Capture of syncytin-Mar1, a fusogenic endogenous retroviral envelope gene involved in placentation in the rodentia squirrel-related clade

Journal of Virology

Volumn 88, Issue 14, 2014, Pages 7915-7928

  Redelsperger, François ^a,b   Cornelis, Guillaume ^a,b,c   Vernochet, Cécile ^a,b   Tennant, Bud C ^d   Catzeflis, François ^e   Mulot, Baptiste ^f   Heidmann, Odile ^a,b   Heidmann, Thierry ^a,b   Dupressoir, Anne ^a,b  

^a CNRS   (France)

^b UNIVERSITÉ PARIS SACLAY   (France)

^c UNIVERSITÉ PARIS DESCARTES   (France)

^d Department of Obstetrics Gynecology   (United States)

^e INSTITUT DES SCIENCES DE L EVOLUTION   (France)

^f ZooParc de Beauval et Beauval Nature ^*  (France)

Author keywords

[No Author keywords available]

Indexed keywords

ADULT; ANIMAL TISSUE; ARTICLE; CELL FUSION; CLADISTICS; CONTROLLED STUDY; ENVELOPE GENE; EX VIVO STUDY; EXPRESSION VECTOR; FEMALE; FETOPLACENTAL UNIT; GENOME; ICTIDOMYS TRIDECEMLINEATUS; IN SITU HYBRIDIZATION; MOLECULAR CLONING; NONHUMAN; NUCLEOTIDE SEQUENCE; PRIORITY JOURNAL; REPRODUCTION; REVERSE TRANSCRIPTION POLYMERASE CHAIN REACTION; SCIURIDAE; SEQUENCE ANALYSIS; SYNCYTIN MAR1 GENE; SYNCYTIOTROPHOBLAST; SYNCYTIUM; TROPHOBLAST; WOODCHUCK;

ANIMALS; CONSERVED SEQUENCE; ENDOGENOUS RETROVIRUSES; FEMALE; GENE EXPRESSION PROFILING; GENE PRODUCTS, ENV; IN SITU HYBRIDIZATION; MOLECULAR SEQUENCE DATA; PLACENTATION; PREGNANCY; PREGNANCY PROTEINS; REAL-TIME POLYMERASE CHAIN REACTION; SCIURIDAE; SEQUENCE ANALYSIS, DNA;

EID: 84904701748     PISSN: 0022538X     EISSN: 10985514     Source Type: Journal    
DOI: 10.1128/JVI.00141-14     Document Type: Article

References (38)

1. Black S, Arnaud F, Palmarini M, Spencer T. 2010. Endogenous retroviruses in trophoblast differentiation and placental development. Am. J. Reprod. Immunol. 64:255-264. http://dx.doi.org/10.1111/j.1600-0897.2010.00860.x.
2. Dupressoir A, Lavialle C, Heidmann T. 2012. From ancestral infectious retroviruses to bona fide cellular genes: role of the captured syncytins in placentation. Placenta 33:663-671. http://dx.doi.org/10.1016/j.placenta.2012.05.005.
3. Lavialle C, Cornelis G, Dupressoir A, Esnault C, Heidmann O, Vernochet C, Heidmann T. 2013. Paleovirology of 'syncytins,' retroviral env genes exapted for a role in placentation. Philos. Trans. R. Soc. Lond. B Biol. Sci. 368:20120507. http://dx.doi.org/10.1098/rstb.2012.0507.
4. 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. http://dx.doi.org/10.1128/JVI.74.7.3321-3329.2000.
5. Mi S, Lee X, Li X, Veldman G, Finnerty H, Racie L, LaVallie E, Tang X, Edouard P, Howes S, Keith JJ, McCoy J. 2000. Syncytin is a captive retroviral envelope protein involved in human placental morphogenesis. Nature 17:785-789.
6. Blaise S, de Parseval N, Bénit 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. U. S. A. 100: 13013-13018. http://dx.doi.org/10.1073/pnas.2132646100.
7. Blaise S, Ruggieri A, Dewannieux M, Cosset F-L, Heidmann T. 2004. Identification of an envelope protein from the FRD family of human endogenous retroviruses (HERV-FRD) conferring infectivity on retroviral particles and functional conservation among simians. J. Virol. 78:1050-1054. http://dx.doi.org/10.1128/JVI.78.2.1050-1054.2004.
8. Dupressoir A, Marceau G, Vernochet C, Bénit 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. U. S. A. 102:725-730. http://dx.doi.org/10.1073/pnas.0406509102.
9. Heidmann O, Vernochet C, Dupressoir A, Heidmann T. 2009. 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 27:107. http://dx.doi.org/10.1186/1742-4690-6-107.
10. Cornelis G, Heidmann O, Bernard-Stoecklin S, Reynaud K, Véron G, Mulot B, Dupressoir A, Heidmann T. 2012. 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. 109:E432-E441. http://dx.doi.org/10.1073/pnas.1115346109.
11. Cornelis G, Heidmann O, Degrelle S, Vernochet C, Lavialle C, Letzelter C, Bernard-Stoecklin S, Hassanin A, Mulot B, Guillomot M, Hue I, Heidmann T, Dupressoir A. 2013. Captured retroviral envelope syncytin gene associated with the unique placental structure of higher ruminants. Proc. Natl. Acad. Sci. U. S. A. 110:E828-E837. http://dx.doi.org/10.1073 /pnas.1215787110.
12. 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. U. S. A. 104:20534-20539. http://dx.doi.org/10.1073/pnas.0707873105.
13. 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. U. S. A. 106:12127-12132. http://dx.doi.org/10.1073/pnas.0902925106.
14. Dupressoir A, Vernochet C, Harper F, Guégan J, Dessen P, Pierron G, Heidmann T. 2011. A pair of co-opted retroviral envelope syncytin genes is required for formation of the two-layered murine placental syncytiotrophoblast. Proc. Natl. Acad. Sci. U. S. A. 108:1164-1173. http://dx.doi.org /10.1073/pnas.1012185108.
15. Vernochet C, Heidmann O, Dupressoir A, Cornelis G, Dessen P, Catzeflis F, Heidmann T. 2011. 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. http: //dx.doi.org/10.1016/j.placenta.2011.08.006.
16. Nakaya Y, Koshi K, Nakagawa S, Hashizume K, Miyazawa T. 2013. Fematrin-1 is involved in fetomaternal cell-to-cell fusion in Bovinae placenta and contributed to diversity of ruminant placentation. J. Virol. 87: 10563-10572. http://dx.doi.org/10.1128/JVI.01398-13.
17. Dunlap KA, Palmarini M, Varela M, Burghardt RC, Hayashi K, Farmer JL, Spencer TE. 2006. Endogenous retroviruses regulate periimplantation placental growth and differentiation. Proc. Natl. Acad. Sci. U. S. A. 103:14390-14395. http://dx.doi.org/10.1073/pnas.0603836103.
18. Stamatakis A. 2006. RAxML-VI-HPC: maximum likelihood-based phylogenetic analyses with thousands of taxa and mixed models. Bioinformatics 22:2688-2690. http://dx.doi.org/10.1093/bioinformatics/btl446.
19. Yang Z. 2007. PAML 4: phylogenetic analysis by maximum likelihood. Mol. Biol. Evol. 24:1586-1591. http://dx.doi.org/10.1093/molbev/msm088.
20. Schwartz S, Zhang Z, Frazer K, Smit A, Riemer C, Bouck J, Gibbs R, Hardison R, Miller W. 2000. PipMaker-A web server for aligning two genomic DNA sequences. Genome Res. 10:577-586. http://dx.doi.org/10.1101/gr.10.4.577.
21. de Parseval N, Lazar V, Bénit L, Casella J, Heidmann T. 2003. Survey of human genes of retroviral origin: identification and transcriptome of the genes with coding capacity for complete envelope proteins. J. Virol. 77: 10414-10422. http://dx.doi.org/10.1128/JVI.77.19.10414-10422.2003.
22. Lavillette D, Marin M, Ruggieri A, Mallet F, Cosset FL, Kabat D. 2002. The envelope glycoprotein of human endogenous retrovirus typeWuses a divergent family of amino acid transporters/cell surface receptors. J. Virol. 76:6442-6452. http://dx.doi.org/10.1128/JVI.76.13.6442-6452.2002.
23. Swanstrom R, Wills JW. 1997. Synthesis, assembly, and processing of viral proteins, p 263-334. In Coffin JM, Hughes SH, Varmus HE (ed), Retroviruses. Cold Spring Harbor Laboratory Press, New York, NY.
24. Vogt VM. 1997. Retroviral virions and genome, p 27-69. In Coffin JM, Hughes CL, Varmus HE (ed), Retroviruses. Cold Spring Harbor Laboratory Press, New York, NY.
25. Steppan S, Kenagy G, Zawadzki C, Robles R, Lyapunova E, Hoffmann R. 2011. Molecular data resolve placement of the Olympic marmot and estimate dates of trans-Beringian interchange. J. Mammal. 92:1028-1037. http://dx.doi.org/10.1644/10-MAMM-A-272.1.
26. Esnault C, Priet S, Ribet D, Vernochet C, Bruls T, Lavialle C, Weissenbach J, Heidmann T. 2008. A placenta-specific receptor for the fusogenic, endogenous retrovirus-derived, human syncytin-2. Proc. Natl. Acad. Sci. U. S. A. 105:17532-17537. http://dx.doi.org/10.1073/pnas.0807413105.
27. Mossman H, Weisfeldt L. 1939. The fetal membranes of a primitive rodent, the thirteen-striped ground squirrel. Am. J. Anat. 64:59-109. http: //dx.doi.org/10.1002/aja.1000640104.
28. Enders AC, Carter AM. 2004. What can comparative studies of placental structure tell us? A review. Placenta 25(Suppl A):S3-S9. http://dx.doi.org /10.1016/j.placenta.2004.01.011.
29. Mercer J, Roth L. 2003. The effects of cenozoic global change on squirrel phylogeny. Science 299:1568-1572. http://dx.doi.org/10.1126/science.1079705.
30. Steppan S, Storz B, Hoffmann R. 2004. Nuclear DNA phylogeny of the squirrels (Mammalia: Rodentia) and the evolution of arboreality from c-myc and RAG1. Mol. Phylogenet. Evol. 30:703-719. http://dx.doi.org /10.1016/S1055-7903(03)00204-5.
31. Fabre P, Hautier L, Dimitrov D, Douzery E. 2012. A glimpse on the pattern of rodent diversification: a phylogenetic approach. BMC Evol. Biol. 12:88. http://dx.doi.org/10.1186/1471-2148-12-88.
32. Nei M, Gojobori T. 1986. Simple methods for estimating the numbers of synonymous and nonsynonymous nucleotide substitutions. Mol. Biol. Evol. 3:418-426.
33. Kosakovsky Pond S, Frost S. 2005. Not so different after all: a comparison of methods for detecting amino acid sites under selection. Mol. Biol. Evol. 22:1208-1222. http://dx.doi.org/10.1093/molbev/msi105.
34. Leiser R, Kaufmann P. 1994. Placental structure: in a comparative aspect. Exp. Clin. Endocrinol. 102:122-134. http://dx.doi.org/10.1055 /s-0029-1211275.
35. Wooding P, Burton GJ. 2008. Comparative placentation: structures, functions, and evolution. Springer-Verlag, Berlin, Germany.
36. Meredith R, Janečka J, Gatesy J, Ryder OA, Fisher CA, Teeling EC, Goodbla A, Eizirik E, Simão TL, Stadler T, Rabosky DL, Honeycutt RL, Flynn JJ, Ingram CM, Steiner C, Williams TL, Robinson TJ, Burk-Herrick A, Westerman M, Ayoub NA, Springer MS, Murphy WJ. 2011. Impacts of the cretaceous terrestrial revolution and KPg extinction on mammal diversification. Science 334:521-524. http://dx.doi.org/10.1126/science.1211028.
37. Blanga-Kanfi S, Miranda H, Penn O, Pupko T, DeBry R, Huchon D. 2009. Rodent phylogeny revised: analysis of six nuclear genes from all major rodent clades. BMC Evol. Biol. 9:71. http://dx.doi.org/10.1186 /1471-2148-9-71.
38. Montgelard C, Forty E, Arnal V, Matthee C. 2008. Suprafamilial relationships among Rodentia and the phylogenetic effect of removing fastevolving nucleotides in mitochondrial, exon and intron fragments. BMC Evol. Biol. 8:321. http://dx.doi.org/10.1186/1471-2148-8-321.