Abstract
Although genetic transfer between viruses and vertebrate hosts occurs less frequently than gene flow between bacteriophages and prokaryotes, it is extensive and has affected the evolution of both parties. With retroviruses, the integration of proviral DNA into chromosomal DNA can result in the activation of adjacent host gene expression and in the transduction of host transcripts into retroviral genomes as oncogenes. Yet in contrast to lysogenic phage, there is little evidence that viral oncogenes persist in a chain of natural transmission or that retroviral transduction is a significant driver of the horizontal spread of host genes. Conversely, integration of proviruses into the host germ line has generated endogenous retroviral genomes (ERV) in all vertebrate genomes sequenced to date. Some of these genomes retain potential infectivity and upon reactivation may transmit to other host species. During mammalian evolution, sequences of retroviral origin have been repurposed to serve host functions, such as the viral envelope glycoproteins crucial to the development of the placenta. Beyond retroviruses, DNA viruses with complex genomes have acquired numerous genes of host origin which influence replication, pathogenesis and immune evasion, while host species have accumulated germline sequences of both DNA and RNA viruses. A codicil is added on lateral transmission of cancer cells between hosts and on migration of host mitochondria into cancer cells.
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References
Aiewsakun P, Katzourakis A (2015) Endogenous viruses: connecting recent and ancient viral evolution. Virology 479–480:26–37. doi:10.1016/j.virol.2015.02.011
Alfano N, Michaux J, Morand S, Aplin K, Tsangaras K, Löber U, Fabre PH, Fitriana Y, Semiadi G, Ishida Y, Helgen KM, Roca AL, Eiden MV, Greenwood AD (2016) Endogenous gibbon ape leukemia virus identified in a rodent (Melomys burtoni subsp.) from Wallacea (Indonesia). J Virol 90:8169–8180. doi:10.1128/JVI.00723-16
Allen JF (2003) Why chloroplasts and mitochondria contain genomes. Comp Funct Genomics 4:31–36. doi:10.1002/cfg.245
Amariglio EN, Hakim I, Brok-Simoni F, Grossman Z, Katzir N, Harmelin A, Ramot B, Rechavi G (1991) Identity of rearranged LINE/c-MYC junction sequences specific for the canine transmissible venereal tumor. Proc Natl Acad Sci U S A 88:8136–8139
Aswad A, Katzourakis A (2014) The first endogenous herpesvirus, identified in the tarsier genome, and novel sequences from primate rhadinoviruses and lymphocryptoviruses. PLoS Genet 10:e1004332
Austin L, Hughes AL, Irausquin S, Friedman R (2010) The evolutionary biology of poxviruses. Infect Genet Evol 10:50. doi:10.1016/j.meegid.2009.10.001
Ávila-Arcos MC, Ho SY, Ishida Y, Nikolaidis N, Tsangaras K, Hönig 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
Babaian A, Mager DL (2016) Endogenous retroviral promoter exaptation in human cancer. Mob DNA 7:24. doi:10.1186/s13100-016-0080-x
Baltimore D (1970) RNA-dependent DNA polymerase of RNA tumour viruses. Nature 226:1209–1211
Banfield WG, Woke PA, Mackay CM, Cooper HL (1965) Mosquito transmission of a reticulum cell sarcoma of hamsters. Science 148:1239–1240
Baum DA, Baum B (2014) An inside-out origin for the eukaryotic cell. BMC Biol 12: 76. doi: 10.1186/s12915-014-0076-2
Bazot Q, Paschos K, Skalska L, Kalchschmidt JS, Parker GA, Allday MJ (2015) Epstein-Barr virus proteins EBNA3A and EBNA3C together induce expression of the oncogenic microRNA cluster miR-221/miR-222 and ablate expression of its target p57KIP2. PLoS Pathog 11:e1005031. doi:10.1371/journal.ppat.1005031
Belshaw R, Pereira V, Katzourakis A, Talbot G, Paces J, Burt A, Tristem M (2004) Long-term reinfection of the human genome by endogenous retroviruses. Proc Natl Acad Sci U S A 101:4894–4899
Belyi V, Levine AJ, Skalka AM (2010) Unexpected inheritance: multiple integrations of ancient bornavirus and ebolavirus/marburgvirus sequences in vertebrate genomes. PLoS Pathog 6:e1001030
Benveniste RE, Todaro GJ (1974) Evolution of C-type viral genes: inheritance of acquired viral genes. Nature 252:456–459
Benveniste RE, Callahan R, Sherr CJ, Chapman V, Todaro GJ (1977) Two distinct endogenous type C viruses isolated from the Asian rodent Mus cervicolor: conservation of virogene sequences in related rodent species. J Virol 21:849–862
Bergthorsson U, Adams KL, Thomason B, Palmer JD (2003) Widespread horizontal transfer of mitochondrial genes in flowering plants. Nature 424:197–201
Bister K (2015) Discovery of oncogenes: the advent of molecular cancer research. Proc Natl Acad Sci U S A. 112:15259–15260. doi:10.1073/pnas.1521145112
Blaise S, de Parseval N, Bénit Land Heidmann T (2003) Genome wide screening for fusogenic human endogenous retrovirus envelopes identifies syncytin 2, a gene conserved on primate evolution. Proc Natl Acad Sci U S A. 100:13013–13018
Blond JL, Lavillette D, Cheynet V, Bouton O, Oriol G, Chapel-Fernandes S, Mandrand B, Mallet F, Cosset FL (2000) An envelope glycoprotein of the human endogenous retrovirus HERV-W expressed in the human placenta and fuses cells expressing the D-type mammalian retrovirus receptor. J Virol 74:3321–3329
Bolin LL, Levy LS (2011) Viral determinants of FeLV infection and pathogenesis: lessons learned from analysis of a natural cohort. Viruses 3:1681–1698. doi:10.3390/v3091681
Bordet J, Ciuca MC (1922) Concerning the theories of the so-called ‘bacteriophage’. Br Med J 2:296
Boshoff C, Endo Y, Collins PD, Takeuchi Y, Reeves JD, Schweickart VL, Siani MA, Sasaki T, Williams TJ, Gray PW, Moore PS, Chang Y, Weiss RA (1997) Angiogenic and HIV-inhibitory functions of KSHV-encoded chemokines. Science 278:290–294
Boyd MT, Bax CMR, Bax BE, Bloxam DL, Weiss RA (1993) The human endogenous retrovirus ERV-3 is upregulated in differentiating placental trophoblast cells. Virology 196:905–909
Brugge JS, Erikson RL (1977) Identification of a transformation-specific antigen induced by by an avian sarcoma virus. Nature 269:346–348
Bugert JJ, Darai G (2000) Poxvirus homologues of cellular genes. Virus Genes 21:111–133
Burstein D, Amaro F, Zusman T, Lifshitz Z, Cohen O, Gilbert JA, Pupko T, Shuman HA, Segal G (2016) Genomic analysis of 38 Legionella species identifies large and diverse effector repertoires 48: 167–175. doi:10.1038/ng.3481
Cairns J, Stent GS, Watson JD (2007) Phage and the origins of molecular biology. Cold Spring Harbor Laboratory Press, New York
Canfield PJ, Sabine JM, Love DN (1988) Virus particles associated with leukaemia in a koala. Aust Vet J 65:327–328
Cavalieri F, Ruscio T, Tinoco R, Benedict S, Davis C, Vogt PK (1985) Isolation of three new avian sarcoma viruses: ASV 9, ASV 17, and ASV 25. Virology 143:680–683
Chang Y, Cesarman E, Pessin MS, Lee F, Culpepper J, Knowles DM, Moore PS (1994) Identification of herpesvirus-like DNA sequences in AIDS-associated Kaposi’s sarcoma. Science 265: 1865–1869
Choi IG, Kim SH (2007) Global extent of horizontal gene transfer. Proc Natl Acad Sci U S A 104:4489–4494. doi:10.1073/pnas.0611557104
Chuong EB, Elde NC, Feschotte C (2017) Regulatory activities of transposable elements: from conflicts to benefits. Nat Rev Genetics 18:71–86. doi:10.1038/nrg.2016.139
Cisek AA, Dabrowska I, Gregorczyk KP, Wyzewski Z (2017) Phage therapy in bacterial infections treatment: one hundred years after the discovery of bacteriophages. Curr Microbiol 74:277–283. doi:10.1007/s00284-016-1166-x
Cohen D (1985) The canine transmissible venereal tumor: a unique result of tumor progression. Adv Cancer Res 43:75–112
Colson P, La Scola B, Levasseur A, Caetano-Anollés G, Raoult D (2017) Mimivirus: leading the way in the discovery of giant viruses of amoebae. Nat Rev Microbiol 15:243–254. doi:10.1038/nrmicro.2016.197
Cornelis G, Vernochet C, Carradec Q, Souquere S, Mulot B, Catzeflis Nilsson MA, Menzies BR, Renfree MB, Pierron G, Zeller U, Heidmann O, Dupressoir A, Heidmann T (2015) Retroviral envelope gene captures and syncytin exaptation for placentation in marsupials. Proc Natl Acad Sci U S A. 112:E487–E496. doi:10.1073/pnas.1417000112
Cordaux R, Batzer MA (2009) The impact of retrotransposons on human genome evolution. Nat Rev Genet 10:691–703. doi:10.1038/nrg2640
Crawford LV, Crawford EM (1961) The properties of Rous sarcoma virus purified by density gradient centrifugation. Virology 13:227–232
Cunningham C, Gatherer D, Baluchova K, Dargan DJ, Thomson M, Griffiths PD, Wilkinson GWG, Schulz TF, Davison AJ (2010) Sequences of complete human cytomegalovirus genomes from infected cell cultures and clinical specimens. J Gen Virol 91:605–615. doi:10.1099/vir.0.015891-0
Daibata M, Taguchi T, Nemoto Y, Taguchi H, Miyoshi I (1999) Inheritance of chromosomally integrated human herpesvirus 6 DNA. Blood 94:1545–1549
Danoya A, Wang T, Keshavarz-Moore E, Fassati A, Chain BM (2013) Importin-7 mediates nuclear trafficking of DNA in mammalian cells. Traffic 14:165–175
Denner J (2016) Expression and function of endogenous retroviruses in the placenta. APMIS 124:31–43. doi:10.1111/apm.12474
d’Herelle F (1917) An invisible microbe that is antagonistic to the dysentery Bacillus. Compt Rend Acad Sci Paris 165:373–375
de Parseval N, Heidmann T (1998) Physiological knockout of the envelope gene of the single-copy ERV-3 human endogenous retrovirus in a fraction of the Caucasian population. J Virol 72:3442–3445
Duesberg PH, Vogt PK (1970) Differences between the ribonucleic acids of transforming and nontransforming avian tumor viruses. Proc Natl Acad Sci U S A 67:1673–1680
Dulbecco R (1952) Production of plaques in monolayer tissue cultures by single particles of an animal virus. Proc Natl Acad Sci U S A 38:747–752
Dunning Hotopp JC, Clark ME, Oliveira DC, Foster JM, Fischer P, Muñoz Torres MC, Giebel JD, Kumar N, Ishmael N, Wang S, Ingram J, Nene RV, Shepard J, Tomkins J, Richards S, Spiro DJ, Ghedin E, Slatko BE, Tettelin H, Werren JH (2007) Widespread lateral gene transfer from intracellular bacteria to multicellular eukaryotes. Science 317:1753–1756
Etienne L, Emerman M (2013) The mongoose, the pheasant, the pox, and the retrovirus. PLoS Biol 11:e1001641. doi:10.1371/journal.pbio.1001641
Farkašová H, Hron T, Pačes 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. 2017 Mar 9. pii: 201621224. doi:10.1073/pnas.1621224114
Feschotte C, Gilbert C (2012) Endogenous viruses: insights into viral evolution and impact on host biology. Nat Rev Genet 13:283–296. doi:10.1038/nrg3199
Fuchs NV, Loewer S, Daley GQ, Izsvák Z, Löwer J, Löwer R (2013) Human endogenous retrovirus K (HML-2) RNA and protein expression is a marker for human embryonic and induced pluripotent stem cells. Retrovirology 10:115. doi:10.1186/1742-4690-10-115
Gershoni M, Templeton AR, Mishmar D (2009) Mitochondrial bioenergetics as a major motive force of speciation. BioEssays 31:642–650. doi:10.1002/bies.200800139
Gilbert C, Feschotte C (2010) Genomic fossils calibrate the long-term evolution of hepadnaviruses. PLoS Biol 8:e1000495
Gomez-Valero L, Buchrieser C. (2013) Genome dynamics in Legionella: the basis of versatility and adaptation to intracellular replication. Cold Spring Harb Perspect Med 3: pii: a009993. doi:10.1101/cshperspect.a009993
Goodier JL (2016) Restricting retrotransposons: a review. Mobile. DNA 7:16. doi:10.1186/s13100-016-0070
Greaves MF, Maia AT, Wiemel JL, Ford AM (2003) Leukemia in twins: lessons in natural history. Blood 102:2321–2333
Griffiths D (2001) Endogenous retroviruses in the human genome sequence. Genome Biol 2: reviews 1017.1-reviews 1017.5
Grow EJ, Flynn RA, Chavez SL, Bayless NL, Wossidlo M, Wesche D, Martin L, Ware C, Blish CA, Chang HY, Reijo Pe RA, Wysocka J (2015) Intrinsic retroviral reactivation in human preimplantation embryos and pluripotent cells. Nature 522: 221–225. doi: 10.1038/nature14308
Guo YE, Steitz JA (2014) Virus meets host microRNA: the destroyer, the booster, the hijacker. Mol Cell Biol 34:3780–3787
Haig DM (2001) Subversion and piracy: DNA viruses and immune evasion. Res Vet Sci 70:205–219
Hanafusa H, Hanafusa T, Rubin H (1963) The defectiveness of Rous sarcoma virus. Proc Natl Acad Sci U S A 49:572–580
Hanger JJ, Bromham LD, McKee JJ, O’Brien TM, Robinson WF (2000) The nucleotide sequence of koala (Phascolarctos cinereus) retrovirus: a novel type C endogenous virus related to gibbon ape leukemia virus. J Virol 74:4264–4272
Hartmann G (2017) Nucleic Acid immunity. Adv Immunol 133:121–169. doi:10.1016/bs.ai.2016.11.001
Hayes HM, Biggar RJ, Pickle LW, Hoover R, Toft JD (1983) Canine transmissible venereal tumor: a model for Kaposi’s sarcoma? Am J Epidemiol 117:108–109
Hayward A, Cornwallis CK, Jern P (2015) Pan-vertebrate comparative genomics unmasks retrovirus macroevolution. Proc Natl Acad Sci U S A 112:464–469
Hayward WS, Neel BG, Astrin SM (1981) Activation of a cellular onc gene by promoter insertion ALV-induced lymphoid leukosis. Nature 290:475–480
Herniou EA, Huguet E, Thézé J, Bézier A, Periquet G, Drezen JM (2013) When parasitic wasps hijacked viruses: genomic and functional evolution of polydnaviruses. Philos Trans R Soc Lond B 368:20130051. doi:10.1098/rstb.2013.0051
Hertig C, Coupar BE, Gould AR, Boyle DB (1997) Field and vaccine strains of fowlpox virus carry integrated sequences from the avian retrovirus, reticuloendotheliosis virus. Virolgy 235:367–376
Hervé CA, Forrest G, Löwer R, Griffiths DJ, Venables PJ (2004) Conservation and loss of the ERV3 open reading frame in primates. Genomics 83:940–943
Hill JA, Ruth HallSedlak R, Magaret A, Huang ML, Zerr DM, Jerome KR, Boeckh M (2016) Efficient identification of inherited chromosomally integrated human herpesvirus 6 using specimen pooling. J Clin Virol 77:71–76
Holzerlandt R, Orengo C, Kellam P, Albà MM (2002) Identification of new herpesvirus gene homologs in the human genome. Genome Res 12:1739–1748. doi:10.1101/gr.334302
Honda T, Tomonaga K (2016) Endogenous non-retroviral RNA virus elements evidence a novel type of antiviral immunity. Mob Genet Elements 6:e1165785. doi:10.1080/2159256X.2016.1165785
Horie M, Honda T, Suzuki Y, Kobayashi Y, Daito T, Oshida T, Ikuta K, Jern P, Gojobori T, Coffin JM, Tomonaga K (2010) Endogenous non-retroviral RNA virus elements in mammalian genomes. Nature 463:84–87. doi:10.1038/nature08695
Horie M, Kobayashi Y, Suzuki Y, Tomonaga K (2013) Comprehensive analysis of endogenous bornavirus-like elements in eukaryote genomes. Phil Trans R Soc B 368:20120499. doi:10.1098/rstb.2012.0499
Hunter T, Sefton BM (1980) Transforming gene product of Rous sarcoma virus phoshorylates tyrosine. Proc Natl Acad Sci U S A 77:1311–1315
Imakawa K, Nakagawa S, Miyazawa T (2015) Baton pass hypothesis: successive incorporation of unconserved endogenous retroviral genes for placentation during mammalian evolution. Genes Cells 10:771–778
Isfort RJ, Jones D, Kost R, Witter R, Kung H-J (1992) Retrovirus insertion into herpesvirus in vitro and in vivo. Proc Natl Acad Sci U S A 89:991–995
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
Ishizaki R, Vogt PK (1966) Immunological relationships among envelope antigens of avian tumor viruses. Virology 30:375–387
Kassiotis G, Stoye JP (2017) Making a virtue of necessity: the pleiotropic role of human endogenous retroviruses in cancer. Phil Trans R Soc B (in press)
Katzir N, Rechavi G, Cohen JB, Unger T, Simoni F, Segal S, Cohen D, Givol D (1985) “Retroposon” insertion into the cellular oncogene c-myc in canine transmissible venereal tumor. Proc Natl Acad Sci U S A 82:1054–1058. doi:10.1073/pnas.82.4.1054
Kawakami TG, Huff SD, Buckley PM, Dungworth DL, Synder SP, Gilden RV (1972) C-type virus associated with gibbon lymphosarcoma. Nat New Biol 235:170–171
Kawakami TG, Sun l, McDowell TS (1978) Natural transmission of gibbon leukemia virus. J Natl Cancer Inst 61:1113–1115
Keogh EV (1938) Ectodermal lesions produced by the virus of Rous sarcoma. Brit J Exp Pathol 19:1–9
Klenerman P, Hengartner H, Zinkernagel RM (1997) A non-retroviral RNA virus persists in DNA form. Nature 390: 298–301
Krupovic M, Koonin EV (2017) Multiple origins of viral capsid proteins from cellular ancestors. Proc Natl Acad Sci U S A 114:E2401–E2410. doi:10.1073/pnas.1621061114
Lane N (2010) Life ascending: the ten great inventions of evolution. Profile Books, London
Lane N (2014) Bioenergetic constraints on the evolution of complex life. Cold Spring Harb Perspect Biol 6:a015982. doi:10.1101/cshperspect.a015982
Lane N (2015) The vital question: why is life the way it is?. Profile Books, London
Lavillette D, Marin M, Ruggieri A, Mallet F, Cosset FL, Kabat D (2002) The envelope glycoprotein of human endogenous retrovirus type W uses a divergent family of amino acid transporters/cell surface receptors. J Virol 76:6442–6652
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 368:20120507. doi:10.1098/rstb.2012.0507
Lee A, Nolan A, Watson J, Tristem M (2013) Identification of an ancient endogenous retrovirus, predating the divergence of the placental mammals. Philos Trans R Soc Lond B Biol Sci 368:20120503
Le Tissier P, Stoye JP, Takeuchi Y, Patience C, Weiss RA (1997) Two sets of human-tropic pig retrovirus. Nature 389:681–682
Levy JA (1978) Xenotropic type C viruses. Curr Top Microbiol Immunol 79:111–213
Lin L, B. Xua B, Rote NS (1999) Expression of endogenous retrovirus ERV-3 induces differentiation in BeWo, a choriocarcinoma model of human placental trophoblast. Placenta 20:109–118
Loenen WAM, Dryden DTF, Raleigh EA, Geoffrey GG, Murray NE (2014) Highlights of the DNA cutters: a short history of the restriction enzymes. Nucleic Acids Res 42(1):3–19. doi:10.1093/nar/gkt990
Lwoff A (1953) Lysogeny. Bacteriol Rev 17:269–337
Magiorkinis G, Belshaw R, Katzourakis A (2015) ‘There and back again’: revisiting the pathophysiological roles of human endogenous retroviruses in the post-genomic era. Phil Trans R Soc B 368:20120504
Maki Y, Bos TJ, Davis C, Starbuck M, Vogt PK (1987) Avian sarcoma virus 17 carries the jun oncogene. Proc Natl Acad Sci U S A 84:2848–2852
Malfavon-Borja R, Feschotte C (2015) Fighting fire with fire: Endogenous retrovirus envelopes as restriction factors. J Virol 89:4047–4050
Margulis L, Maniotis A, MacAllister J, Scythes BO, Hall J et al (2009) Spirochete round bodies, syphilis, Lyme disease & AIDS: resurgence of “the great imitator”? Symbiosis 47:51–58
Margulis L (2009) Genome acquisition in horizontal gene transfer: symbiogenesis and macromolecular sequence analysis. Methods Mol Biol 532:181–191. doi:10.1007/978-1-60327-853-9_10
Martin GS (1970) Rous sarcoma virus: a function required for the maintenance of the transformed state. Nature 227:1021–1023
Martin GS (2004) The road to Src. Oncogene 23:7910–7917
Martin WF (2011) Early evolution without a tree of life. Biol Direct 6:36
Martin WF, Garg S, Zimorski V (2015) Endosymbiotic theories for eukaryote origin. Phil Trans R Soc B 370:20140330. doi:10.1098/rstb.2014.0330
Metzger MJ Reinisch C, Sherry J, Goff SP (2015) Horizontal transmission of clonal cancer cells causes leukemia in soft-shell clams. Cell 161: 255–263
Metzger MJ, Villalba A, Carballal MJ, Iglesias D, Sherry J, Reinisch C, Muttray AF, Baldwin SA, Goff SP (2016) Widespread transmission of independent cancer lineages within multiple bivalve species. Nature 534:705–709
Mi S, Lee X, Li X, Veldman GM, Finnerty H, Racie L, LaVallie E, Tang XY, Edouard P, Howes S, Keith JC, McCoy JM (2000) Syncytin is a captive retroviral envelope protein involved in human placental morphogenesis. Nature 403:785–789
Miles BD, Robinson HL (1985) High-frequency transduction of c-erbB in avian leukosis virus-induced erythroblastosis. J Virol 54:295–303
Moyes D, Griffiths DJ, Venable PJ (2007) Insertional polymorphisms: a new lease of life for endogenous retroviruses in human disease. Trends Genet 23:326–333
Murchison EP, Schulz-Trieglaff OB, Ning Z, Alexandrov LB, Bauer MJ, Fu B, Hims M, Ding Z, Ivakhno S, Stewart C, Ng BL, Wong W, Aken B, White S, Alsop A, Becq J, Bignell GR, Cheetham RK, Cheng W, Connor TR, Cox AJ, Feng ZP, Gu Y, Grocock RJ, Harris SR, Khrebtukova I, Kingsbury Z, Kowarsky M, Kreiss A, Luo S, Marshall J, McBride DJ, Murray L, Pearse AM, Raine K, Rasolonjatovo I, Shaw R, Tedder P, Tregidgo C, Vilella AJ, Wedge DC, Woods GM, Gormley N, Humphray S, Schroth G, Smith G, Hall K, Searle SM, Carter NP, Papenfuss AT, Futreal PA, Campbell PJ, Yang F, Bentley DR, Evers DJ, Stratton MR (2012) Genome sequencing and analysis of the Tasmanian devil and its transmissible cancer. Cell 148:780–791
Murchison EP, Wedge DC, Alexandrov LB, Fu B, Martincorena I, Ning Z, Tubio JM, Werner EI, Allen J, De Nardi AB, Donelan EM, Marino G, Fassati A, Campbell PJ, Yang F, Burt A, Weiss RA, Stratton MR (2014) Transmissible dog cancer genome reveals the origin and history of an ancient cell lineage. Science 343:437–440
Murgia C, Pritchard KJ, Kim SK, Fassati A, Weiss RA (2006) Clonal origin and evolution of a transmissible cancer. Cell 126:477–487
Nalesnik MA, Woodle ES, DiMaio JM, Vasudev B, Teperman LW, Covington S, Taranto S, Gockerman JP, Shapiro R, Sharma V, Swinnen LJ, Yoshida A, Ison MG (2011) Donor-transmitted malignancies in organ transplantation: assessment of clinical risk. Amer J Transplant 11:1140–1147. doi:10.1111/j.1600-6143.2011.03565.x
Neil JC, Fulton R, Rigby M, Stewart M (1991) Feline leukemia virus: generation of pathogenic and oncogenic variants. Curr Top Microbiol Immunol 171:67–93
Niewiadomska AM, Gifford RJ (2013) The extraordinary evolutionary history of the reticuloendotheliosis viruses. PLoS Biol 11:e1001642
Novinski MA (1876) Zur Frage uber die Impfung der Krebsigen Geschwulste. Zentralbl Med Wissensch 14:790–791
Odom MR, Hendrickson RC, Lefkowitz EJ (2009) Poxvirus protein evolution: family wide assessment of possible horizontal gene transfer events. Virus Res 144:233–249. doi:10.1016/j.virusres.2009.05.006
Pasquier J, Guerrouahen BS, Al Thawadi H, Ghiabi P, Maleki M, Abu-Kaoud N, Jacob A, Mirshahi M, Galas L, Rafii S, Le Foll F, Rafii A (2013) Preferential transfer of mitochondria from endothelial to cancer cells through tunneling nanotubes modulates chemoresistance. J Transl Med 11:94. doi:10.1186/1479-5876-11-94
Patience C, Takeuchi Y, Weiss RA (1997) Infection of human cells by an endogenous retrovirus of pigs. Nat Medicine 3:282–286
Payne LN, Pani PK, Weiss RA (1971) A dominant epistatic gene which inhibits cellular susceptibility to RSV(RAV-O). J Gen Virol 13:455–462
PearseAM, Swift K (2006) Allograft theory: transmission of devil facial-tumour disease. Nature 439: 549
Pellett PE, Ablashi DV, Ambros PF, Agut H, Caserta MT, Descamps V, Flamand L, Gautheret-Dejean A, Hall CB, Kamble RT, Kuehl U, Lassner D, Lautenschlager I, Loomis KS, Luppi M, Lusso P, Medveczky PG, Montoya JG, Mori Y, Ogata M, Pritchett JC, Rogez S, Seto E, Ward KN, Yoshikawa T, Razonable RR Raymund R (2012) Chromosomally integrated human herpesvirus 6: questions and answers. Rev Med Virol 22:144–155
Ptashne M (2004) A genetic switch: phage lambda revisited, 3rd edn. Cold Harbor Spring Laboratory Press, New York. ISBN 978-0-87969-716-7
Pye RJ, Pemberton D, Tovar C, Tubio JM, Dun KA, Fox S, Darby J, Hayes D, Knowles GW, Kreiss A, Siddle HV, Swift K, Lyons AB, Murchison EP, Woods GM (2016) A second transmissible cancer in Tasmanian devils. Proc Natl Acad Sci U S A. 113(2):374–379. doi:10.1073/pnas.1519691113
Radzvilavicius AL, Hadjivasiliou Z, Pomiankowski A, Lane N (2016) Selection for mitochondrial quality drives evolution of the germline. PLoS Biol 14:e2000410. doi:10.1371/journal.pbio.2000410
Rebbeck CA, Leroi AM, Burt A (2011) Mitochondrial capture by a transmissible cancer. Science 331: 303
Rebollo R, Romanish MT, Mager DL (2012) Transposable elements: an abundant and natural source of regulatory sequences for host genes. Annu Rev Genet 46:21–42
Refardt D, Bergmiller T, Kümmerli R (2013) Altruism can evolve when relatedness is low: evidence from bacteria committing suicide upon phage infection. Proc R Soc B 280:20123035
Robbez-Masson L, Rowe HM (2015) Retrotransposons shape species-specific embryonic stem cell networks. Retrovirology 12:45. doi:10.1186/s12977-015-0173-5
Rohrschneider L, Reynolds S (1985) Regulation of cellular morphology by the Rous sarcoma virus src gene: analysis of fusiform mutants. Mol Cell Biol 5:3097–3107
Rosenberg N, Jolicoeur P (1997) Retroviral pathogenesis. In: Coffin JM, Hughes SH, Varmus HE (eds) Retroviruses. Cold Spring Harbor Laboratory Press, pp 475–585
Ross SR (2010) Mouse mammary tumor virus molecular biology and oncogenesis. Viruses 2:2000–2012
Rous P (1911) A sarcoma of the fowl transmissible by an agent separable from the tumor cells. J Exp Med 13: 397–411. doi:10.1084/jem.13.4.397
Rovnak J, Quackenbush SL (2010) Walleye dermal sarcoma virus: molecular biology and oncogenesis. Viruses 2:1984–1999
Roy SW, Gilbert W (2006). The evolution of spliceosomal introns: patterns, puzzles and progress. Nat Rev Genetics. 7: 211–221. doi:10.1038/nrg1807
Roy-Burman P (1995) Endogenous env elements: partners in generation of pathogenic feline leukemia viruses. Virus Genes 11:147–161
Rubin H, Vogt PK (1962) An avian leukosis virus associated with stocks of Rous sarcoma virus. Virology 17:184–194
Ruboyianes R, Worobey M (2016) Foamy-like endogenous retroviruses are extensive and abundant in teleosts. Virus Evol 2: vew032. doi: 10.1093/ve/vew03
Sagan L (1967) On the origin of mitosing cells. J Theoret Biol 14: 225–274. doi:10.1016/0022-5193(67)90079-3
Sankaran N (2014) When viruses were not in style: parallels in the histories of chicken sarcoma viruses and bacteriophages. Stud Hist Philos Biol Biomed Sci 48:189–199
Sanz-Ramos R, Stoye JP (2013) Capsid-binding retrovirus restriction factors: discovery, restriction specificity and implications for the development of novel therapeutics. J Gen Virol 94:2587–2598. doi:10.1099/vir.0.058180-0
Shimizu A, Nakatani Y, Nakamura T, Jinno-Oue A, Ishikawa O, Boeke JD, Takeuchi Y, Hoshino H (2014) Characterisation of cytoplasmic DNA complementary to non-retroviral RNA viruses in human cells. Sci Rep 4:5074. doi:10.1038/srep05074
Schlesinger S, Goff SP (2015) Retroviral transcriptional regulation and embryonic stem cells: war and peace. Mol Cell Biol 35:770–777
Shimode S, Nakagawa S, Miyazawa T (2015) Multiple invasions of an infectious retrovirus in cat genomes. Sci Rep 5:8164. doi:10.1038/srep08164
Shojima T, Yoshikawa R, Hoshino S, Shimode S, Nakagawa S, Ohata T, Nakaoka R, Miyazawa T (2013) Identification of a novel subgroup of koala retrovirus from koalas in Japanese zoos. J Virol 87:9943–9948
Siddle HV, Kaufman J (2015) Immunology of transmissible tumours. Immunology 144:11–20
Simmons G, Clarke D, McKe J, Young P, Meers J (2014) Discovery of a novel retrovirus sequence in an Australian native rodent (Melomys burtoni): a putative link between gibbon ape leukemia virus and koala retrovirus. PLoS ONE 9:e106954
Søe K, Andersen TL, Hobolt-Pedersen AS, Bjerregaard B, Larsson LI, Delaissé JM (2009) Involvement of human endogenous retroviral syncytin-1 in human osteoclast fusion. J Mol Biol 392:301–318
Stefan E, Bister K (2017) MYC and RAF: key effectors in cellular signaling and major drivers in human cancer. Curr Topics Microbiol Immunol (this Volume)
Stehelin D, Varmus HE, Bishop JM, Vogt PK (1976) DNA related to the transforming gene(s) of avian sarcoma viruses is present in normal avian DNA. Nature 260:170–173
Stern A, Sorek R (2011) The phage-host arms-race: shaping the evolution of microbes. BioEssays 33:43–51. doi:10.1002/bies.201000071
Stewart H, Jarrett O, Hosie MJ, Willett BJ (2011) Are endogenous feline leukemia viruses really endogenous? Vet Immunol Immunopathol 143:325–331
Stoye JP (2012) Studies of endogenous retroviruses reveal a continuing evolutionary saga. Nat Rev Microbiol 10:395–406
Strakova A, Ní Leathlobhair M, Wang GD, Yin TT, Airikkala-Otter I, Allen JL, Allum KM, Bansse-Issa L, Bisson JL, Castillo Domracheva A, de Castro KF, Corrigan AM, Cran HR, Crawford JT, Cutter SM, Delgadillo Keenan L, Donelan EM, Faramade IA, Flores Reynoso E, Fotopoulou E, Fruean SN, Gallardo-Arrieta F, Glebova O, Häfelin Manrique RF, Henriques JJ, Ignatenko N, Koenig D, Lanza-Perea M, Lobetti R, Lopez Quintana AM, Losfelt T, Marino G, Martincorena I, Martínez Castañeda S, Martínez-López MF, Meyer M, Nakanwagi B, De Nardi AB, Neunzig W, Nixon SJ, Onsare MM, Ortega-Pacheco A, Peleteiro MC, Pye RJ, Reece JF, Rojas Gutierrez J, Sadia H, Schmeling SK, Shamanova O, Ssuna RK, Steenland-Smit AE, Svitich A, Thoya Ngoka I, Vițălaru BA, de Vos AP, de Vos JP, Walkinton O, Wedge DC, Wehrle-Martinez AS, van der Wel MG, Widdowson SA, Murchison EP (2016) Mitochondrial genetic diversity, selection and recombination in a canine transmissible cancer. eLife 5: e14552. doi:10.7554/eLife.14552
Strand MR, Burke GR (2014) Polydnaviruses: nature’s genetic engineers. Annu Rev Virol 1:335–354. doi:10.1146/annurev-virology-031413-085451
Summers WC (1999) Felix d’Herelle and the origins of molecular biology. Yale University Press, New Haven
Svoboda J (1960) Presence of chicken tumour virus in the sarcoma of adult rat inoculated after birth with Rous sarcoma virus. Nature 186:980–981
Svoboda J (1966) Basic aspects of the interaction of oncogenic viruses with heterologous cells. Int Rev Exp Pathol 5:25–66
Tan AS, Baty JW, Dong LF, Bezawork-Geleta A, Endaya B, Goodwin J Bajzikova M, Kovarova J, Peterka M, Yan B, Pesdar EA, Sobol M, Filimonenko A, Stuart S, Vondrusova M, Kluckova K, Sachaphibulkij K, Rohlena J, Hozak P, Truksa J, Eccles D, Haupt LM, Griffiths LR, Neuzil J, Berridge MV (2015) Mitochondrial genome acquisition restores respiratory function and tumorigenic potential of cancer cells without mitochondrial DNA. Cell Metab 21:81–94
Tarlinton RE, Meers J, Young PR (2006) Retroviral invasion of the koala genome. Nature 442:79–81
Taylor DJ, Leach RW, Bruenn J (2010) Filoviruses are ancient and integrated into mammalian genomes. BMC Evol Biol 10:193. doi: 10.1186/1471-2148-10-193
Temin HM (1960) The control of cellular morphology on embryonic cells infected with Rous sarcoma virus in vitro. Virology 10:182–197
Temin HM (1962) Separation of morphological conversion and virus production in Rous sarcoma virus infection. Cold Spring Harb Symp Quant Biol 27:407–414
Temin HM (1964) Nature of the provirus of Rous sarcoma. Natl Cancer Inst Monog 17:557–570
Temin HM, Mizutani S (1970) RNA-dependent DNA polymerase in virions of Rous sarcoma virus. Nature 226:1211–1213
Temin HM, Rubin H (1958) Characteristics of an assay for Rous sarcoma virus and Rous sarcoma cells in tissue culture. Virology 6:669–688
Thielen GH, Goud D, Fowler M, Dungworth DL (1971) C-type virus in tumor tissue of a woolly monkey (Lagothrix spp) with fibrosarcoma. J Natl Cancer Inst 47:731–743
Ting CN, Rosenberg MP, Snow MP, Samuelson LC, Meisler MH (1992) Endogenous retroviral sequences are required for tissue-specific expression of a human salivary amylase gene. Genes Dev 6:1457–1465
Toyoshima K, Vogt PK (1969) Temperature sensitive mutants of an avian sarcoma virus. Virology 39:930–931
Twort FW (1915) An investigation on the nature of ultramicroscopic viruses. Lancet 2:1241–1243
Van Valen L (1973) A new evolutionary law. Evol Theor 1:1–30
Vargas A, Toufaily C, LeBellego F, Rassart É, Lafond J, Barbeau B (2011) Reduced expression of both syncytin 1 and syncytin 2 correlates with severity of preeclampsia. Reprod Sci 18:1085–1091
Varmus HE (2017) How tumor virology evolved into cancer biology and transformed oncology. Annu Rev Cancer Biol 1:11.1–11.18 doi:10.1146/annurev-cancerbio-050216-034315
Venables P, Brookes SM, Griffiths D, Weiss RA, Boyd MT (1995) Abundance of an endogenous retroviral envelope protein in placental trophoblasts suggests a biological function. Virology 211:589–592
Vendramin R, Marine JC, Leucci E (2017) Non-coding RNAs: the dark side of nuclear-mitochondrial communication. EMBO J pii: e201695546. doi:10.15252/embj.201695546
Vogt M, Dulbecco R (1960) Virus-cell interaction with a tumor-producing virus. Proc Natl Acad Sci U S A 46:365–370
Vogt PK (1967) A virus released by “nonproducing” Rous sarcoma cells. Proc Natl Acad Sci U S A 58:801–808
Vogt PK (2002) Fortuitous convergences: the beginnings of JUN. Nat Rev Cancer 2:465–469
Vogt PK (2012) Retroviral oncogenes: a historical primer. Nat Rev Cancer 12:639–648
Vogt PK, Hu SS (1977) The genetic structure of RNA tumor viruses. Annu Rev Genet 11:203–238
Vogt PK, Ishizaki R (1965) Reciprocal patterns of genetic resistance to avian tumor viruses in two lines of chickens. Virology 26:664–672
Volz A, Sutter G (2017) Modified Vaccinia Virus Ankara: history, value in basic research, and current perspectives for vaccine development. Adv Virus Res 97:187–243. doi:10.1016/bs.aivir.2016.07.001
Warren JM, Simmons MP, Wu Z, Sloan DB (2016) Linear plasmids and the rate of sequence evolution in plant mitochondrial genomes. Genome Biol Evol 8(2):364–374. doi:10.1093/gbe/evw003
Weiss RA (1967) Spontaneous virus production from “non-virus producing” Rous sarcoma cells. Virology 32:19–23
Weiss RA (2006) The discovery of endogenous retroviruses. Retrovirology 2006(3):67
Weiss RA, Esparza J (2015) The prevention and eradication of smallpox: a commentary on Sloane (1755) ‘An account of inoculation’. Philos Trans R Soc Lond B 370: pii: 20140378. doi:10.1098/rstb.2014.0378
Weiss RA, Kellam P (1997) Illicit viral DNA. Nature 390:235
Weiss RA, Vogt PK (2011) 100 years of Rous sarcoma virus. J Exp Med 208:2351–2355
Woese CR, Fox GE (1977) Phylogenetic structure of the prokaryotic domain: the primary kingdoms. Proc Natl Acad Sci U S A. 74:5088–5090
Xu W, Stadler CK, Gorman K, Jensen N, Kim D, Zheng H, Tang S, Switzer WM, Pye GW, Eiden MV (2013) An exogenous retrovirus isolated from koalas with malignant neoplasias in a US zoo. Proc Natl Acad Sci U S A 110:11547–11552. doi:10.1073/pnas.1304704110
Yenerall P, Zhou L (2012) Identifying the mechanisms of intron gain: progress and trends. Biol Direct 7:29. doi:10.1186/1745-6150-7-29
Zhdanov VM (1975) Integration of viral genomes. Nature 256:471–473
Acknowledgements
I am indebted to my mentors early in my career, Warren Levinson, Jan Svoboda and Peter K Vogt for providing a stimulating intellectual environment combined with a rigorous approach to experimental research. I am grateful to Klaus Bister, Ariberto Fassati and Paul Kellam for constructive discussions.
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Weiss, R.A. (2017). Exchange of Genetic Sequences Between Viruses and Hosts. In: Hunter, E., Bister, K. (eds) Viruses, Genes, and Cancer. Current Topics in Microbiology and Immunology, vol 407. Springer, Cham. https://doi.org/10.1007/82_2017_21
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