The Phylogeny of Placental Evolution Through Dynamic Integrations of Retrotransposons

Progress in Molecular Biology and Translational Science

Volumn 145, Issue , 2017, Pages 89-109

  Imakawa, K ^a   Nakagawa, S ^b  

^a UNIVERSITY OF TOKYO   (Japan)

^b TOKAI UNIVERSITY SCHOOL OF MEDICINE   (Japan)

Author keywords

Baton pass; Diversity; Evolution; Mammals; Placenta; Retrotransposon

Indexed keywords

FEMATRIN 1; INTERFERON; PATERNALLY EXPRESSED 10; PATERNALLY EXPRESSED 11; PLACENTA PROTEIN; RUM1 PROTEIN; SUSHI ICHI RETROTRANSPOSON HOMOLOG 7; SYNCYTIN 1; SYNCYTIN 2; SYNCYTIN A; SYNCYTIN B; UNCLASSIFIED DRUG; RETROPOSON;

CELL FUSION; CLASSIFICATION; ENDOGENOUS RETROVIRUS; GENE LOCUS; GENETIC VARIABILITY; GENOME ANALYSIS; HUMAN; MOLECULAR DYNAMICS; MOLECULAR EVOLUTION; MOLECULAR PHYLOGENY; MULTIGENE FAMILY; NONHUMAN; PLACENTA; PLACENTA DEVELOPMENT; PLACENTA FUNCTION; PROTEIN FAMILY; RETROPOSON; RETROVIRUS INFECTION; RUMINANT; STRUCTURE ANALYSIS; SYNCYTIOTROPHOBLAST; TRANSCRIPTION INITIATION; TRANSCRIPTION REGULATION; VIRUS GENE; ANIMAL; CYTOLOGY; FEMALE; GENETICS; METABOLISM; PHYLOGENY; PREGNANCY; TROPHOBLAST; VIROLOGY;

ANIMALS; ENDOGENOUS RETROVIRUSES; EVOLUTION, MOLECULAR; FEMALE; PHYLOGENY; PLACENTA; PREGNANCY; RETROELEMENTS; TROPHOBLASTS;

EID: 85009495787     PISSN: 18771173     EISSN: 18780814     Source Type: Book Series    
DOI: 10.1016/bs.pmbts.2016.12.004     Document Type: Chapter

References (75)

1. 1 Mess, A., Carter, A.M., Evolutionary transformations of fetal membrane characters in Eutheria with special reference to Afrotheria. J Exp Zool B Mol Dev Evol 306 (2006), 140–163.
2. 2 Mess, A., Evolutionary transformations of chorioallantoic placental characters in rodentia with special reference to hystricognath species. J Exp Zool A Comp Exp Biol 299 (2003), 78–98.
3. 3 Carter, A.M., Enders, A.C., Comparative aspects of trophoblast development and placentation. Reprod Biol Endocrinol, 2, 2004, 46.
4. 4 Wildman, D.E., Chen, C., Erez, O., Grossman, L.I., Goodman, R.R., Evolution of the mammalian placenta revealed by phylogenetic analysis. Proc Natl Acad Sci USA 103 (2006), 3203–3208.
5. 5 Enders, A.C., Blankenship, T.N., Conley, A.J., Jones, C.J., Structure of the midterm placenta of the spotted hyena, Crocuta crocuta, with emphasis on the diverse hemophagous regions. Cells Tissues Organs 183 (2006), 141–155.
6. 6 Lavialle, C., Cornelis, G., Dupressoir, A., et al. Paleovirology of ‘syncytins’, retroviral env genes exapted for a role in placentation. Philos Trans R Soc Lond B Biol Sci, 368, 2013, 20120507.
7. 7 dos Reis, M., Inoue, J., Hasegawa, M., Asher, R.J., Donoghue, P.C., Yang, Z., Phylogenomic data sets provide both precision and accuracy in estimating the timescale of placental mammal evolution. Proc R Soc Lond B Biol Sci 279 (2012), 3491–3500.
8. 8 Imakawa, K., Nakagawa, S., Miyazawa, T., Baton pass hypothesis: successive incorporation of unconserved endogenous retroviral genes for placentation during mammalian evolution. Genes Cells 20 (2015), 771–788.
9. 9 Rezende, L.C., Barbeito, C.G., Favaron, P.O., Mess, A., Miglino, M.A., The fetomaternal interface in the placenta of three species of armadillos (Eutheria, Xenarthra, Dasypodidae). Reprod Biol Endocrinol, 10, 2012, 38.
10. 10 Carter, A.M., Mess, A., Evolution of the placenta and associated reproductive characters in bats. J Exp Zool Part B Mol Develop Evol 310B (2008), 428–449.
11. 11 Bischof, P., Irminger-Finger, I., The human cytotrophoblastic cell, a mononuclear chameleon. Int J Biochem Cell Biol 37 (2005), 1–16.
12. 12 Moffett, A., Loke, C., Immunology of placentation in eutherian mammals. Nat Rev Immunol 6 (2006), 584–594.
13. 13 Bhiwgade, D.A., Singh, A.B., Manekar, A.P., Menon, S.N., Ultrastructural development of chorioallantoic placenta in the Indian Miniopterus bat, Miniopterus schreibersii fuliginosus (Hodgson). Acta Anat (Basel) 145 (1992), 248–264.
14. 14 Pfarrer, C., Winther, H., Leiser, R., Dantzer, V., The development of the endotheliochorial mink placenta: light microscopy and scanning electron microscopical morphometry of maternal vascular casts. Anat Embryol (Berl) 199 (1999), 63–74.
15. 15 Wooding, F.B., Role of binucleate cells in fetomaternal cell fusion at implantation in the sheep. Am J Anat 170 (1984), 233–250.
16. 16 Hoffman, L.H., Wooding, F.B., Giant and binucleate trophoblast cells of mammals. J Exp Zool 266 (1993), 559–577.
17. 17 King, B.F., Mossman, H.W., The fetal membranes and unusual giant cell placenta of the jerboa (Jaculus) and jumping mouse (Zapus). Am J Anat 140 (1974), 405–431.
18. 18 Oduor-Okelo, D., Musewe, V.O., Gombe, S., Electron microscopic study of the chorioallantoic placenta of the rock hyrax (Heterohyrax brucei). J Reprod Fertil 68 (1983), 311–318.
19. 19 Carter, A.M., Blankenship, T.N., Künzle, H., Enders, A.C., Structure of the definitive placenta of the tenrec, Echinops telfairi. Placenta 25 (2004), 218–232.
20. 20 Huppertz, B., Kaufmann, P., Kingdom, J., Trophoblast turnover in health and disease. Fetal Matern Med Rev 13 (2002), 103–118.
21. 21 Lander, E.S., Linton, L.M., Birren, B., et al. Initial sequencing and analysis of the human genome. Nature 409 (2001), 860–921.
22. 22 Chinwalla, A.T., Cook, L.L., Delehaunty, K.D., et al. Initial sequencing and comparative analysis of the mouse genome. Nature 429 (2002), 520–562.
23. 23 Luo, Z.X., Yuan, C.X., Meng, Q.J., Ji, Q., A Jurassic eutherian mammal and divergence of marsupials and placentals. Nature 476 (2011), 442–445.
24. 24 Ono, R., Kobayashi, S., Wagatsuma, H., et al. A retrotransposon-derived gene, PEG10, is a novel imprinted gene located on human chromosome 7q21. Genomics 73 (2001), 232–237.
25. 25 Suzuki, S., Ono, R., Narita, T., et al. Retrotransposon silencing by DNA methylation can drive mammalian genomic imprinting. PLoS Genet, 3, 2007, e55.
26. 26 Ono, R., Nakamura, K., Inoue, K., et al. Deletion of Peg10, an imprinted gene acquired from a retrotransposon, causes early embryonic lethality. Nat Genet 38 (2006), 101–106.
27. 27 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 40 (2008), 243–248.
28. 28 Naruse, M., Ono, R., Irie, M., et al. Sirh7/Ldoc1 knockout mice exhibit placental P4 overproduction and delayed parturition. Development 141 (2014), 4763–4771.
29. 29 Dupressoir, A., Lavialle, C., Heidmann, T., From ancestral infectious retroviruses to bona fide cellular genes: role of the captured syncytins in placentation. Placenta 33 (2012), 663–671.
30. 30 de Parseval, N., Lazar, V., Casella, J.F., Benit, L., Heidmann, T., Survey of human genes of retroviral origin: identification and transcriptome of the genes with coding capacity for complete envelop protein. J Virol 77 (2003), 10414–10422.
31. 31 Blaise, S., de Parseval, N., Heidmann, T., Functional characterization of two newly identified human endogenous retroviruses coding envelop genes. Retrovirology, 2, 2005, 19.
32. 32 Blaise, S., de Parseval, N., Bénit, L., Heidmann, T., Genomewide screening for fusogenic human endogenous retrovirus envelopes identifies syncytin-2, a gene conserved on primate evolution. Proc Natl Acad Sci USA 100 (2003), 13013–13018.
33. 33 Mi, S., Lee, X., Li, X., et al. Syncytin is a captive envelope protein involved in human placental morphogenesis. Nature 403 (2000), 785–789.
34. 34 Kudaka, W., Oda, T., Jinno, Y., Yoshimi, N., Aoki, Y., Cellular localization of placenta-specific human endogenous retrovirus (HERV) transcripts and their possible implication in pregnancy-induced hypertension. Placenta 29 (2008), 282–289.
35. 35 Chang, C., Chen, P.T., Chang, G.D., Huang, C.J., Chen, H., Functional characterization of the placental fusogenic membrane protein syncytin. Biol Reprod 71 (2004), 1956–1962.
36. 36 Chen, C.P., Chen, L.F., Yang, S.R., et al. Functional characterization of the human placental fusogenic membrane protein syncytin 2. Biol Reprod 79 (2008), 815–823.
37. 37 Yu, C., Shen, K., Lin, M., et al. GCMa regulates the syncytin-mediated trophoblastic fusion. J Biol Chem 277 (2002), 50062–50068.
38. 38 Muroi, Y., Sakurai, T., Hanashi, A., Kubota, K., Nagaoka, K., Imakawa, K., CD9 regulates transcription factor GCM1 and ERVWE1 expression through the cAMP/protein kinase A signaling pathway. Reproduction 138 (2009), 945–951.
39. 39 Tachibana, I., Helmer, M.E., Role of transmembrane 4 superfamily (TM4SF) proteins CD9 and CD81 in muscle cell fusion and myotube maintenance. J Cell Biol 146 (1999), 893–904.
40. 40 Le Naour, F., Rubinstein, E., Jasmin, C., Prenant, M., Boucheix, C., Severely reduced female fertility in CD9-deficient mice. Science 287 (2000), 319–321.
41. 41 Liang, C.Y., Wang, L.J., Chen, C.P., Chen, L.F., Chen, Y.H., Chen, H., GCM1 regulation of the expression of syncytin-2 and its cognate receptor MFSD2A in human placenta. Biol Reprod 83 (2010), 387–395.
42. 42 Okahara, G., Matsubara, S., Oda, T., Sugimoto, J., Jinno, Y., Kanaya, F., Expression analyses of human endogenous retroviruses (HERVs): tissue-specific and dedvelopmental stage-dependent expression of HERVs. Genomics 84 (2004), 982–990.
43. 43 Blond, J.L., 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. J Virol 74 (2000), 3321–3329.
44. 44 Hayward, M.D., Pötgens, A.J., Drewlo, S., Kaufmann, P., Rasko, J.E., Distribution of human endogenous retrovirus type W receptor in normal human villous placenta. Pathology 39 (2007), 406–412.
45. 45 Kudo, Y., Boyd, C.A., Changes in expression and function of syncytin and its receptor, amino acid transport system B (ASCT2), in human placental choriocarcinoma BeWo cells during syncytialization. Placenta 23 (2002), 536–541.
46. 46 Mangeney, M., Renard, M., Schlecht-Louf, G., et al. Placental syncytins: genetic disjunction between the fusogenic and immunosuppressive activity of retroviral envelope proteins. Proc Natl Acad Sci USA 104 (2007), 20534–20539.
47. 47 Cáceres, M., Comparative Sequencing Program, N.I.S.C., Thomas, J.W., The gene of retroviral origin Syncytin 1 is specific to hominoids and is inactive in Old World monkeys. J Hered 97 (2006), 100–106.
48. 48 Pötgens, A.J., Schmitz, U., Bose, P., Versmold, A., Kaufmann, P., Frank, H.G., Mechanisms of syncytial fusion: a review. Placenta 23:suppl A (2002), S107–S113.
49. 49 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. Proc Natl Acad Sci USA 102 (2005), 725–730.
50. 50 Rawn, S.M., Cross, J.C., The evolution, regulation, and function of placenta-specific genes. Annu Rev Cell Dev Biol 24 (2008), 159–181.
51. 51 Dupressoir, A., Vernochet, C., Bawa, O., et al. Syncytin-A knockout mice demonstrate the crucial role in placentation of a fusogenic, endogenous retrovirus-derived, envelop gene. Proc Natl Acad Sci USA 106 (2009), 12127–12132.
52. 52 Schubert, S.W., Lamoureux, N., Kilian, K., Klein-Hitpass, L., Hashemolhosseini, S., Identification of integrin-alpha4, Rb1, and syncytin-A as murine placental target genes of the transcription factor GCMa/Gcm1. J Biol Chem 283 (2008), 5460–5465.
53. 53 Schreiber, J., Riethmacher-Sonnenberg, E., Riethmacher, D., et al. Placental failure in mice lacking the mammalian homolog of glial cells missing, GCMa. Mol Cell Biol 20 (2000), 2466–2474.
54. 54 Baba, K., Nakaya, Y., Shojima, T., et al. Identification of novel endogenous Betaretroviruses which are transcribed in the bovine placenta. J Virol 85 (2011), 1237–1245.
55. 55 Cornelis, G., Heidmann, O., Degrelle, S.A., et al. Captured retroviral envelope syncytin gene associated with the unique placental structure of higher ruminants. Proc Natl Acad Sci USA 110 (2013), E828–837.
56. 56 Nakagawa, S., Bai, H., Sakurai, T., et al. Dynamic evolution of endogenous retrovirus-derived genes expressed in bovine conceptuses during the period of placentation. Genome Biol Evol 5 (2013), 296–306.
57. 57 Palmarini, M., Hallwirth, C., York, D., et al. Molecular cloning and functional analysis of three type D endogenous retroviruses of sheep reveal a different cell tropism from that of the highly related exogenous Jaagsiekte sheep retrovirus. J Virol 74 (2000), 8065–8076.
58. 58 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 87 (2013), 10563–10572.
59. 59 Nakaya, Y., Miyazawa, T., Dysfunction of bovine endogenous retrovirus K2 envelop glycoprotein is related to unsuccessful intracellular trafficking. J Virol 88 (2013), 6896–6905.
60. 60 Katoh, K., Standley, D.M., MAFFT multiple sequence alignment software version 7: improvements in performance and usability. Mol Biol Evol 30 (2013), 772–780.
61. 61 Capella-Gutiérrez, S., Silla-Martínez, J.M., Gabaldón, T., trimAl: a tool for automated alignment trimming in large-scale phylogenetic analyses. Bioinformatics 25 (2009), 1972–1973.
62. 62 Le, S.Q., Gascuel, O., An improved general amino acid replacement matrix. Mol Biol Evol 7 (2008), 1307–1320.
63. 63 Darriba, D., Taboada, G.L., Doallo, R., Posada, D., ProtTest 3: fast selection of best-fit models of protein evolution. Bioinformatics 27 (2011), 1164–1165.
64. 64 Stamatakis, A., RAxML version 8: a tool for phylogenetic analysis and post-analysis of large phylogenies. Bioinformatics 30 (2014), 1312–1313.
65. 65 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, 6, 2009, 107.
66. 66 Cornelis, G., Heidmann, O., Bernard-Stoecklin, S., et al. Ancestral capture of syncytin-Car1, a fusogenic endogenous retroviral envelope gene involved in placentation and conserved in Carnivora. Proc Natl Acad Sci USA 109 (2012), E432–441.
67. 67 Redelsperger, F., Cornelis, G., Vernochet, C., et al. Capture of syncytin-Mar1, a fusogenic endogenous retroviral envelope gene involved in placentation in the Rodentia squirrel-related clade. J Virol 88 (2014), 7915–7928.
68. 68 Cornelis, G., Vernochet, C., Malicorne, S., et al. Retroviral envelope syncytin capture in an ancestrally diverged mammalian clade for placentation in the primitive Afrotherian tenrecs. Proc Natl Acad Sci USA 111 (2014), E4332–E4341.
69. 69 Cornelis, G., Vernochet, C., Carradec, Q., et al. Retroviral envelope gene captures and syncytin exaptation for placentation in marsupials. Proc Natl Acad Sci USA 112 (2015), E487–E496.
70. 70 Carter, A.M., Evolution of placental structure and function in ruminants. Juengel, J.L., Miyamoto, A., Price, C., Reynolds, L.P., Smith, M.F., Webb, R., (eds.) Reproduction in Domestic Ruminants VIII, 2014, Context Products Ltd., Leicestershire, UK, 387–398.
71. 71 Nakamura, Y., Imakawa, K., Retroviral endogenization and its role in the genital tract during mammalian evolution. J Mamm Ova Res 28 (2011), 203–218.
72. 72 Esnault, C., Priet, S., Ribet, D., et al. A placenta-specific receptor for the fusogenic, endogenous retrovirus-derived, human syncytin-2. Proc Natl Acad Sci USA 105 (2008), 17532–17537.
73. 73 Dewannieux, M., Heidmann, T., Endogenous retroviruses: acquisition, amplification and taming of genome invaders. Curr Opin Virol 3 (2013), 646–656.
74. 74 Platanias, L.C., Mechanisms of type-I- and type-II-interferon-mediated signaling. Nat Rev Immunol 5 (2005), 375–386.
75. 75 Chuong, E.B., Elde, N.C., Feschotte, C., Regulatory evolution of innate immunity through co-option of endogenous retroviruses. Science 351 (2016), 1083–1087.