Transposable element recruitments in the mammalian placenta: Impacts and mechanisms

Briefings in Functional Genomics

Volumn 11, Issue 4, 2012, Pages 267-276

  Emera, Deena ^a   Wagner, Günter P ^b  

^a YALE UNIVERSITY SCHOOL OF MEDICINE   (United States)

^b YALE UNIVERSITY   (United States)

Author keywords

Placental evolution; Prolactin; Regulatory evolution; Syncytin; Transposable elements

Indexed keywords

CD8 ANTIGEN; CYCLIC AMP; PROLACTIN;

ARTICLE; CELL DIFFERENTIATION; CELL LEVEL; ENDOMETRIUM CELL; ENVELOPE GENE; GENE EXPRESSION; GENE FUNCTION; GENE REGULATORY NETWORK; GENE STRUCTURE; LIFE CYCLE; MAMMAL; MOLECULAR EVOLUTION; NONHUMAN; PLACENTA; PROTEIN EXPRESSION; RETROPOSON; SIGNAL TRANSDUCTION; TRANSPOSON; TROPHOBLAST;

ANIMALS; DNA TRANSPOSABLE ELEMENTS; ENDOMETRIUM; EPISTASIS, GENETIC; FEMALE; GENOME; HUMANS; MALE; MICE; MODELS, BIOLOGICAL; PHENOTYPE; PHYLOGENY; PLACENTA; PREGNANCY; PROLACTIN; PROMOTER REGIONS, GENETIC; RETROELEMENTS; SHEEP;

EID: 84863918449     PISSN: 20412649     EISSN: 20412657     Source Type: Journal    
DOI: 10.1093/bfgp/els013     Document Type: Article

References (57)

1. Feschotte C. Opinion: transposable elements and the evolution of regulatory networks. Nat Rev Genet 2008;9: 397-05.
2. Mossman HW. Comparative morphogenesis of the fetal membranes and accessory uterine structures. Contrib Embryol 1937;26:133-37.
3. Wooding P, Burton G. Comparative Placentation: Structures, Functions and Evolution. Berlin: Springer, 2008.
4. Harris JR. Placental endogenous retrovirus (ERV): structural, functional, and evolutionary significance. Bioessays 1998;20:307-16.
5. Lynch VJ, Leclerc RD, May G, et al. Transposon-mediated rewiring of gene regulatory networks contributed to the evolution of pregnancy in mammals. Nat Genet 2011;43: 1154-59.
6. Muir A, Lever A, Moffett A. Expression and functions of human endogenous retroviruses in the placenta: an update. Placenta 2004;25:S16-25.
7. Sugimoto J, Schust DJ. Human endogenous retroviruses and the placenta. Reprod Sci 2009;16:1023-33.
8. Schulte AM, Wellstein A. Structure and phylogenetic analysis of an endogenous retrovirus inserted into the human growth factor gene pleiotrophin. JVirol 1998;72:6065-72.
9. Bi S, Gavrilova O, Gong DW, et al. Identification of a placental enhancer for the human leptin gene. J Biol Chem 1997;272:30583-88.
10. Bieche I, Laurent A, Laurendeau I, et al. Placenta-specific INSL4 expression is mediated by a human endogenous retrovirus element. Biol Reprod 2003;68:1422-29.
11. Volff JN. Turning junk into gold: domestication of transposable elements and the creation of new genes in eukaryotes. Bioessays 2006;28:913-22.
12. Barsh GS, Seeburg PH, Gelinas RE. The human growth-hormone gene family: structure and evolution of the chromosomal locus. Nucleic Acids Res 1983;11:3939-58.
13. Haig D. Placental growth hormone-related proteins and prolactin-related proteins. Placenta 2008;29:S36-41.
14. Haig D. Genetic conflicts in human-pregnancy. QRev Biol 1993;68:495-32.
15. Crespi B, Semeniuk C. Parent-offspring conflict in the evolution of vertebrate reproductive mode. Am Nat 2004; 163:635-53.
16. Peaston AE, Evsikov AV, Graber JH, et al. Retrotransposons regulate host genes in mouse oocytes and preimplantation embryos. Dev Cell 2004;7:597-606.
17. Rubin CM, Vandevoort CA, Teplitz RL, et al. Alu repeated DNAs are differentially methylated in primate germ-cells. Nucleic Acids Res 1994;22:5121-27.
18. Slotkin RK, Martienssen R. Transposable elements and the epigenetic regulation of the genome. NatRev Genet 2007;8: 272-85.
19. Renfree MB, Hore TA, Shaw G, et al. Evolution of genomic imprinting: insights from Marsupials and Monotremes. Annu RevGenomicsHum Genet 2009;10:241-62.
20. Ono R, Nakamura K, Inoue K, et al. Deletion of Peg10, an imprinted gene acquired from a retrotransposon, causes early embryonic lethality. Nat Genet 2006;38:101-06.
21. Sekita Y, Wagatsuma H, Nakamura K, et al. Role of retrotransposon-derived imprinted gene, Rtl1, in the feto-maternal interface of mouse placenta. Nat Genet 2008; 40:243-48.
22. Blaise S, de Parseval N, Benit L, et al. Genomewide screening for fusogenic human endogenous retrovirus envelopes identifies syncytin 2, a gene conserved on primate evolution. ProcNatl Acad SciUSA 2003;100:13013-18.
23. Mallet F, Bouton O, Prudhomme S, et al. The endogenous retroviral locus ERVWE1 is a bona fide gene involved in hominoid placental physiology. Proc Natl Acad Sci USA 2004;101:1731-36.
24. Blond JL, Lavillette D, Cheynet V, et al. 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. JVirol 2000;74: 3321-29.
25. Frendo JL, Olivier D, Cheynet V, et al. Direct involvement of HERV-W env glycoprotein in human trophoblast cell fusion and differentiation. Mol Cell Biol 2003;23: 3566-74.
26. Malassine A, Handschuh K, Tsatsaris V, et al. Expression of HERV-W Env glycoprotein (syncytin) in the extravillous trophoblast of first trimester human placenta. Placenta 2005; 26:556-62.
27. Mangeney M, Renard M, Schlecht-Louf G, et al. Placental syncytins: genetic disjunction between the fusogenic and immunosuppressive activity of retroviral envelope proteins. ProcNatl Acad SciUSA 2007;104:20534-39.
28. Dupressoir A, Marceau G, Vernochet C, et al. Syncytin-A and syncytin-B, two fusogenic placenta-specific murine envelope genes of retroviral origin conserved in Muridae. ProcNatl Acad SciUSA 2005;102:725-30.
29. Dupressoir A, Vernochet C, Bawa O, et al. Syncytin- A knockout mice demonstrate the critical role in placentation of a fusogenic, endogenous retrovirus-derived, envelope gene. ProcNatl Acad SciUSA 2009;106:12127-32.
30. Heidmann O, Vernochet C, Dupressoir A, et al. 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;6:107.
31. Vernochet C, Heidmann O, Dupressoir A, et al. A syncytin-like endogenous retrovirus envelope gene of the guinea pig specifically expressed in the placenta junctional zone and conserved in Caviomorpha. Placenta 2011;32: 885-92.
32. Dunlap KA, Palmarini M, Varela M, et al. Endogenous retroviruses regulate periimplantation placental growth and differentiation. ProcNatl Acad SciUSA 2006;103:14390-95.
33. Emera D, Casola C, Lynch VJ, et al. Convergent evolution of endometrial prolactin expression in primates, mice, and elephants through the independent recruitment of transposable elements. Mol Biol Evol 2011 doi: 10.1093/ molbev/msr189.
34. Emera D, Wagner G. Transformation of a transposon into a derived PRL promoter with function during human pregnancy. Proc Natl Acad Sci USA 2012 (In press).
35. Jabbour HN, Critchley HOD. Potential roles of decidual prolactin in early pregnancy. Reproduction 2001;121: 197-205.
36. Bao L, Tessier C, Prigent-Tessier A, et al. Decidual prolactin silences the expression of genes detrimental to pregnancy. Endocrinology 2007;148:2326-34.
37. Gerlo S, Davis JRE, Mager DL, et al. Prolactin in man: a tale of two promoters. Bioessays 2006;28:1051-55.
38. Wallis M. Episodic evolution of protein hormones: molecular evolution of pituitary prolactin. J Mol Evol 2000;50: 465-73.
39. Medstrand P, van de Lagemaat LN, Dunn CA, et al. Impact of transposable elements on the evolution of mammalian gene regulation. Cytogenet GenomeRes 2005;110:342-52.
40. Landry JR, Mager DL. Functional analysis of the endogenous retroviral promoter of the human endothelin B receptor gene. JVirol 2003;77:7459-66.
41. Hambor JE, Mennone J, Coon ME, et al. Identification and characterization of an Alu-containing, T-cell-specific enhancer located in the last intron of the human CD8-alpha gene. Mol Cell Biol 1993;13:7056-70.
42. Ackerman H, Udalova I, Hull J, et al. Evolution of a polymorphic regulatory element in interferon-gamma through transposition and mutation. Mol Biol Evol 2002;19:884-90.
43. Thornburg BG, Gotea V, Makalowski W. Transposable elements as a significant source of transcription regulating signals. Gene 2006;365:104-10.
44. Rebeiz M, Pool JE, Kassner VA, et al. Stepwise modification of a modular enhancer underlies adaptation in a Drosophila population. Science 2009;326:1663-67.
45. Dunn CA, de Lagemaat LNV, Baillie GJ, et al. Endogenous retrovirus long terminal repeats as ready-to-use mobile promoters: the case of primate beta 3GAL-T5. Gene 2005;364: 2-12.
46. Cohen CJ, Lock WM, Mager DL. Endogenous retroviral LTRs as promoters for human genes: a critical assessment. Gene 2009;448:105-14.
47. Fuke C, Shimabukuro M, Petronis A, et al. Age related changes in 5-methylcytosine content in human peripheral leukocytes and placentas: an HPLC-based study. Ann Hum Genet 2004;68:196-204.
48. Novakovic B, Wong NC, Sibson M, et al. DNA methylation-mediated down-regulation of DNA methyltransferase- 1 (DNMT1) is coincident with, but not essential for, global hypomethylation in human placenta. JBiolChem 2010;285:9583-93.
49. Wildman DE. Review: toward an integrated evolutionary understanding of the mammalian placenta. Placenta 2011;32: S142-45.
50. van de Lagemaat LN, Landry JR, Mager DL, et al. Transposable elements in mammals promote regulatory variation and diversification of genes with specialized functions. Trends Genet 2003;19:530-36.
51. Harcourt AH, Harvey PH, Larson SG, et al. Testis weight, body-weight and breeding system in primates. Nature 1981; 293:55-57.
52. Kaessmann H. Origins, evolution, and phenotypic impact of new genes. Genome Res 2010;20:1313-26.
53. Birkhead TR, Pizzari T. Postcopulatory sexual selection. Nat Rev Genet 2002;3:262-73.
54. Bowen R. Placental Structure and Classification. http://www .vivo.colostate.edu/hbooks/pathphys/reprod/placenta/ structure.html (31 March 2012, date last accessed).
55. Benirschke K, Kaufmann P. Functional anatomy of the non-primate placenta. Placenta 1981;(Suppl.1):13-28.
56. Moffett A, Loke C. Immunology of placentation in eutherian mammals. Nat Rev Immunol 2006;6:584-94.
57. Wildman DE, Chen CY, Erez O, et al. Evolution of the mammalian placenta revealed by phylogenetic analysis. ProcNatl Acad SciUSA 2006;103:3203-08.