White-nose syndrome is associated with increased replication of a naturally persisting coronaviruses in bats

Scientific Reports

Volumn 8, Issue 1, 2018, Pages

  Davy, Christina M ^a   Donaldson, Michael E ^a   Subudhi, Sonu ^b   Rapin, Noreen ^b   Warnecke, Lisa ^c,d   Turner, James M ^c,e   Bollinger, Trent K ^b   Kyle, Christopher J ^a   Dorville, Nicole A S Y ^c   Kunkel, Emma L ^c   Norquay, Kaleigh J O ^c   Dzal, Yvonne A ^c   Willis, Craig K R ^c   Misra, Vikram ^b  

^a TRENT UNIVERSITY   (Canada)

^b UNIVERSITY OF SASKATCHEWAN   (Canada)

^c UNIVERSITY OF WINNIPEG   (Canada)

^d UNIVERSITY OF HAMBURG   (Germany)

^e CHARLES STURT UNIVERSITY   (Australia)

Author keywords

[No Author keywords available]

Indexed keywords

VIRUS ANTIBODY; VIRUS RNA;

ANIMAL; ASCOMYCETES; BAT; BIOLOGICAL MODEL; CORONAVIRINAE; GENE EXPRESSION REGULATION; GENETICS; IMMUNOLOGY; INNATE IMMUNITY; INTESTINE; MALE; METABOLISM; MICROBIOLOGY; MIXED INFECTION; MYCOSIS; PHYSIOLOGY; VETERINARY MEDICINE; VIROLOGY; VIRUS REPLICATION;

ANIMALS; ANTIBODIES, VIRAL; ASCOMYCOTA; CHIROPTERA; COINFECTION; CORONAVIRUS; GENE EXPRESSION REGULATION; IMMUNITY, INNATE; INTESTINES; MALE; MODELS, BIOLOGICAL; MYCOSES; RNA, VIRAL; VIRUS REPLICATION;

EID: 85055079899     PISSN: None     EISSN: 20452322     Source Type: Journal    
DOI: 10.1038/s41598-018-33975-x     Document Type: Article

References (69)

1. Ge, X. Y. et al. Isolation and characterization of a bat SARS-like coronavirus that uses the ACE2 receptor. Nature 503, 535–538, 10.1038/nature12711 (2013)
2. Corman, V. M. et al. Rooting the phylogenetic tree of middle East respiratory syndrome coronavirus by characterization of a conspecific virus from an African bat. J Virol 88, 11297–11303, 10.1128/JVI.01498-14 (2014)
3. Ithete, N. L. et al. Close relative of human Middle East respiratory syndrome coronavirus in bat, South Africa. Emerg Infect Dis 19, 1697–1699, 10.3201/eid1910.130946 (2013)
4. Yang, L. et al. MERS-related betacoronavirus in Vespertilio superans bats, China. Emerg Infect Dis 20, 1260–1262, 10.3201/eid2007.140318 (2014)
5. Anthony, S. J. et al. Further Evidence for Bats as the Evolutionary Source of Middle East Respiratory Syndrome Coronavirus. MBio 8, 10.1128/mBio.00373-17 (2017)
6. Huang, Y. W. et al. Origin, evolution, and genotyping of emergent porcine epidemic diarrhea virus strains in the United States. MBio 4, e00737–00713, 10.1128/mBio.00737-13 (2013)
7. Zhou, P. et al. Fatal swine acute diarrhoea syndrome caused by an HKU2-related coronavirus of bat origin. Nature 556, 255–258, 10.1038/s41586-018-0010-9 (2018)
8. Halpin, K., Young, P. L., Field, H. E. & Mackenzie, J. S. Isolation of Hendra virus from pteropid bats: a natural reservoir of Hendra virus. J Gen Virol 81, 1927–1932 (2000)
9. Yob, J. M. et al. Nipah virus infection in bats (order Chiroptera) in peninsular Malaysia. Emerg Infect Dis 7, 439–441, 10.3201/eid0703.010312 (2001)
10. Towner, J. S. et al. Isolation of genetically diverse Marburg viruses from Egyptian fruit bats. PLoS Pathog 5, e1000536, 10.1371/journal.ppat.1000536 (2009)
11. Leroy, E. M. et al. Fruit bats as reservoirs of Ebola virus. Nature 438, 575–576, 10.1038/438575a (2005)
12. Vijaykrishna, D. et al. Evolutionary insights into the ecology of coronaviruses. J Virol 81, 4012–4020, 10.1128/JVI.02605-06 (2007)
13. Drexler, J. F. et al. Bats host major mammalian paramyxoviruses. Nat Commun 3, 796, 10.1038/ncomms1796 (2012)
14. Freuling, C., Vos, A., Johnson, N., Fooks, A. R. & Muller, T. Bat rabies–a Gordian knot? Berl Munch Tierarztl Wochenschr 122, 425–433 (2009)
15. Gonzalez, J. P., Pourrut, X. & Leroy, E. Ebolavirus and other filoviruses. Curr Top Microbiol Immunol 315, 363–387 (2007)
16. Chu, D. K. et al. Coronaviruses in bent-winged bats (Miniopterus spp.). J Gen Virol 87, 2461–2466, 10.1099/vir.0.82203-0 (2006)
17. Halpin, K. et al. Pteropid bats are confirmed as the reservoir hosts of henipaviruses: a comprehensive experimental study of virus transmission. Am J Trop Med Hyg 85, 946–951, 10.4269/ajtmh.2011.10-0567 (2011)
18. Middleton, D. J. et al. Experimental Nipah virus infection in pteropid bats (Pteropus poliocephalus). J Comp Pathol 136, 266–272, 10.1016/j.jcpa.2007.03.002 (2007)
19. Baker, M. L., Schountz, T. & Wang, L. F. Antiviral immune responses of bats: a review. Zoonoses Public Health 60, 104–116, 10.1111/j.1863-2378.2012.01528.x (2013)
20. O’Shea, T. J. et al. Bat flight and zoonotic viruses. Emerg Infect Dis 20, 741–745, 10.3201/eid2005.130539 (2014)
21. Plowright, R. K. et al. Ecological dynamics of emerging bat virus spillover. Proc Biol Sci 282, 20142124, 10.1098/rspb.2014.2124 (2015)
22. Plowright, R. K. et al. Urban habituation, ecological connectivity and epidemic dampening: the emergence of Hendra virus from flying foxes (Pteropus spp.). Proc Biol Sci 278, 3703–3712, 10.1098/rspb.2011.0522 (2011)
23. Webber, Q. M. R. et al. Social network characteristics and predicted pathogen transmission in summer colonies of female big brown bats (Eptesicus fuscus). Behavioral Ecology and Sociobiology 70, 701–712, 10.1007/s00265-016-2093-3 (2016)
24. Drexler, J. F. et al. Amplification of emerging viruses in a bat colony. Emerg Infect Dis 17, 449–456, 10.3201/eid1703.100526 (2011)
25. Field, H. et al. Hendra virus infection dynamics in Australian fruit bats. PLoS One 6, e28678, 10.1371/journal.pone.0028678 (2011)
26. Plowright, R. K. et al. Reproduction and nutritional stress are risk factors for Hendra virus infection in little red flying foxes (Pteropus scapulatus). Proc Biol Sci 275, 861–869, 10.1098/rspb.2007.1260 (2008)
27. Pourrut, X. et al. Spatial and temporal patterns of Zaire ebolavirus antibody prevalence in the possible reservoir bat species. J Infect Dis 196(Suppl 2), S176–183, 10.1086/520541 (2007)
28. Rahman, S. A. et al. Characterization of Nipah virus from naturally infected Pteropus vampyrus bats, Malaysia. Emerg Infect Dis 16, 1990–1993, 10.3201/eid1612.091790 (2010)
29. McMichael, L. et al. Physiological stress and Hendra virus in flying-foxes (Pteropus spp.), Australia. PLoS One 12, e0182171, 10.1371/journal.pone.0182171 (2017)
30. Roizman, B. & Sears, A. E. In Fields Virology Vol. 2 (eds Fields, B. N., Knipe, D. M. & Howley, P. M.) 2231–2295 Lippincott-Raven (1996)
31. Amman, B. R. et al. Seasonal pulses of Marburg virus circulation in juvenile Rousettus aegyptiacus bats coincide with periods of increased risk of human infection. PLoS Pathog 8, e1002877, 10.1371/journal.ppat.1002877 (2012)
32. Subudhi, S. et al. A persistently infecting coronavirus in hibernating Myotis lucifugus, the North American little brown bat. J Gen Virol 98, 2297–2309, 10.1099/jgv.0.000898 (2017)
33. Dominguez, S. R., O’Shea, T. J., Oko, L. M. & Holmes, K. V. 1 coronaviruses in bats in North America. Emerg Infect Dis 13, 1295–1300, 10.3201/eid1309.070491 (2007). Detection of group
34. Blehert, D. S. et al. Bat white-nose syndrome: an emerging fungal pathogen? Science 323, 227, 10.1126/science.1163874 (2009)
35. Frick, W. F. et al. An emerging disease causes regional population collapse of a common North American bat species. Science 329, 679–682, 10.1126/science.1188594 (2010)
36. Lorch, J. M. et al. Experimental infection of bats with Geomyces destructans causes white-nose syndrome. Nature 480, 376–378, 10.1038/nature10590 (2011)
37. Warnecke, L. et al. Inoculation of bats with European Geomyces destructans supports the novel pathogen hypothesis for the origin of white-nose syndrome. Proc Natl Acad Sci USA 109, 6999–7003, 10.1073/pnas.1200374109 (2012)
38. Field, K. A. et al. The White-Nose Syndrome Transcriptome: Activation of Anti-fungal Host Responses in Wing Tissue of Hibernating Little Brown Myotis. PLoS Pathog 11, e1005168, 10.1371/journal.ppat.1005168 (2015)
39. Davy, C. M. et al. The other white-nose syndrome transcriptome: Tolerant and susceptible hosts respond differently to the pathogen. Ecol Evol 7, 7161–7170, 10.1002/ece3.3234 (2017)
40. Verant, M. L. et al. White-nose syndrome initiates a cascade of physiologic disturbances in the hibernating bat host. BMC Physiol 14, 10, 10.1186/s12899-014-0010-4 (2014)
41. Warnecke, L. et al. Pathophysiology of white-nose syndrome in bats: a mechanistic model linking wing damage to mortality. Biol Lett 9, 20130177, 10.1098/rsbl.2013.0177 (2013)
42. McGuire, L. P., Mayberry, H. W. & Willis, C. K. R. White-nose syndrome increases torpid metabolic rate and evaporative water loss in hibernating bats. Am J Physiol Regul Integr Comp Physiol 313, R680–R686, 10.1152/ajpregu.00058.2017 (2017)
43. Rapin, N. et al. Activation of innate immune-response genes in little brown bats (Myotis lucifugus) infected with the fungus Pseudogymnoascus destructans. PLoS One 9, e112285, 10.1371/journal.pone.0112285 (2014)
44. Pauli, G., Moura Mascarin, G., Eilenberg, J. & Delalibera Júnior, I. Within-Host Competition between Two Entomopathogenic Fungi and a Granulovirus In. Insects 9 10.3390/insects9020064 (2018)
45. Whitfield, S. M. et al. Infection and co-infection by the amphibian chytrid fungus and ranavirus in wild Costa Rican frogs. Dis Aquat Organ 104, 173–178, 10.3354/dao02598 (2013)
46. Osborne, C. et al. Alphacoronaviruses in New World bats: prevalence, persistence, phylogeny, and potential for interaction with humans. PLoS One 6, e19156, 10.1371/journal.pone.0019156 (2011)
47. Strong, J. E. et al. Stimulation of Ebola virus production from persistent infection through activation of the Ras/MAPK pathway. Proc Natl Acad Sci USA 105, 17982–17987, 10.1073/pnas.0809698105 (2008)
48. Mizutani, T. et al. Mechanisms of establishment of persistent SARS-CoV-infected cells. Biochem Biophys Res Commun 347, 261–265, 10.1016/j.bbrc.2006.06.086 (2006)
49. Mizutani, T., Fukushi, S., Saijo, M. & Kurane, I. Characterization of persistent SARS-CoV infection in Vero E6 cells. Adv Exp Med Biol 581, 323–326 (2006)
50. Palacios, G., Jabado, O., Renwick, N., Briese, T. & Lipkin, W. I. Severe acute respiratory syndrome coronavirus persistence in Vero cells. Chin Med J (Engl) 118, 451–459 (2005)
51. Ng, C. T. & Oldstone, M. B. IL-10: achieving balance during persistent viral infection. Curr Top Microbiol Immunol 380, 129–144, 10.1007/978-3-662-43492-5_6 (2014)
52. Puntambekar, S. S. et al. Shifting hierarchies of interleukin-10-producing T cell populations in the central nervous system during acute and persistent viral encephalomyelitis. J Virol 85, 6702–6713, 10.1128/JVI.00200-11 (2011)
53. Wilson, E. B. & Brooks, D. G. The role of IL-10 in regulating immunity to persistent viral infections. Curr Top Microbiol Immunol 350, 39–65, 10.1007/82_2010_96 (2011)
54. Hernández, P. P. et al. Interferon-λ and interleukin 22 act synergistically for the induction of interferon-stimulated genes and control of rotavirus infection. Nat Immunol 16, 698–707, 10.1038/ni.3180 (2015)
55. Wolk, K. & Sabat, R. Interleukin-22: a novel T- and NK-cell derived cytokine that regulates the biology of tissue cells. Cytokine Growth Factor Rev 17, 367–380, 10.1016/j.cytogfr.2006.09.001 (2006)
56. Krebs, D. L. et al. SOCS-6 binds to insulin receptor substrate 4, and mice lacking the SOCS-6 gene exhibit mild growth retardation. Mol Cell Biol 22, 4567–4578 (2002)
57. Hensley, L. E. et al. Interferon-beta 1a and SARS coronavirus replication. Emerg Infect Dis 10, 317–319, 10.3201/eid1002.030482 (2004)
58. Falzarano, D. et al. Inhibition of novel beta coronavirus replication by a combination of interferon-alpha2b and ribavirin. Sci Rep 3, 1686, 10.1038/srep01686 (2013)
59. Finlin, B. S. et al. RERG is a novel ras-related, estrogen-regulated and growth-inhibitory gene in breast cancer. J Biol Chem 276, 42259–42267, 10.1074/jbc.M105888200 (2001)
60. Langwig, K. E. et al. Sociality, density-dependence and microclimates determine the persistence of populations suffering from a novel fungal disease, white-nose syndrome. Ecol Lett 15, 1050–1057, 10.1111/j.1461-0248.2012.01829.x (2012)
61. Andrews, S. FastQC A Quality Control tool for High Throughput Sequence Data. http://www.bioinformatics.babraham.ac.uk/projects/fastqc/ citeulike-article-id:11583827
62. Bolger, A. M., Lohse, M. & Usadel, B. Trimmomatic: a flexible trimmer for Illumina sequence data. Bioinformatics 30, 2114–2120, 10.1093/bioinformatics/btu170 (2014)
63. Kim, D. et al. TopHat2: accurate alignment of transcriptomes in the presence of insertions, deletions and gene fusions. Genome Biol 14, R36, 10.1186/gb-2013-14-4-r36 (2013)
64. Cunningham, F. et al. Ensembl 2015. Nucleic Acids Res 43, D662–669, 10.1093/nar/gku1010 (2015)
65. Liao, Y., Smyth, G. K. & Shi, W. featureCounts: an efficient general purpose program for assigning sequence reads to genomic features. Bioinformatics 30, 923–930, 10.1093/bioinformatics/btt656 (2014)
66. Varet, H., Brillet-Guéguen, L., Coppée, J. Y. & Dillies, M. A. SARTools: A DESeq2- and EdgeR-Based R Pipeline for Comprehensive Differential Analysis of RNA-Seq Data. PLoS One 11, e0157022, 10.1371/journal.pone.0157022 (2016)
67. Benjamini, Y. & Hochberg, Y. Controlling the False Discovery Rate: A Practical and Powerful Approach to Multiple Testing. Journal of the Royal Statistical Society. Series B (Methodological) 57, 289–300, 10.2307/2346101 (1995)
68. Reimand, J. et al. g:Profiler-a web server for functional interpretation of gene lists (2016 update). Nucleic Acids Res 44, W83–89, 10.1093/nar/gkw199 (2016)
69. Supek, F., Bošnjak, M., Škunca, N. & Šmuc, T. REVIGO summarizes and visualizes long lists of gene ontology terms. PLoS One 6, e21800, 10.1371/journal.pone.0021800 (2011)