Skip to main content
SpringerLink
Log in

The Evolutionary Interplay Between Exogenous and Endogenous Sheep Betaretroviruses

  • Chapter
  • First Online:
Book cover Viruses: Essential Agents of Life

  • 2849 Accesses

Abstract

Sheep betaretroviruses represent an interesting model to study the ­complex evolutionary interplay between host and pathogen in natural settings. In infected sheep, the exogenous and pathogenic Jaagsiekte sheep retrovirus (JSRV) coexists with at least 27 highly related endogenous JSRVs (enJSRVs). During evolution, some enJSRVs were co-opted by the host as they fulfilled important biological functions, including protection against infections by related exogenous retroviruses as well as conceptus development and placental morphogenesis. In particular, recent studies demonstrate that transdominant enJSRVs (i.e., those that are able to block JSRV replication) were positively selected during sheep domestication. Interestingly, viruses escaping these loci have recently emerged (less than 200 years ago). Overall, these findings suggest that the process of endogenization is still ongoing in sheep and, therefore, the evolutionary interplay between endogenous and exogenous sheep betaretroviruses and their hosts has not reached equilibrium.

This is a preview of subscription content, log in via an institution to check access.

Access this chapter

Log in via an institution
Chapter
USD 29.95
Price excludes VAT (USA)
  • Available as PDF
  • Read on any device
  • Instant download
  • Own it forever
eBook
USD 129.00
Price excludes VAT (USA)
  • Available as EPUB and PDF
  • Read on any device
  • Instant download
  • Own it forever
Softcover Book
USD 169.00
Price excludes VAT (USA)
  • Compact, lightweight edition
  • Dispatched in 3 to 5 business days
  • Free shipping worldwide - see info
Hardcover Book
USD 169.99
Price excludes VAT (USA)
  • Durable hardcover edition
  • Dispatched in 3 to 5 business days
  • Free shipping worldwide - see info

Tax calculation will be finalised at checkout

Purchases are for personal use only

Institutional subscriptions

References

  • Alberti A, Murgia C, Liu SL, Mura M, Cousens C, Sharp M, Miller AD, Palmarini M (2002) Envelope-induced cell transformation by ovine betaretroviruses. J Virol 76:5387–5394

    Article  PubMed  CAS  Google Scholar 

  • Armezzani A, Arnaud F, Caporale M, di Meo G, Iannuzzi L, Murgia C, Palmarini M (2011) The signal peptide of a recently integrated endogenous sheep betaretrovirus envelope plays a major role in eluding gag-mediated late restriction. J Virol 85:7118–7128

    Article  PubMed  CAS  Google Scholar 

  • 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 (2007a) A paradigm for virus-host coevolution: sequential counter-adaptations between endogenous and exogenous retroviruses. PLoS Pathog 3:e170

    Article  PubMed  Google Scholar 

  • Arnaud F, Murcia PR, Palmarini M (2007b) Mechanisms of late restriction induced by an endogenous retrovirus. J Virol 81:11441–11451

    Article  PubMed  CAS  Google Scholar 

  • Arnaud F, Black SG, Murphy L, Griffiths DJ, Neil SJ, Spencer TE, Palmarini M (2010) Interplay between ovine bone marrow stromal cell antigen 2/tetherin and endogenous retroviruses. J Virol 84:4415–4425

    Article  PubMed  CAS  Google Scholar 

  • Bazer FW, Burghardt RC, Johnson GA, Spencer TE, Wu G (2008) Interferons and progesterone for establishment and maintenance of pregnancy: interactions among novel cell signaling ­pathways. Reprod Biol 8:179–211

    PubMed  Google Scholar 

  • Black SG, Arnaud F, Burghardt RC, Satterfield MC, Fleming JA, Long CR, Hanna C, Murphy L, Biek R, Palmarini M, Spencer TE (2010) Viral particles of endogenous betaretroviruses are released in the sheep uterus and infect the conceptus trophectoderm in a transspecies embryo transfer model. J Virol 84:9078–9085

    Article  PubMed  CAS  Google Scholar 

  • 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

    Article  PubMed  CAS  Google Scholar 

  • 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 is expressed in the human placenta and fuses cells expressing the type D mammalian retrovirus receptor. J Virol 74:3321–3329

    Article  PubMed  CAS  Google Scholar 

  • Byun H, Halani N, Mertz JA, Ali AF, Lozano MM, Dudley JP (2010) Retroviral Rem protein requires processing by signal peptidase and retrotranslocation for nuclear function. Proc Natl Acad Sci USA 107:12287–12292

    Article  PubMed  CAS  Google Scholar 

  • Caporale M, Arnaud F, Mura M, Golder M, Murgia C, Palmarini M (2009) The signal peptide of a simple retrovirus envelope functions as a posttranscriptional regulator of viral gene expression. J Virol 83:4591–4604

    Article  PubMed  CAS  Google Scholar 

  • Chow YH, Alberti A, Mura M, Pretto C, Murcia P, Albritton LM, Palmarini M (2003) Transformation of rodent fibroblasts by the jaagsiekte sheep retrovirus envelope is receptor independent and does not require the surface domain. J Virol 77:6341–6350

    Article  PubMed  CAS  Google Scholar 

  • Cornelis G, Heidmann O, Bernard-Stoecklin S, Reynaud K, Véron G, Mulot B, Dupressoir A, Heidmann T (2012) From the cover: ancestral capture of syncytin-Car1, a fusogenic endogenous retroviral envelope gene involved in placentation and conserved in Carnivora. Proc Natl Acad Sci USA 109:E432–E441

    Article  PubMed  CAS  Google Scholar 

  • Dewannieux M, Ribet D, Heidmann T (2010) Risks linked to endogenous retroviruses for vaccine production: a general overview. Biologicals 38:366–370

    Article  PubMed  Google Scholar 

  • Dunlap KA, Palmarini M, Spencer TE (2006a) Ovine endogenous betaretroviruses (enJSRVs) and placental morphogenesis. Placenta 27(Suppl A):S135–S140

    Article  PubMed  Google Scholar 

  • Dunlap KA, Palmarini M, Varela M, Burghardt RC, Hayashi K, Farmer JL, Spencer TE (2006b) Endogenous retroviruses regulate periimplantation placental growth and differentiation. Proc Natl Acad Sci USA 103:14390–14395

    Article  PubMed  CAS  Google Scholar 

  • 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

    Article  PubMed  CAS  Google Scholar 

  • Dupressoir A, Vernochet C, Bawa O, Harper F, Pierron G, Opolon P, Heidmann T (2009) Syncytin-a knockout mice demonstrate the critical role in placentation of a fusogenic, endogenous retro­virus-derived, envelope gene. Proc Natl Acad Sci USA 106:12127–12132

    Article  PubMed  CAS  Google Scholar 

  • Elleder D, Kim O, Padhi A, Bankert JG, Simeonov I, Schuster SC, Wittekindt NE, Motameny S, Poss M (2011) Polymorphic integrations of an endogenous gammaretrovirus in the mule deer genome. J Virol 86(5):2787–2796

    Article  PubMed  Google Scholar 

  • Evans DT, Serra-Moreno R, Singh RK, Guatelli JC (2010) BST-2/tetherin: a new component of the innate immune response to enveloped viruses. Trends Microbiol 18:388–396

    Article  PubMed  CAS  Google Scholar 

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

    Article  PubMed  CAS  Google Scholar 

  • Goodier JL, Kazazian HH Jr (2008) Retrotransposons revisited: the restraint and rehabilitation of parasites. Cell 135:23–35

    Article  PubMed  CAS  Google Scholar 

  • Harris JR (1991) The evolution of placental mammals. FEBS Lett 295:3–4

    Article  PubMed  CAS  Google Scholar 

  • Hassanin A, Douzery EJ (2003) Molecular and morphological phylogenies of ruminantia and the alternative position of the moschidae. Syst Biol 52:206–228

    Article  PubMed  Google Scholar 

  • Hofacre A, Nitta T, Fan H (2009) Jaagsiekte sheep retrovirus encodes a regulatory factor, Rej, required for synthesis of Gag protein. J Virol 83:12483–12498

    Article  PubMed  CAS  Google Scholar 

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

    Article  PubMed  CAS  Google Scholar 

  • Maeda N, Palmarini M, Murgia C, Fan H (2001) Direct transformation of rodent fibroblasts by jaagsiekte sheep retrovirus DNA. Proc Natl Acad Sci USA 98:4449–4454

    Article  PubMed  CAS  Google Scholar 

  • Maeda N, Fu W, Ortín A, De las Heras M, Fan H (2005) Roles of the Ras-MEK-mitogen-activated protein kinase and phosphatidylinositol 3-kinase-Akt-mTOR pathways in jaagsiekte sheep retrovirus-induced transformation of rodent fibroblast and epithelial cell lines. J Virol 79:4440–4450

    Article  PubMed  CAS  Google Scholar 

  • Mangeney M, Renard M, Schlecht-Louf G, Bouallaga I, Heidmann O, Letzelter C, Richaud A, Ducos B, Heidmann T (2007) Placental syncytins: genetic disjunction between the fusogenic and immunosuppressive activity of retroviral envelope proteins. Proc Natl Acad Sci USA 104:20534–20539

    Article  PubMed  CAS  Google Scholar 

  • McGee-Estrada K, Fan H (2006) In vivo and in vitro analysis of factor binding sites in jaagsiekte sheep retrovirus long terminal repeat enhancer sequences: roles of HNF-3, NF-I, and C/EBP for activity in lung epithelial cells. J Virol 80:332–341

    Article  PubMed  CAS  Google Scholar 

  • McGee-Estrada K, Palmarini M, Fan H (2002) HNF-3beta is a critical factor for the expression of the jaagsiekte sheep retrovirus long terminal repeat in type II pneumocytes but not in Clara cells. Virology 292:87–97

    Article  PubMed  CAS  Google Scholar 

  • 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 placental morphogenesis. Nature 403:785–789

    Article  PubMed  CAS  Google Scholar 

  • 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 USA 101:11117–11122

    Article  PubMed  CAS  Google Scholar 

  • Murcia PR, Arnaud F, Palmarini M (2007) The transdominant endogenous retrovirus enJS56A1 associates with and blocks intracellular trafficking of jaagsiekte sheep retrovirus Gag. J Virol 81:1762–1772

    Article  PubMed  CAS  Google Scholar 

  • Murgia C, Caporale M, Ceesay O, Di Francesco G, Ferri N, Varasano V, Palmarini M, De las Heras M (2011) Lung adenocarcinoma originates from retrovirus infection of proliferating type 2 pneumocytes during pulmonary post-natal development or tissue repair. PLoS Pathog 7:e1002014

    Article  PubMed  CAS  Google Scholar 

  • Neil SJ, Zang T, Bieniasz PD (2008) Tetherin inhibits retrovirus release and is antagonized by HIV-1 Vpu. Nature 451:425–430

    Article  PubMed  CAS  Google Scholar 

  • Nitta T, Hofacre A, Hull S, Fan H (2009) Identification and mutational analysis of a Rej response element in jaagsiekte sheep retrovirus RNA. J Virol 83:12499–12511

    Article  PubMed  CAS  Google Scholar 

  • Ortín A, Minguijón E, Dewar P, García M, Ferrer LM, Palmarini M, Gonzalez L, Sharp JM, De las Heras M (1998) Lack of a specific immune response against a recombinant capsid protein of jaagsiekte sheep retrovirus in sheep and goats naturally affected by enzootic nasal tumour or sheep pulmonary adenomatosis. Vet Immunol Immunopathol 61:229–237

    Article  PubMed  Google Scholar 

  • Palmarini M, Holland MJ, Cousens C, Dalziel RG, Sharp JM (1996) Jaagsiekte retrovirus ­establishes a disseminated infection of the lymphoid tissues of sheep affected by pulmonary adenomatosis. J Gen Virol 77:2991–2998

    Article  PubMed  CAS  Google Scholar 

  • Palmarini M, Sharp JM, De las Heras M, Fan H (1999a) Jaagsiekte sheep retrovirus is necessary and sufficient to induce a contagious lung cancer in sheep. J Virol 73:6964–6972

    PubMed  CAS  Google Scholar 

  • Palmarini M, Sharp JM, Lee C, Fan H (1999b) In vitro infection of ovine cell lines by jaagsiekte sheep retrovirus. J Virol 73:10070–10078

    PubMed  CAS  Google Scholar 

  • Palmarini M, Hallwirth C, York D, Murgia C, de Oliveira T, Spencer T, Fan H (2000) Molecular cloning and functional analysis of three type D endogenous retroviruses of sheep reveal a different cell tropism from that of the highly related exogenous jaagsiekte sheep retrovirus. J Virol 74:8065–8076

    Article  PubMed  CAS  Google Scholar 

  • Palmarini M, Gray CA, Carpenter K, Fan H, Bazer FW, Spencer TE (2001a) Expression of endogenous betaretroviruses in the ovine uterus: effects of neonatal age, estrous cycle, pregnancy, and progesterone. J Virol 75:11319–11327

    Article  PubMed  CAS  Google Scholar 

  • Palmarini M, Maeda N, Murgia C, De-Fraja C, Hofacre A, Fan H (2001b) A phosphatidylinositol 3-kinase docking site in the cytoplasmic tail of the jaagsiekte sheep retrovirus transmembrane protein is essential for envelope-induced transformation of NIH 3 T3 cells. J Virol 75:11002–11009

    Article  PubMed  CAS  Google Scholar 

  • Palmarini M, Murgia C, Fan H (2002) Spliced and prematurely polyadenylated jaagsiekte sheep retrovirus-specific RNAs from infected or transfected cells. Virology 294:180–188

    Article  PubMed  CAS  Google Scholar 

  • Sharp JM, Herring AJ (1983) Sheep pulmonary adenomatosis: demonstration of a protein which cross- reacts with the major core proteins of Mason-Pfizer monkey virus and mouse mammary tumour virus. J Gen Virol 64:2323–2327

    Article  PubMed  CAS  Google Scholar 

  • Spencer T, Ott T, Bazer F (1996) tau-interferon: pregnancy recognition signal in ruminants. Proc Soc Exp Biol Med 213:215–229

    PubMed  CAS  Google Scholar 

  • Spencer TE, Stagg AG, Joyce MM, Jenster G, Wood CG, Bazer FW, Wiley AA, Bartol FF (1999) Discovery and characterization of endometrial epithelial messenger ribonucleic acids using the ovine uterine gland knockout model. Endocrinology 140:4070–4080

    Article  PubMed  CAS  Google Scholar 

  • Spencer TE, Mura M, Gray CA, Griebel PJ, Palmarini M (2003) Receptor usage and fetal expression of ovine endogenous betaretroviruses: implications for coevolution of endogenous and exogenous retroviruses. J Virol 77:749–753

    Article  PubMed  CAS  Google Scholar 

  • Stoye JP (2009) Proviral protein provides placental function. Proc Natl Acad Sci USA 106:11827–11828

    Article  PubMed  CAS  Google Scholar 

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

    Article  PubMed  CAS  Google Scholar 

  • Van Damme N, Goff D, Katsura C, Jorgenson RL, Mitchell R, Johnson MC, Stephens EB, Guatelli J (2008) The interferon-induced protein BST-2 restricts HIV-1 release and is downregulated from the cell surface by the viral Vpu protein. Cell Host Microbe 3:245–252

    Article  PubMed  Google Scholar 

  • Varela M, Chow YH, Sturkie C, Murcia P, Palmarini M (2006) Association of RON tyrosine kinase with the jaagsiekte sheep retrovirus envelope glycoprotein. Virology 350:347–357

    Article  PubMed  CAS  Google Scholar 

  • Varela M, Spencer TE, Palmarini M, Arnaud F (2009) Friendly viruses: the special relationship between endogenous retroviruses and their host. Ann N Y Acad Sci 1178:157–172

    Article  PubMed  CAS  Google Scholar 

  • Vernochet C, Heidmann O, Dupressoir A, Cornelis G, Dessen P, Catzeflis F, Heidmann T (2011) A syncytin-like endogenous retrovirus envelope gene of the guinea pig specifically expressed in the placenta junctional zone and conserved in Caviomorpha. Placenta 32:885–892

    Article  PubMed  CAS  Google Scholar 

  • Villarreal LP (1997) On viruses, sex, and motherhood. J Virol 71:859–865

    PubMed  CAS  Google Scholar 

  • York DF, Vigne R, Verwoerd DW, Querat G (1992) Nucleotide sequence of the jaagsiekte retro­virus, an exogenous and endogenous type D and B retrovirus of sheep and goats. J Virol 66:4930–4939

    PubMed  CAS  Google Scholar 

Download references

Acknowledgments

We are grateful to the members of the Laboratory of Viral Pathogenesis of the University of Glasgow Centre for Virus Research (CVR) for stimulating discussions. Work in the laboratory of the authors is supported by a programme grant of the Wellcome Trust, by a Strategic Research Developmental Grant by the Scottish Funding Council, and by NIH grant HD052745. M.P. is a Wolfson-Royal Society Research Merit Awardee.

Author information

Authors and Affiliations

  1. MRC – University of Glasgow Centre for Virus Research, Institute of Infection, Immunity and Inflammation, College of Medical, Veterinary and Life Sciences, University of Glasgow, Glasgow, Scotland, UK

    Alessia Armezzani, Lita Murphy & Massimo Palmarini

  2. Department of Animal Sciences, School of Molecular Biosciences, Center Reproductive Biology, Washington State University, Pullman, WA, USA

    Thomas E. Spencer

  3. UMR754, INRA, Université Claude Bernard, Ecole Pratique des Hautes Etudes, Université de Lyon, SFR BioSciences Gerland-Lyon Sud, Lyon, France

    Frédérick Arnaud

Authors
  1. Alessia Armezzani
    View author publications

    You can also search for this author in PubMed Google Scholar

  2. Lita Murphy
    View author publications

    You can also search for this author in PubMed Google Scholar

  3. Thomas E. Spencer
    View author publications

    You can also search for this author in PubMed Google Scholar

  4. Massimo Palmarini
    View author publications

    You can also search for this author in PubMed Google Scholar

  5. Frédérick Arnaud
    View author publications

    You can also search for this author in PubMed Google Scholar

Corresponding author

Correspondence to Frédérick Arnaud .

Editor information

Editors and Affiliations

  1. Telos - Philosophische Praxis, Vogelsangstr. 18c, Bürmoos, 5111, Austria

    Günther Witzany

Rights and permissions

Reprints and permissions

Copyright information

© 2012 Springer Science+Business Media Dordrecht

About this chapter

Cite this chapter

Armezzani, A., Murphy, L., Spencer, T.E., Palmarini, M., Arnaud, F. (2012). The Evolutionary Interplay Between Exogenous and Endogenous Sheep Betaretroviruses. In: Witzany, G. (eds) Viruses: Essential Agents of Life. Springer, Dordrecht. https://doi.org/10.1007/978-94-007-4899-6_15

Download citation

Publish with us

Policies and ethics

Search

Navigation