Analyze Diet
Frontiers in veterinary science2021; 8; 693416; doi: 10.3389/fvets.2021.693416

Differential Expression Pattern of Retroviral Envelope Gene in the Equine Placenta.

Abstract: Endogenous retroviruses (ERVs) are proviral phases of exogenous retroviruses, which have coevolved with vertebrate genomes for millions of years. The conservation of ERV genes throughout evolution suggests their beneficial effects on their hosts' survival. An example of such positive selection is demonstrated by the syncytin gene, which encodes a protein with affinity for various mammalian placentas that is involved in the formation of syncytiotrophoblasts. Although the horse has an epitheliochorial placenta, in which the fetal trophoblasts are simply apposed to the intact uterine epithelium, we have previously demonstrated that the equine ERV (EqERV) RNA is unexpectedly expressed in placental tissue. In the present study, we investigated the mRNA expression pattern of the EqERV gene in different parts of the equine placenta, to gain more insight into its putative role in the fetal-maternal relationship. To this end, we used reverse transcription-quantitative PCR (RT-qPCR) and hybridization assays to analyze different target areas of the equine placenta. The retroviral gene is expressed in the equine placenta, even though there is no syncytium or erosion of the uterine endometrium. The gene is also expressed in all the sampled areas, although with some quantitative differences. We suggest that these differences are attributable to variations in the density, height, and degree of morphological complexity of the chorionic villi forming the microcotyledons. The involvement of the EqERV gene in different functional pathways affecting the fetus-mother relationship can be hypothesized.
Publication Date: 2021-07-09 PubMed ID: 34307531PubMed Central: PMC8298818DOI: 10.3389/fvets.2021.693416Google 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.
  • 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 is about the investigation of the expression patterns of the EqERV gene, a type of endogenous retrovirus, in different parts of the horse placenta. The researchers hypothesize that this gene might have a role in the equine fetal-maternal relationship.

Understanding Endogenous Retroviruses (ERVs)

  • ERVs are remnants of exogenous retroviruses. They have integrated into the genome of vertebrate species, co-evolving with them for millions of years.
  • The fact that ERVs have been conserved over evolutionary time suggests they have been beneficial for the survival of their host species.
  • A well-known example of a beneficial ERV gene is the syncytin gene. It codes for a protein that interacts with the placental tissue in various mammals, playing a critical role in the formation of syncytiotrophoblasts, which are important structural elements in the placenta.

The EqERV Gene and the Equine Placenta

  • The horse placenta is epitheliochorial, meaning the fetal tissue (the trophoblasts) is situated directly next to the intact uterine lining (the endometrium).
  • Despite this structure of the equine placenta, which does not involve the formation of syncytiotrophoblasts, the researchers have previously found expression of the equine ERV (EqERV) gene in this tissue.
  • This led the team to investigate the RNA expression pattern of this gene in varying parts of the equine placenta to understand its potential role in the relationship between fetus and mother in equine species.

Study Methodology

  • The team used reverse transcription-quantitative PCR (RT-qPCR) and hybridization techniques to analyze the EqERV gene expression in different targeted areas of the horse placenta.
  • They discovered that the gene is expressed across all tested areas of the equine placenta. This expression occurs even without the formation of a syncytium or erosion of the endometrium, which are typically associated with placental ERV gene expression.
  • They also noted that the level of EqERV expression showed some variation across different placental areas. The team suggested that differences in the density, height and complexity of the chorionic villi (structures forming the microcotyledons in the placenta) could account for these variations in gene expression.

Implications and Hypotheses

  • The findings from this research suggest that the EqERV gene may be involved in the functional processing of pregnancy in equines and could influence the relationship between the fetus and the mother.
  • Further research can explore how and to what extent this particular ERV gene impacts equine reproduction and fetal development, which can provide useful insights into reproductive health and disease in these animals.

Cite This Article

APA
Stefanetti V, Pascucci L, Wilsher S, Cappelli K, Capomaccio S, Reale L, Passamonti F, Coletti M, Crociati M, Monaci M, Marenzoni ML. (2021). Differential Expression Pattern of Retroviral Envelope Gene in the Equine Placenta. Front Vet Sci, 8, 693416. https://doi.org/10.3389/fvets.2021.693416

Publication

ISSN: 2297-1769
NlmUniqueID: 101666658
Country: Switzerland
Language: English
Volume: 8
Pages: 693416
PII: 693416

Researcher Affiliations

Stefanetti, Valentina
  • Department of Veterinary Medicine, University of Perugia, Perugia, Italy.
Pascucci, Luisa
  • Department of Veterinary Medicine, University of Perugia, Perugia, Italy.
Wilsher, Sandra
  • The Paul Mellon Laboratory of Equine Reproduction, 'Brunswick', Newmarket, United Kingdom.
Cappelli, Katia
  • Department of Veterinary Medicine, University of Perugia, Perugia, Italy.
Capomaccio, Stefano
  • Department of Veterinary Medicine, University of Perugia, Perugia, Italy.
Reale, Lara
  • Department of Agricultural, Food and Environmental Sciences, University of Perugia, Perugia, Italy.
Passamonti, Fabrizio
  • Department of Veterinary Medicine, University of Perugia, Perugia, Italy.
Coletti, Mauro
  • Department of Veterinary Medicine, University of Perugia, Perugia, Italy.
Crociati, Martina
  • Department of Veterinary Medicine, University of Perugia, Perugia, Italy.
  • Centre for Perinatal and Reproductive Medicine, University of Perugia, Perugia, Italy.
Monaci, Maurizio
  • Department of Veterinary Medicine, University of Perugia, Perugia, Italy.
  • Centre for Perinatal and Reproductive Medicine, University of Perugia, Perugia, Italy.
Marenzoni, Maria Luisa
  • Department of Veterinary Medicine, University of Perugia, Perugia, Italy.

Conflict of Interest Statement

The authors declare that the research was conducted in the absence of any commercial or financial relationships that could be construed as a potential conflict of interest.

References

This article includes 45 references
  1. Boeke JD, Stoye JP. Retrotransposons, endogenous retroviruses, and the evolution of retroelements. Retroviruses Cold Spring Harbor, NY: Cold Spring Harbor Laboratory Press.
  2. 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
  3. Gifford R, Tristem M. The evolution, distribution and diversity of endogenous retroviruses.. Virus Genes 2003 May;26(3):291-315.
    doi: 10.1023/A:1024455415443pubmed: 12876457google scholar: lookup
  4. 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.
  5. Bock M, Stoye JP. Endogenous retroviruses and the human germline.. Curr Opin Genet Dev 2000 Dec;10(6):651-5.
    doi: 10.1016/S0959-437X(00)00138-6pubmed: 11088016google scholar: lookup
  6. Varela M, Spencer TE, Palmarini M, Arnaud F. Friendly viruses: the special relationship between endogenous retroviruses and their host.. Ann N Y Acad Sci 2009 Oct;1178:157-72.
  7. 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
  8. 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
  9. 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
  10. 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
  11. 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
  12. Cornelis G, Vernochet C, Malicorne S, Souquere S, Tzika AC, Goodman SM, Catzeflis F, Robinson TJ, Milinkovitch MC, Pierron G, Heidmann O, Dupressoir A, Heidmann T. Retroviral envelope syncytin capture in an ancestrally diverged mammalian clade for placentation in the primitive Afrotherian tenrecs.. Proc Natl Acad Sci U S A 2014 Oct 14;111(41):E4332-41.
    doi: 10.1073/pnas.1412268111pmc: PMC4205661pubmed: 25267646google scholar: lookup
  13. Cornelis G, Vernochet C, Carradec Q, Souquere S, Mulot B, Catzeflis F, Nilsson MA, Menzies BR, Renfree MB, Pierron G, Zeller U, Heidmann O, Dupressoir A, Heidmann T. Retroviral envelope gene captures and syncytin exaptation for placentation in marsupials.. Proc Natl Acad Sci U S A 2015 Feb 3;112(5):E487-96.
    doi: 10.1073/pnas.1417000112pmc: PMC4321253pubmed: 25605903google scholar: lookup
  14. Lavialle C, Cornelis G, Dupressoir A, Esnault C, Heidmann O, Vernochet C, Heidmann T. Paleovirology of 'syncytins', retroviral env genes exapted for a role in placentation.. Philos Trans R Soc Lond B Biol Sci 2013 Sep 19;368(1626):20120507.
    doi: 10.1098/rstb.2012.0507pmc: PMC3758191pubmed: 23938756google scholar: lookup
  15. 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
  16. 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
  17. 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
  18. 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.00927-18pmc: PMC6232481pubmed: 30209175google scholar: lookup
  19. Gim JA, Kim HS. Identification and Expression Analyses of Equine Endogenous Retroviruses in Horses.. Mol Cells 2017 Oct;40(10):796-804.
    doi: 10.14348/molcells.2017.0141pmc: PMC5682256pubmed: 29047258google scholar: lookup
  20. Stefanetti V, Marenzoni ML, Passamonti F, Cappelli K, Garcia-Etxebarria K, Coletti M, Capomaccio S. High Expression of Endogenous Retroviral Envelope Gene in the Equine Fetal Part of the Placenta.. PLoS One 2016;11(5):e0155603.
  21. Carter AM, Enders AC. The evolution of epitheliochorial placentation.. Annu Rev Anim Biosci 2013 Jan;1:443-67.
  22. Whitwell KE, Jeffcott LB. Morphological studies on the fetal membranes of the normal singleton foal at term.. Res Vet Sci 1975 Jul;19(1):44-55.
    doi: 10.1016/S0034-5288(18)33552-5pubmed: 1153897google scholar: lookup
  23. Cottrill CM, Jeffers-Lo J, Ousey JC, McGladdery AJ, Ricketts SW, Silver M, Rossdale PD. The placenta as a determinant of fetal well-being in normal and abnormal equine pregnancies.. J Reprod Fertil Suppl 1991;44:591-601.
    pubmed: 1795302
  24. Schlafer DH. Examination of the placenta. Equine Reproduction Oxford: Wiley-Blackwell. p. 99–110.
  25. 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.
  26. 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
  27. 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.
  28. 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
  29. Vernochet C, Heidmann O, Dupressoir A, Cornelis G, Dessen P, Catzeflis F, Heidmann T. A syncytin-like endogenous retrovirus envelope gene of the guinea pig specifically expressed in the placenta junctional zone and conserved in Caviomorpha.. Placenta 2011 Nov;32(11):885-92.
  30. Wooding FB, Wathes DC. Binucleate cell migration in the bovine placentome.. J Reprod Fertil 1980 Jul;59(2):425-30.
    doi: 10.1530/jrf.0.0590425pubmed: 7431300google scholar: lookup
  31. Wooding FBP, Osborn D, Killian GJ. Trinucleate uterine epithelial cells as evidence for White-tail Deer trophoblast binucleate cell migration and as markers of placental binucleate cell dynamics in a variety of wild ruminants.. Placenta 2018 Feb;62:34-42.
  32. Nakaya Y, Koshi K, Nakagawa S, Hashizume K, Miyazawa T. Fematrin-1 is involved in fetomaternal cell-to-cell fusion in Bovinae placenta and has contributed to diversity of ruminant placentation.. J Virol 2013 Oct;87(19):10563-72.
    doi: 10.1128/JVI.01398-13pmc: PMC3807419pubmed: 23864631google scholar: lookup
  33. 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
  34. Dunlap KA, Palmarini M, Spencer TE. Ovine endogenous betaretroviruses (enJSRVs) and placental morphogenesis.. Placenta 2006 Apr;27 Suppl A:S135-40.
  35. Allen WR. Fetomaternal interactions and influences during equine pregnancy.. Reproduction 2001 Apr;121(4):513-27.
    doi: 10.1530/reprod/121.4.513pubmed: 11277870google scholar: lookup
  36. Dunlap KA, Palmarini M, Adelson DL, Spencer TE. Sheep endogenous betaretroviruses (enJSRVs) and the hyaluronidase 2 (HYAL2) receptor in the ovine uterus and conceptus.. Biol Reprod 2005 Aug;73(2):271-9.
    doi: 10.1095/biolreprod.105.039776pubmed: 15788753google scholar: lookup
  37. 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
  38. Heidmann O, Béguin A, Paternina J, Berthier R, Deloger M, Bawa O, Heidmann T. HEMO, an ancestral endogenous retroviral envelope protein shed in the blood of pregnant women and expressed in pluripotent stem cells and tumors.. Proc Natl Acad Sci U S A 2017 Aug 8;114(32):E6642-E6651.
    doi: 10.1073/pnas.1702204114pmc: PMC5559007pubmed: 28739914google scholar: lookup
  39. Mangeney M, Heidmann T. Tumor cells expressing a retroviral envelope escape immune rejection in vivo.. Proc Natl Acad Sci U S A 1998 Dec 8;95(25):14920-5.
    doi: 10.1073/pnas.95.25.14920pmc: PMC24551pubmed: 9843991google scholar: lookup
  40. Mangeney M, de Parseval N, Thomas G, Heidmann T. The full-length envelope of an HERV-H human endogenous retrovirus has immunosuppressive properties.. J Gen Virol 2001 Oct;82(Pt 10):2515-2518.
    doi: 10.1099/0022-1317-82-10-2515pubmed: 11562544google scholar: lookup
  41. 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
  42. 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
  43. Yoon JH, Abdelmohsen K, Gorospe M. Posttranscriptional gene regulation by long noncoding RNA.. J Mol Biol 2013 Oct 9;425(19):3723-30.
    doi: 10.1016/j.jmb.2012.11.024pmc: PMC3594629pubmed: 23178169google scholar: lookup
  44. Bracher V, Mathias S, Allen WR. Influence of chronic degenerative endometritis (endometrosis) on placental development in the mare.. Equine Vet J 1996 May;28(3):180-188.
  45. Wilsher S, Allen WR. The effects of maternal age and parity on placental and fetal development in the mare.. Equine Vet J 2003 Jul;35(5):476-83.
    doi: 10.2746/042516403775600550pubmed: 12875326google scholar: lookup

Citations

This article has been cited 0 times.