no. 12: 1381. https://doi.org/10.3390/v12121381