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Differential Evolutionary Fate of an Ancestral Primate Endogenous Retrovirus Envelope Gene, the EnvV , Captured for a Function in Placentation


Syncytins are envelope genes of retroviral origin that have been co-opted for a role in placentation. They promote cell–cell fusion and are involved in the formation of a syncytium layer—the syncytiotrophoblast—at the materno-fetal interface. They were captured independently in eutherian mammals, and knockout mice demonstrated that they are absolutely required for placenta formation and embryo survival. Here we provide evidence that these “necessary” genes acquired “by chance” have a definite lifetime with diverse fates depending on the animal lineage, being both gained and lost in the course of evolution. Analysis of a retroviral envelope gene, the envV gene, present in primate genomes and belonging to the endogenous retrovirus type V (ERV-V) provirus, shows that this captured gene, which entered the primate lineage >45 million years ago, behaves as a syncytin in Old World monkeys, but lost its canonical fusogenic activity in other primate lineages, including humans. In the Old World monkeys, we show—by in situ analyses and ex vivo assays—that envV is both specifically expressed at the level of the placental syncytiotrophoblast and fusogenic, and that it further displays signs of purifying selection based on analysis of non-synonymous to synonymous substitution rates. We further show that purifying selection still operates in the primate lineages where the gene is no longer fusogenic, indicating that degeneracy of this ancestral syncytin is a slow, lineage-dependent, and multi-step process, in which the fusogenic activity would be the first canonical property of this retroviral envelope gene to be lost.


Vyšlo v časopise: Differential Evolutionary Fate of an Ancestral Primate Endogenous Retrovirus Envelope Gene, the EnvV , Captured for a Function in Placentation. PLoS Genet 9(3): e32767. doi:10.1371/journal.pgen.1003400
Kategorie: Research Article
prolekare.web.journal.doi_sk: https://doi.org/10.1371/journal.pgen.1003400

Souhrn

Syncytins are envelope genes of retroviral origin that have been co-opted for a role in placentation. They promote cell–cell fusion and are involved in the formation of a syncytium layer—the syncytiotrophoblast—at the materno-fetal interface. They were captured independently in eutherian mammals, and knockout mice demonstrated that they are absolutely required for placenta formation and embryo survival. Here we provide evidence that these “necessary” genes acquired “by chance” have a definite lifetime with diverse fates depending on the animal lineage, being both gained and lost in the course of evolution. Analysis of a retroviral envelope gene, the envV gene, present in primate genomes and belonging to the endogenous retrovirus type V (ERV-V) provirus, shows that this captured gene, which entered the primate lineage >45 million years ago, behaves as a syncytin in Old World monkeys, but lost its canonical fusogenic activity in other primate lineages, including humans. In the Old World monkeys, we show—by in situ analyses and ex vivo assays—that envV is both specifically expressed at the level of the placental syncytiotrophoblast and fusogenic, and that it further displays signs of purifying selection based on analysis of non-synonymous to synonymous substitution rates. We further show that purifying selection still operates in the primate lineages where the gene is no longer fusogenic, indicating that degeneracy of this ancestral syncytin is a slow, lineage-dependent, and multi-step process, in which the fusogenic activity would be the first canonical property of this retroviral envelope gene to be lost.


Zdroje

1. BlackSG, ArnaudF, PalmariniM, SpencerTE (2010) Endogenous retroviruses in trophoblast differentiation and placental development. Am J Reprod Immunol 64: 255–264 doi:10.1111/j.1600-0897.2010.00860.x.

2. DupressoirA, LavialleC, HeidmannT (2012) From ancestral infectious retroviruses to bona fide cellular genes: role of the captured syncytins in placentation. Placenta 33: 663–671 doi:10.1016/j.placenta.2012.05.005.

3. MiS, LeeX, LiX, VeldmanG, FinnertyH, et al. (2000) Syncytin is a captive retroviral envelope protein involved in human placental morphogenesis. Nature 17: 785–789 doi:10.1038/35001608.

4. BlondJL, LavilletteD, CheynetV, BoutonO, OriolG, 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: 3321–3329 doi:10.1128/JVI.74.7.3321-3329.2000.

5. MalletF, BoutonO, PrudhommeS, CheynetV, OriolG, et al. (2004) The endogenous retroviral locus ERVWE1 is a bona fide gene involved in hominoid placental physiology. Proc Natl Acad Sci U S A 101: 1731–1736 doi:10.1073/pnas.0305763101.

6. BonnaudB, BeliaeffJ, BoutonO, OriolG, DuretL, et al. (2005) Natural history of the ERVWE1 endogenous retroviral locus. Retrovirology 2: 57 doi:10.1186/1742-4690-2-57.

7. CaceresM, ThomasJW (2006) The gene of retroviral origin Syncytin 1 is specific to hominoids and is inactive in Old World monkeys. J Hered 97: 100–106 doi:10.1093/jhered/esj011.

8. BlaiseS, de ParsevalN, BénitL, HeidmannT (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 doi:10.1073/pnas.2132646100.

9. BlaiseS, RuggieriA, DewannieuxM, CossetF-L, HeidmannT (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 doi:10.1128/JVI.78.2.1050-1054.2004.

10. DupressoirA, MarceauG, VernochetC, BénitL, KanellopoulosC, 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 U S A 102: 725–730 doi:10.1073/pnas.0406509102.

11. HeidmannO, VernochetC, DupressoirA, HeidmannT (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 doi:10.1186/1742-4690-6-107.

12. CornelisG, HeidmannO, Bernard-StoecklinS, ReynaudK, VeronG, 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 U S A 109: E432–441 doi:10.1073/pnas.1115346109.

13. CornelisG, HeidmannO, DegrelleSA, VernochetC, LavialleC, et al. (in press) A captured retroviral envelope syncytin gene associated with the unique placental structure of higher rumunants. Proc Natl Acad Sci U S A In press.

14. FrendoJL, OlivierD, CheynetV, BlondJL, BoutonO, et al. (2003) Direct involvement of HERV-W Env glycoprotein in human trophoblast cell fusion and differentiation. Mol Cell Biol 23: 3566–3574 doi:10.1128/MCB.23.10.3566-3574.2003.

15. MalassineA, HandschuhK, TsatsarisV, GerbaudP, CheynetV, et al. (2005) Expression of HERV-W Env glycoprotein (syncytin) in the extravillous trophoblast of first trimester human placenta. Placenta 26: 556–562 doi:10.1016/j.placenta.2004.09.002.

16. MuirA, LeverAM, MoffettA (2006) Human endogenous retrovirus-W envelope (syncytin) is expressed in both villous and extravillous trophoblast populations. J Gen Virol 87: 2067–2071 doi:10.1099/vir.0.81412-0.

17. MalassineA, BlaiseS, HandschuhK, LalucqueH, DupressoirA, et al. (2007) Expression of the fusogenic HERV-FRD Env glycoprotein (syncytin 2) in human placenta is restricted to villous cytotrophoblastic cells. Placenta 28: 185–191 doi:10.1016/j.placenta.2006.03.001.

18. VargasA, MoreauJ, LandryS, LeBellegoF, ToufailyC, et al. (2009) Syncytin-2 plays an important role in the fusion of human trophoblast cells. J Mol Biol 392: 301–318 doi:10.1016/j.jmb.2009.07.025.

19. MangeneyM, RenardM, Schlecht-LoufG, BouallagaI, HeidmannO, et al. (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 doi:10.1073/pnas.0707873105.

20. DupressoirA, VernochetC, BawaO, HarperF, PierronG, 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 U S A 106: 12127–12132 doi:10.1073/pnas.0902925106.

21. DupressoirA, VernochetC, HarperF, GueganJ, DessenP, 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 U S A 108: E1164–1173 doi:10.1073/pnas.1112304108.

22. de ParsevalN, LazarV, BénitL, CasellaJ, HeidmannT (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 doi:10.1128/JVI.77.19.10414-10422.2003.

23. VillesenP, AagaardL, WiufC, PedersenFS (2004) Identification of endogenous retroviral reading frames in the human genome. Retrovirology 1: 32 doi:10.1186/1742-4690-1-32.

24. BlaiseS, de ParsevalN, HeidmannT (2005) Functional characterization of two newly identified Human Endogenous Retrovirus coding envelope genes. Retrovirology 2: 19 doi:10.1186/1742-4690-2-19.

25. LarssonE, AnderssonAC, NilssonBO (1994) Expression of an endogenous retrovirus (ERV3 HERV-R) in human reproductive and embryonic tissues–evidence for a function for envelope gene products. Ups J Med Sci 99: 113–120.

26. HervéCA, ForrestG, LowerR, GriffithsDJ, VenablesPJ (2004) Conservation and loss of the ERV3 open reading frame in primates. Genomics 83: 940–943 doi:10.1016/j.ygeno.2003.10.003.

27. KjeldbjergAL, VillesenP, AagaardL, PedersenFS (2008) Gene conversion and purifying selection of a placenta-specific ERV-V envelope gene during simian evolution. BMC Evol Biol 8: 266 doi:10.1186/1471-2148-8-266.

28. AagaardL, VillesenP, KjeldbjergAL, PedersenFS (2005) The approximately 30-million-year-old ERVPb1 envelope gene is evolutionarily conserved among hominoids and Old World monkeys. Genomics 86: 685–691 doi:10.1016/j.ygeno.2005.08.011.

29. PerelmanP, JohnsonWE, RoosC, SeuanezHN, HorvathJE, et al. (2011) A molecular phylogeny of living primates. PLoS Genet 7: e1001342 doi:10.1371/journal.pgen.1001342.

30. de ParsevalN, HeidmannT (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: 3442–3445.

31. CossetFL, LavilletteD (2011) Cell entry of enveloped viruses. Adv Genet 73: 121–183 doi:10.1016/B978-0-12-380860-8.00004-5.

32. LeiserR, KaufmannP (1994) Placental structure : in a comparative aspect. Exp Clin Endocrinol 102: 122–134.

33. CarterAM, EndersAC (2004) Comparative aspects of trophoblast development and placentation. Reprod Biol Endocrinol 2: 46 doi:10.1186/1477-7827-2-46.

34. Wooding P, Burton G (2008) Haemochorial Placentation: Mouse, Rabbit, Man, Apes, Monkeys. . In: Springer, editor. Comparative Placentation: Structures, Functions and Evolution. Berlin. pp. 185–230.

35. CarterAM, PijnenborgR (2011) Evolution of invasive placentation with special reference to non-human primates. Best Pract Res Clin Obstet Gynaecol 25: 249–257 doi:10.1016/j.bpobgyn.2010.10.010.

36. EndersAC, BlankenshipTN, FazleabasAT, JonesCJ (2001) Structure of anchoring villi and the trophoblastic shell in the human, baboon and macaque placenta. Placenta 22: 284–303 doi:10.1053/plac.2001.0626.

37. KingBF (1993) Development and structure of the placenta and fetal membranes of nonhuman primates. J Exp Zool 266: 528–540 doi:10.1177/0192623308326095.

38. de RijkE, Van EschE (2008) The macaque placenta-A mini-review. Toxicol Pathol 36: 108S–118S doi:10.1177/0192623308326095.

39. EndersAC, BlankenshipTN (1999) Comparative placental structure. Adv Drug Deliv Rev 38: 3–15 doi:10.1016/S0169-409X(99)00003-4.

40. BlankenshipTN, KingBF (1994) Developmental expression of Ki-67 antigen and proliferating cell nuclear antigen in macaque placentas. Dev Dyn 201: 324–333 doi:10.1002/aja.1002010404.

41. NeiM, GojoboriT (1986) Simple methods for estimating the numbers of synonymous and nonsynonymous nucleotide substitutions. Mol Biol Evol 3: 418–426.

42. YangZ (2007) PAML 4: phylogenetic analysis by maximum likelihood. Mol Biol Evol 24: 1586–1591 doi:10.1093/molbev/msm088.

43. Kosakovsky PondSL, FrostSD (2005) Not so different after all: a comparison of methods for detecting amino acid sites under selection. Mol Biol Evol 22: 1208–1222 doi:10.1093/molbev/msi105.

44. VarelaM, SpencerTE, PalmariniM, ArnaudF (2009) Friendly viruses: the special relationship between endogenous retroviruses and their host. Ann N Y Acad Sci 1178: 157–172 doi:10.1111/j.1749-6632.2009.05002.x.

45. de ParsevalN, CasellaJ, GressinL, HeidmannT (2001) Characterization of the three HERV-H proviruses with an open envelope reading frame encompassing the immunosuppressive domain and evolutionary history in primates. Virology 279: 558–569.

46. WalterMA, SpillettDJ, ThomasP, WeissenbachJ, GoodfellowPN (1994) A method for constructing radiation hybrid maps of whole genomes. Nat Genet 7: 22–28 doi:10.1038/ng0594-22.

47. GouyM, GuindonS, GascuelO (2009) SeaView version 4: A multiplatform graphical user interface for sequence alignment and phylogenetic tree building. Mol Biol Evol 27: 221–224 doi:10.1093/molbev/msp259.

48. StamatakisA (2006) RAxML-VI-HPC: maximum likelihood-based phylogenetic analyses with thousands of taxa and mixed models. Bioinformatics 22: 2688–2690 doi:10.1093/bioinformatics/btl446.

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Genetika Reprodukčná medicína

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