Transcriptomics reveal antiviral gene induction in the egyptian rousette bat is antagonized in vitro by marburg virus infection

Viruses

Volumn 10, Issue 11, 2018, Pages

  Arnold, Catherine E ^a   Guito, Jonathan C ^b   Altamura, Louis A ^a   Lovett, Sean P ^a   Nagle, Elyse R ^a   Palacios, Gustavo F ^a   Sanchez Lockhart, Mariano ^a,c   Towner, Jonathan S ^b  

^a UNITED STATES ARMY MEDICAL RESEARCH INSTITUTE OF INFECTIOUS DISEASES   (United States)

^b CENTERS FOR DISEASE CONTROL AND PREVENTION   (United States)

^c UNIVERSITY OF NEBRASKA MEDICAL CENTER   (United States)

Author keywords

Egyptian rousette bat; Marburg virus; Transcriptomics; VP35

Indexed keywords

CALGRANULIN C; IFIT1 PROTEIN; INTERFERON INDUCED HELICASE C DOMAIN CONTAINING PROTEIN 1; INTERFERON REGULATORY FACTOR 7; MITOGEN ACTIVATED PROTEIN KINASE 1; OAS1 PROTEIN; PEPTIDES AND PROTEINS; RETINOIC ACID INDUCIBLE PROTEIN I; SST PROTEIN; STAT1 PROTEIN; STAT2 PROTEIN; STAT3 PROTEIN; TRIM24 PROTEIN; TUMOR NECROSIS FACTOR ALPHA INDUCED PROTEIN 3; UNCLASSIFIED DRUG; INTERFERON; TRANSCRIPTOME;

ANIMAL CELL; ARTICLE; CONTROLLED STUDY; DOWN REGULATION; GENE; GENE EXPRESSION; GENE INDUCTION; HUMAN; INTERFERON GENE; MARBURG HEMORRHAGIC FEVER; MARBURGVIRUS; NONHUMAN; PHENOTYPE; REAL TIME POLYMERASE CHAIN REACTION; REVERSE TRANSCRIPTION POLYMERASE CHAIN REACTION; RNA ISOLATION; RNA SEQUENCE; SIGNAL TRANSDUCTION; TRANSCRIPTOMICS; UPREGULATION; VIRUS INFECTION; VIRUS REPLICATION; ANIMAL; BAT; CELL LINE; DISEASE RESISTANCE; GENE EXPRESSION PROFILING; GENE EXPRESSION REGULATION; GENETICS; HOST PATHOGEN INTERACTION; INNATE IMMUNITY; PHYSIOLOGY; PROCEDURES; VIROLOGY;

ANIMALS; CELL LINE; CHIROPTERA; DISEASE RESISTANCE; GENE EXPRESSION PROFILING; GENE EXPRESSION REGULATION; HOST-PATHOGEN INTERACTIONS; IMMUNITY, INNATE; INTERFERONS; MARBURG VIRUS DISEASE; MARBURGVIRUS; TRANSCRIPTOME;

EID: 85056271112     PISSN: None     EISSN: 19994915     Source Type: Journal    
DOI: 10.3390/v10110607     Document Type: Article

References (50)

1. Halpin, K.; Hyatt, A.D.; Fogarty, R.; Middleton, D.; Bingham, J.; Epstein, J.H.; Rahman, S.A.; Hughes, T.; Smith, C.; Field, H.E.; et al. Pteropid bats are confirmed as the reservoir hosts of henipaviruses: A comprehensive experimental study of virus transmission. Am. J. Trop. Med. Hyg. 2011, 85, 946–951. [CrossRef] [PubMed]
2. Li, W.; Shi, Z.; Yu, M.; Ren, W.; Smith, C.; Epstein, J.H.; Wang, H.; Crameri, G.; Hu, Z.; Zhang, H.; et al. Bats are natural reservoirs of SARS-like coronaviruses. Science 2005, 310, 676–679. [CrossRef] [PubMed]
3. Kortepeter, M.G.; Bausch, D.G.; Bray, M. Basic clinical and laboratory features of filoviral hemorrhagic fever. J. Infect. Dis. 2011, 204 (Suppl. 3), S810–S816. [CrossRef] [PubMed]
4. Amman, B.R.; Swanepoel, R.; Nichol, S.T.; Towner, J.S. Ecology of Filoviruses. Curr. Top. Microbiol. Immunol. 2017, 411, 23–61. [CrossRef] [PubMed]
5. Towner, J.S.; Pourrut, X.; Albarino, C.G.; Nkogue, C.N.; Bird, B.H.; Grard, G.; Ksiazek, T.G.; Gonzalez, J.P.; Nichol, S.T.; Leroy, E.M. Marburg virus infection detected in a common African bat. PLoS ONE 2007, 2, e764. [CrossRef] [PubMed]
6. Towner, J.S.; Amman, B.R.; Sealy, T.K.; Carroll, S.A.; Comer, J.A.; Kemp, A.; Swanepoel, R.; Paddock, C.D.; Balinandi, S.; Khristova, M.L.; et al. Isolation of genetically diverse Marburg viruses from Egyptian fruit bats. PLoS Pathog. 2009, 5, e1000536. [CrossRef] [PubMed]
7. Swanepoel, R.; Smit, S.B.; Rollin, P.E.; Formenty, P.; Leman, P.A.; Kemp, A.; Burt, F.J.; Grobbelaar, A.A.; Croft, J.; Bausch, D.G.; et al. Studies of reservoir hosts for Marburg virus. Emerg. Infect. Dis. 2007, 13, 1847–1851. [CrossRef] [PubMed]
8. Schuh, A.J.; Amman, B.R.; Jones, M.E.; Sealy, T.K.; Uebelhoer, L.S.; Spengler, J.R.; Martin, B.E.; Coleman-McCray, J.A.; Nichol, S.T.; Towner, J.S. Modelling filovirus maintenance in nature by experimental transmission of Marburg virus between Egyptian rousette bats. Nat. Commun. 2017, 8, 14446. [CrossRef] [PubMed]
9. Amman, B.R.; Jones, M.E.; Sealy, T.K.; Uebelhoer, L.S.; Schuh, A.J.; Bird, B.H.; Coleman-McCray, J.D.; Martin, B.E.; Nichol, S.T.; Towner, J.S. Oral shedding of Marburg virus in experimentally infected Egyptian fruit bats (Rousettus aegyptiacus). J. Wildl. Dis. 2015, 51, 113–124. [CrossRef] [PubMed]
10. Jones, M.E.; Schuh, A.J.; Amman, B.R.; Sealy, T.K.; Zaki, S.R.; Nichol, S.T.; Towner, J.S. Experimental Inoculation of Egyptian Rousette Bats (Rousettus aegyptiacus) with Viruses of the Ebolavirus and Marburgvirus Genera. Viruses 2015, 7, 3420–3442. [CrossRef] [PubMed]
11. Paweska, J.T.; Jansen van Vuren, P.; Masumu, J.; Leman, P.A.; Grobbelaar, A.A.; Birkhead, M.; Clift, S.; Swanepoel, R.; Kemp, A. Virological and serological findings in Rousettus aegyptiacus experimentally inoculated with vero cells-adapted hogan strain of Marburg virus. PLoS ONE 2012, 7, e45479. [CrossRef] [PubMed]
12. Lubaki, N.M.; Younan, P.; Santos, R.I.; Meyer, M.; Iampietro, M.; Koup, R.A.; Bukreyev, A. The Ebola Interferon Inhibiting Domains Attenuate and Dysregulate Cell-Mediated Immune Responses. PLoS Pathog. 2016, 12, e1006031. [CrossRef] [PubMed]
13. Kash, J.C.; Mühlberger, E.; Carter, V.; Grosch, M.; Perwitasari, O.; Proll, S.C.; Thomas, M.J.; Weber, F.; Klenk, H.-D.; Katze, M.G. Global Suppression of the Host Antiviral Response by Ebola-and Marburgviruses: Increased Antagonism of the Type I Interferon Response Is Associated with Enhanced Virulence. J. Virol. 2006, 80, 3009–3020. [CrossRef] [PubMed]
14. Guito, J.C.; Albarino, C.G.; Chakrabarti, A.K.; Towner, J.S. Novel activities by ebolavirus and marburgvirus interferon antagonists revealed using a standardized in vitro reporter system. Virology 2017, 501, 147–165. [CrossRef] [PubMed]
15. Ilinykh, P.A.; Lubaki, N.M.; Widen, S.G.; Renn, L.A.; Theisen, T.C.; Rabin, R.L.; Wood, T.G.; Bukreyev, A. Different Temporal Effects of Ebola Virus VP35 and VP24 Proteins on Global Gene Expression in Human Dendritic Cells. J. Virol. 2015, 89, 7567–7583. [CrossRef] [PubMed]
16. Yen, B.C.; Basler, C.F. Effects of Filovirus Interferon Antagonists on Responses of Human Monocyte-Derived Dendritic Cells to RNA Virus Infection. J. Virol. 2016, 90, 5108–5118. [CrossRef] [PubMed]
17. Kuzmin, I.V.; Schwarz, T.M.; Ilinykh, P.A.; Jordan, I.; Ksiazek, T.G.; Sachidanandam, R.; Basler, C.F.; Bukreyev, A. Innate Immune Responses of Bat and Human Cells to Filoviruses: Commonalities and Distinctions. J. Virol. 2017. [CrossRef] [PubMed]
18. Holzer, M.; Krahling, V.; Amman, F.; Barth, E.; Bernhart, S.H.; Carmelo, V.A.; Collatz, M.; Doose, G.; Eggenhofer, F.; Ewald, J.; et al. Differential transcriptional responses to Ebola and Marburg virus infection in bat and human cells. Sci. Rep. 2016, 6, 34589. [CrossRef] [PubMed]
19. Hartman, A.L.; Bird, B.H.; Towner, J.S.; Antoniadou, Z.A.; Zaki, S.R.; Nichol, S.T. Inhibition of IRF-3 activation by VP35 is critical for the high level of virulence of ebola virus. J. Virol. 2008, 82, 2699–2704. [CrossRef] [PubMed]
20. Zhou, P.; Tachedjian, M.; Wynne, J.W.; Boyd, V.; Cui, J.; Smith, I.; Cowled, C.; Ng, J.H.; Mok, L.; Michalski, W.P.; et al. Contraction of the type I IFN locus and unusual constitutive expression of IFN-alpha in bats. Proc. Natl. Acad. Sci. USA 2016, 113, 2696–2701. [CrossRef] [PubMed]
21. Kuhl, A.; Hoffmann, M.; Muller, M.A.; Munster, V.J.; Gnirss, K.; Kiene, M.; Tsegaye, T.S.; Behrens, G.; Herrler, G.; Feldmann, H.; et al. Comparative analysis of Ebola virus glycoprotein interactions with human and bat cells. J. Infect. Dis. 2011, 204 (Suppl. 3), S840–S849. [CrossRef] [PubMed]
22. Pavlovich, S.S.; Lovett, S.P.; Koroleva, G.; Guito, J.C.; Arnold, C.E.; Nagle, E.R.; Kulcsar, K.; Lee, A.; Thibaud-Nissen, F.; Hume, A.J.; et al. The Egyptian Rousette Genome Reveals Unexpected Features of Bat Antiviral Immunity. Cell 2018. [CrossRef] [PubMed]
23. Lee, A.K.; Kulcsar, K.A.; Elliott, O.; Khiabanian, H.; Nagle, E.R.; Jones, M.E.; Amman, B.R.; Sanchez-Lockhart, M.; Towner, J.S.; Palacios, G.; et al. De novo transcriptome reconstruction and annotation of the Egyptian rousette bat. BMC Genom. 2015, 16, 1033. [CrossRef] [PubMed]
24. Albarino, C.G.; Uebelhoer, L.S.; Vincent, J.P.; Khristova, M.L.; Chakrabarti, A.K.; McElroy, A.; Nichol, S.T.; Towner, J.S. Development of a reverse genetics system to generate recombinant Marburg virus derived from a bat isolate. Virology 2013, 446, 230–237. [CrossRef] [PubMed]
25. Albarino, C.G.; Wiggleton Guerrero, L.; Spengler, J.R.; Uebelhoer, L.S.; Chakrabarti, A.K.; Nichol, S.T.; Towner, J.S. Recombinant Marburg viruses containing mutations in the IID region of VP35 prevent inhibition of Host immune responses. Virology 2015, 476, 85–91. [CrossRef] [PubMed]
26. Vandesompele, J.; De Preter, K.; Pattyn, F.; Poppe, B.; Van Roy, N.; De Paepe, A.; Speleman, F. Accurate normalization of real-time quantitative RT-PCR data by geometric averaging of multiple internal control genes. Genome Boil. 2002, 3, Research0034.
27. Bolger, A.M.; Lohse, M.; Usadel, B. Trimmomatic: A flexible trimmer for Illumina sequence data. Bioinformatics 2014, 30, 2114–2120. [CrossRef] [PubMed]
28. Bray, N.L.; Pimentel, H.; Melsted, P.; Pachter, L. Near-optimal probabilistic RNA-seq quantification. Nat. Biotechnol. 2016, 34, 525–527. [CrossRef] [PubMed]
29. Pimentel, H.; Bray, N.L.; Puente, S.; Melsted, P.; Pachter, L. Differential analysis of RNA-seq incorporating quantification uncertainty. Nat. Methods 2017, 14, 687–690. [CrossRef] [PubMed]
30. Consortium, G. Human genomics. The Genotype-Tissue Expression (GTEx) pilot analysis: Multitissue gene regulation in humans. Science 2015, 348, 648–660. [CrossRef] [PubMed]
31. Feagins, A.R.; Basler, C.F. Lloviu virus VP24 and VP35 proteins function as innate immune antagonists in human and bat cells. Virology 2015, 485, 145–152. [CrossRef] [PubMed]
32. Basler, C.F.; Mikulasova, A.; Martinez-Sobrido, L.; Paragas, J.; Muhlberger, E.; Bray, M.; Klenk, H.D.; Palese, P.; Garcia-Sastre, A. The Ebola virus VP35 protein inhibits activation of interferon regulatory factor 3. J. Virol. 2003, 77, 7945–7956. [CrossRef] [PubMed]
33. Schumann, M.; Gantke, T.; Muhlberger, E. Ebola virus VP35 antagonizes PKR activity through its C-terminal interferon inhibitory domain. J. Virol. 2009, 83, 8993–8997. [CrossRef] [PubMed]
34. Bale, S.; Julien, J.P.; Bornholdt, Z.A.; Krois, A.S.; Wilson, I.A.; Saphire, E.O. Ebolavirus VP35 coats the backbone of double-stranded RNA for interferon antagonism. J. Virol. 2013, 87, 10385–10388. [CrossRef] [PubMed]
35. Luthra, P.; Ramanan, P.; Mire, C.E.; Weisend, C.; Tsuda, Y.; Yen, B.; Liu, G.; Leung, D.W.; Geisbert, T.W.; Ebihara, H.; et al. Mutual antagonism between the Ebola virus VP35 protein and the RIG-I activator PACT determines infection outcome. Cell Host Microbe 2013, 14, 74–84. [CrossRef] [PubMed]
36. Leung, L.W.; Park, M.S.; Martinez, O.; Valmas, C.; Lopez, C.B.; Basler, C.F. Ebolavirus VP35 suppresses IFN production from conventional but not plasmacytoid dendritic cells. Immunol. Cell Boil. 2011, 89, 792–802. [CrossRef] [PubMed]
37. Baker, M.L.; Schountz, T.; Wang, L.F. Antiviral immune responses of bats: A review. Zoonoses Public Health 2013, 60, 104–116. [CrossRef] [PubMed]
38. Yaddanapudi, K.; Palacios, G.; Towner, J.S.; Chen, I.; Sariol, C.A.; Nichol, S.T.; Lipkin, W.I. Implication of a retrovirus-like glycoprotein peptide in the immunopathogenesis of Ebola and Marburg viruses. FASEB J. 2006, 20, 2519–2530. [CrossRef] [PubMed]
39. Ning, S.; Huye, L.E.; Pagano, J.S. Regulation of the transcriptional activity of the IRF7 promoter by a pathway independent of interferon signaling. J. Boil. Chem. 2005, 280, 12262–12270. [CrossRef] [PubMed]
40. Sariol, C.A.; Munoz-Jordan, J.L.; Abel, K.; Rosado, L.C.; Pantoja, P.; Giavedoni, L.; Rodriguez, I.V.; White, L.J.; Martinez, M.; Arana, T.; et al. Transcriptional activation of interferon-stimulated genes but not of cytokine genes after primary infection of rhesus macaques with dengue virus type 1. Clin. Vaccine Immunol. 2007, 14, 756–766. [CrossRef] [PubMed]
41. Servant, M.J.; Grandvaux, N.; Hiscott, J. Multiple signaling pathways leading to the activation of interferon regulatory factor 3. Biochem. Pharmacol. 2002, 64, 985–992. [CrossRef]
42. Perng, Y.C.; Lenschow, D.J. ISG15 in antiviral immunity and beyond. Nat. Rev. Microbiol. 2018. [CrossRef] [PubMed]
43. 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. [CrossRef] [PubMed]
44. Malakhova, O.A.; Zhang, D.E. ISG15 inhibits Nedd4 ubiquitin E3 activity and enhances the innate antiviral response. J. Boil. Chem. 2008, 283, 8783–8787. [CrossRef] [PubMed]
45. De La Cruz-Rivera, P.C.; Kanchwala, M.; Liang, H.; Kumar, A.; Wang, L.F.; Xing, C.; Schoggins, J.W. The IFN Response in Bats Displays Distinctive IFN-Stimulated Gene Expression Kinetics with Atypical RNASEL Induction. J. Immunol. 2018, 200, 209–217. [CrossRef] [PubMed]
46. Zhang, D.; Zhang, D.-E. Interferon-Stimulated Gene 15 and the Protein ISGylation System. J. Interferon Cytokine Res. 2011, 31, 119–130. [CrossRef] [PubMed]
47. Villarroya-Beltri, C.; Guerra, S.; Sánchez-Madrid, F. ISGylation—A key to lock the cell gates for preventing the spread of threats. J. Cell Sci. 2017, 130, 2961–2969. [CrossRef] [PubMed]
48. Samarajiwa, S.A.; Mangan, N.E.; Hardy, M.P.; Najdovska, M.; Dubach, D.; Braniff, S.-J.; Owczarek, C.M.; Hertzog, P.J. Soluble IFN Receptor Potentiates In Vivo Type I IFN Signaling and Exacerbates TLR4-Mediated Septic Shock. J. Immunol. 2014, 192, 4425–4435. [CrossRef] [PubMed]
49. Park, J.H.; Yang, S.W.; Park, J.M.; Ka, S.H.; Kim, J.-H.; Kong, Y.-Y.; Jeon, Y.J.; Seol, J.H.; Chung, C.H. Positive feedback regulation of p53 transactivity by DNA damage-induced ISG15 modification. Nat. Commun. 2016, 7, 12513. [CrossRef] [PubMed]
50. Hummer, B.T.; Li, X.L.; Hassel, B.A. Role for p53 in gene induction by double-stranded RNA. J. Virol. 2001, 75, 7774–7777. [CrossRef] [PubMed]