Bats are natural reservoir hosts for many viruses that produce no clinical symptoms in bats. Therefore, bats may have evolved effective mechanisms to control viral replication. However, little information is available on bat immune responses to viral infection. Type I interferon (IFN) plays a key role in controlling viral infections. In this study, we report the cloning, expression, and biological activity of interferon β (IFNβ) from the Chinese microbat species, Myotis davidii. We demonstrated the upregulation of IFNB and IFN-stimulated genes in a kidney cell line derived from M. davidii after treatment with polyI:C or infection with Sendai virus. Furthermore, the recombinant IFNβ inhibited vesicular stomatitis virus and bat adenovirus replication in cell lines from two bat species, M. davidii and Rhinolophus sinicus. We provide the first in vitro evidence of IFNβ antiviral activity in microbats, which has important implications for virus interactions with these hosts.
Arnold K, Bordoli L, Kopp J, Schwede T. 2006. The SWISSMODEL workspace: a web-based environment for protein structure homology modelling. Bioinformatics, 22: 195–201.
Baker ML, Schountz T, Wang LF. 2013. Antiviral immune responses of bats: a review. Zoonoses Public Health, 60: 104–116.
Baker ML, Tachedjian M, Wang LF. 2010. Immunoglobulin heavy chain diversity in Pteropid bats: evidence for a diverse and highly specific antigen binding repertoire. Immunogenetics, 62: 173–184.
Biesold SE, Ritz D, Gloza-Rausch F, Wollny R, Drexler JF, Corman VM, Kalko EKV, Oppong S, Drosten C, Mueller MA. 2011. Type I interferon reaction to viral infection in interferoncompetent, immortalized cell lines from the African fruit bat Eidolon helvum. PloS One, 6: e28131.
Brook EC, Dobson A. 2015. Bats as ‘special’ reservoirs for emerging zoonotic pathogens. Trends Microbiol, 23: 172–180.
Chua KB, Koh CL, Hooi PS, Wee KF, Khong JH, Chua BH, Chan YP, Lim ME, Lam SK. 2002. Isolation of Nipah virus from Malaysian Island flying-foxes. Microbes Infect, 4: 145–151.
Cowled C, Baker M, Tachedjian M, Zhou P, Bulach D, Wang LF. 2011. Molecular characterisation of Toll-like receptors in the black flying fox Pteropus alecto. Dev Comp Immunol, 35: 7–18.
Cowled C, Baker ML, Zhou P, Tachedjian M, Wang LF. 2012. Molecular characterisation of RIG-I-like helicases in the black flying fox, Pteropus alecto. Dev Comp Immunol, 36: 657–664.
Crameri G, Todd S, Grimley S, McEachern JA, Marsh GA, Smith C, Tachedjian M, De Jong C, Virtue ER, Yu M, Bulach D, Liu JP, Michalski WP, Middleton D, Field HE, Wang LF. 2009. Establishment, immortalisation and characterisation of pteropid bat cell lines. PLoS One, 4: e8266.
Fernandez M, Porosnicu M, Markovic D, Barber GN. 2002. Genetically engineered vesicular stomatitis virus in gene therapy: application for treatment of malignant disease. J Virol., 76: 895–904.
Ge XY, Li JL, Yang XL, Chmura AA, Zhu G, Epstein JH, Mazet JK, Hu B, Zhang W, Peng C, Zhang YJ, Luo CM, Tan B, Wang N, Zhu Y, Crameri G, Zhang SY, Wang LF, Daszak P, Shi ZL. 2013. Isolation and characterization of a bat SARS-like coronavirus that uses the ACE2 receptor. Nature., 28: 535–538.
Halpin K, Young PL, Field HE, Mackenzie JS. 2000. Isolation of Hendra virus from pteropid bats: a natural reservoir of Hendra virus. J Gen Virol, 81: 1927–1932.
Hayman DT, Bowen RA, Cryan PM, McCracken GF, O'Shea TJ, Peel AJ, Gilbert A, Webb CT, Wood JLN. 2013. Ecology of Zoonotic Infectious Diseases in Bats: Current Knowledge and Future Directions. Zoonoses and Public Health, 60: 2–21.
He X, Korytař T, Schatz J, Freuling CM, Müller T, Köllner B. 2014. Anti-lyssaviral activity of interferons κ and ω from the serotine bat, Eptesicus serotinus. J Virol., 88: 5444–5454.
Janardhana V, Tachedjian M, Crameri G, Cowled C, Wang LF, Baker ML. 2012. Cloning, expression and antiviral activity of IFNgamma from the Australian fruit bat, Pteropus alecto. Dev Comp Immunol, 36: 610–618.
Jones KE, Patel NG, Levy MA, Storeygard A, Balk D, Gittleman JL, Daszak P. 2008. Global trends in emerging infectious diseases. Nature, 451: 990–993.
Kepler TB, Sample C, Hudak K, Roach J, Haines A, Walsh A, Ramsburg EA. 2010. Chiropteran types I and II interferon genes inferred from genome sequencing traces by a statistical genefamily assembler. BMC Genomics, 11: 444.
Lau SK, Woo PC, Li KS, Huang Y, Tsoi HW, Wong BH, Wong SS, Leung SY, Chan KH, Yuen KY. 2005. Severe acute respiratory syndrome coronavirus-like virus in Chinese horseshoe bats. Proc Natl Acad Sci U S A, 102: 14040–14045.
Li J, Zhang G, Cheng D, Ren H, Qian M, Du B. 2015. Molecular characterization of RIG-I, STAT-1 and IFN-beta in the horseshoe bat. Gene, 561: 115–123.
Li W, Shi Z, Yu M, Ren W, Smith C, Epstein JH, Wang H, Crameri G, Hu Z, Zhang H, Zhang J, McEachern J, Field H, Daszak P, Eaton BT, Zhang S, Wang LF. 2005. Bats are natural reservoirs of SARS-like coronaviruses. Science, 310: 676–679.
Li Y, Ge X, Zhang H, Zhou P, Zhu Y, Zhang Y, Yuan J, Wang LF, Shi Z. 2010. Host range, prevalence, and genetic diversity of adenoviruses in bats. J Virol, 84: 3889–3897.
Marchler-Bauer A, Lu S, Anderson JB, Chitsaz F, Derbyshire MK, DeWeese-Scott C, Fong JH, Geer LY, Geer RC, Gonzales NR, Gwadz M, Hurwitz DI, Jackson JD, Ke Z, Lanczycki CJ, Lu F, Marchler GH, Mullokandov M, Omelchenko MV, Robertson CL, Song JS, Thanki N, Yamashita RA, Zhang D, Zhang N, Zheng C, Bryant SH. 2011. CDD: a Conserved Domain Database for the functional annotation of proteins. Nucleic Acids Res, 39: D225–229.
Marsh GA, Wang LF. 2012. Hendra and Nipah viruses: why are they so deadly? Curr Opin Virol, 2: 242–247.
Middleton DJ, Morrissy CJ, van der Heide BM, Russell GM, Braun MA, Westbury HA, Halpin K, Daniels PW. 2007. Experimental Nipah virus infection in pteropid bats (Pteropus poliocephalus). J Comp Pathol, 136: 266–272.
O'Shea TJ, Cryan PM, Cunningham AA, Fooks AR, Hayman DT, Luis AD, Peel AJ, Plowright RK, Wood JL. 2014. Bat flight and zoonotic viruses. Emerg Infect Dis, 20: 741–745.
Omatsu T, Bak EJ, Ishii Y, Kyuwa S, Tohya Y, Akashi H, Yoshikawa Y. 2008. Induction and sequencing of Rousette bat interferon alpha and beta genes. Vet Immunol Immunopathol, 124: 169–176.
Papenfuss AT, Baker ML, Feng ZP, Tachedjian M, Crameri G, Cowled C, Ng J, Janardhana V, Field HE, Wang LF. 2012. The immune gene repertoire of an important viral reservoir, the Australian black flying fox. BMC Genomics, 13: 261.
Plowright RK, Field HE, Smith C, Divljan A, Palmer C, Tabor G, Daszak P, Foley JE. 2008. Reproduction and nutritional stress are risk factors for Hendra virus infection in little red flying foxes (Pteropus scapulatus). Proceedings of the Royal Society B-Biological Sciences, 275: 861–869.
Pourrut X, Souris M, Towner JS, Rollin PE, Nichol ST, Gonzalez JP, Leroy E. 2009. Large serological survey showing cocirculation of Ebola and Marburg viruses in Gabonese bat populations, and a high seroprevalence of both viruses in Rousettus aegyptiacus. BMC Infect Dis, 9: 159.
Randall RE, Goodbourn S. 2008. Interferons and viruses: an interplay between induction, signalling, antiviral responses and virus countermeasures. J Gen Virol, 89: 1–47.
Shi Z. 2013. Emerging infectious diseases associated with bat viruses. Sci China Life Sci, 56: 678–682.
Thompson JD, Higgins DG, Gibson TJ. 1994. CLUSTAL W: improving the sensitivity of progressive multiple sequence alignment through sequence weighting, position-specific gap penalties and weight matrix choice. Nucleic Acids Res, 22: 4673–4680.
Turmelle AS, Jackson FR, Green D, McCracken GF, Rupprecht CE. 2010. Host immunity to repeated rabies virus infection in big brown bats. J Gen Virol, 91: 2360–2366.
Virtue ER, Marsh GA, Baker ML, Wang LF. 2011. Interferon production and signaling pathways are antagonized during henipavirus infection of fruit bat cell lines. PLoS One, 6: e22488.
Wang LF, Walker PJ, Poon LL. 2011. Mass extinctions, biodiversity and mitochondrial function: are bats ‘special’ as reservoirs for emerging viruses? Curr Opin Virol, 1: 649–657.
Williamson MM, Hooper PT, Selleck PW, Gleeson LJ, Daniels PW, Westbury HA, Murray PK. 1998. Transmission studies of Hendra virus (equine morbillivirus) in fruit bats, horses and cats. Aust Vet J, 76: 813–818.
Williamson MM, Hooper PT, Selleck PW, Westbury HA, Slocombe RF. 2000. Experimental hendra virus infectionin pregnant guinea-pigs and fruit Bats (Pteropus poliocephalus). J Comp Pathol, 122: 201–207.
Zhang G, Cowled C, Shi Z, Huang Z, Bishop-Lilly KA, Fang X, Wynne JW, Xiong Z, Baker ML, Zhao W, Tachedjian M, Zhu Y, Zhou P, Jiang X, Ng J, Yang L, Wu L, Xiao J, Feng Y, Chen Y, Sun X, Zhang Y, Marsh GA, Crameri G, Broder CC, Frey KG, Wang LF, Wang J. 2013. Comparative analysis of bat genomes provides insight into the evolution of flight and immunity. Science, 339: 456–460.
Zhou P, Cowled C, Marsh GA, Shi Z, Wang LF, Baker ML. 2011a. Type III IFN receptor expression and functional characterisation in the pteropid bat, Pteropus alecto. PLoS One, 6: e25385.
Zhou P, Cowled C, Todd S, Crameri G, Virtue ER, Marsh GA, Klein R, Shi Z, Wang LF, Baker ML. 2011b. Type III IFNs in pteropid bats: differential expression patterns provide evidence for distinct roles in antiviral immunity. J Immunol, 186: 3138–3147.
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Liang, YZ., Wu, LJ., Zhang, Q. et al. Cloning, expression, and antiviral activity of interferon β from the Chinese microbat, Myotis davidii . Virol. Sin. 30, 425–432 (2015). https://doi.org/10.1007/s12250-015-3668-2
- IFN-stimulated genes
- antiviral activity