1932

Abstract

Despite a small genome size, bats have comparable diversity of retroviral and non-retroviral endogenous sequences to other mammals. These include Class I and Class II retroviral sequences, foamy viruses, and deltaretroviruses, as well as filovirus, bornavirus, and parvovirus endogenous viral elements. Some of these endogenous viruses are sufficiently preserved in bat genomes to be expressed, with potential effects for host biology. It is clear that the bat immune system differs when compared with other mammals, yet the role that virus-derived endogenous elements may have played in the evolution of bat immunity is poorly understood. In this review, we discuss some of the bat-specific immune mechanisms that may have resulted in a virus-tolerant phenotype and link these to the long-standing virus-host coevolution that may have allowed a large diversity of endogenous retroviruses and other endogenous viral elements to colonize bat genomes. We also consider the possible effects of endogenization in the evolution of the bat immune system.

Keyword(s): batsERVsEVEsevolutionimmunityviruses
Loading

Article metrics loading...

/content/journals/10.1146/annurev-virology-092818-015613
2020-09-29
2024-10-16
Loading full text...

Full text loading...

/deliver/fulltext/virology/7/1/annurev-virology-092818-015613.html?itemId=/content/journals/10.1146/annurev-virology-092818-015613&mimeType=html&fmt=ahah

Literature Cited

  1. 1. 
    Jones KE, Bininda-Emonds OR, Gittleman JL 2005. Bats, clocks, and rocks: diversification patterns in Chiroptera. Evolution 59:2243–55
    [Google Scholar]
  2. 2. 
    Teeling EC, Vernes SC, Dávalos LM, Ray DA, Gilbert MTP 2018. Bat biology, genomes, and the Bat1K Project: to generate chromosome-level genomes for all living bat species. Annu. Rev. Anim. Biosci. 6:23–46
    [Google Scholar]
  3. 3. 
    Teeling EC, Springer MS, Madsen O, Bates P, O'Brien SJ, Murphy WJ 2005. A molecular phylogeny for bats illuminates biogeography and the fossil record. Science 307:580–84
    [Google Scholar]
  4. 4. 
    Agnarsson I, Zambrana-Torrelio CM, Flores-Saldana NP, May-Collado LJ 2011. A time-calibrated species-level phylogeny of bats (Chiroptera, Mammalia). PLOS Curr 3:RRN1212
    [Google Scholar]
  5. 5. 
    Meredith RW, Janečka JE, Gatesy J, Ryder OA, Fisher CA et al. 2011. Impacts of the Cretaceous Terrestrial Revolution and KPg extinction on mammal diversification. Science 334:6055521–24
    [Google Scholar]
  6. 6. 
    Kunz TH, Braun de Torrez E, Bauer D, Lobova T, Fleming TH 2011. Ecosystem services provided by bats. Ann. N. Y. Acad. Sci. 1223:1–38
    [Google Scholar]
  7. 7. 
    Calisher CH, Childs JE, Field HE, Holmes KV, Schountz T 2006. Bats: important reservoir hosts of emerging viruses. Clin. Microbiol. Rev. 19:531–45
    [Google Scholar]
  8. 8. 
    Olival KJ, Hosseini PR, Zambrana-Torrelio C, Ross N, Bogich TL, Daszak P 2017. Host and viral traits predict zoonotic spillover from mammals. Nature 546:766064650Looks at viral diversity in wildlife to predict virus spillover.
    [Google Scholar]
  9. 9. 
    Wang LF, Anderson DE. 2019. Viruses in bats and potential spillover to animals and humans. Curr. Opin. Virol. 34:79–89
    [Google Scholar]
  10. 10. 
    Luis AD, Hayman DT, O'Shea TJ, Cryan PM, Gilbert AT et al. 2013. A comparison of bats and rodents as reservoirs of zoonotic viruses: Are bats special. ? Proc. R. Soc. B 280:175620122753
    [Google Scholar]
  11. 11. 
    Wang LF, Walker PJ, Poon LL 2011. Mass extinctions, biodiversity and mitochondrial function: Are bats ‘special’ as reservoirs for emerging viruses. ? Curr. Opin. Virol. 1:6649–57
    [Google Scholar]
  12. 12. 
    Kurth R, Bannert N. 2010. Retroviruses: Molecular Biology, Genomics and Pathogenesis Norfolk, UK: Caister Acad.
    [Google Scholar]
  13. 13. 
    Katzourakis A, Gifford RJ. 2010. Endogenous viral elements in animal genomes. PLOS Genet 6:e1001191
    [Google Scholar]
  14. 14. 
    Aiewsakun P, Katzourakis A. 2015. Endogenous viruses: connecting recent and ancient viral evolution. Virology 479:26–37Summarizes research on non-retroviral EVEs found in mammalian genomes.
    [Google Scholar]
  15. 15. 
    Gilbert C, Feschotte C. 2010. Genomic fossils calibrate the long-term evolution of hepadnaviruses. PLOS Biol 8:e1000495
    [Google Scholar]
  16. 16. 
    Broecker F, Moelling K. 2019. Evolution of immune systems from viruses and transposable elements. Front. Microbiol. 10:51Looks at evolution of immune systems in response to virus infection and EVE presence.
    [Google Scholar]
  17. 17. 
    Chen J, Foroozesh M, Qin Z 2019. Transactivation of human endogenous retroviruses by tumor viruses and their functions in virus-associated malignancies. Oncogenesis 8:16
    [Google Scholar]
  18. 18. 
    Engel ME, Hiebert SW. 2010. The enemy within: dormant retroviruses awaken. Nat. Med. 16:517–18
    [Google Scholar]
  19. 19. 
    Weiss RA. 2013. On the concept and elucidation of endogenous retroviruses. Philos. Trans. R. Soc. B 368:162620120494
    [Google Scholar]
  20. 20. 
    Katzourakis A, Tristem M, Pybus OG, Gifford RJ 2007. Discovery and analysis of the first endogenous lentivirus. PNAS 104:156261–65
    [Google Scholar]
  21. 21. 
    Han GZ, Worobey M. 2015. A primitive endogenous lentivirus in a colugo: insights into the early evolution of lentiviruses. Mol. Biol. Evol. 32:211–15
    [Google Scholar]
  22. 22. 
    Hayward A, Cornwallis CK, Jern P 2015. Pan-vertebrate comparative genomics unmasks retrovirus macroevolution. PNAS 112:464–69
    [Google Scholar]
  23. 23. 
    Johnson WE. 2015. Endogenous retroviruses in the genomics era. Annu. Rev. Virol. 2:135–59
    [Google Scholar]
  24. 24. 
    Hayward JA, Tachedjian M, Cui J, Field H, Holmes EC et al. 2013. Identification of diverse full-length endogenous betaretroviruses in megabats and microbats. Retrovirology 10:35
    [Google Scholar]
  25. 25. 
    Zhang G, Cowled C, Shi Z, Huang Z, Bishop-Lilly KA et al. 2013. Comparative analysis of bat genomes provides insight into the evolution of flight and immunity. Science 339:456–60
    [Google Scholar]
  26. 26. 
    Escalera-Zamudio M, Mendoza MLZ, Heeger F, Loza-Rubio E, Rojas-Anaya E et al. 2015. A novel endogenous betaretrovirus in the common vampire bat (Desmodus rotundus) suggests multiple independent infection and cross-species transmission events. J. Virol. 89:5180–84
    [Google Scholar]
  27. 27. 
    Tarlinton RE, Meers J, Young PR 2006. Retroviral invasion of the koala genome. Nature 442:79–81
    [Google Scholar]
  28. 28. 
    Cui J, Tachedjian G, Tachedjian M, Holmes EC, Zhang S, Wang LF 2012. Identification of diverse groups of endogenous gammaretroviruses in mega- and microbats. J. Gen. Virol. 93:2037–45
    [Google Scholar]
  29. 29. 
    Jebb D, Huang Z, Pippel M, Hughes GM, Lavrichenko K 2019. Six new reference-quality bat genomes illuminate the molecular basis and evolution of bat adaptations. bioRxiv. https://doi.org/10.1101/836874 High-quality assemblies of six bat genomes with comparison to seven other mammalian genomes.
    [Crossref] [Google Scholar]
  30. 30. 
    Zhuo X, Feschotte C. 2015. Cross-species transmission and differential fate of an endogenous retrovirus in three mammal lineages. PLOS Pathog 11:e1005279
    [Google Scholar]
  31. 31. 
    Skirmuntt EC, Katzourakis A. 2019. The evolution of endogenous retroviral envelope genes in bats and their potential contribution to host biology. Virus Res 270:197645
    [Google Scholar]
  32. 32. 
    Cui J, Tachedjian M, Wang L, Tachedjian G, Wang LF, Zhang S 2012. Discovery of retroviral homologs in bats: implications for the origin of mammalian gammaretroviruses. J. Virol. 86:4288–93
    [Google Scholar]
  33. 33. 
    Zhuo X, Rho M, Feschotte C 2013. Genome-wide characterization of endogenous retroviruses in the bat Myotis lucifugus reveals recent and diverse infections. J. Virol. 87:8493–501
    [Google Scholar]
  34. 34. 
    Cui J, Tachedjian G, Wang LF 2015. Bats and rodents shape mammalian retroviral phylogeny. Sci. Rep. 5:16561
    [Google Scholar]
  35. 35. 
    Gifford R, Kabat P, Martin J, Lynch C, Tristem M 2005. Evolution and distribution of class II-related endogenous retroviruses. J. Virol. 79:6478–86
    [Google Scholar]
  36. 36. 
    Farkasova H, Hron T, Paces J, Hulva P, Benda P et al. 2017. Discovery of an endogenous Deltaretrovirus in the genome of long-fingered bats (Chiroptera: Miniopteridae). PNAS 114:3145–50
    [Google Scholar]
  37. 37. 
    Hron T, Farkašová H, Gifford R, Benda P, Hulva P et al. 2018. Remnants of an ancient Deltaretrovirus in the genomes of horseshoe bats (Rhinolophidae). Viruses 10:4185
    [Google Scholar]
  38. 38. 
    Drexler JF, Corman VM, Muller MA, Maganga GD, Vallo P et al. 2012. Bats host major mammalian paramyxoviruses. Nat. Commun. 3:796
    [Google Scholar]
  39. 39. 
    Hayman DT, Bowen RA, Cryan PM, McCracken GF, O'Shea TJ et al. 2013. Ecology of zoonotic infectious diseases in bats: current knowledge and future directions. Zoonoses Public Health 60:2–21
    [Google Scholar]
  40. 40. 
    Escalera-Zamudio M, Rojas-Anaya E, Kolokotronis SO, Taboada B, Loza-Rubio E et al. 2016. Bats, primates, and the evolutionary origins and diversification of mammalian gammaherpesviruses. mBio 7:e01425-16
    [Google Scholar]
  41. 41. 
    Belyi VA, Levine AJ, Skalka AM 2010. Unexpected inheritance: multiple integrations of ancient bornavirus and Ebolavirus/Marburgvirus sequences in vertebrate genomes. PLOS Pathog 6:e1001030
    [Google Scholar]
  42. 42. 
    Horie M, Honda T, Suzuki Y, Kobayashi Y, Daito T et al. 2010. Endogenous non-retroviral RNA virus elements in mammalian genomes. Nature 463:72778487
    [Google Scholar]
  43. 43. 
    Taylor DJ, Leach RW, Bruenn J 2010. Filoviruses are ancient and integrated into mammalian genomes. BMC Evol. Biol. 10:193
    [Google Scholar]
  44. 44. 
    Mendoza MLZ, Xiong ZJ, Escalera-Zamudio M, Runge AK, Theze J et al. 2018. Hologenomic adaptations underlying the evolution of sanguivory in the common vampire bat. Nat. Ecol. Evol. 2:659–68
    [Google Scholar]
  45. 45. 
    Horie M, Kobayashi Y, Honda T, Fujino K, Akasaka T et al. 2016. An RNA-dependent RNA polymerase gene in bat genomes derived from an ancient negative-strand RNA virus. Sci. Rep. 6:25873
    [Google Scholar]
  46. 46. 
    Ludwig H, Bode L. 2000. Borna disease virus: new aspects on infection, disease, diagnosis and epidemiology. Rev. Sci. Tech. 19:259–88
    [Google Scholar]
  47. 47. 
    Kinnunen PM, Palva A, Vaheri A, Vapalahti O 2013. Epidemiology and host spectrum of Borna disease virus infections. J. Gen. Virol. 94:247–62
    [Google Scholar]
  48. 48. 
    Cui J, Wang LF. 2015. Genomic mining reveals deep evolutionary relationships between Bornaviruses and bats. Viruses 7:5792–800
    [Google Scholar]
  49. 49. 
    Fujino K, Horie M, Honda T, Merriman DK, Tomonaga K 2014. Inhibition of Borna disease virus replication by an endogenous bornavirus-like element in the ground squirrel genome. PNAS 111:3613175–80
    [Google Scholar]
  50. 50. 
    Geib T, Sauder C, Venturelli S, Hässler C, Staeheli P, Schwemmle M 2003. Selective virus resistance conferred by expression of Borna disease virus nucleocapsid components. J. Virol. 77:74283–90
    [Google Scholar]
  51. 51. 
    Herzog S, Frese K, Rott R 1991. Studies on the genetic control of resistance of black hooded rats to Borna disease. J. Gen. Virol. 72:3535–40
    [Google Scholar]
  52. 52. 
    Parrish NF, Fujino K, Shiromoto Y, Iwasaki YW, Ha H et al. 2015. piRNAs derived from ancient viral processed pseudogenes as transgenerational sequence-specific immune memory in mammals. RNA 21:1691–703
    [Google Scholar]
  53. 53. 
    Zong J, Yao X, Yin J, Zhang D, Ma H 2009. Evolution of the RNA-dependent RNA polymerase (RdRP) genes: duplications and possible losses before and after the divergence of major eukaryotic groups. Gene 447:129–39
    [Google Scholar]
  54. 54. 
    Maillard PV, Ciaudo C, Marchais A, Li Y, Jay F et al. 2013. Antiviral RNA interference in mammalian cells. Science 342:6155235–38
    [Google Scholar]
  55. 55. 
    Honda T, Tomonaga K. 2016. Endogenous non-retroviral RNA virus elements evidence a novel type of antiviral immunity. Mobile Genet. Elem. 6:31548–54
    [Google Scholar]
  56. 56. 
    Timothy F, Booth DR, Beniac MJ, Rabb L, Lamboo L 2015. Filovirus structure and morphogenesis. Biology and Pathogenesis of Rhabdo- and Filoviruses AK Pattnaik, MA Whitt 427–51 Hackensack, NJ: World Sci. Publ. Co.
    [Google Scholar]
  57. 57. 
    Negredo A, Palacios G, Vazquez-Moron S, Gonzalez F, Dopazo H et al. 2011. Discovery of an ebolavirus-like filovirus in Europe. PLOS Pathog 7:e1002304
    [Google Scholar]
  58. 58. 
    Kuhn JH. 2018. Ebolavirus and Marburgvirus infections. Harrison's Principles of Internal Medicine JL Jameson, AS Fauci, DL Kasper, SL Hauser, DL Longo, J Loscalzo 1509–15 New York: McGraw-Hill Educ.
    [Google Scholar]
  59. 59. 
    Yang XL, Tan CW, Anderson DE, Jiang RD, Li B et al. 2019. Characterization of a filovirus (Měnglà virus) from Rousettus bats in China. Nat. Microbiol. 4:39095
    [Google Scholar]
  60. 60. 
    Leroy EM, Kumulungui B, Pourrut X, Rouquet P, Hassanin A et al. 2005. Fruit bats as reservoirs of Ebola virus. Nature 438:575–76
    [Google Scholar]
  61. 61. 
    Pourrut X, Souris M, Towner JS, Rollin PE, Nichol ST et al. 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
    [Google Scholar]
  62. 62. 
    Banyard AC, Evans JS, Luo TR, Fooks AR 2014. Lyssaviruses and bats: emergence and zoonotic threat. Viruses 6:2974–90
    [Google Scholar]
  63. 63. 
    Kondoh T, Manzoor R, Nao N, Maruyama J, Furuyama W et al. 2017. Putative endogenous filovirus VP35-like protein potentially functions as an IFN antagonist but not a polymerase cofactor. PLOS ONE 12:10e0186450
    [Google Scholar]
  64. 64. 
    Cotmore SF, Tattersall P. 2014. Parvoviruses: Small does not mean simple. Annu. Rev. Virol. 2:517–37
    [Google Scholar]
  65. 65. 
    Arriagada G, Gifford RJ. 2014. Parvovirus-derived endogenous viral elements in two South American rodent genomes. J. Virol. 88:12158–62
    [Google Scholar]
  66. 66. 
    Kapoor A, Simmonds P, Lipkin WI 2010. Discovery and characterization of mammalian endogenous parvoviruses. J. Virol. 84:12628–35
    [Google Scholar]
  67. 67. 
    Liu HQ, Fu YP, Xie JT, Cheng JS, Ghabrial SA et al. 2011. Widespread endogenization of densoviruses and parvoviruses in animal and human genomes. J. Virol. 85:9863–76
    [Google Scholar]
  68. 68. 
    Penzes JJ, Marsile-Medun S, Agbandje-McKenna M, Gifford RJ 2018. Endogenous amdoparvovirus-related elements reveal insights into the biology and evolution of vertebrate parvoviruses. Virus Evol 4:vey026
    [Google Scholar]
  69. 69. 
    Lau SKP, Ahmed SS, Tsoi HW, Yeung HC, Li KSM et al. 2017. Bats host diverse parvoviruses as possible origin of mammalian dependoparvoviruses and source for bat-swine interspecies transmission. J. Gen. Virol. 98:3046–59
    [Google Scholar]
  70. 70. 
    Bill CA, Summers J. 2004. Genomic DNA double-strand breaks are targets for hepadnaviral DNA integration. PNAS 101:1113540
    [Google Scholar]
  71. 71. 
    Shackelton LA, Parrish CR, Truyen U, Holmes EC 2005. High rate of viral evolution associated with the emergence of carnivore parvovirus. PNAS 102:379–84
    [Google Scholar]
  72. 72. 
    Chen AY, Qiu JM. 2010. Parvovirus infection-induced cell death and cell cycle arrest. Future Virol 5:731–43
    [Google Scholar]
  73. 73. 
    Muhldorfer K, Speck S, Kurth A, Lesnik R, Freuling C et al. 2011. Diseases and causes of death in European bats: dynamics in disease susceptibility and infection rates. PLOS ONE 6:e29773
    [Google Scholar]
  74. 74. 
    Picard-Meyer E, Servat A, Wasniewski M, Gaillard M, Borel C, Cliquet F 2017. Bat rabies surveillance in France: first report of unusual mortality among serotine bats. BMC Vet. Res. 13:387
    [Google Scholar]
  75. 75. 
    Johara MY, Field H, Rashdi AM, Morrissy C, van der Heide B et al. 2001. Nipah virus infection in bats (order Chiroptera) in peninsular Malaysia. Emerging Infect. Dis. 7:439–41
    [Google Scholar]
  76. 76. 
    Baker ML, Schountz T, Wang LF 2013. Antiviral immune responses of bats: a review. Zoonoses Public Health 60:104–16
    [Google Scholar]
  77. 77. 
    Banerjee A, Baker ML, Kulcsar K, Misra V, Plowright R, Mossman K 2020. Novel insights into immune systems of bats. Front. Immunol. 11:26
    [Google Scholar]
  78. 78. 
    Brook CE, Dobson AP. 2015. Bats as ‘special’ reservoirs for emerging zoonotic pathogens. Trends Microbiol 23:172–80
    [Google Scholar]
  79. 79. 
    Schountz T, Baker ML, Butler J, Munster V 2017. Immunological control of viral infections in bats and the emergence of viruses highly pathogenic to humans. Front. Immunol. 8:1098
    [Google Scholar]
  80. 80. 
    Omatsu T, Bak EJ, Ishii Y, Kyuwa S, Tohya Y et al. 2008. Induction and sequencing of Rousette bat interferon α and β genes. Vet. Immunol. Immunopathol. 124:169–76
    [Google Scholar]
  81. 81. 
    Becker DJ, Nachtmann C, Argibay HD, Botto G, Escalera-Zamudio M et al. 2019. Leukocyte profiles reflect geographic range limits in a widespread Neotropical bat. Integr. Comp. Biol. 59:51176–89
    [Google Scholar]
  82. 82. 
    Sarkar SK, Chakravarty AK. 1991. Analysis of immunocompetent cells in the bat, Pteropus giganteus: isolation and scanning electron microscopic characterization. Dev. Comp. Immunol. 15:4423–30
    [Google Scholar]
  83. 83. 
    Ng CT, Sullivan BM, Teijaro JR, Lee AM, Welch M et al. 2015. Blockade of interferon beta, but not interferon alpha, signaling controls persistent viral infection. Cell Host Microbe 17:5653–61
    [Google Scholar]
  84. 84. 
    Fabozzi G, Nabel CS, Dolan MA, Sullivan NJ 2011. Ebolavirus proteins suppress the effects of small interfering RNA by direct interaction with the mammalian RNA interference pathway. J. Virol. 85:62512–23
    [Google Scholar]
  85. 85. 
    Leung DW, Prins KC, Borek DM, Farahbakhsh M, Tufariello JM et al. 2010. Structural basis for dsRNA recognition and interferon antagonism by Ebola VP35. Nat. Struct. Mol. Biol. 17:2165–72
    [Google Scholar]
  86. 86. 
    Xu W, Edwards MR, Borek DM, Feagins AR, Mittal A et al. 2014. Ebola virus VP24 targets a unique NLS binding site on karyopherin alpha 5 to selectively compete with nuclear import of phosphorylated STAT1. Cell Host Microbe 16:2187–200
    [Google Scholar]
  87. 87. 
    Subudhi S, Rapin N, Misra V 2019. Immune system modulation and viral persistence in bats: understanding viral spillover. Viruses 11:2192
    [Google Scholar]
  88. 88. 
    Bratsch S, Wertz N, Chaloner K, Kunz TH, Butler JE 2011. The little brown bat, M. lucifugus, displays a highly diverse V H, D H and J H repertoire but little evidence of somatic hypermutation. Dev. Comp. Immunol. 35:421–30
    [Google Scholar]
  89. 89. 
    Boehme KW, Compton T. 2004. Innate sensing of viruses by toll-like receptors. J. Virol. 78:7867–73
    [Google Scholar]
  90. 90. 
    Iha K, Omatsu T, Watanabe S, Ueda N, Taniguchi S et al. 2010. Molecular cloning and expression analysis of bat Toll-like receptors 3, 7 and 9. J. Vet. Med. Sci. 72:217–20
    [Google Scholar]
  91. 91. 
    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
    [Google Scholar]
  92. 92. 
    Escalera-Zamudio M, Zepeda-Mendoza ML, Loza-Rubio E, Rojas-Anaya E, Mendez-Ojeda ML et al. 2015. The evolution of bat nucleic acid-sensing Toll-like receptors. Mol. Ecol. 24:5899–909
    [Google Scholar]
  93. 93. 
    Ahn M, Cui J, Irving AT, Wang LF 2016. Unique loss of the PYHIN gene family in bats amongst mammals: implications for inflammasome sensing. Sci. Rep. 6:21722
    [Google Scholar]
  94. 94. 
    Zhou P, Tachedjian M, Wynne JW, Boyd V, Cui J et al. 2016. Contraction of the type I IFN locus and unusual constitutive expression of IFN-alpha in bats. PNAS 113:2696–701
    [Google Scholar]
  95. 95. 
    Xie J, Li Y, Shen X, Goh G, Zhu Y et al. 2018. Dampened STING-dependent interferon activation in bats. Cell Host Microbe 23:297–301
    [Google Scholar]
  96. 96. 
    Kuzmin IV, Schwarz TM, Ilinykh PA, Jordan I, Ksiazek TG et al. 2017. Innate immune responses of bat and human cells to filoviruses: commonalities and distinctions. J. Virol. 91:e02471-16
    [Google Scholar]
  97. 97. 
    Philbin VJ, Iqbal M, Boyd Y, Goodchild MJ, Beal RK et al. 2005. Identification and characterization of a functional, alternatively spliced Toll‐like receptor 7 (TLR7) and genomic disruption of TLR8 in chickens. Immunology 114:4507–21
    [Google Scholar]
  98. 98. 
    Lauw FN, Caffrey DR, Golenbock DT 2005. Of mice and man: TLR11 (finally) finds profilin. Trends Immunol 26:509–11
    [Google Scholar]
  99. 99. 
    Bat1K 2019. Bat1K Consortium https://bat1k.ucd.ie/Bat1K
    [Google Scholar]
  100. 100. 
    Eisenstein M. 2018. Bat research takes wing. Lab. Anim. 47:97–100
    [Google Scholar]
  101. 101. 
    Feschotte C, Gilbert C. 2012. Endogenous viruses: insights into viral evolution and impact on host biology. Nat. Rev. Genet. 13:283–96
    [Google Scholar]
  102. 102. 
    Chuong EB. 2018. The placenta goes viral: Retroviruses control gene expression in pregnancy. PLOS Biol 16:e3000028
    [Google Scholar]
  103. 103. 
    Ophinni Y, Palatini U, Hayashi Y, Parrish NF 2019. piRNA-guided CRISPR-like immunity in Eukaryotes. Trends Immunol 40:11998–1010Summary of evidence that EVEs can act in a manner analogous to CRISPR-Cas immunity.
    [Google Scholar]
  104. 104. 
    Whitfield ZJ, Dolan PT, Kunitomi M, Tassetto M, Seetin MG et al. 2017. The diversity, structure, and function of heritable adaptive immunity sequences in the Aedes aegypti genome. Curr. Biol. 27:223511–19
    [Google Scholar]
  105. 105. 
    Tassetto M, Kunitomi M, Whitfield ZJ, Dolan PT, Sánchez-Vargas I et al. 2019. Control of RNA viruses in mosquito cells through the acquisition of vDNA and endogenous viral elements. eLife 8:e41244
    [Google Scholar]
  106. 106. 
    Mandl JN, Schneider C, Schneider DS, Baker ML 2018. Going to bat(s) for studies of disease tolerance. Front. Immunol. 9:2112
    [Google Scholar]
  107. 107. 
    Pritham EJ, Feschotte C. 2007. Massive amplification of rolling-circle transposons in the lineage of the bat Myotis lucifugus. . PNAS 104:1895–900
    [Google Scholar]
  108. 108. 
    Ray DA, Pagan JTH, Thompson ML, Stevens RD 2007. Bats with hATs: evidence for recent DNA transposon activity in genus Myotis. Mol. Biol. Evol 24:3632–39
    [Google Scholar]
  109. 109. 
    Arnaud F, Caporale M, Varela M, Biek R, Chessa B et al. 2007. A paradigm for virus-host coevolution: sequential counter-adaptations between endogenous and exogenous retroviruses. PLOS Pathog 3:1716–29
    [Google Scholar]
  110. 110. 
    Chuong EB, Elde NC, Feschotte C 2016. Regulatory evolution of innate immunity through co-option of endogenous retroviruses. Science 351:62771083–87
    [Google Scholar]
  111. 111. 
    Aswad A, Katzourakis A. 2012. Paleovirology and virally derived immunity. Trends Ecol. Evol. 27:627–36
    [Google Scholar]
  112. 112. 
    Cardenas WB, Loo YM, Gale M, Hartman AL, Kimberlin CR et al. 2006. Ebola virus VP35 protein binds double-stranded RNA and inhibits alpha/beta interferon production induced by RIG-I signaling. J. Virol. 80:5168–78
    [Google Scholar]
  113. 113. 
    Katzourakis A. 2013. Paleovirology: inferring viral evolution from host genome sequence data. Philos. Trans. R. Soc. B 368: https://doi.org/10.1098/rstb.2012.0493
    [Crossref] [Google Scholar]
  114. 114. 
    Harris RS, Liddament MT. 2004. Retroviral restriction by APOBEC proteins. Nat. Rev. Immunol. 4:868–77
    [Google Scholar]
  115. 115. 
    Ozato K, Shin DM, Chang TH, Morse HC 2008. TRIM family proteins and their emerging roles in innate immunity. Nat. Rev. Immunol. 8:849–60
    [Google Scholar]
  116. 116. 
    Lahouassa H, Daddacha W, Hofmann H, Ayinde D, Logue EC et al. 2013. SAMHD1 restricts the replication of human immunodeficiency virus type 1 by depleting the intracellular pool of deoxynucleoside triphosphates. Nat. Immunol. 13:22328
    [Google Scholar]
  117. 117. 
    Hayward JA, Tachedjian M, Cui J, Cheng AZ, Johnson A et al. 2018. Differential evolution of antiretroviral restriction factors in pteropid bats as revealed by APOBEC3 gene complexity. Mol. Biol. Evol. 35:1626–37
    [Google Scholar]
  118. 118. 
    Kassiotis G, Stoye JP. 2016. Immune responses to endogenous retroelements: taking the bad with the good. Nat. Rev. Immunol. 16:4207–19
    [Google Scholar]
  119. 119. 
    Young GR, Ploquin MJ, Eksmond U, Wadwa M, Stoye JP, Kassiotis G 2012. Negative selection by an endogenous retrovirus promotes a higher-avidity CD4+ T cell response to retroviral infection. PLOS Pathog 8:5e1002709
    [Google Scholar]
  120. 120. 
    Brook CE, Boots M, Chandran K, Dobson AP, Drosten C et al. 2020. Accelerated viral dynamics in bat cell lines, with implications for zoonotic emergence. eLife 9:e48401
    [Google Scholar]
  121. 121. 
    Hayman DTS. 2019. Bat tolerance to viral infections. Nat. Microbiol. 4:728–29
    [Google Scholar]
  122. 122. 
    Huang Z, Whelan CV, Foley NM, Jebb D, Touzalin F et al. 2019. Longitudinal comparative transcriptomics reveals unique mechanisms underlying extended healthspan in bats. Nat. Ecol. Evol. 3:1110–20
    [Google Scholar]
  123. 123. 
    Mi S, Lee X, Li X, Veldman GM, Finnerty H et al. 2000. Syncytin is a captive retroviral envelope protein involved in human placental morphogenesis. Nature 403:785–89
    [Google Scholar]
/content/journals/10.1146/annurev-virology-092818-015613
Loading
/content/journals/10.1146/annurev-virology-092818-015613
Loading

Data & Media loading...

  • Article Type: Review Article
This is a required field
Please enter a valid email address
Approval was a Success
Invalid data
An Error Occurred
Approval was partially successful, following selected items could not be processed due to error