For best viewing of the website please use Mozilla Firefox or Google Chrome.
Citation: Jialu Zheng, Yutong Wei, Guan-Zhu Han. The diversity and evolution of retroviruses: Perspectives from viral “fossils” .VIROLOGICA SINICA, 2022, 37(1) : 11-18.

The diversity and evolution of retroviruses: Perspectives from viral “fossils”

  • Corresponding author: Guan-Zhu Han,
  • Received Date: 18 August 2021
    Accepted Date: 12 October 2021
    Available online: 19 January 2022
  • Retroviruses exclusively infect vertebrates, causing a variety of diseases. The replication of retroviruses requires reverse transcription and integration into host genomes. When infecting germline cells, retroviruses become inherited vertically, forming endogenous retroviruses (ERVs). ERVs document past viral infections, providing molecular fossils for studying the evolutionary history of retroviruses. In this review, we summarize the recent advances in understanding the diversity and evolution of retroviruses from the perspectives of viral fossils, and discuss the effects of ERVs on the evolution of host biology.

  • 加载中
    1. Aiewsakun P (2020) Avian and serpentine endogenous foamy viruses, and new insights into the macroevolutionary history of foamy viruses. Virus Evol 6:vez057.

    2. Aiewsakun P, Katzourakis A (2017) Marine origin of retroviruses in the early Palaeozoic Era. Nat Commun 8:13954.

    3. Aiewsakun P, Simmonds P, Katzourakis A (2019) The First Co-Opted Endogenous Foamy Viruses and the Evolutionary History of Reptilian Foamy Viruses. Viruses 11:641.

    4. Arnaud F, Caporale M, Varela M, Biek R, Chessa B, Alberti A, Golder M, Mura M, Zhang YP, Yu L, Pereira F, Demartini JC, Leymaster K, Spencer TE, Palmarini M (2007) A paradigm for virus-host coevolution: sequential counter-adaptations between endogenous and exogenous retroviruses. PLoS Pathog 3:e170.

    5. Aswad A, Katzourakis A (2012) Paleovirology and virally derived immunity. Trends Ecol Evol 27:627-636.

    6. Avila-Arcos MC, Ho SY, Ishida Y, Nikolaidis N, Tsangaras K, Honig K, Medina R, Rasmussen M, Fordyce SL, Calvignac-Spencer S, Willerslev E, Gilbert MT, Helgen KM, Roca AL, Greenwood AD (2013) One hundred twenty years of koala retrovirus evolution determined from museum skins. Mol Biol Evol 30:299-304.

    7. Bannert N, Kurth R (2006) The evolutionary dynamics of human endogenous retroviral families. Annu Rev Genomics Hum Genet 7:149-173.

    8. Belshaw R, Katzourakis A, Paces J, Burt A, Tristem M (2005) High copy number in human endogenous retrovirus families is associated with copying mechanisms in addition to reinfection. Mol Biol Evol 22:814-817.

    9. 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.

    10. Best S, Le Tissier P, Towers G, Stoye JP (1996) Positional cloning of the mouse retrovirus restriction gene Fv1. Nature 382:826-829.

    11. Bhardwaj N, Coffin JM (2014) Endogenous retroviruses and human cancer: is there anything to the rumors? Cell Host Microbe 15:255-259.

    12. Blaise S, de Parseval N, Benit L, Heidmann T (2003) Genomewide screening for fusogenic human endogenous retrovirus envelopes identifies syncytin 2, a gene conserved on primate evolution. Proc Natl Acad Sci USA 100:13013-13018.

    13. Blomberg J, Benachenhou F, Blikstad V, Sperber G, Mayer J (2009) Classification and nomenclature of endogenous retroviral sequences (ERVs): problems and recommendations. Gene 448:115-123.

    14. Boso G, Buckler-White A, Kozak CA. 2018. Ancient evolutionary origin and positive selection of the retroviral restriction factor Fv1 in muroid rodents. J Virol 92:e00850-18.

    15. Brady T, Lee YN, Ronen K, Malani N, Berry CC, Bieniasz PD, Bushman FD (2009) Integration target site selection by a resurrected human endogenous retrovirus. Genes Dev 23:633-642.

    16. Chen M, Guo X, Zhang L (2021b) Unexpected Discovery and Expression of Amphibian Class II Endogenous Retroviruses. J Virol 95:e01806-e01820.

    17. Chen Y, Wei X, Zhang G, Holmes EC, Cui J (2019) Identification and evolution of avian endogenous foamy viruses. Virus Evol 5:vez049.

    18. Chen Y, Zhang YY, Wei X, Cui J (2021a) Multiple Infiltration and Cross-Species Transmission of Foamy Viruses across the Paleozoic to the Cenozoic Era. J Virol 95:e0048421.

    19. Chuong EB, Elde NC, Feschotte C (2016) Regulatory evolution of innate immunity through co-option of endogenous retroviruses. Science 351:1083-1087.

    20. Chuong EB, Elde NC, Feschotte C (2017) Regulatory activities of trans- posable elements: from conflicts to benefits. Nat Rev Genet 18:71-86.

    21. Coffin JM, Hughes SH, Varmus HE (1997) The Interactions of Retroviruses and their Hosts. In: Coffin JM, Hughes SH, Varmus HE, editors. Retroviruses. Cold Spring Harbor (NY): Cold Spring Harbor Laboratory Press.

    22. Cornelis G, Funk M, Vernochet C, Leal F, Tarazona OA, Meurice G, Heidmann O, Dupressoir A, Miralles A, Ramirez-Pinilla MP, Heidmann T (2017) An endogenous retroviral envelope syncytin and its cognate receptor identified in the viviparous placental Mabuya lizard. Proc Natl Acad Sci U S A 114:E10991-E11000.

    23. Cui J, Holmes EC (2012) Endogenous lentiviruses in the ferret genome. J Virol 86:3383-3385.

    24. Duffy S, Shackelton LA, Holmes EC (2008) Rates of evolutionary change in viruses: patterns and determinants. Nat Rev Genet 9:267-276.

    25. Dupressoir A, Marceau G, Vernochet C, Benit L, Kanellopoulos C, Sapin V, Heidmann T (2005) Syncytin-A and syncytin-B, two fusogenic placenta-specific murine envelope genes of retroviral origin conserved in Muridae. Proc Natl Acad Sci USA 102:725-730.

    26. Emerman M, Malik HS (2010) Paleovirology--modern consequences of ancient viruses. PLoS Biol 8:e1000301.

    27. Farkasova H, Hron T, Paces J, Hulva P, Benda P, Gifford RJ, Elleder D (2017) Discovery of an endogenous Deltaretrovirus in the genome of long-fingered bats (Chiroptera: Miniopteridae). Proc Natl Acad Sci U S A 114:3145-3150.

    28. Feschotte C (2008) Transposable elements and the evolution of regulatory networks. Nat Rev Genet 9:397-405.

    29. Feschotte C, Gilbert C (2012) Endogenous viruses: insights into viral evolution and impact on host biology. Nat Rev Genet 13:283-296.

    30. Finnegan DJ (2012) Retrotransposons. Curr Biol 22: R432-R437.

    31. Frank JA, Feschotte C (2017) Co-option of endogenous viral sequences for host cell function. Curr Opin Virol 25:81-89.

    32. Gago S, Elena SF, Flores R, Sanjuan R (2009) Extremely high mutation rate of a hammerhead viroid. Science 323:1308.

    33. Gifford R, Tristem M (2003) The evolution, distribution and diversity of endogenous retroviruses. Virus Genes 26:291-315.

    34. Gifford RJ, Blomberg J, Coffin JM, Fan H, Heidmann T, Mayer J, Stoye J, Tristem M, Johnson WE (2018) Nomenclature for endogenous retrovirus (ERV) loci. Retrovirology 15:59.

    35. Gifford RJ, Katzourakis A, Tristem M, Pybus OG, Winters M, Shafer RW (2008) A transitional endogenous lentivirus from the genome of a basal primate and implications for lentivirus evolution. Proc Natl Acad Sci USA 105:20362-20367.

    36. Gilbert C, Maxfield DG, Goodman SM, Feschotte C (2009) Parallel germline infiltration of a lentivirus in two Malagasy lemurs. PLoS Genet 5:e1000425.

    37. Goff SP (2007) Host factors exploited by retroviruses. Nat Rev Microbiol 5:253-263.

    38. Han GZ, Worobey M (2012a) An endogenous foamy-like viral element in the coelacanth genome. PLoS Pathog 8:e1002790.

    39. Han GZ, Worobey M (2012b) Endogenous lentiviral elements in the weasel family (Mustelidae). Mol Biol Evol 29:2905-2908.

    40. Han GZ, Worobey M (2012c) An endogenous foamy virus in the aye-aye (Daubentonia madagascariensis). J Virol 86:7696-7698.

    41. Han GZ, Worobey M (2014) Endogenous viral sequences from the Cape golden mole (Chrysochloris asiatica) reveal the presence of foamy viruses in all major placental mammal clades. PLoS One 9:e97931.

    42. Han GZ, Worobey M (2015) A primitive endogenous lentivirus in a colugo: insights into the early evolution of lentiviruses. Mol Biol Evol 32:211-215.

    43. Hartl D, Clark A (2006) Principles of Population Genetics. Sinauer Associates.

    44. Hayward A (2017) Origin of the retroviruses: when, where, and how? Curr Opin Virol 25:23-27.

    45. Hayward A, Cornwallis CK, Jern P (2015) Pan-vertebrate comparative genomics unmasks retrovirus macroevolution. Proc Natl Acad Sci U S A 112:464-469.

    46. Hayward A, Grabherr M, Jern P (2013) Broad-scale phylogenomics provides insights into retrovirus-host evolution. Proc Natl Acad Sci U S A 110:20146-20151.

    47. Hendrickson RC, Orton RJ, Siddell SG, Smith DB (2018) Virus taxonomy: the database of the International Committee on Taxonomy of Viruses (ICTV). Nucleic Acids Res 46:D708-D717.

    48. Holmes EC (2011) The evolution of endogenous viral elements. Cell Host Microbe 10:368-377.

    49. Hron T, Farkasova H, Gifford RJ, Benda P, Hulva P, Gorfol T, Paces J, Elleder D (2018) Remnants of an Ancient Deltaretrovirus in the Genomes of Horseshoe Bats (Rhinolophidae). Viruses 10:185.

    50. Hron T, Farkasova H, Padhi A, Paces J, Elleder D (2016) Life History of the Oldest Lentivirus: Characterization of ELVgv Integrations in the Dermopteran Genome. Mol Biol Evol 33:2659-2669.

    51. Hughes DC (2001) Alternative splicing of the human VEGFGR-3/FLT4 gene as a consequence of an integrated human endogenous retrovirus. Journal of Molecular Evolution 53:77-79.

    52. Ishida Y, Zhao K, Greenwood AD, Roca AL (2015) Proliferation of endogenous retroviruses in the early stages of a host germ line invasion. Mol Biol Evol 32:109-120.

    53. Jern P, Coffin JM (2008) Effects of retroviruses on host genome function. Annu Rev Genet 42:709-732.

    54. Johnson WE (2015) Endogenous retroviruses in the genomics era. Annu Rev Virol 2:135-159.

    55. Johnson WE, Coffin JM (1999) Constructing primate phylogenies from ancient retrovirus sequences. Proc Natl Acad Sci U S A 96:10254-10260.

    56. Katzourakis A (2013) Paleovirology: inferring viral evolution from host genome sequence data. Philos Trans R Soc Lond B Biol Sci 368:20120493.

    57. Katzourakis A, Aiewsakun P, Jia H, Wolfe ND, LeBreton M, Yoder AD, Switzer WM (2014) Discovery of prosimian and afrotherian foamy viruses and potential cross species transmissions amidst stable and ancient mammalian co-evolution. Retrovirology 11:61.

    58. Katzourakis A, Tristem M, Pybus OG, Gifford RJ (2007) Discovery and analysis of the first endogenous lentivirus. Proc Natl Acad Sci USA 104:6261-6265.

    59. Keckesova Z, Ylinen LM, Towers GJ, Gifford RJ, Katzourakis A (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.

    60. Kozak CA, Gromet NJ, Ikeda H, Buckler CE (1984) A unique sequence related to the ecotropic murine leukemia virus is associated with the Fv-4 resistance gene. Proc Natl Acad Sci U S A 81:834-837.

    61. Kury P, Nath A, Creange A, Dolei A, Marche P, Gold J, Giovannoni G, Hartung HP, Perron H (2018) Human Endogenous Retroviruses in Neurological Diseases. Trends Mol Med 24:379-394.

    62. Lavialle C, Cornelis G, Dupressoir A, Esnault C, Heidmann O, Vernochet C, Heidmann T (2013) Paleovirology of ‘syncytins’, retroviral env genes exapted for a role in placentation. Philos Trans R Soc Lond B Biol Sci 368:20120507.

    63. Lee A, Huntley D, Aiewsakun P, Kanda RK, Lynn C, Tristem M (2014) Novel denisovan and neanderthal retroviruses. J Virol 88:12907-12909.

    64. Lima-Junior DS, Krishnamurthy SR, Bouladoux N, Collins N, Han SJ, Chen EY, Constantinides MG, Link VM, Lim AI, Enamorado M, Cataisson C, Gil L, Rao I, Farley TK, Koroleva G, Attig J, Yuspa SH, Fischbach MA, Kassiotis G, Belkaid Y (2021) Endogenous retroviruses promote homeostatic and inflammatory responses to the microbiota. Cell 184:3794-3811.

    65. Magiorkinis G, Gifford RJ, Katzourakis A, De Ranter J, Belshaw R (2012) Env-less endogenous retroviruses are genomic superspreaders. Proc Natl Acad Sci U S A 109:7385-7390.

    66. Martins H, Villesen P (2011) Improved integration time estimation of endogenous retroviruses with phylogenetic data. PLoS One 6:e14745.

    67. McDougall AS, Terry A, Tzavaras T, Cheney C, Rojko J, Neil JC (1994) Defective endogenous proviruses are expressed in feline lymphoid cells: evidence for a role in natural resistance to subgroup B feline leukemia viruses. J Virol 68:2151-2160.

    68. Mi S, Lee X, Li X, Veldman GM, Finnerty H, Racie L, LaVallie E, Tang XY, Edouard P, Howes S, Keith JC Jr, McCoy JM (2000) Syncytin is a captive retroviral envelope protein involved in human placenta morphogenesis. Nature 403:785-789.

    69. Mura M, Murcia P, Caporale M, Spencer TE, Nagashima K, Rein A, Palmarini M (2004) Late viral interference induced by transdominant Gag of an endogenous retrovirus. Proc Natl Acad Sci U S A 101:11117-11122.

    70. Ngo MH, Arnal M, Sumi R, Kawasaki J, Miyake A, Grant CK, Otoi T, Fernandez de Luco D, Nishigaki K (2019) Tracking the Fate of Endogenous Retrovirus Segregation in Wild and Domestic Cats. J Virol 93:e01324-19.

    71. Palmarini M, Mura M, Spencer TE (2004) Endogenous betaretroviruses of sheep: teaching new lessons in retroviral interference and adaptation. J Gen Virol 85:1-13.

    72. Pasquesi GIM, Perry BW, Vandewege MW, Ruggiero RP, Schield DR, Castoe TA (2020) Vertebrate Lineages Exhibit Diverse Patterns of Transposable Element Regulation and Expression across Tissues. Genome Biol Evol 12:506-521.

    73. Polani S, Roca AL, Rosensteel BB, Kolokotronis SO, Bar-Gal GK (2010) Evolutionary dynamics of endogenous feline leukemia virus proliferation among species of the domestic cat lineage. Virology 405:397-407.

    74. Redelsperger F, Raddi N, Bacquin A, Vernochet C, Mariot V, Gache V, Blanchard-Gutton N, Charrin S, Tiret L, Dumonceaux J, Dupressoir A, Heidmann T (2016) Genetic Evidence That Captured Retroviral Envelope syncytins Contribute to Myoblast Fusion and Muscle Sexual Dimorphism in Mice. PLoS Genet 12:e1006289.

    75. Repaske R, Steele PE, O’Neill RR, Rabson AB, Martin MA (1985) Nucleotide sequence of a full-length human endogenous retroviral segment. J Virol 54:764-772.

    76. Roca AL, Pecon-Slattery J, O'Brien SJ (2004) Genomically intact endogenous feline leukemia viruses of recent origin. J Virol 78: 4370-4375.

    77. Ruboyianes R, Worobey M (2016) Foamy-like endogenous retroviruses are extensive and abundant in teleosts. Virus Evol 2:vew032.

    78. Sexton CE, Tillett RL, Han MV (2021) The essential but enigmatic regulatory role of HERVH in pluripotency. Trends Genet S0168-9525(21)00197-00199.

    79. Song Y, Li X, Wei X, Cui J (2021) Human Endogenous Retroviruses as Biomedicine Markers. Virol Sin doi: 10.1007/s12250-021-00387-7.

    80. Sperber GO, Airola T, Jern P, Blomberg J (2007) Automated recognition of retroviral sequences in genomic data--RetroTector. Nucleic Acids Res 35:4964-4976.

    81. Stoye JP (2001) Endogenous retroviruses: still active after all these years? Curr Biol 11:R914-R916.

    82. Stoye JP (2012) Studies of endogenous retroviruses reveal a continuing evolutionary saga. Nat Rev Microbiol 10:395-406.

    83. Sun MA, Wolf G, Wang Y, Senft AD, Ralls S, Jin J, Dunn-Fletcher CE, Muglia LJ, Macfarlan TS (2021) Endogenous retroviruses drive lineage-specific regulatory evolution across primate and rodent placentae. Mol Biol Evol doi: 10.1093/molbev/msab223.

    84. Tarlinton RE, Meers J, Young PR (2006) Retroviral invasion of the koala genome. Nature 442:79-81.

    85. Telesnitsky A (2010) Retroviruses: Molecular Biology, Genomics and Pathogenesis. Future Virol 5:539-543.

    86. Tikhonenko AT, Lomovskaya OL (1990) Avian endogenous provirus (ev-3) env gene sequencing: implication for pathogenic retrovirus origination. Virus Genes 3:251-258.

    87. Tristem M, Herniou E, Summers K, Cook J (1996) Three retroviral sequences in amphibians are distinct from those in mammals and birds. J Virol 70:4864-4870.

    88. Tristem M, Myles T, Hill F (1995) A highly divergent retroviral sequence in the tuatara (Sphenodon). Virology 210:206-211.

    89. Turner G, Barbulescu M, Su M, Jensen-Seaman MI, Kidd KK, Lenz J (2001) Insertional polymorphisms of full-length endogenous retroviruses in humans. Curr Biol 11:1531-1535.

    90. Van Dooren S, Salemi M, Vandamme AM (2001) Dating the origin of the African human T-cell lymphotropic virus type-i (HTLV-I) subtypes. Mol Biol Evol 18:661-671.

    91. Voisset C, Weiss RA, Griffiths DJ. (2008). Human RNA “rumor” viruses: the search for novel human retroviruses in chronic disease. Microbiol Mol Biol Rev 72:157-196.

    92. Wang J, Han GZ (2020) Frequent Retroviral Gene Co-option during the Evolution of Vertebrates. Mol Biol Evol 37:3232-3242.

    93. Wang J, Han GZ (2021a) A Sister Lineage of Sampled Retroviruses Corroborates the Complex Evolution of Retroviruses. Mol Biol Evol 38:1031-1039.

    94. Wang J, Han GZ (2021b) Unearthing LTR Retrotransposon gag Genes Co-opted in the Deep Evolution of Eukaryotes. Mol Biol Evol 38:3267-3278.

    95. Wei X, Chen Y, Duan G, Holmes EC, Cui J (2019) A reptilian endogenous foamy virus sheds light on the early evolution of retroviruses. Virus Evol 5:vez001.

    96. Weiss RA (2013) On the concept and elucidation of endogenous retroviruses. Philosophical Transactions of the Royal Society B: Biological Sciences 368:20120494.

    97. Wertheim JO, Worobey M (2009) Dating the age of the SIV lineages that gave rise to HIV-1 and HIV-2. PLoS Comput Biol 5:e1000377.

    98. Wildschutte JH, Williams ZH, Montesion M, Subramanian RP, Kidd JM, Coffin JM (2016) Discovery of unfixed endogenous retrovirus insertions in diverse human populations. Proc Natl Acad Sci U S A 113:E2326-E2334.

    99. Xu X, Zhao H, Gong Z, Han GZ (2018) Endogenous retroviruses of non-avian/mammalian vertebrates illuminate diversity and deep history of retroviruses. PLoS Pathog 14:e1007072.

    100. Yan Y, Buckler-White A, Wollenberg K, Kozak CA (2009) Origin, antiviral function and evidence for positive selection of the gammaretrovirus restriction gene Fv1 in the genus Mus. Proc Natl Acad Sci U S A 106:3259-3263.

    101. Yap MW, Colbeck E, Ellis SA, Stoye JP (2014) Evolution of the Retroviral Restriction Gene Fv1: Inhibition of Non-MLV Retroviruses. PLoS Pathog 10:e1003968.

    102. Young GR, Yap MW, Michaux JR, Steppan SJ, Stoye JP. 2018. Evolutionary journey of the retroviral restriction gene Fv1. Proc Natl Acad Sci U S A 115:10130-10135.

    103. Zhang Y, Maksakova IA, Gagnier L, van de Lagemaat LN, Mager DL (2008) Genome-wide assessments reveal extremely high levels of polymorphism of two active families of mouse endogenous retroviral elements. PLoS Genet 4:e1000007.

    104. Zheng J, Wang J, Gong Z, Han GZ (2021) Molecular fossils illuminate the evolution of retroviruses following a macroevolutionary transition from land to water. PLoS Pathog 17:e1009730.

    105. Zhou B, Qi F, Wu F, Nie H, Song Y, Shao L, Han J, Wu Z, Saiyin H, Wei G, Wang P, Ni T, Qian F (2019) Endogenous Retrovirus-Derived Long Noncoding RNA Enhances Innate Immune Responses via Derepressing RELA Expression. mBio 10:e00937-19

  • 加载中

Article Metrics

Article views(2693) PDF downloads(17) Cited by()

Proportional views

    The diversity and evolution of retroviruses: Perspectives from viral “fossils”

      Corresponding author: Guan-Zhu Han,
    • Jiangsu Key Laboratory for Microbes and Functional Genomics, College of Life Sciences, Nanjing Normal University, Nanjing, 210023, China

    Abstract: Retroviruses exclusively infect vertebrates, causing a variety of diseases. The replication of retroviruses requires reverse transcription and integration into host genomes. When infecting germline cells, retroviruses become inherited vertically, forming endogenous retroviruses (ERVs). ERVs document past viral infections, providing molecular fossils for studying the evolutionary history of retroviruses. In this review, we summarize the recent advances in understanding the diversity and evolution of retroviruses from the perspectives of viral fossils, and discuss the effects of ERVs on the evolution of host biology.

    Reference (105) Relative (20)



    DownLoad:  Full-Size Img  PowerPoint