1932

Abstract

Endogenous retroviruses comprise millions of discrete genetic loci distributed within the genomes of extant vertebrates. These sequences, which are clearly related to exogenous retroviruses, represent retroviral infections of the deep past, and their abundance suggests that retroviruses were a near-constant presence throughout the evolutionary history of modern vertebrates. Endogenous retroviruses contribute in myriad ways to the evolution of host genomes, as mutagens and as sources of genetic novelty (both coding and regulatory) to be acted upon by the twin engines of random genetic drift and natural selection. Importantly, the richness and complexity of endogenous retrovirus data can be used to understand how viruses spread and adapt on evolutionary timescales by combining population genetics and evolutionary theory with a detailed understanding of retrovirus biology (gleaned from the study of extant retroviruses). In addition to revealing the impact of viruses on organismal evolution, such studies can help us better understand, by looking back in time, how life-history traits, as well as ecological and geological events, influence the movement of viruses within and between populations.

Loading

Article metrics loading...

/content/journals/10.1146/annurev-virology-100114-054945
2015-11-09
2024-03-28
Loading full text...

Full text loading...

/deliver/fulltext/virology/2/1/annurev-virology-100114-054945.html?itemId=/content/journals/10.1146/annurev-virology-100114-054945&mimeType=html&fmt=ahah

Literature Cited

  1. Coffin JM, Hughes SH, Varmus HE. 1.  1997. Retroviruses Cold Spring Harbor, NY: Cold Spring Harbor Lab. Press
  2. Levine AJ, Enquist LW. 2.  2006. History of virology. Fields Virology 1 DM Knipe, PM Howley 3–23 Philadelphia: Lippincott Williams & Wilkins, 5th ed.. [Google Scholar]
  3. Goff SP. 3.  2013. Retroviridae. Fields Virology 2 DM Knipe, PM Howley 1424–73 Philadelphia: Lippincott Williams & Wilkins, 6th ed.. [Google Scholar]
  4. Kozak CA. 4.  2014. Origins of the endogenous and infectious laboratory mouse gammaretroviruses. Viruses 7:1–26 [Google Scholar]
  5. Tarlinton R, Meers J, Young P. 5.  2008. Biology and evolution of the endogenous koala retrovirus. Cell. Mol. Life Sci. 65:3413–21 [Google Scholar]
  6. Temin HM, Mizutani S. 6.  1970. RNA-dependent DNA polymerase in virions of Rous sarcoma virus. Nature 226:1211–13 [Google Scholar]
  7. Baltimore D. 7.  1970. RNA-dependent DNA polymerase in virions of RNA tumour viruses. Nature 226:1209–11 [Google Scholar]
  8. Weiss RA. 8.  2006. The discovery of endogenous retroviruses. Retrovirology 3:67 [Google Scholar]
  9. Rosenthal PN, Robinson HL, Robinson WS, Hanafusa T, Hanafusa H. 9.  1971. DNA in uninfected and virus-infected cells complementary to avian tumor virus RNA. PNAS 68:2336–40 [Google Scholar]
  10. Varmus HE, Weiss RA, Friis RR, Levinson W, Bishop JM. 10.  1972. Detection of avian tumor virus-specific nucleotide sequences in avian cell DNAs. PNAS 69:20–24 [Google Scholar]
  11. Baluda MA. 11.  1972. Widespread presence, in chickens, of DNA complementary to the RNA genome of avian leukosis viruses. PNAS 69:576–80 [Google Scholar]
  12. Martin MA, Bryan T, Rasheed S, Khan AS. 12.  1981. Identification and cloning of endogenous retroviral sequences present in human DNA. PNAS 78:4892–96 [Google Scholar]
  13. Hayward A, Grabherr M, Jern P. 13.  2013. Broad-scale phylogenomics provides insights into retrovirus-host evolution. PNAS 110:20146–51 [Google Scholar]
  14. Hayward A, Cornwallis CK, Jern P. 14.  2015. Pan-vertebrate comparative genomics unmasks retrovirus macroevolution. PNAS 112:464–69 [Google Scholar]
  15. Gifford R, Tristem M. 15.  2003. The evolution, distribution and diversity of endogenous retroviruses. Virus Genes 26:291–315 [Google Scholar]
  16. Jern P, Coffin JM. 16.  2008. Effects of retroviruses on host genome function. Annu. Rev. Genet. 42:709–32 [Google Scholar]
  17. Benveniste RE, Lieber MM, Livingston DM, Sherr CJ, Todaro GJ, Kalter SS. 17.  1974. Infectious C-type virus isolated from a baboon placenta. Nature 248:17–20 [Google Scholar]
  18. Kato S, Matsuo K, Nishimura N, Takahashi N, Takano T. 18.  1987. The entire nucleotide sequence of baboon endogenous virus DNA: a chimeric genome structure of murine type C and simian type D retroviruses. Jpn. J. Genet. 62:127–37 [Google Scholar]
  19. van der Kuyl AC, Dekker JT, Goudsmit J. 19.  1995. Distribution of baboon endogenous virus among species of African monkeys suggests multiple ancient cross-species transmissions in shared habitats. J. Virol. 69:7877–87 [Google Scholar]
  20. Weiss RA, Griffiths D, Takeuchi Y, Patience C, Venables P. 20.  1999. Retroviruses: ancient and modern. Arch. Virol. Suppl. 15:171–77 [Google Scholar]
  21. Turner G, Barbulescu M, Su M, Jensen-Seaman MI, Kidd KK, Lenz J. 21.  2001. Insertional polymorphisms of full-length endogenous retroviruses in humans. Curr. Biol. 11:1531–35 [Google Scholar]
  22. Subramanian RP, Wildschutte JH, Russo C, Coffin JM. 22.  2011. Identification, characterization, and comparative genomic distribution of the HERV-K (HML-2) group of human endogenous retroviruses. Retrovirology 8:90 [Google Scholar]
  23. King AMQ, Adams MJ, Carstens EB, Lefkowitz EJ. 23.  2012. Virus Taxonomy: Ninth Report of the International Committee on Taxonomy of Viruses San Diego, CA: Academic
  24. Blomberg J, Benachenhou F, Blikstad V, Sperber G, Mayer J. 24.  2009. Classification and nomenclature of endogenous retroviral sequences (ERVs): problems and recommendations. Gene 448:115–23 [Google Scholar]
  25. Mayer J, Blomberg J, Seal RL. 25.  2011. A revised nomenclature for transcribed human endogenous retroviral loci. Mob. DNA 2:7 [Google Scholar]
  26. Emerman M, Malik HS. 26.  2010. Paleovirology—modern consequences of ancient viruses. PLOS Biol. 8:e1000301 [Google Scholar]
  27. Lock LF, Keshet E, Gilbert DJ, Jenkins NA, Copeland NG. 27.  1988. Studies of the mechanism of spontaneous germline ecotropic provirus acquisition in mice. EMBO J. 7:4169–77 [Google Scholar]
  28. Stieh DJ, Maric D, Kelley ZL, Anderson MR, Hattaway HZ. 28.  et al. 2014. Vaginal challenge with an SIV-based dual reporter system reveals that infection can occur throughout the upper and lower female reproductive tract. PLOS Pathog. 10:e1004440 [Google Scholar]
  29. Magiorkinis G, Gifford RJ, Katzourakis A, De Ranter J, Belshaw R. 29.  2012. Env-less endogenous retroviruses are genomic superspreaders. PNAS 109:7385–90 [Google Scholar]
  30. Jaenisch R, Schnieke A, Harbers K. 30.  1985. Treatment of mice with 5-azacytidine efficiently activates silent retroviral genomes in different tissues. PNAS 82:1451–55 [Google Scholar]
  31. Harbers K, Schnieke A, Stuhlmann H, Jähner D, Jaenisch R. 31.  1981. DNA methylation and gene expression: endogenous retroviral genome becomes infectious after molecular cloning. PNAS 78:7609–13 [Google Scholar]
  32. Rowe HM, Friedli M, Offner S, Verp S, Mesnard D. 32.  et al. 2013. De novo DNA methylation of endogenous retroviruses is shaped by KRAB-ZFPs/KAP1 and ESET. Development 140:519–29 [Google Scholar]
  33. Rowe HM, Jakobsson J, Mesnard D, Rougemont J, Reynard S. 33.  et al. 2010. KAP1 controls endogenous retroviruses in embryonic stem cells. Nature 463:237–40 [Google Scholar]
  34. Matsui T, Leung D, Miyashita H, Maksakova IA, Miyachi H. 34.  et al. 2010. Proviral silencing in embryonic stem cells requires the histone methyltransferase ESET. Nature 464:927–31 [Google Scholar]
  35. Lukic S, Nicolas JC, Levine AJ. 35.  2014. The diversity of zinc-finger genes on human chromosome 19 provides an evolutionary mechanism for defense against inherited endogenous retroviruses. Cell Death Differ. 21:381–87 [Google Scholar]
  36. Wolf D, Goff S. 36.  2007. TRIM28 mediates primer binding site-targeted silencing of murine leukemia virus in embryonic cells. Cell 131:46–57 [Google Scholar]
  37. Chiu YL, Greene WC. 37.  2008. The APOBEC3 cytidine deaminases: an innate defensive network opposing exogenous retroviruses and endogenous retroelements. Annu. Rev. Immunol. 26:317–53 [Google Scholar]
  38. Schumacher AJ, Nissley DV, Harris RS. 38.  2005. APOBEC3G hypermutates genomic DNA and inhibits Ty1 retrotransposition in yeast. PNAS 102:9854–59 [Google Scholar]
  39. Schumacher AJ, Haché G, Macduff DA, Brown WL, Harris RS. 39.  2008. The DNA deaminase activity of human APOBEC3G is required for Ty1, MusD, and human immunodeficiency virus type 1 restriction. J. Virol. 82:2652–60 [Google Scholar]
  40. Johnson WE. 40.  2013. Rapid adversarial co-evolution of viruses and cellular restriction factors. Curr. Top. Microbiol. Immunol. 371:123–51 [Google Scholar]
  41. Perez-Caballero D, Soll SJ, Bieniasz PD. 41.  2008. Evidence for restriction of ancient primate gammaretroviruses by APOBEC3 but not TRIM5α proteins. PLOS Pathog. 4:e1000181 [Google Scholar]
  42. Jern P, Stoye JP, Coffin JM. 42.  2007. Role of APOBEC3 in genetic diversity among endogenous murine leukemia viruses. PLOS Genet. 3:2014–22 [Google Scholar]
  43. Kaiser SM, Malik HS, Emerman M. 43.  2007. Restriction of an extinct retrovirus by the human TRIM5 antiviral protein. Science 316:1756–58 [Google Scholar]
  44. Lee YN, Bieniasz PD. 44.  2007. Reconstitution of an infectious human endogenous retrovirus. PLOS Pathog. 3:e10 [Google Scholar]
  45. Jha AR, Nixon DF, Rosenberg MG, Martin JN, Deeks SG. 45.  et al. 2011. Human endogenous retrovirus K106 (HERV-K106) was infectious after the emergence of anatomically modern humans. PLOS ONE 6:e20234 [Google Scholar]
  46. Belshaw R, Dawson ALA, Woolven-Allen J, Redding J, Burt A, Tristem M. 46.  2005. Genomewide screening reveals high levels of insertional polymorphism in the human endogenous retrovirus family HERV-K(HML2): implications for present-day activity. J. Virol. 79:12507–14 [Google Scholar]
  47. Hughes JF, Coffin JM. 47.  2004. Human endogenous retrovirus K solo-LTR formation and insertional polymorphisms: implications for human and viral evolution. PNAS 101:1668–72 [Google Scholar]
  48. Chessa B, Pereira F, Arnaud F, Amorim A, Goyache F. 48.  et al. 2009. Revealing the history of sheep domestication using retrovirus integrations. Science 324:532–36 [Google Scholar]
  49. Tarlinton RE, Meers J, Young PR. 49.  2006. Retroviral invasion of the koala genome. Nature 442:79–81 [Google Scholar]
  50. Ishida Y, Zhao K, Greenwood AD, Roca AL. 50.  2015. Proliferation of endogenous retroviruses in the early stages of a host germ line invasion. Mol. Biol. Evol. 32:109–20 [Google Scholar]
  51. Denner J, Young PR. 51.  2013. Koala retroviruses: characterization and impact on the life of koalas. Retrovirology 10:108 [Google Scholar]
  52. Ávila-Arcos MC, Ho SYW, Ishida Y, Nikolaidis N, Tsangaras K. 52.  et al. 2013. One hundred twenty years of koala retrovirus evolution determined from museum skins. Mol. Biol. Evol. 30:299–304 [Google Scholar]
  53. Schnieke A, Stuhlmann H, Harbers K, Chumakov I, Jaenisch R. 53.  1983. Endogenous Moloney leukemia virus in nonviremic Mov substrains of mice carries defects in the proviral genome. J. Virol. 45:505–13 [Google Scholar]
  54. Maksakova IA, Mager DL, Reiss D. 54.  2008. Keeping active endogenous retroviral-like elements in check: the epigenetic perspective. Cell. Mol. Life Sci. 65:3329–47 [Google Scholar]
  55. Benachenhou F, Jern P, Oja M, Sperber G, Blikstad V. 55.  et al. 2009. Evolutionary conservation of orthoretroviral long terminal repeats (LTRs) and ab initio detection of single LTRs in genomic data. PLOS ONE 4:e5179 [Google Scholar]
  56. Mitchell RS, Beitzel BF, Schroder ARW, Shinn P, Chen H. 56.  et al. 2004. Retroviral DNA integration: ASLV, HIV, and MLV show distinct target site preferences. PLOS Biol. 2:e234 [Google Scholar]
  57. Sverdlov ED. 57.  2000. Retroviruses and primate evolution. Bioessays 22:161–71 [Google Scholar]
  58. Dunn CA, van de Lagemaat LN, Baillie GJ, Mager DL. 58.  2005. Endogenous retrovirus long terminal repeats as ready-to-use mobile promoters: the case of primate β3GAL-T5. Gene 364:2–12 [Google Scholar]
  59. Stoye JP, Fenner S, Greenoak GE, Moran C, Coffin JM. 59.  1988. Role of endogenous retroviruses as mutagens: the hairless mutation of mice. Cell 54:383–91 [Google Scholar]
  60. Chang CM, Coville JL, Coquerelle G, Gourichon D, Oulmouden A, Tixier-Boichard M. 60.  2006. Complete association between a retroviral insertion in the tyrosinase gene and the recessive white mutation in chickens. BMC Genomics 7:19 [Google Scholar]
  61. Bacon LD, Smith E, Crittenden LB, Havenstein GB. 61.  1988. Association of the slow feathering (K) and an endogenous viral (ev21) gene on the Z chromosome of chickens. Poult. Sci. 67:191–97 [Google Scholar]
  62. Matsumine H, Herbst MA, Ou SH, Wilson JD, McPhaul MJ. 62.  1991. Aromatase mRNA in the extragonadal tissues of chickens with the henny-feathering trait is derived from a distinctive promoter structure that contains a segment of a retroviral long terminal repeat. Functional organization of the Sebright, Leghorn, and Campine aromatase genes. J. Biol. Chem. 266:19900–7 [Google Scholar]
  63. David VA, Menotti-Raymond M, Wallace AC, Roelke M, Kehler J. 63.  et al. 2014. Endogenous retrovirus insertion in the KIT oncogene determines White and White spotting in domestic cats. Genes Genomes Genet. 4:1881–91 [Google Scholar]
  64. Wragg D, Mwacharo JM, Alcalde JA, Wang C, Han JL. 64.  et al. 2013. Endogenous retrovirus EAV-HP linked to blue egg phenotype in Mapuche fowl. PLOS ONE 8:e71393 [Google Scholar]
  65. Wang Z, Qu L, Yao J, Yang X, Li G. 65.  et al. 2013. An EAV-HP insertion in 5′ flanking region of SLCO1B3 causes blue eggshell in the chicken. PLOS Genet. 9:e1003183 [Google Scholar]
  66. Hartl DL, Clark AG. 66.  2007. Principles of Population Genetics Sunderland, MA: Sinauer
  67. Gillespie JH. 67.  1991. The Causes of Molecular Evolution Oxford, UK: Oxford Univ. Press
  68. Gould SJ, Vrba E. 68.  1982. Exaptation—a missing term in the science of form. Paleobiology 8:4–15 [Google Scholar]
  69. Arnaud F, Caporale M, Varela M, Biek R, Chessa B. 69.  et al. 2007. A paradigm for virus-host coevolution: sequential counter-adaptations between endogenous and exogenous retroviruses. PLOS Pathog. 3:e170 [Google Scholar]
  70. Arnaud F, Varela M, Spencer TE, Palmarini M. 70.  2008. Endogenous retroviruses. Cell. Mol. Life Sci. 65:3422–32 [Google Scholar]
  71. Mura M, Murcia P, Caporale M, Spencer TE, Nagashima K. 71.  et al. 2004. Late viral interference induced by transdominant Gag of an endogenous retrovirus. PNAS 101:11117–22 [Google Scholar]
  72. Coffin JM. 72.  1992. Superantigens and endogenous retroviruses: a confluence of puzzles. Science 255:411–13 [Google Scholar]
  73. Wu T, Yan Y, Kozak CA. 73.  2005. Rmcf2, a xenotropic provirus in the Asian mouse species Mus castaneus, blocks infection by polytropic mouse gammaretroviruses. J. Virol. 79:9677–84 [Google Scholar]
  74. Jung YT, Lyu MS, Buckler-White A, Kozak CA. 74.  2002. Characterization of a polytropic murine leukemia virus proviral sequence associated with the virus resistance gene Rmcf of DBA/2 mice. J. Virol. 76:8218–24 [Google Scholar]
  75. Yan Y, Buckler-White A, Wollenberg K, Kozak CA. 75.  2009. Origin, antiviral function and evidence for positive selection of the gammaretrovirus restriction gene Fv1 in the genus Mus. PNAS 106:3259–63 [Google Scholar]
  76. Gardner MB, Kozak CA, O'Brien SJ. 76.  1991. The Lake Casitas wild mouse: evolving genetic resistance to retroviral disease. Trends Genet. 7:22–27 [Google Scholar]
  77. Dandekar S, Rossitto P, Pickett S, Mockli G, Bradshaw H. 77.  et al. 1987. Molecular characterization of the Akvr-1 restriction gene: a defective endogenous retrovirus-borne gene identical to Fv-4r. J. Virol. 61:308–14 [Google Scholar]
  78. Best S, Tissier PL, Towers G, Stoye JP. 78.  1996. Positional cloning of the mouse retrovirus restriction gene Fvl. Nature 382:826–29 [Google Scholar]
  79. Ito J, Watanabe S, Hiratsuka T, Kuse K, Odahara Y. 79.  et al. 2013. Refrex-1, a soluble restriction factor against feline endogenous and exogenous retroviruses. J. Virol. 87:12029–40 [Google Scholar]
  80. Cornelis G, Vernochet C, Carradec Q, Souquere S, Mulot B. 80.  et al. 2015. Retroviral envelope gene captures and syncytin exaptation for placentation in marsupials. PNAS 112:E487–96 [Google Scholar]
  81. Dupressoir A, Lavialle C, Heidmann T. 81.  2012. From ancestral infectious retroviruses to bona fide cellular genes: role of the captured syncytins in placentation. Placenta 33:663–71 [Google Scholar]
  82. Lavialle C, Cornelis G, Dupressoir A, Esnault C, Heidmann O. 82.  et al. 2013. Paleovirology of “syncytins,” retroviral env genes exapted for a role in placentation. Philos. Trans. R. Soc. B 368:20120507 [Google Scholar]
  83. Cohen CJ, Lock WM, Mager DL. 83.  2009. Endogenous retroviral LTRs as promoters for human genes: a critical assessment. Gene 448:105–14 [Google Scholar]
  84. Stoye JP. 84.  2012. Studies of endogenous retroviruses reveal a continuing evolutionary saga. Nat. Rev. Microbiol. 10:395–406 [Google Scholar]
  85. Feschotte C, Gilbert C. 85.  2012. Endogenous viruses: insights into viral evolution and impact on host biology. Nat. Rev. Genet. 13:283–96 [Google Scholar]
  86. Han GZ, Worobey M. 86.  2012. An endogenous foamy-like viral element in the coelacanth genome. PLOS Pathog. 8e1002790
  87. Lee A, Nolan A, Watson J, Tristem M. 87.  2013. Identification of an ancient endogenous retrovirus, predating the divergence of the placental mammals. Philos. Trans. R. Soc. B 368:20120503 [Google Scholar]
  88. Katzourakis A, Gifford RJ, Tristem M, Gilbert MTP, Pybus OG. 88.  2009. Macroevolution of complex retroviruses. Science 325:1512 [Google Scholar]
  89. Johnson WE, Coffin JM. 89.  1999. Constructing primate phylogenies from ancient retrovirus sequences. PNAS 96:10254–60 [Google Scholar]
  90. Bininda-Emonds ORP, Cardillo M, Jones KE, MacPhee RDE, Beck RMD. 90.  et al. 2007. The delayed rise of present-day mammals. Nature 446:507–12 [Google Scholar]
  91. Keckesova Z, Ylinen LMJ, Towers GJ, Gifford RJ, Katzourakis A. 91.  2009. Identification of a RELIK orthologue in the European hare (Lepus europaeus) reveals a minimum age of 12 million years for the lagomorph lentiviruses. Virology 384:7–11 [Google Scholar]
  92. Katzourakis A, Tristem M, Pybus OG, Gifford RJ. 92.  2007. Discovery and analysis of the first endogenous lentivirus. PNAS 104:6261–65 [Google Scholar]
  93. Telesnitsky A, Goff SP. 93.  1997. Reverse Transcriptase and the Generation of Retroviral DNA Cold Spring Harbor, NY: Cold Spring Harbor Lab. Press
  94. Dangel AW, Baker BJ, Mendoza AR, Yu CY. 94.  1995. Complement component C4 gene intron 9 as a phylogenetic marker for primates: long terminal repeats of the endogenous retrovirus ERV-K(C4) are a molecular clock of evolution. Immunogenetics 42:41–52 [Google Scholar]
  95. Martins H, Villesen P. 95.  2011. Improved integration time estimation of endogenous retroviruses with phylogenetic data. PLOS ONE 6:e14745 [Google Scholar]
  96. Hughes JF, Coffin JM. 96.  2005. Human endogenous retroviral elements as indicators of ectopic recombination events in the primate genome. Genetics 171:1183–94 [Google Scholar]
  97. Gifford RJ, Katzourakis A, Tristem M, Pybus OG, Winters M, Shafer RW. 97.  2008. A transitional endogenous lentivirus from the genome of a basal primate and implications for lentivirus evolution. PNAS 105:20362–67 [Google Scholar]
  98. Eizirik E, Murphy WJ, O'Brien SJ. 98.  2001. Molecular dating and biogeography of the early placental mammal radiation. J. Hered. 92:212–19 [Google Scholar]
  99. Gifford R, Kabat P, Martin J, Lynch C, Tristem M. 99.  2005. Evolution and distribution of Class II-related endogenous retroviruses. J. Virol. 79:6478–86 [Google Scholar]
  100. Xiong Y, Eickbush TH. 100.  1990. Origin and evolution of retroelements based upon their reverse transcriptase sequences. EMBO J. 9:3353–62 [Google Scholar]
  101. Jern P, Sperber GO, Blomberg J. 101.  2005. Use of endogenous retroviral sequences (ERVs) and structural markers for retroviral phylogenetic inference and taxonomy. Retrovirology 2:50 [Google Scholar]
  102. Bolisetty M, Blomberg J, Benachenhou F, Sperber G, Beemon K. 102.  2012. Unexpected diversity and expression of avian endogenous retroviruses. mBio 3:e00344–12 [Google Scholar]
  103. Brady T, Lee YN, Ronen K, Malani N, Berry CC. 103.  et al. 2009. Integration target site selection by a resurrected human endogenous retrovirus. Genes Dev. 23:633–42 [Google Scholar]
  104. Katzourakis A, Magiorkinis G, Lim AG, Gupta S, Belshaw R, Gifford R. 104.  2014. Larger mammalian body size leads to lower retroviral activity. PLOS Pathog. 10:e1004214 [Google Scholar]
  105. Bénit L, Dessen P, Heidmann T. 105.  2001. Identification, phylogeny, and evolution of retroviral elements based on their envelope genes. J. Virol. 75:11709–19 [Google Scholar]
  106. Henzy JE, Johnson WE. 106.  2013. Pushing the endogenous envelope. Philos. Trans. R. Soc. B 368:20120506 [Google Scholar]
  107. Henzy JE, Coffin JM. 107.  2013. Betaretroviral envelope subunits are noncovalently associated and restricted to the mammalian class. J. Virol. 87:1937–46 [Google Scholar]
  108. Henzy JE, Gifford RJ, Johnson WE, Coffin JM. 108.  2014. A novel recombinant retrovirus in the genomes of modern birds combines features of avian and mammalian retroviruses. J. Virol. 88:2398–405 [Google Scholar]
  109. Sonigo P, Barker C, Hunter E, Wain-Hobson S. 109.  1986. Nucleotide sequence of Mason-Pfizer monkey virus: an immunosuppressive D-type retrovirus. Cell 45:375–85 [Google Scholar]
  110. van der Kuyl AC, Mang R, Dekker JT, Goudsmit J. 110.  1997. Complete nucleotide sequence of simian endogenous type D retrovirus with intact genome organization: evidence for ancestry to simian retrovirus and baboon endogenous virus. J. Virol. 71:3666–76 [Google Scholar]
  111. Mang R, Goudsmit J, van der Kuyl AC. 111.  1999. Novel endogenous type C retrovirus in baboons: complete sequence, providing evidence for baboon endogenous virus gag-pol ancestry. J. Virol. 73:7021–26 [Google Scholar]
  112. van der Kuyl AC, Dekker JT, Goudsmit J. 112.  1999. Discovery of a new endogenous type C retrovirus (FcEV) in cats: evidence for RD-114 being an FcEV(Gag-Pol)/baboon endogenous virus BaEV(Env) recombinant. J. Virol. 73:7994–8002 [Google Scholar]
  113. Hayward JA, Tachedjian M, Cui J, Field H, Holmes EC. 113.  et al. 2013. Identification of diverse full-length endogenous betaretroviruses in megabats and microbats. Retrovirology 10:35 [Google Scholar]
  114. Denesvre C, Soubieux D, Pin G, Hue D, Dambrine G. 114.  2003. Interference between avian endogenous ev/J 4.1 and exogenous ALV-J retroviral envelopes. J. Gen. Virol. 84:3233–38 [Google Scholar]
  115. Huder JB, Böni J, Hatt JM, Soldati G, Lutz H, Schüpbach J. 115.  2002. Identification and characterization of two closely related unclassifiable endogenous retroviruses in pythons (Python molurus and Python curtus). J. Virol. 76:7607–15 [Google Scholar]
  116. Benson SJ, Ruis BL, Fadly AM, Conklin KF. 116.  1998. The unique envelope gene of the subgroup J avian leukosis virus derives from ev/J proviruses, a novel family of avian endogenous viruses. J. Virol. 72:10157–64 [Google Scholar]
  117. Gallaher WR. 117.  1996. Similar structural models of the transmembrane proteins of Ebola and avian sarcoma viruses. Cell 85:477–78 [Google Scholar]
  118. Stenglein MD, Sanders C, Kistler AL, Ruby JG, Franco JY. 118.  et al. 2012. Identification, characterization, and in vitro culture of highly divergent arenaviruses from boa constrictors and annulated tree boas: candidate etiological agents for snake inclusion body disease. mBio 3:e00180–12 [Google Scholar]
  119. Evans DT, Elder JH, Desrosiers RC. 119.  2013. Nonhuman lentiviruses. Fields Virology 2: DM Knipe, PM Howley 1584–612, 6th ed.. [Google Scholar]
  120. Apetrei C, Robertson DL, Marx PA. 120.  2004. The history of SIVS and AIDS: epidemiology, phylogeny and biology of isolates from naturally SIV infected non-human primates (NHP) in Africa. Front. Biosci. 9:225–54 [Google Scholar]
  121. Cui J, Holmes EC. 121.  2012. Endogenous lentiviruses in the ferret genome. J. Virol. 86:3383–85 [Google Scholar]
  122. Hron T, Fábryová H, Pačes J, Elleder D. 122.  2014. Endogenous lentivirus in Malayan colugo (Galeopterus variegatus), a close relative of primates. Retrovirology 11:84 [Google Scholar]
  123. Han GZ, Worobey M. 123.  2012. Endogenous lentiviral elements in the weasel family (Mustelidae). Mol. Biol. Evol. 29:2905–8 [Google Scholar]
  124. Gilbert C, Maxfield DG, Goodman SM, Feschotte C. 124.  2009. Parallel germline infiltration of a lentivirus in two Malagasy lemurs. PLOS Genet. 5:e1000425 [Google Scholar]
  125. van der Loo W, Abrantes J, Esteves PJ. 125.  2009. Sharing of endogenous lentiviral gene fragments among leporid lineages separated for more than 12 million years. J. Virol. 83:2386–88 [Google Scholar]
  126. Gifford RJ. 126.  2012. Viral evolution in deep time: lentiviruses and mammals. Trends Genet. 28:89–100 [Google Scholar]
  127. Basta HA, Cleveland SB, Clinton RA, Dimitrov AG, McClure MA. 127.  2009. Evolution of teleost fish retroviruses: characterization of new retroviruses with cellular genes. J. Virol. 83:10152–62 [Google Scholar]
  128. Chong AY, Kojima KK, Jurka J, Ray DA, Smit AFA. 128.  et al. 2014. Evolution and gene capture in ancient endogenous retroviruses—insights from the crocodilian genomes. Retrovirology 11:71 [Google Scholar]
  129. Löwer R, Tönjes RR, Korbmacher C, Kurth R, Löwer J. 129.  1995. Identification of a Rev-related protein by analysis of spliced transcripts of the human endogenous retroviruses HTDV/HERV-K. J. Virol. 69:141–49 [Google Scholar]
  130. McCarthy KR, Johnson WE. 130.  2014. Plastic proteins and monkey blocks: how lentiviruses evolved to replicate in the presence of primate restriction factors. PLOS Pathog. 10:e1004017 [Google Scholar]
  131. Meyerson NR, Sawyer SL. 131.  2011. Two-stepping through time: mammals and viruses. Trends Microbiol. 19:286–94 [Google Scholar]
  132. Goff S. 132.  2004. Retrovirus restriction factors. Mol. Cell 16:849–59 [Google Scholar]
  133. Neil S, Bieniasz P. 133.  2009. Human immunodeficiency virus, restriction factors, and interferon. J. Interferon Cytokine Res. 29:569–80 [Google Scholar]
  134. Kitamura Y, Ayukawa T, Ishikawa T, Kanda T, Yoshiike K. 134.  1996. Human endogenous retrovirus K10 encodes a functional integrase. J. Virol. 70:3302–6 [Google Scholar]
  135. Goldstone DC, Yap MW, Robertson LE, Haire LF, Taylor WR. 135.  et al. 2010. Structural and functional analysis of prehistoric lentiviruses uncovers an ancient molecular interface. Cell Host Microbe 8:248–59 [Google Scholar]
  136. Ganser-Pornillos BK, Yeager M, Sundquist WI. 136.  2008. The structural biology of HIV assembly. Curr. Opin. Struct. Biol. 18:203–17 [Google Scholar]
  137. Sokolskaja E, Luban J. 137.  2006. Cyclophilin, TRIM5, and innate immunity to HIV-1. Curr. Opin. Microbiol. 9:404–8 [Google Scholar]
  138. Dewannieux M, Harper F, Richaud A, Letzelter C, Ribet D. 138.  et al. 2006. Identification of an infectious progenitor for the multiple-copy HERV-K human endogenous retroelements. Genome Res. 16:1548–56 [Google Scholar]
  139. Rahm N, Yap M, Snoeck J, Zoete V, Muñoz M. 139.  et al. 2011. Unique spectrum of activity of prosimian TRIM5α against exogenous and endogenous retroviruses. J. Virol. 85:4173–83 [Google Scholar]
  140. Soll SJ, Neil SJD, Bieniasz PD. 140.  2010. Identification of a receptor for an extinct virus. PNAS 107:19496–501 [Google Scholar]
  141. Dewannieux M, Blaise S, Heidmann T. 141.  2005. Identification of a functional envelope protein from the HERV-K family of human endogenous retroviruses. J. Virol. 79:15573–77 [Google Scholar]
  142. Kaelber JT, Demogines A, Harbison CE, Allison AB, Goodman LB. 142.  et al. 2012. Evolutionary reconstructions of the transferrin receptor of Caniforms supports canine parvovirus being a re-emerged and not a novel pathogen in dogs. PLOS Pathog. 8:e1002666 [Google Scholar]
  143. Demogines A, Abraham J, Choe H, Farzan M, Sawyer SL. 143.  2013. Dual host-virus arms races shape an essential housekeeping protein. PLOS Biol. 11:e1001571 [Google Scholar]
  144. Magin C, Löwer R, Löwer J. 144.  1999. cORF and RcRE, the Rev/Rex and RRE/RxRE homologues of the human endogenous retrovirus family HTDV/HERV-K. J. Virol. 73:9496–507 [Google Scholar]
  145. Yang J, Bogerd HP, Peng S, Wiegand H, Truant R, Cullen BR. 145.  1999. An ancient family of human endogenous retroviruses encodes a functional homolog of the HIV-1 Rev protein. PNAS 96:13404–8 [Google Scholar]
  146. Boese A, Sauter M, Mueller-Lantzsch N. 146.  2000. A Rev-like NES mediates cytoplasmic localization of HERV-K cORF. FEBS Lett. 468:65–67 [Google Scholar]
  147. Hofacre A, Nitta T, Fan H. 147.  2009. Jaagsiekte sheep retrovirus encodes a regulatory factor, Rej, required for synthesis of Gag protein. J. Virol. 83:12483–98 [Google Scholar]
  148. Mertz JA, Simper MS, Lozano MM, Payne SM, Dudley JP. 148.  2005. Mouse mammary tumor virus encodes a self-regulatory RNA export protein and is a complex retrovirus. J. Virol. 79:14737–47 [Google Scholar]
  149. Johnson WE. 149.  2010. Endless forms most viral. PLOS Genet. 6:e1001210 [Google Scholar]
  150. Holmes EC. 150.  2011. The evolution of endogenous viral elements. Cell Host Microbe 10:368–77 [Google Scholar]
  151. Tristem M. 151.  2000. Identification and characterization of novel human endogenous retrovirus families by phylogenetic screening of the human genome mapping project database. J. Virol. 74:3715–30 [Google Scholar]
  152. Bénit L, Calteau A, Heidmann T. 152.  2003. Characterization of the low-copy HERV-Fc family: evidence for recent integrations in primates of elements with coding envelope genes. Virology 312:159–68 [Google Scholar]
  153. Stocking C, Kozak CA. 153.  2008. Murine endogenous retroviruses. Cell. Mol. Life Sci. 65:3383–98 [Google Scholar]
/content/journals/10.1146/annurev-virology-100114-054945
Loading
/content/journals/10.1146/annurev-virology-100114-054945
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