Retroviral envelope gene captures and syncytin exaptation for placentation in marsupials

Proceedings of the National Academy of Sciences of the United States of America

Volumn 112, Issue 5, 2015, Pages E487-E496

  Cornelis, Guillaume ^a,b,c   Vernochet, Cécile ^a,b   Carradec, Quentin ^a,b   Souquere, Sylvie ^a,b   Mulot, Baptiste ^d   Catzeflis, François ^e   Nilsson, Maria A ^f   Menzies, Brandon R ^g   Renfree, Marilyn B ^g   Pierron, Gérard ^a,b   Zeller, Ulrich ^h   Heidmann, Odile ^a,b   Dupressoir, Anne ^a,b   Heidmann, Thierry ^a,b  

^a Institut Gustave Roussy   (France)

^b UNIVERSITÉ PARIS SACLAY   (France)

^c UNIVERSITÉ PARIS DESCARTES   (France)

^d ZooParc de Beauval   (France)

^e UNIV MONTPELLIER   (France)

^f BIODIVERSITY AND CLIMATE RESEARCH CENTRE BIK F   (Germany)

^g UNIVERSITY OF MELBOURNE   (Australia)

^h HUMBOLDT UNIVERSITY   (Germany)

Author keywords

Endogenous retrovirus; Envelope protein; Fusogenic activity; Marsupials; Syncytiotrophoblast

Indexed keywords

SYNCYTIN; UNCLASSIFIED DRUG; VIRUS PROTEIN; PLACENTA PROTEIN; VIRUS ENVELOPE PROTEIN;

ARTICLE; CELL FUSION; CONSERVATION GENETICS; CONTROLLED STUDY; ENVELOPE GENE; EX VIVO STUDY; MARSUPIAL; NONHUMAN; NUCLEOTIDE SEQUENCE; OPOSSUM; PLACENTA; PLACENTAL MAMMALS; PRIORITY JOURNAL; PROTEIN ANALYSIS; PROTEIN EXPRESSION; PURIFYING SELECTION; REPRODUCTION; RETROVIRUS; SOUTH AMERICAN; UTERUS; VIRUS PARTICLE; ANIMAL; CLASSIFICATION; FEMALE; GENE EXPRESSION PROFILING; GENETIC TRANSCRIPTION; GENETICS; IN SITU HYBRIDIZATION; MOLECULAR GENETICS; PHYLOGENY; PHYSIOLOGY; PREGNANCY; RETROVIRIDAE;

DIDELPHIDAE; DIDELPHIMORPHIA; EUTHERIA; MACROPUS EUGENII; MAMMALIA; METATHERIA; MONODELPHIS; MYA;

ANIMALS; FEMALE; GENE EXPRESSION PROFILING; GENE PRODUCTS, ENV; GENES, ENV; IN SITU HYBRIDIZATION; MARSUPIALIA; MOLECULAR SEQUENCE DATA; PHYLOGENY; PLACENTA; PREGNANCY; PREGNANCY PROTEINS; RETROVIRIDAE; TRANSCRIPTION, GENETIC; VIRAL ENVELOPE PROTEINS;

EID: 84922309125     PISSN: 00278424     EISSN: 10916490     Source Type: Journal    
DOI: 10.1073/pnas.1417000112     Document Type: Article

References (40)

1. Meredith RW, et al. (2011) Impacts of the Cretaceous Terrestrial Revolution and KPg extinction on mammal diversification. Science 334(6055):521-524.
2. Luo Z-X, Yuan C-X, Meng Q-J, Ji Q (2011) A Jurassic eutherian mammal and divergence of marsupials and placentals. Nature 476(7361):442-445.
3. Freyer C, Zeller U, Renfree MB (2003) The marsupial placenta: A phylogenetic analysis. J Exp Zoolog A Comp Exp Biol 299(1):59-77.
4. 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(9):663-671.
5. Lavialle C, et al. (2013) Paleovirology of 'syncytins', retroviral env genes exapted for a role in placentation. Philos Trans R Soc Lond B Biol Sci 368(1626):20120507.
6. Blond JL, et al. (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(7):3321-3329.
7. Mi S, et al. (2000) Syncytin is a captive retroviral envelope protein involved in human placental morphogenesis. Nature 403(6771):785-789.
8. Mallet F, et al. (2004) The endogenous retroviral locus ERVWE1 is a bona fide gene involved in hominoid placental physiology. Proc Natl Acad Sci USA 101(6):1731-1736.
9. Cáceres M, Thomas JW; NISC Comparative Sequencing Program (2006) The gene of retroviral origin Syncytin 1 is specific to hominoids and is inactive in Old World monkeys. J Hered 97(2):100-106.
10. 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 USA 100(22):13013-13018.
11. 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 (HERVFRD) conferring infectivity and functional conservation among simians. J Virol 78(2): 1050-1054.
12. Mangeney M, et al. (2007) Placental syncytins: Genetic disjunction between the fusogenic and immunosuppressive activity of retroviral envelope proteins. Proc Natl Acad Sci USA 104(51):20534-20539.
13. Dupressoir A, et al. (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(3):725-730.
14. Vernochet C, et al. (2014) The captured retroviral envelope Syncytin-A and Syncytin-B genes are conserved in the Spalacidae together with hemotrichorial placentation. Biol Reprod, 10.1095/biolreprod.114.124818.
15. Dupressoir A, et al. (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(29):12127-12132.
16. Dupressoir A, et al. (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 USA 108(46):E1164-E1173.
17. 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 6:107.
18. Cornelis G, et al. (2012) Ancestral capture of syncytin-Car1, a fusogenic endogenous retroviral envelope gene involved in placentation and conserved in Carnivora. Proc Natl Acad Sci USA 109(7):E432-E441.
19. Cornelis G, et al. (2013) Captured retroviral envelope syncytin gene associated with the unique placental structure of higher ruminants. Proc Natl Acad Sci USA 110(9): E828-E837.
20. Cornelis G, et al. (2014) Retroviral envelope syncytin capture in an ancestrally diverged mammalian clade for placentation in the primitive Afrotherian tenrecs. Proc Natl Acad Sci USA 111(41):E4332-E4341.
21. Dunlap KA, et al. (2006) Endogenous retroviruses regulate periimplantation placental growth and differentiation. Proc Natl Acad Sci USA 103(39):14390-14395.
22. Zeller U, Freyer C (2001) Early ontogeny and placentation of the grey short ? tailed opossum, Monodelphis domestica (Didelphidae: Marsupialia): Contribution to the reconstruction of the marsupial morphotype. J Zoological Syst Evol Res 39(3):137-158.
23. Yang Z (2007) PAML 4: Phylogenetic analysis by maximum likelihood. Mol Biol Evol 24(8):1586-1591.
24. Kosakovsky Pond SL, Frost SDW (2005) Not so different after all: A comparison of methods for detecting amino acid sites under selection. Mol Biol Evol 22(5): 1208-1222.
25. Hervé CA, Forrest G, Löwer R, Griffiths DJ, Venables PJW (2004) Conservation and loss of the ERV3 open reading frame in primates. Genomics 83(5):940-943.
26. Kato N, et al. (1987) Tissue-specific expression of human provirus ERV3 mRNA in human placenta: Two of the three ERV3 mRNAs contain human cellular sequences. J Virol 61(7):2182-2191.
27. Boyd MT, Bax CM, Bax BE, Bloxam DL, Weiss RA (1993) The human endogenous retrovirus ERV-3 is upregulated in differentiating placental trophoblast cells. Virology 196(2):905-909.
28. Venables PJ, 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(2):589-592.
29. 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(4):3442-3445.
30. Esnault C, Cornelis G, Heidmann O, Heidmann T (2013) Differential evolutionary fate of an ancestral primate endogenous retrovirus envelope gene, the EnvV syncytin, captured for a function in placentation. PLoS Genet 9(3):e1003400.
31. Freyer C, Zeller U, Renfree MB (2002) Ultrastructure of the placenta of the tammar wallaby, Macropus eugenii: Comparison with the grey short-tailed opossum, Monodelphis domestica. J Anat 201(2):101-119.
32. Harris JR (1998) Placental endogenous retrovirus (ERV): Structural, functional, and evolutionary significance. BioEssays 20(4):307-316.
33. Black SG, et al. (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(18):9078-9085.
34. Chessa B, et al. (2009) Revealing the history of sheep domestication using retrovirus integrations. Science 324(5926):532-536.
35. Palmarini M, et al. (2001) Expression of endogenous betaretroviruses in the ovine uterus: Effects of neonatal age, estrous cycle, pregnancy, and progesterone. J Virol 75(23):11319-11327.
36. Stamatakis A (2006) RAxML-VI-HPC: Maximum likelihood-based phylogenetic analyses with thousands of taxa and mixed models. Bioinformatics 22(21):2688-2690.
37. Bininda-Emonds ORP, et al. (2007) The delayed rise of present-day mammals. Nature 446(7135):507-512.
38. Nilsson MA, et al. (2010) Tracking marsupial evolution using archaic genomic retroposon insertions. PLoS Biol 8(7):e1000436.
39. de A Carvalho B, et al. (2011) Phylogenetic relationships and phylogeographic patterns in Monodelphis (Didelphimorphia: Didelphidae). J Mammal 92(1):121-133.
40. Solari S (2010) A molecular perspective on the diversification of short-tailed opossums. Mastozoología Neotropical 17(2):317-333.