FREE SHIPPING over $40
OVER 9000 FIVE-STAR REVIEWS
5% OFF ALL SUBSCRIPTIONS
100% HAPPINESS GUARANTEE
Analyze Diet
0
Home / Equine Research Bank / PLoS One / High Expression of Endogenous Retroviral Envelope Gene in th...
PloS one2016; 11(5); e0155603; doi: 10.1371/journal.pone.0155603

High Expression of Endogenous Retroviral Envelope Gene in the Equine Fetal Part of the Placenta.

Abstract: Endogenous retroviruses (ERVs) are proviral phases of exogenous retroviruses that have co-evolved with vertebrate genomes for millions of years. Previous studies have identified the envelope (env) protein genes of retroviral origin preferentially expressed in the placenta which suggests a role in placentation based on their membrane fusogenic capacity and therefore they have been named syncytins. Until now, all the characterized syncytins have been associated with three invasive placentation types: the endotheliochorial (Carnivora), the synepitheliochorial (Ruminantia), and the hemochorial placentation (human, mouse) where they play a role in the syncytiotrophoblast formation. The purpose of the present study was to evaluate whether EqERV env RNA is expressed in horse tissues as well and investigate if the horse, possessing an epitheliochorial placenta, has "captured" a common retroviral env gene with syncytin-like properties in placental tissues. Interestingly, although in the equine placenta there is no syncytiotrophoblast layer at the maternal-fetal interface, our results showed that EqERV env RNA is highly expressed at that level, as expected for a candidate syncytin-like gene but with reduced abundance in the other somatic tissues (nearly 30-fold lower) thus suggesting a possible role in the placental tissue. Although the horse is one of the few domestic animals with a sequenced genome, few studies have been conducted about the EqERV and their expression in placental tissue has never been investigated.
Get Full Text
Publication Date: 2016-05-13 PubMed ID: 27176223PubMed Central: PMC4866760DOI: 10.1371/journal.pone.0155603Google Scholar: Lookup
The Equine Research Bank provides access to a large database of publicly available scientific literature. Inclusion in the Research Bank does not imply endorsement of study methods or findings by Mad Barn.
LinkedInCopy
  • Journal Article

Summary

This research summary has been generated with artificial intelligence and may contain errors and omissions. Refer to the original study to confirm details provided. Submit correction.

The study investigates the high tendency of a certain retroviral gene to express within the placental part of a horse fetus, implying a possible role in the placentation process.

Research Objective and Background

  • Endogenous retroviruses (ERVs) are inherited forms of exogenous retroviruses that have developed hand-in-hand with vertebrate genomes for many millions of years. These ERVs have envelope protein genes (env) of retroviral origin which are often found to be expressed in the placenta. This activity suggests an active role for these genes in creating the placenta, due to their capabilities to fuse to the membrane.
  • These genes are called syncytins and up until now, they have only been associated with three types of invasive placentation: the endotheliochorial (found in carnivores), the synepitheliochorial (found in ruminants), and the hemochorial placentation (found in humans and mice), where they actively participate in the formation of the syncytiotrophoblast.
  • The aim of this study was to verify whether the envelope RNA of the horse endogenous retrovirus (EqERV env RNA) is expressed in horse tissues, particularly in the horse’s placenta which is epitheliochorial—a form not previously associated with syncytins.

Findings and Implications

  • Although the equine placenta lacks a syncytiotrophoblast layer at the maternal-fetal interface, the results of the study show that EqERV env RNA is indeed highly expressed at this site—a characteristic of a presumptive syncytin-like gene. The same gene was found to be less abundant in other somatic tissues, almost 30 times lower, implying a possible role in the placental tissue.
  • The revelation that horses, too, may harbor a retroviral env gene with syncytin-like properties within their placental tissues, may offer fresh insights into the evolution of equine placenta and could pave the way for new avenues of research. Moreover, although the horse is among the handful of domestic animals with a sequenced genome, there have been little studies examining EqERV and their expression in the placental tissue had not been previously explored.

Conclusions

  • The discovery of a potential syncytin-like gene in horses—organisms with a placenta type not previously associated with syncytins—suggests a wider role for these genes than previously believed. With EqERV env RNA showing high expression in equine placental tissue, the study provides a fascinating breakthrough that shines a new light on how placental tissue may evolve and operate.

Cite This Article

APA
Stefanetti V, Marenzoni ML, Passamonti F, Cappelli K, Garcia-Etxebarria K, Coletti M, Capomaccio S. (2016). High Expression of Endogenous Retroviral Envelope Gene in the Equine Fetal Part of the Placenta. PLoS One, 11(5), e0155603. https://doi.org/10.1371/journal.pone.0155603

Publication

PloS one
ISSN: 1932-6203
NlmUniqueID: 101285081
Country: United States
Language: English
Volume: 11
Issue: 5
Pages: e0155603
PII: e0155603

Researcher Affiliations

Stefanetti, Valentina
  • Department of Veterinary Medicine, University of Perugia, Perugia, Italy.
Marenzoni, Maria Luisa
  • Department of Veterinary Medicine, University of Perugia, Perugia, Italy.
Passamonti, Fabrizio
  • Department of Veterinary Medicine, University of Perugia, Perugia, Italy.
Cappelli, Katia
  • Department of Veterinary Medicine, University of Perugia, Perugia, Italy.
Garcia-Etxebarria, Koldo
  • Department of Genetics, Physical Anthropology and Animal Physiology, University of Basque Country-UPV/EHU, BioCruces Health Research Institute, Leioa, Spain.
Coletti, Mauro
  • Department of Veterinary Medicine, University of Perugia, Perugia, Italy.
Capomaccio, Stefano
  • Department of Veterinary Medicine, University of Perugia, Perugia, Italy.

MeSH Terms

  • Animals
  • Endogenous Retroviruses / genetics
  • Female
  • Fetus / virology
  • Gene Expression Regulation, Viral
  • Genes, env
  • Horses / virology
  • Placenta / virology
  • Pregnancy
  • RNA, Viral / genetics
  • RNA, Viral / metabolism
  • Viral Envelope Proteins / genetics

Conflict of Interest Statement

The authors have declared that no competing interests exist.

References

This article includes 38 references
  1. Gifford R, Tristem M. The evolution, distribution and diversity of endogenous retroviruses.. Virus Genes 2003 May;26(3):291-315.
    pubmed: 12876457doi: 10.1023/a:1024455415443google scholar: lookup
  2. Dupressoir A, Lavialle C, Heidmann T. From ancestral infectious retroviruses to bona fide cellular genes: role of the captured syncytins in placentation.. Placenta 2012 Sep;33(9):663-71.
    doi: 10.1016/j.placenta.2012.05.005pubmed: 22695103google scholar: lookup
  3. Gifford R, Kabat P, Martin J, Lynch C, Tristem M. Evolution and distribution of class II-related endogenous retroviruses.. J Virol 2005 May;79(10):6478-86.
    doi: 10.1128/JVI.79.10.6478-6486.2005pmc: PMC1091674pubmed: 15858031google scholar: lookup
  4. Garcia-Etxebarria K, Jugo BM. Detection and characterization of endogenous retroviruses in the horse genome by in silico analysis.. Virology 2012 Dec 5;434(1):59-67.
    doi: 10.1016/j.virol.2012.08.047pubmed: 23026066google scholar: lookup
  5. Prudhomme S, Bonnaud B, Mallet F. Endogenous retroviruses and animal reproduction.. Cytogenet Genome Res 2005;110(1-4):353-64.
    doi: 10.1159/000084967pubmed: 16093687google scholar: lookup
  6. Cornelis G, Heidmann O, Degrelle SA, Vernochet C, Lavialle C, Letzelter C, Bernard-Stoecklin S, Hassanin A, Mulot B, Guillomot M, Hue I, Heidmann T, Dupressoir A. Captured retroviral envelope syncytin gene associated with the unique placental structure of higher ruminants.. Proc Natl Acad Sci U S A 2013 Feb 26;110(9):E828-37.
    doi: 10.1073/pnas.1215787110pmc: PMC3587263pubmed: 23401540google scholar: lookup
  7. Boeke JD, Stoye JP. Retrotransposons, Endogenous Retroviruses, and the Evolution of Retroelements. Retroviruses Cold Spring Harbor (NY): Cold Spring Harbor Laboratory Press; 1997.
  8. 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. Syncytin is a captive retroviral envelope protein involved in human placental morphogenesis.. Nature 2000 Feb 17;403(6771):785-9.
    doi: 10.1038/35001608pubmed: 10693809google scholar: lookup
  9. Chuong EB. Retroviruses facilitate the rapid evolution of the mammalian placenta.. Bioessays 2013 Oct;35(10):853-61.
    doi: 10.1002/bies.201300059pmc: PMC4332834pubmed: 23873343google scholar: lookup
  10. Mangeney M, Renard M, Schlecht-Louf G, Bouallaga I, Heidmann O, Letzelter C, Richaud A, Ducos B, Heidmann T. Placental syncytins: Genetic disjunction between the fusogenic and immunosuppressive activity of retroviral envelope proteins.. Proc Natl Acad Sci U S A 2007 Dec 18;104(51):20534-9.
    doi: 10.1073/pnas.0707873105pmc: PMC2154466pubmed: 18077339google scholar: lookup
  11. Cornelis G, Heidmann O, Bernard-Stoecklin S, Reynaud K, Véron G, Mulot B, Dupressoir A, Heidmann T. Ancestral capture of syncytin-Car1, a fusogenic endogenous retroviral envelope gene involved in placentation and conserved in Carnivora.. Proc Natl Acad Sci U S A 2012 Feb 14;109(7):E432-41.
    doi: 10.1073/pnas.1115346109pmc: PMC3289388pubmed: 22308384google scholar: lookup
  12. Dupressoir A, Marceau G, Vernochet C, Bénit L, Kanellopoulos C, Sapin V, Heidmann T. Syncytin-A and syncytin-B, two fusogenic placenta-specific murine envelope genes of retroviral origin conserved in Muridae.. Proc Natl Acad Sci U S A 2005 Jan 18;102(3):725-30.
    doi: 10.1073/pnas.0406509102pmc: PMC545540pubmed: 15644441google scholar: lookup
  13. Heidmann O, Vernochet C, Dupressoir A, Heidmann T. Identification of an endogenous retroviral envelope gene with fusogenic activity and placenta-specific expression in the rabbit: a new "syncytin" in a third order of mammals.. Retrovirology 2009 Nov 27;6:107.
    doi: 10.1186/1742-4690-6-107pmc: PMC2789053pubmed: 19943933google scholar: lookup
  14. Vernochet C, Redelsperger F, Harper F, Souquere S, Catzeflis F, Pierron G, Nevo E, Heidmann T, Dupressoir A. The captured retroviral envelope syncytin-A and syncytin-B genes are conserved in the Spalacidae together with hemotrichorial placentation.. Biol Reprod 2014 Dec;91(6):148.
    doi: 10.1095/biolreprod.114.124818pubmed: 25339103google scholar: lookup
  15. Dupressoir A, Vernochet C, Bawa O, Harper F, Pierron G, Opolon P, Heidmann T. Syncytin-A knockout mice demonstrate the critical role in placentation of a fusogenic, endogenous retrovirus-derived, envelope gene.. Proc Natl Acad Sci U S A 2009 Jul 21;106(29):12127-32.
    doi: 10.1073/pnas.0902925106pmc: PMC2715540pubmed: 19564597google scholar: lookup
  16. Dunlap KA, Palmarini M, Varela M, Burghardt RC, Hayashi K, Farmer JL, Spencer TE. Endogenous retroviruses regulate periimplantation placental growth and differentiation.. Proc Natl Acad Sci U S A 2006 Sep 26;103(39):14390-5.
    doi: 10.1073/pnas.0603836103pmc: PMC1599973pubmed: 16980413google scholar: lookup
  17. Wade CM, Giulotto E, Sigurdsson S, Zoli M, Gnerre S, Imsland F, Lear TL, Adelson DL, Bailey E, Bellone RR, Blöcker H, Distl O, Edgar RC, Garber M, Leeb T, Mauceli E, MacLeod JN, Penedo MC, Raison JM, Sharpe T, Vogel J, Andersson L, Antczak DF, Biagi T, Binns MM, Chowdhary BP, Coleman SJ, Della Valle G, Fryc S, Guérin G, Hasegawa T, Hill EW, Jurka J, Kiialainen A, Lindgren G, Liu J, Magnani E, Mickelson JR, Murray J, Nergadze SG, Onofrio R, Pedroni S, Piras MF, Raudsepp T, Rocchi M, Røed KH, Ryder OA, Searle S, Skow L, Swinburne JE, Syvänen AC, Tozaki T, Valberg SJ, Vaudin M, White JR, Zody MC, Lander ES, Lindblad-Toh K. Genome sequence, comparative analysis, and population genetics of the domestic horse.. Science 2009 Nov 6;326(5954):865-7.
    doi: 10.1126/science.1178158pmc: PMC3785132pubmed: 19892987google scholar: lookup
  18. Brown K, Moreton J, Malla S, Aboobaker AA, Emes RD, Tarlinton RE. Characterisation of retroviruses in the horse genome and their transcriptional activity via transcriptome sequencing.. Virology 2012 Nov 10;433(1):55-63.
    doi: 10.1016/j.virol.2012.07.010pubmed: 22868041google scholar: lookup
  19. Kayis SA, Atli MO, Kurar E, Bozkaya F, Semacan A, Aslan S, Guzeloglu A. Rating of putative housekeeping genes for quantitative gene expression analysis in cyclic and early pregnant equine endometrium.. Anim Reprod Sci 2011 May;125(1-4):124-32.
    doi: 10.1016/j.anireprosci.2011.02.019pubmed: 21411251google scholar: lookup
  20. Cappelli K, Felicetti M, Capomaccio S, Spinsanti G, Silvestrelli M, Supplizi AV. Exercise induced stress in horses: selection of the most stable reference genes for quantitative RT-PCR normalization.. BMC Mol Biol 2008 May 19;9:49.
    doi: 10.1186/1471-2199-9-49pmc: PMC2412902pubmed: 18489742google scholar: lookup
  21. Klein C, Rutllant J, Troedsson MH. Expression stability of putative reference genes in equine endometrial, testicular, and conceptus tissues.. BMC Res Notes 2011 Apr 12;4:120.
    doi: 10.1186/1756-0500-4-120pmc: PMC3083352pubmed: 21486450google scholar: lookup
  22. Vandesompele J, De Preter K, Pattyn F, Poppe B, Van Roy N, De Paepe A, Speleman F. Accurate normalization of real-time quantitative RT-PCR data by geometric averaging of multiple internal control genes.. Genome Biol 2002 Jun 18;3(7):RESEARCH0034.
    pmc: PMC126239pubmed: 12184808doi: 10.1186/gb-2002-3-7-research0034google scholar: lookup
  23. van der Kuyl AC. Characterization of a full-length endogenous beta-retrovirus, EqERV-beta1, in the genome of the horse (Equus caballus).. Viruses 2011 Jun;3(6):620-8.
    doi: 10.3390/v3060620pmc: PMC3185775pubmed: 21994749google scholar: lookup
  24. Baba K, Nakaya Y, Shojima T, Muroi Y, Kizaki K, Hashizume K, Imakawa K, Miyazawa T. Identification of novel endogenous betaretroviruses which are transcribed in the bovine placenta.. J Virol 2011 Feb;85(3):1237-45.
    doi: 10.1128/JVI.01234-10pmc: PMC3020495pubmed: 21084469google scholar: lookup
  25. Bittmann I, Mihica D, Plesker R, Denner J. Expression of porcine endogenous retroviruses (PERV) in different organs of a pig.. Virology 2012 Nov 25;433(2):329-36.
    doi: 10.1016/j.virol.2012.08.030pubmed: 22975674google scholar: lookup
  26. Matousková M, Blazková J, Pajer P, Pavlícek A, Hejnar J. CpG methylation suppresses transcriptional activity of human syncytin-1 in non-placental tissues.. Exp Cell Res 2006 Apr 15;312(7):1011-20.
    doi: 10.1016/j.yexcr.2005.12.010pubmed: 16427621google scholar: lookup
  27. Allen WR, Hamilton DW, Moor RM. The origin of equine endometrial cups. II. Invasion of the endometrium by trophoblast.. Anat Rec 1973 Dec;177(4):485-501.
    doi: 10.1002/ar.1091770403pubmed: 4762726google scholar: lookup
  28. Noronha LE, Huggler KE, de Mestre AM, Miller DC, Antczak DF. Molecular evidence for natural killer-like cells in equine endometrial cups.. Placenta 2012 May;33(5):379-86.
    doi: 10.1016/j.placenta.2012.01.018pmc: PMC3319276pubmed: 22357194google scholar: lookup
  29. Allen WR. Fetomaternal interactions and influences during equine pregnancy.. Reproduction 2001 Apr;121(4):513-27.
    pubmed: 11277870
  30. Zhang Y, Shi J, Liu S. Recent advances in the study of active endogenous retrovirus envelope glycoproteins in the mammalian placenta.. Virol Sin 2015 Aug;30(4):239-48.
    doi: 10.1007/s12250-015-3617-0pubmed: 26311491google scholar: lookup
  31. Harris JR. Placental endogenous retrovirus (ERV): structural, functional, and evolutionary significance.. Bioessays 1998 Apr;20(4):307-16.
    doi: 10.1002/(SICI)1521-1878(199804)20:4<307::AID-BIES7>3.0.CO;2-Mpubmed: 9619102google scholar: lookup
  32. Samuel CA, Allen WR, Steven DH. Studies on the equine placenta II. Ultrastructure of the placental barrier.. J Reprod Fertil 1976 Nov;48(2):257-264.
    pubmed: 1033277doi: 10.1530/jrf.0.0480257google scholar: lookup
  33. Lokossou AG, Toudic C, Barbeau B. Implication of human endogenous retrovirus envelope proteins in placental functions.. Viruses 2014 Nov 24;6(11):4609-27.
    doi: 10.3390/v6114609pmc: PMC4246240pubmed: 25421890google scholar: lookup
  34. Derfuss T, Curtin F, Guebelin C, Bridel C, Rasenack M, Matthey A, Du Pasquier R, Schluep M, Desmeules J, Lang AB, Perron H, Faucard R, Porchet H, Hartung HP, Kappos L, Lalive PH. A phase IIa randomized clinical study testing GNbAC1, a humanized monoclonal antibody against the envelope protein of multiple sclerosis associated endogenous retrovirus in multiple sclerosis patients - a twelve month follow-up.. J Neuroimmunol 2015 Aug 15;285:68-70.
    doi: 10.1016/j.jneuroim.2015.05.019pubmed: 26198921google scholar: lookup
  35. Ruprecht K, Mayer J, Sauter M, Roemer K, Mueller-Lantzsch N. Endogenous retroviruses and cancer.. Cell Mol Life Sci 2008 Nov;65(21):3366-82.
    doi: 10.1007/s00018-008-8496-1pubmed: 18818873google scholar: lookup
  36. Isbel L, Whitelaw E. Endogenous retroviruses in mammals: an emerging picture of how ERVs modify expression of adjacent genes.. Bioessays 2012 Sep;34(9):734-8.
    doi: 10.1002/bies.201200056pubmed: 22736292google scholar: lookup
  37. Kudaka W, Oda T, Jinno Y, Yoshimi N, Aoki Y. Cellular localization of placenta-specific human endogenous retrovirus (HERV) transcripts and their possible implication in pregnancy-induced hypertension.. Placenta 2008 Mar;29(3):282-9.
    doi: 10.1016/j.placenta.2007.11.009pubmed: 18158183google scholar: lookup
  38. Vargas A, Toufaily C, LeBellego F, Rassart É, Lafond J, Barbeau B. Reduced expression of both syncytin 1 and syncytin 2 correlates with severity of preeclampsia.. Reprod Sci 2011 Nov;18(11):1085-91.
    doi: 10.1177/1933719111404608pubmed: 21493955google scholar: lookup

Citations

This article has been cited 6 times.
  1. Stefanetti V, Pascucci L, Wilsher S, Cappelli K, Capomaccio S, Reale L, Passamonti F, Coletti M, Crociati M, Monaci M, Marenzoni ML. Differential Expression Pattern of Retroviral Envelope Gene in the Equine Placenta. Front Vet Sci 2021;8:693416.
    doi: 10.3389/fvets.2021.693416pubmed: 34307531google scholar: lookup
  2. Bergallo M, Marozio L, Botta G, Tancredi A, Daprà V, Galliano I, Montanari P, Coscia A, Benedetto C, Tovo PA. Human Endogenous Retroviruses Are Preferentially Expressed in Mononuclear Cells From Cord Blood Than From Maternal Blood and in the Fetal Part of Placenta. Front Pediatr 2020;8:244.
    doi: 10.3389/fped.2020.00244pubmed: 32478020google scholar: lookup
  3. Cappelli K, Gialletti R, Tesei B, Bassotti G, Fettucciari K, Capomaccio S, Bonfili L, Cuccioloni M, Eleuteri AM, Spaterna A, Laus F. Guanylin, Uroguanylin and Guanylate Cyclase-C Are Expressed in the Gastrointestinal Tract of Horses. Front Physiol 2019;10:1237.
    doi: 10.3389/fphys.2019.01237pubmed: 31611814google scholar: lookup
  4. Liu C, Xu J, Wen F, Yang F, Li X, Geng D, Li L, Chen J, Zheng J. Upregulation of syncytin-1 promotes invasion and metastasis by activating epithelial-mesenchymal transition-related pathway in endometrial carcinoma. Onco Targets Ther 2019;12:31-40.
    doi: 10.2147/OTT.S191041pubmed: 30588028google scholar: lookup
  5. Zhu H, Gifford RJ, Murcia PR. Distribution, Diversity, and Evolution of Endogenous Retroviruses in Perissodactyl Genomes. J Virol 2018 Dec 1;92(23).
    doi: 10.1128/JVI.00927-18pubmed: 30209175google scholar: lookup
  6. Read JE, Cabrera-Sharp V, Kitscha P, Cartwright JE, King PJ, Fowkes RC, de Mestre AM. Glial Cells Missing 1 Regulates Equine Chorionic Gonadotrophin Beta Subunit via Binding to the Proximal Promoter. Front Endocrinol (Lausanne) 2018;9:195.
    doi: 10.3389/fendo.2018.00195pubmed: 29755409google scholar: lookup
Subscribe to our newsletter
Join 99,344 horse owners like you who receive our email updates on horse health and nutrition.