Hemochorial placentation: Development, function, and adaptations

Biology of Reproduction

Volumn 99, Issue 1, 2018, Pages 196-211

  Soares, Michael J ^a,b   Varberg, Kaela M ^a   Iqbal, Khursheed ^a  

^a UNIVERSITY OF KANSAS SCHOOL OF MEDICINE   (United States)

^b Institute for Medical Research   (United States)

Author keywords

Hemochorial placentation; Pregnancy; Trophoblast

Indexed keywords

CELL LINEAGE; CELL PLASTICITY; CELL POPULATION; EMBRYONIC STRUCTURES; ENDOCRINE SYSTEM; EVOLUTIONARY ADAPTATION; HEMOCHORIAL PLACENTATION; HUMAN; HUMAN EMBRYONIC STEM CELL; IN VITRO STUDY; MOUSE; MUTAGENESIS; NONHUMAN; PATHOGENESIS; PLACENTA DEVELOPMENT; PLACENTA FUNCTION; PREGNANCY DISORDER; PRIORITY JOURNAL; REVIEW; RODENT; SIGNAL TRANSDUCTION; STEM CELL; SUP-M2-TS CELL LINE; TRANSPOSON; TROPHOBLAST; UTERUS;

EID: 85055284843     PISSN: 00063363     EISSN: 15297268     Source Type: Journal    
DOI: 10.1093/biolre/ioy049     Document Type: Review

References (260)

1. GundlingWE Jr, Wildman DE. A review of inter-and intraspecific variation in the eutherian placenta. Philos Trans R Soc Lond B Biol Sci 2015; 370:20140072.
2. Maltepe E, Fisher SJ. Placenta: the forgotten organ. Annu Rev Cell Dev Biol 2015; 31:523-552.
3. Soncin F, Natale D, Parast MM. Signaling pathways in mouse and human trophoblast differentiation: a comparative review. Cell Mol Life Sci 2015; 72:1291-1302.
4. Burton GJ, Fowden AL, Thornburg KL. Placental origins of chronic disease. Physiol Rev 2016; 96:1509-1565.
5. Roberts RM, Green JA, Schulz LC. The evolution of the placenta. Reproduction 2016; 152:R179-R189.
6. Latos PA, Hemberger M. From the stem of the placental tree: trophoblast stem cells and their progeny. Development 2016; 143:3650-3660.
7. Sibley CP. Treating the dysfunctional placenta. J Endocrinol 2017; 234:R81-R97.
8. Amoroso EC. The evolution of viviparity. Proc R Soc Med 1968; 61:1188-1200.
9. Soares MJ, Varberg KM. Trophoblast. In: Spencer, T, Flaws, J (eds.), Encyclopedia of Reproduction, vol. 2. New York: Elsevier, 2018.
10. Biggers JD, Bell JE, Benos DJ.Mammalian blastocyst: transport functions in a developing epithelium. Am J Physiol 1988; 255:C419-C432.
11. Cockburn K, Rossant J. Making the blastocyst: lessons from the mouse. J Clin Invest 2010; 120:995-1003.
12. Aplin JD, Ruane PT. Embryo-epithelium interactions during implantation at a glance. J Cell Sci 2017; 130:15-22.
13. Gardner RL, Beddington RS. Multi-lineage 'stem' cells in the mammalian embryo. J Cell Sci 1988; 10(Supplement 10):11-27.
14. Rossant J. Stem cells from the mammalian blastocyst. Stem Cells 2001; 19:477-482.
15. Simmons DG, Cross JC. Determinants of trophoblast lineage and cell subtype specification in the mouse placenta. Dev Biol 2005; 284:12-24.
16. Soares MJ, Chakraborty D, Karim Rumi MA, Konno T, Renaud SJ. Rat placentation: an experimental model for investigating the hemochorial maternal-fetal interface. Placenta 2012; 33:233-243.
17. Walentin K, Hinze C, Schmidt-Ott KM. The basal chorionic trophoblast cell layer: an emerging coordinator of placenta development. Bioessays 2016; 38:254-265.
18. Red-Horse K, Zhou Y, Genbacev O, Prakobphol A, Foulk R, Mc-Master M, Fisher SJ. Trophoblast differentiation during embryo implantation and formation of the maternal-fetal interface. J Clin Invest 2004; 114:744-754.
19. Huppertz B. The anatomy of the normal placenta. J Clin Pathol 2008; 61:1296-1302.
20. Velicky P, Knöfler M, Pollheimer J. Function and control of human invasive trophoblast subtypes: intrinsic vs. maternal control. Cell Adh Migr 2016; 10:154-162.
21. James JL, Carter AM, Chamley LW. Human placentation from nidation to 5 weeks of gestation. Part I: What do we know about formative placental development following implantation?Placenta 2012; 33:327-334.
22. Enders AC, Schlafke S. Cytological aspects of trophoblast-uterine interaction in early implantation. Am J Anat 1969; 125:1-29.
23. Schlafke S, Enders AC. Cellular basis of interaction between trophoblast and uterus at implantation. Biol Reprod 1975; 12:41-65.
24. Georgiades P, Ferguson-Smith AC, Burton GJ. Comparative developmental anatomy of the murine and human definitive placentae. Placenta 2002; 23:3-19.
25. Soares MJ, Chakraborty D, Kubota K, Renaud SJ, Rumi MA. Adaptive mechanisms controlling uterine spiral artery remodeling during the establishment of pregnancy. Int J Dev Biol 2014; 58:247-259.
26. Pijnenborg R, Robertson WB, Brosens I, Dixon G. Review article: Trophoblast invasion and the establishment of haemochorial placentation in man and laboratory animals. Placenta 1981; 2:71-91.
27. Pijnenborg R, Vercruysse L, Hanssens M. The uterine spiral arteries in human pregnancy: facts and controversies. Placenta 2006; 27:939-958.
28. Kaufmann P, Black S, Huppertz B. Endovascular trophoblast invasion: implications for the pathogenesis of intrauterine growth retardation and preeclampsia. Biol Reprod 2003; 69:1-7.
29. Damsky CH, Librach C, Lim KH, Fitzgerald ML, McMaster MT, Janatpour M, Zhou Y, Logan SK, Fisher SJ. Integrin switching regulates normal trophoblast invasion. Development 1994; 120:3657-3666.
30. Zhou Y, Fisher SJ, Janatpour M, Genbacev O, Dejana E, Wheelock M, Damsky CH. Human cytotrophoblasts adopt a vascular phenotype as they differentiate. A strategy for successful endovascular invasion?J Clin Invest 1997; 99:2139-2151.
31. Damsky CH, Fisher SJ. Trophoblast pseudo-vasculogenesis: faking it with endothelial adhesion receptors. Curr Opin Cell Biol 1998; 10:660-666.
32. Harris LK. Review: Trophoblast-vascular cell interactions in early pregnancy: how to remodel a vessel. Placenta 2010; 31(Suppl):S93-S98.
33. Ain R, Canham LN, Soares MJ. Gestation stage-dependent intrauterine trophoblast cell invasion in the rat andmouse: novel endocrine phenotype and regulation. Dev Biol 2003; 260:176-190.
34. Pijnenborg R, Vercruysse L. Animal models of deep trophoblast invasion. In: Pijnenborg, R, Brosens, I, Romero, R (eds.), Placental Bed Disorders: Basic Science and its Translation to Obstetrics. Cambridge: Cambridge University Press; 2010:127-139.
35. Soares MJ, Chapman BM, Rasmussen CA, Dai G, Kamei T, Orwig KE. Differentiation of trophoblast endocrine cells. Placenta 1996; 17:277-289.
36. Soares MJ. The prolactin and growth hormone families: pregnancyspecific hormones/cytokines at the maternal-fetal interface. Reprod Biol Endocrinol 2004; 2:51.
37. Costa MA. The endocrine function of human placenta: an overview. Reprod Biomed Online 2016; 32:14-43.
38. Carter AM. Evolution of placental function in mammals: the molecular basis of gas and nutrient transfer, hormone secretion, and immune responses. Physiol Rev 2012; 92:1543-1576.
39. Dilworth MR, Sibley CP. Review: Transport across the placenta of mice and women. Placenta 2013; 34(Suppl):S34-S39.
40. Díaz P, Powell TL, Jansson T. The role of placental nutrient sensing in maternal-fetal resource allocation. Biol Reprod 2014; 91:82.
41. Erlebacher A. Immunology of the maternal-fetal interface. Annu Rev Immunol 2013; 31:387-411.
42. Hakkola J, Pelkonen O, Pasanen M, Raunio H. Xenobiotic-metabolizing cytochrome P450 enzymes in the human feto-placental unit: role in intrauterine toxicity. Crit Rev Toxicol 1998; 28:35-72.
43. Joshi AA, Vaidya SS, St-Pierre MV, Mikheev AM, Desino KE, Nyandege AN, Audus KL, Unadkat JD, Gerk PM. Placental ABC transporters: biological impact and pharmaceutical significance. Pharm Res 2016; 33:2847-2878.
44. Arora N, Sadovsky Y, Dermody TS, Coyne CB. Microbial vertical transmission during human pregnancy. Cell Host Microbe 2017; 21:561-567.
45. van Dijk M, Oudejans C. (Epi)genetics of pregnancy-associated diseases. Front Genet 2013; 4:180.
46. Pisarska MD, Akhlaghpour M, Lee B, Barlow GM, Xu N, Wang ET, Mackey AJ, Farber CR, Rich SS, Rotter JI, Chen YI, Goodarzi MO et al. Optimization of techniques for multiple platform testing in small, precious samples such as human chorionic villus sampling. Prenat Diagn 2016; 36:1061-1070.
47. Imudia AN, Suzuki Y, Kilburn BA, Yelian FD, Diamond MP, Romero R, Armant DR. Retrieval of trophoblast cells from the cervical canal for prediction of abnormal pregnancy: a pilot study. Hum Reprod 2009; 24:2086-2092.
48. Drewlo S, Armant DR. Quo vadis, trophoblast?Exploring the new ways of an old cell lineage. Placenta 2017; 60(Suppl 1):S27-S31.
49. Nelson AC, Mould AW, Bikoff EK, Robertson EJ. Single-cell RNA-seq reveals cell type-specific transcriptional signatures at the maternal-foetal interface during pregnancy. Nat Comms 2016; 7:11414.
50. Gormley M, Ona K, Kapidzic M, Garrido-Gomez T, Zdravkovic T, Fisher SJ. Preeclampsia: novel insights from global RNA profiling of trophoblast subpopulations. Am J Obstet Gynecol 2017; 217:200.e1-200.e17.
51. Pavličev M, Wagner GP, Chavan AR, Owens K, Maziarz J, Dunn-Fletcher C, Kallapur SG, Muglia L, Jones H. Single-cell transcriptomics of the human placenta: inferring the cell communication network of the maternal-fetal interface. Genome Res 2017; 27:349-361.
52. Pattillo RA, Gey GO. The establishment of a cell line of human hormonesynthesizing trophoblastic cells in vitro. Cancer Res 1968; 28:1231-1236.
53. Kohler PO, Bridson WE. Isolation of hormone-producing clonal lines of human choriocarcinoma. J Clin Endocrinol Metab 1971; 32:683-687.
54. Pattillo RA, Ruckert A, Hussa R, Bernstein R, Delfs E. The Jar cell line-continuous human multihormone production and controls. In Vitro 1971; 6:398.
55. Ringler GE. In vitro systems for the study of human placental endocrine function. Endocr Rev 1990; 11:105-123.
56. Graham CH, Hawley TS, Hawley RG, MacDougall JR, Kerbel RS, Khoo N, Lala PK. Establishment and characterization of first trimester human trophoblast cells with extended lifespan. Exp Cell Res 1993; 206:204-211.
57. Choy MY, Manyonda IT. The phagocytic activity of human first trimester extravillous trophoblast. Hum Reprod 1998; 13:2941-2949.
58. Straszewski-Chavez SL, Abrahams VM, Alvero AB, Aldo PB, Ma Y, Guller S, Romero R, Mor G. The isolation and characterization of a novel telomerase immortalized first trimester trophoblast cell line, Swan 7. Placenta 2009; 30:939-948.
59. Sullivan MH. Endocrine cell lines from the placenta. Mol Cell Endocrinol 2004; 22:103-119.
60. Whitley GS. Production of human trophoblast cell lines. Methods Mol Med 2006; 121:219-228.
61. Lee CQ, Gardner L, Turco M, Zhao N, Murray MJ, Coleman N, Rossant J, Hemberger M, Moffett A. What is trophoblast?A combination of criteria define human first-trimester trophoblast. Stem Cell Rep 2016; 6:257-272.
62. Wice B, Menton D, Geuze H, Schwartz AL. Modulators of cyclic AMP metabolism induce syncytiotrophoblast formation in vitro. Exp Cell Res 1990; 186:306-316.
63. Matsuura K, Jigami T, Taniue K, Morishita Y, Adachi S, Senda T, Nonaka A, Aburatani H, Nakamura T, Akiyama T. Identification of a link between Wnt/β-catenin signalling and the cell fusion pathway. Nat Commun 2011; 2:548.
64. Lu J, Zhang S, Nakano H, Simmons DG, Wang S, Kong S, Wang Q, Shen L, Tu Z, Wang W, Wang B, Wang H et al. A positive feedback loop involving Gcm1 and Fzd5 directs chorionic branching morphogenesis in the placenta. PLoS Biol 2013; 11:e1001536.
65. Kliman HJ, Nestler JE, Sermasi E, Sanger JM, Purification, characterization, and in vitro differentiation of cytotrophoblasts from human term placentae. Endocrinology 1986; 118:1567-1582.
66. Thordarson G, Folger P, Talamantes F. Development of a placental cell culture system for studying the control of mouse placental lactogen II secretion. Placenta 1987; 8:573-585.
67. Lu XJ, Deb S, Soares MJ. Spontaneous differentiation of trophoblast cells along the spongiotrophoblast cell pathway: expression of members of the placental prolactin gene family and modulation by retinoic acid. Dev Biol 1994; 163:86-97.
68. Aplin JD. In vitro analysis of trophoblast invasion. Methods Mol Med 2006; 122:45-57.
69. Petroff MG, Phillips TA, Ka H, Pace JL, Hunt JS. Isolation and culture of term human trophoblast cells. Methods Mol Med 2006; 121:203-217.
70. Orendi K, Kivity V, SammarM, Grimpel Y, Gonen R, Meiri H, Lubzens E, Huppertz B. Placental and trophoblastic in vitro models to study preventive and therapeutic agents for preeclampsia. Placenta 2011; 32:S49-S54.
71. Schneider H. The role of the placenta in nutrition of the human fetus. Am J Obstet Gynecol 1991; 164:967-973.
72. Teshima S, Shimosato Y, Koide T, Kuroki M, Kikuchi Y, Aizawa M. Transplantable choriocarcinoma of rats induced by fetectomy and its biological activities. Gan 1983; 74:205-212.
73. Verstuyf A, Sobis H, Goebels J, Fonteyn E, Cassiman JJ, Vandeputte M. Establishment and characterization of a continuousin vitro line from a rat choriocarcinoma. Int J Cancer 1990; 45:752-756.
74. Faria TN, Soares MJ. Trophoblast cell differentiation: establishment, characterization, and modulation of a rat trophoblast cell line expressing members of the placental prolactin family. Endocrinology 1991; 129:2895-2906.
75. Hamlin GP, Lu XJ, Roby KF, Soares MJ. Recapitulation of the pathway for trophoblast giant cell differentiation in vitro: stage-specific expression of members of the prolactin gene family. Endocrinology 1994; 134:2390-2396.
76. Kamei T, Hamlin GP, Chapman BM, Burkhardt AL, Bolen JB, Soares MJ. Signaling pathways controlling trophoblast cell differentiation: src family protein tyrosine kinases in the rat. Biol Reprod 1997; 57:1302-1311.
77. Kamei T, Jones SR, Chapman BM, McGonigle KL, Dai G, Soares MJ. The phosphatidylinositol 3-kinase/Akt signaling pathway modulates the endocrine differentiation of trophoblast cells. Mol Endocrinol 2002; 16:1469-1481.
78. Kent LN, Konno T, SoaresMJ. Phosphatidylinositol 3 kinase modulation of trophoblast cell differentiation. BMC Dev Biol 2010; 10:97.
79. Kent LN, Rumi MA, Kubota K, Lee DS, SoaresMJ. FOSL1 is integral to establishing the maternal-fetal interface. Mol Cell Biol 2011; 31:4801-4813.
80. Kubota K, Kent LN, Rumi MA, Roby KF, Soares MJ. Dynamic regulation of AP-1 transcriptional complexes directs trophoblast differentiation. Mol Cell Biol 2015; 35:3163-3177.
81. Sahgal N, Canham LN, Canham B, SoaresMJ. Rcho-1 trophoblast stem cells: a model system for studying trophoblast cell differentiation. Methods Mol Med 2006; 121:159-178.
82. Tanaka S, Kunath T, Hadjantonakis AK, Nagy A, Rossant J. Promotion of trophoblast stem cell proliferation by FGF4. Science 1998; 282:2072-2075.
83. Chung Y, Klimanskaya I, Becker S, Marh J, Lu SJ, Johnson J, Meisner L, Lanza R. Embryonic and extraembryonic stem cell lines derived from single mouse blastomeres. Nature 2006; 439:216-219.
84. Erlebacher A, Price KA, Glimcher LH. Maintenance of mouse trophoblast stem cell proliferation by TGF-beta/activin. Dev Biol 2004; 275:158-169.
85. Guzman-Ayala M, Ben-Haim N, Beck S, Constam DB. Nodal protein processing and fibroblast growth factor 4 synergize to maintain a trophoblast stem cell microenvironment. Proc Natl Acad Sci USA 2004; 101:15656-15660.
86. Kubaczka C, Senner C, Arauzo-Bravo MJ, Sharma N, Kuckenberg P, Becker A, Zimmer A, Brustle O, Peitz M, Hemberger M, Schorle H. Derivation and maintenance of murine trophoblast stem cells under defined conditions. Stem Cell Rep 2014; 2:232-242.
87. Ohinata Y, Tsukiyama T. Establishment of trophoblast stem cells under defined culture conditions in mice. PLoS One 2014; 9:e107308.
88. Asanoma K, Rumi MA, Kent LN, Chakraborty D, Renaud SJ, Wake N, Lee DS, Kubota K, Soares MJ. FGF4-dependent stem cells derived from rat blastocysts differentiate along the trophoblast lineage. Dev Biol 2011; 351:110-119.
89. Kibschull M, Winterhager E. Connexins and trophoblast cell lineage development. Methods Mol Med 2006; 121:149-158.
90. Konno T, Rempel LA, Rumi MA, Graham AR, Asanoma K, Renaud SJ, Soares MJ. Chromosome-substituted rat strains provide insights into the genetics of placentation. Physiol Genomics 2011; 43:930-941.
91. Chakraborty D, Cui W, Rosario GX, Scott RL, Dhakal P, Renaud SJ, Tachibana M, Rumi MA, Mason CW, Krieg AJ, Soares MJ. HIFKDM3A-MMP12 regulatory circuit ensures trophoblast plasticity and placental adaptations to hypoxia. Proc Natl Acad Sci USA 2016; 113:E7212-E7221.
92. Thomson JA, Itskovitz-Eldor J, Shapiro SS, Waknitz MA, Swiergiel JJ, Marshall VS, Jones JM. Embryonic stem cell lines derived from human blastocysts. Science 1998; 282:1145-1147.
93. Ezashi T, Telugu BP, Roberts RM. Model systems for studying trophoblast differentiation from human pluripotent stem cells. Cell Tissue Res 2012; 349:809-824.
94. Xu RH, Chen X, Li DS, Li R, Addicks GC, Glennon C, Zwaka TP, Thomson JA. BMP4 initiates human embryonic stem cell differentiation to trophoblast. Nat Biotechnol 2002; 20:1261-1264.
95. Yabe S, Alexenko AP, Amita M, Yang Y, Schust DJ, Sadovsky Y, Ezashi T, Roberts RM. Comparison of syncytiotrophoblast generated from human embryonic stem cells and from term placentas. Proc Natl Acad Sci USA 2016; 113:E2598-E2607.
96. Roberts RM, Loh KM, Amita M, Bernardo AS, Adachi K, Alexenko AP, Schust DJ, Schulz LC, Telugu BP, Ezashi T, Pedersen RA. Differentiation of trophoblast cells from human embryonic stem cells: to be or not to be?Reproduction 2014; 147:D1-D12.
97. Okae H, Toh H, Sato T, Hiura H, Takahashi S, Shirane K, Kabayama Y, Suyama M, Sasaki H, Arima T. Derivation of human trophoblast stem cells. Cell Stem Cell 2018; 22:50.e6-63.e6.
98. Yang Y, Liu B, Xu J, Wang J, Wu J, Shi C, Xu Y, Dong J, Wang C, Lai W, Zhu J, Xiong L et al. Derivation of Pluripotent Stem Cells with In Vivo Embryonic and Extraembryonic Potency. Cell 2017; 169:243-257.e25.
99. Yang J, Ryan DJ, Wang W, Tsang JC, Lan G, Masaki H, Gao X, Antunes L, Yu Y, Zhu Z, Wang J, Kolodziejczyk AA et al. Establishment of mouse expanded potential stem cells. Nature 2017; 550:393-397.
100. Zdravkovic T, Nazor KL, Larocque N, Gormley M, Donne M, Hunkapillar N, Giritharan G, Bernstein HS, Wei G, Hebrok M, Zeng X, Genbacev O et al. Human stem cells from single blastomeres reveal pathways of embryonic or trophoblast fate specification. Development 2015; 142:4010-4025.
101. Benchetrit H, Herman S, van Wietmarschen N, Wu T, Makedonski K, Maoz N, Yom Tov N, Stave D, Lasry R, Zayat V, Xiao A, Lansdorp PM et al. Extensive nuclear reprogramming underlies lineage conversion into functional trophoblast stem-like cells. Cell Stem Cell 2015; 17:543-556.
102. Kubaczka C, Senner CE, Cierlitza M, Arauzo-Bravo MJ, Kuckenberg P, Peitz M, Hemberger M, Schorle H. Direct induction of trophoblast stem cells from murine fibroblasts. Cell Stem Cell 2015; 17:557-568.
103. Harrison SE, Sozen B, Christodoulou N, Kyprianou C, Zernicka-Goetz M. Assembly of embryonic and extraembryonic stem cells to mimic embryogenesis in vitro. Science 2017; 356:6334.
104. Zhu D, Gong X, Miao L, Fang J, Zhang J. Efficient induction of syncytiotrophoblast layer II cells from trophoblast stem cells by canonical Wnt signaling activation. Stem Cell Rep 2017; 9:2034-2049.
105. VandeVoort CA, Thirkill TL, Douglas GC. Blastocyst-derived trophoblast stem cells from the rhesus monkey. Stem Cells Dev 2007; 16:779-788.
106. Grigor'eva EV, Shevchenko AI, Mazurok NA, Elisaphenko EA, Zhelezova AI, Shilov AG, Dyban PA, Dyban AP, Noniashvili EM, Slobodyanyuk SY, Nesterova TB, Brockdorff N et al. FGF4 independent derivation of trophoblast stem cells from the common vole. PLoS One 2009; 4:e7161.
107. Tan T, Tang X, Zhang J, Niu Y, Chen H, Li B, Wei Q, Ji W. Generation of trophoblast stem cells from rabbit embryonic stem cells with BMP4. PLoS One 2011; 6:e17124.
108. Huang X, Han X, Uyunbilig B, Zhang M, Duo S, Zuo Y, Zhao Y, Yun T, Tai D, Wang C, Li J, Li X et al. Establishment of bovine trophoblast stem-like cells from in vitro-produced blastocyst-stage embryos using two inhibitors. Stem Cells Dev 2014; 23:1501-1514.
109. Hou D, Su M, Li X, Li Z, Yun T, Zhao Y, Zhang M, Zhao L, Li R, Yu H, Li X. The efficient derivation of trophoblast cells from porcine in vitro fertilized and parthenogenetic blastocysts and culture with ROCK inhibitor Y-27632. PLoS One 2015; 10:e0142442.
110. Hou Z, Romero R, Uddin M, Than NG, Wildman DE. Adaptive history of single copy genes highly expressed in the term human placenta. Genomics 2009; 93:33-41.
111. Wildman DE. Review: Toward an integrated evolutionary understanding of the mammalian placenta. Placenta 2011; 32(Suppl 2):S142-S145.
112. Cox B, Kotlyar M, Evangelou AI, Ignatchenko V, Ignatchenko A, Whiteley K, Jurisica I, Adamson SL, Rossant J, Kislinger T. Comparative systems biology of human and mouse as a tool to guide the modeling of human placental pathology. Mol Syst Biol 2009; 5:279.
113. Armstrong DL, McGowen MR, Weckle A, Pantham P, Caravas J, Agnew D, Benirschke K, Savage-Rumbaugh S, Nevo E, Kim CJ, Wagner GP, Romero R et al. The core transcriptome of mammalian placentas and the divergence of expression with placental shape. Placenta 2017; 57: 71-78.
114. Rossant J, Cross JC. Placental development: lessons from mousemutants. Nat Rev Genet 2001; 2:538-548.
115. Carter AM. Animal models of human placentation-a review. Placenta 2007; 28(Suppl A):S41-S47.
116. Mess A, Zaki N, Kadyrov M, Korr H, Kaufmann P. Caviomorph placentation as a model for trophoblast invasion. Placenta 2007; 28:1234-1238.
117. Guillemot F, Nagy A, Auerbach A, Rossant J, Joyner AL. Essential role of Mash-2 in extraembryonic development. Nature 1994; 371: 333-336.
118. Chawengsaksophak K, de Graaff W, Rossant J, Deschamps J, Beck F. Cdx2 is essential for axial elongation in mouse development. Proc Natl Acad Sci USA 2004; 101:7641-7645.
119. Chawengsaksophak K, James R, Hammond VE, Köntgen F, Beck F. Homeosis and intestinal tumours in Cdx2 mutant mice. Nature 1997; 386:84-87.
120. Luo J, Sladek R, Bader JA, Matthyssen A, Rossant J, Giguère V. Placental abnormalities in mouse embryos lacking the orphan nuclear receptor ERR-?. Nature 1997; 388:778-782.
121. Ma GT, Roth ME, Groskopf JC, Tsai FY, Orkin SH, Grosveld F, Engel JD, Linzer DI. GATA-2 and GATA-3 regulate trophoblast-specific gene expression in vivo. Development 1997; 124:907-914.
122. Riley P, Anson-Cartwright L, Cross JC. The Hand1 bHLH transcription factor is essential for placentation and cardiac morphogenesis. Nat Genet 1998; 18:271-275.
123. Yamamoto H, Flannery ML, Kupriyanov S, Pearce J, McKercher SR, Henkel GW, Maki RA, Werb Z, Oshima RG. Defective trophoblast function in mice with a targeted mutation of Ets2. Genes Dev 1998; 12:1315-1326.
124. Barak Y, Nelson MC, Ong ES, Jones YZ, Ruiz-Lozano P, Chien KR, Koder A, Evans RM. PPAR?Is required for placental, cardiac, and adipose tissue development. Mol Cell 1999; 4:585-595.
125. Morasso MI, Grinberg A, Robinson G, Sargent TD, Mahon KA. Placental failure in mice lacking the homeobox gene Dlx3. Proc Natl Acad Sci USA 1999; 96:162-167.
126. Anson-Cartwright L, Dawson K, Holmyard D, Fisher SJ, Lazzarini RA, Cross JC. The glial cells missing-1 protein is essential for branching morphogenesis in the chorioallantoic placenta. Nat Genet 2000; 25:311-314.
127. Russ AP, Wattler S, Colledge WH, Aparicio SA, Carlton MB, Pearce JJ, Barton SC, SuraniMA, Ryan K, NehlsMC, Wilson V, EvansMJ. Eomesodermin is required for mouse trophoblast development and mesoderm formation. Nature 2000; 404:95-99.
128. Auman HJ, Nottoli T, Lakiza O, Winger Q, Donaldson S, Williams T. Transcription factor AP-2 gamma is essential in the extra-embryonic lineages for early postimplantation development. Development 2002; 129:2733-2747.
129. Werling U, Schorle H. Transcription factor gene AP-2 gamma essential for early murine development. Mol Cell Biol 2002; 22:3149-3156.
130. Donnison M, Beaton A, Davey HW, Broadhurst R, L'Huillier P, Pfeffer PL. Loss of the extraembryonic ectoderm in Elf5 mutants leads to defects in embryonic patterning. Development 2005; 132:2299-2308.
131. Yagi R, Kohn MJ, Karavanova I, Kaneko KJ, Vullhorst D, DePamphilis ML, Buonanno A. Transcription factor TEAD4 specifies the trophectoderm lineage at the beginning of mammalian development. Development 2007; 134:3827-3836.
132. Nishioka N, Yamamoto S, Kiyonari H, Sato H, Sawada A, Ota M, Nakao K, Sasaki H. Tead4 is required for specification of trophectoderm in pre-implantation mouse embryos. Mech Dev 2008; 125: 270-283.
133. Alders M, Hodges M, Hadjantonakis AK, Postmus J, van Wijk I, Bliek J, de Meulemeester M, Westerveld A, Guillemot F, Oudejans C, Little P, Mannens M. The Human Achaete-Scute Homologue 2 (ASCL2, HASH2) maps to chromosome 11p15.5, close to IGF2 and is expressed in extravillus trophoblasts. Hum Mol Genet 1997; 6:859-867.
134. Schaiff WT, Carlson MG, Smith SD, Levy R, Nelson DM, Sadovsky Y. Peroxisome proliferator-activated receptor-gamma modulates differentiation of human trophoblast in a ligand-specific manner. J Clin Endocrinol Metab 2000; 85:3874-3881.
135. Loregger T, Pollheimer J, Knöfler M. Regulatory transcription factors controlling function and differentiation of human trophoblast-a review. Placenta 2003; 24:S104-S110.
136. Adjaye J, Huntriss J, Herwig R, BenKahla A, Brink TC, Wierling C, Hultschig C, Groth D, Yaspo ML, Picton HM, Gosden RG, Lehrach H. Primary differentiation in the human blastocyst: comparative molecular portraits of inner cell mass and trophectoderm cells. Stem Cells 2005; 23:1514-1525.
137. Baczyk D, Drewlo S, Proctor L, Dunk C, Lye S, Kingdom J. Glial cell missing-1 transcription factor is required for the differentiation of the human trophoblast. Cell Death Differ 2009; 16:719-727.
138. Staun-Ram E, Goldman S, Shalev E. Ets-2 and p53 mediate cAMPinduced MMP-2 expression, activity and trophoblast invasion. Reprod Biol Endocrinol 2009; 7:135.
139. Hemberger M, Udayashankar R, Tesar P, Moore H, Burton GJ. ELF5-enforced transcriptional networks define an epigenetically regulated trophoblast stem cell compartment in the human placenta. Hum Mol Genet 2010; 19:2456-2467.
140. Chui A, Evseenko DA, Brennecke SP, Keelan JA, Kalionis B, Murthi P. Homeobox gene Distal-less 3 (DLX3) is a regulator of villous cytotrophoblast differentiation. Placenta 2011; 32:745-751.
141. Kumar P, Mendelson CR. Estrogen-related receptor gamma (ERRgamma) mediates oxygen-dependent induction of aromatase (CYP19) gene expression during human trophoblast differentiation. Mol Endocrinol 2011; 25:1513-1526.
142. Niakan KK, Eggan K. Analysis of human embryos from zygote to blastocyst reveals distinct gene expression patterns relative to the mouse. Dev Biol 2013; 375:54-64.
143. Haider S, Meinhardt G, Saleh L, Fiala C, Pollheimer J, Knöfler M. Notch1 controls development of the extravillous trophoblast lineage in the human placenta. Proc Natl Acad Sci USA 2016; 113:E7710-E7719.
144. Lee B, Kroener LL, Xu N, Wang ET, Banks A, Williams J, 3rd, Goodarzi MO, Chen YI, Tang J, Wang Y, Gangalapudi V, Pisarska MD. Function and hormonal regulation of GATA3 in human first trimester placentation. Biol Reprod 2016; 95:113.
145. Krendl C, Shaposhnikov D, Rishko V, Ori C, Ziegenhain C, Sass S, Simon L, MullerNS, Straub T, Brooks KE, Chavez SL, EnardWet al.GATA2/3-TFAP2A/C transcription factor network couples human pluripotent stem cell differentiation to trophectoderm with repression of pluripotency. Proc Natl Acad Sci USA 2017; 114:E9579-E9588.
146. Wenzel PL, Leone G. Expression of Cre recombinase in early diploid trophoblast cells of the mouse placenta. Genesis 2007; 45:129-134.
147. Nadeau V, Guillemette S, Bélanger LF, Jacob O, Roy S, Charron J. Map2k1 and Map2k2 genes contribute to the normal development of syncytiotrophoblasts during placentation. Development 2009; 136:1363-1374.
148. Hu D, Cross JC. Ablation of Tpbpa-positive trophoblast precursors leads to defects in maternal spiral artery remodeling in the mouse placenta. Dev Biol 2011; 358:231-239.
149. Mould A, Morgan MA, Li L, Bikoff EK, Robertson EJ. Blimp1/Prdm1 governs terminal differentiation of endovascular trophoblast giant cells and defines multipotent progenitors in the developing placenta. Genes Dev 2012; 26:2063-2074.
150. Ouseph MM, Li J, Chen HZ, Pécot T, Wenzel P, Thompson JC, Comstock G, Chokshi V, Byrne M, Forde B, Chong JL, Huang K et al. Atypical E2F repressors and activators coordinate placental development. Dev Cell 2012; 22:849-862.
151. Zhou CC, Chang J, Mi T, Abbasi S, Gu D, Huang L, Zhang W, Kellems RE, Schwartz RJ, Xia Y. Targeted expression of Cre recombinase provokes placental-specific DNA recombination in transgenic mice. PLoS One 2012; 7:e29236.
152. Crish J, Conti MA, Sakai T, Adelstein RS, Egelhoff TT. Keratin 5-Credriven excision of nonmuscle myosin IIA in early embryo trophectoderm leads to placenta defects and embryonic lethality. Dev Biol 2013; 382:136-148.
153. Al-Soudy AS, Nakanishi T, Mizuno S, Hasegawa Y, Shawki HH, Katoh MC, Basha WA, Ibrahim AE, El-Shemy HA, Iseki H, Yoshiki A, Hiromori Y et al. Germline recombination in a novel Cre transgenic line, Pr13b1-Cre mouse. Genesis 2016; 54:389-397.
154. Nadeau V, Charron J. Essential role of the ERK/MAPK pathway in blood-placental barrier formation. Development 2014; 141:2825-2837.
155. Outhwaite JE, McGuire V, Simmons DG. Genetic ablation of placental sinusoidal trophoblast giant cells causes fetal growth restriction and embryonic lethality. Placenta 2015; 36:951-955.
156. Moreau JL, Artap ST, Shi H, Chapman G, Leone G, Sparrow DB, Dunwoodie SL. Cited2 is required in trophoblasts for correct placental capillary patterning. Dev Biol 2014; 392:62-79.
157. Dow LE, Lowe SW. Life in the fast lane: mammalian disease models in the genomics era. Cell 2012; 148:1099-1109.
158. Dow LE. Modeling disease in vivo with CRISPR/Cas9. Trends Mol Med 2015; 21:609-621.
159. Georgiades P, Cox B, Gertsenstein M, Chawengsaksophak K, Rossant J. Trophoblast-specific gene manipulation using lentivirus-based vectors. Biotech 2007; 42:317-325.
160. Malashicheva A, Kanzler B, Tolkunova E, Trono D, Tomilin A. Lentivirus as a tool for lineage-specific gene manipulations. Genesis 2007; 45:456-459.
161. Okada Y, Ueshin Y, Isotani A, Saito-Fujita T, Nakashima H, Kimura K, Mizoguchi A, Oh-Hora M, Mori Y, Ogata M, Oshima RG, Okabe M et al. Complementation of placental defects and embryonic lethality by trophoblast-specific lentiviral gene transfer. Nat Biotechnol 2007; 25:233-237.
162. Tobita T, Kiyozumi D, IkawaM. Placenta-specific gene manipulation using lentiviral vector and its application. Placenta 2017; 59(Suppl 1):S37-S43.
163. Lee DS, Rumi MA, Konno T, Soares MJ. In vivo genetic manipulation of the rat trophoblast cell lineage using lentiviral vector delivery. Genesis 2009; 47:433-439.
164. Purcell SH, Cantlon JD, Wright CD, Henkes LE, Seidel GE, Jr, Anthony RV. The involvement of proline-rich 15 in early conceptus development in sheep. Biol Reprod 2009; 81:1112-1121.
165. Bou G, Liu S, SunM, Zhu J, Xue B, Guo J, Zhao Y, Qu B, Weng X, Wei Y, Lei L, Liu Z. CDX2 is essential for cell proliferation and polarity in porcine blastocysts. Development 2017; 144:1296-1306.
166. Skoda G, Hoffmann OI, Gocza E, Bodrogi L, Kerekes A, Bosze Z, Hiripi L. Placenta-specific gene manipulation in rabbits. J Biotechnol 2017; 259:86-90.
167. Brosens IA, Robertson WB, Dixon HG. The role of the spiral arteries in the pathogenesis of preeclampsia. Obstet Gynecol Annu 1972; 1:177-191.
168. Fisher SJ. The placental problem: linking abnormal cytotrophoblast differentiation to the maternal symptoms of preeclampsia. Reprod Biol Endocrinol 2004; 2:53.
169. Brosens I, Pijnenborg R, Vercruysse L, Romero R. The "GreatObstetrical Syndromes" are associated with disorders of deep placentation. Am J Obstet Gynecol 2011; 204:193-201.
170. Zhou Y, Damsky CH, Chiu K, Roberts JM, Fisher SJ. Preeclampsia is associated with abnormal expression of adhesion molecules by invasive cytotrophoblasts. J Clin Invest 1993; 91:950-960.
171. Zhou Y, Damsky CH, Fisher SJ. Preeclampsia is associated with failure of human cytotrophoblasts tomimic a vascular adhesion phenotype. One cause of defective endovascular invasion in this syndrome?J Clin Invest 1997; 99:2152-2164.
172. Rosario GX, Ain R, Konno T, Soares MJ. Intrauterine fate of invasive trophoblast cells?Placenta 2009; 30:457-463.
173. Fidler IJ. Timeline: The pathogenesis of cancer metastasis: the 'seed and soil' hypothesis revisited. Nat Rev Cancer 2003; 3:453-458.
174. Cha J, Sun X, Dey SK. Mechanisms of implantation: strategies for successful pregnancy. Nat Med 2012; 18:1754-1767.
175. Zhang J, Chen Z, Smith GN, Croy BA. Natural killer cell-triggered vascular transformation: maternal care before birth?Cell Mol Immunol 2011; 8:1-11.
176. Zhang J, Dunk C, Croy AB, Lye SJ. To serve and to protect: the role of decidual innate immune cells on human pregnancy. Cell Tissue Res 2016; 363:249-265.
177. Nancy P, Tagliani E, Tay CS, Asp P, Levy DE, Erlebacher A. Chemokine gene silencing in decidual stromal cells limits T cell access to the maternalfetal interface. Science 2012; 336:1317-1321.
178. Konno T, Graham AR, Rempel LA, Ho-Chen JK, Alam SM, Bu P, Rumi MA, Soares MJ. Subfertility linked to combined luteal insufficiency and uterine progesterone resistance. Endocrinology 2010; 151:4537-4550.
179. Cooke PS, Spencer TE, Bartol FF, Hayashi K. Uterine glands: development, function and experimentalmodel systems. MolHum Reprod 2013; 19:547-558.
180. Filant J, Spencer TE. Endometrial glands are essential for blastocyst implantation and decidualization in the mouse uterus. Biol Reprod 2013; 88:93.
181. Davila J, Laws MJ, Kannan A, Li Q, Taylor RN, Bagchi MK, Bagchi IC. Rac1 regulates endometrial secretory function to control placental development. PLoS Genet 2015; 11:e1005458.
182. Dhakal P, Rumi MA, Kubota K, Chakraborty D, Chien J, Roby KF, Soares MJ. Neonatal progesterone programs adult uterine responses to progesterone and susceptibility to uterine dysfunction. Endocrinology 2015; 156:3791-3803.
183. Rabaglino MB, Post Uiterweer ED, Jeyabalan A, Hogge WA, Conrad KP. Bioinformatics approach reveals evidence for impaired endometrial maturation before and during early pregnancy in women who developed preeclampsia. Hypertension. 2015; 65:421-429.
184. Conrad KP, Rabaglino MB, Post Uiterweer ED. Emerging role for dysregulated decidualization in the genesis of preeclampsia. Placenta 2017; 60:119-129.
185. Garrido-Gomez T, Dominguez F, Quiñonero A, Diaz-Gimeno P, Kapidzic M, Gormley M, Ona K, Padilla-Iserte P, McMaster M, Genbacev O, Perales A, Fisher SJ et al. Defective decidualization during and after severe preeclampsia reveals a possible maternal contribution to the etiology. Proc Natl Acad Sci USA 2017; 114:E8468-E8477.
186. Woods L, Perez-Garcia V, Kieckbusch J, Wang X, DeMayo F, Colucci F, Hemberger M. Decidualisation and placentation defects are a major cause of age-related reproductive decline. Nat Commun 2017; 8:352.
187. Hanna J, Mandelboim O. When killers become helpers. Trends Immunol 2007; 28:201-206.
188. Sharma S. Natural killer cells and regulatory T cells in early pregnancy loss. Int J Dev Biol 2014; 58:219-229.
189. Guimond MJ, Luross JA, Wang B, Terhorst C, Danial S, Croy BA. Absence of natural killer cells during murine pregnancy is associated with reproductive compromise in TgE26 Mice. Biol Reprod 1997; 56:169-179.
190. Barber EM, Pollard JW. The uterine NK cell population requires IL-15 but these cells are not required for pregnancy nor the resolution of a Listeria monocytogenes infection. J Immunol 2003; 171:37-46.
191. Chakraborty D, Rumi MA, Konno T, Soares MJ. Natural killer cells direct hemochorial placentation by regulating hypoxia-inducible factor dependent trophoblast lineage decisions. Proc Natl Acad Sci USA 2011; 108:16295-16300.
192. Fu B, Zhou Y, Ni X, Tong X, Xu X, Dong Z, Sun R, Tian Z, Wei H. Natural killer cells promote fetal development through the secretion of growth-promoting factors. Immunity 2017; 47:1100.e6-1113.e6.
193. Renaud SJ, Scott RL, Chakraborty D, Rumi MA, Soares MJ. Natural killer-cell deficiency alters placental development in rats. Biol Reprod 2017; 96:145-158.
194. Hanna J, Goldman-Wohl D, Hamani Y, Avraham I, Greenfield C, Natanson-Yaron S, Prus D, Cohen-Daniel L, Arnon TI, Manaster I, Gazit R, Yutkin V et al. Decidual NK cells regulate key developmental processes at the human fetal-maternal interface. Nat Med 2006; 12:1065-1074.
195. Moffett A, Chazara O, Colucci F. Maternal allo-recognition of the fetus. Fertil Steril 2017; 107:1269-1272.
196. Murphy SP, Fast LD, Hanna NN, Sharma S. Uterine NK cells mediate inflammation-induced fetal demise in IL-10-null mice. J Immunol 2005; 175:4084-4090.
197. Yougbaré I, Tai WS, Zdravic D, Oswald BE, Lang S, Zhu G, Leong-Poi H, Qu D, Yu L, Dunk C, Zhang J, Sled JG et al. Activated NK cells cause placental dysfunction and miscarriages in fetal alloimmune thrombocytopenia. Nat Commun 2017; 8:224.
198. Beura LK, Hamilton SE, Bi K, Schenkel JM, Odumade OA, Casey KA, Thompson EA, Fraser KA, Rosato PC, Filali-Mouhim A, Sekaly RP, Jenkins MK et al. Normalizing the environment recapitulates adult human immune traits in laboratory mice. Nature 2016; 532:512-516.
199. Simpson ER, Zhao Y, Agarwal VR, Michael MD, Bulun SE, Hinshelwood MM, Graham-Lorence S, Sun T, Fisher CR, Qin K, Mendelson CR. Aromatase expression in health and disease. Recent Prog Horm Res 1997; 52:185-213.
200. Roberts RM, Chen Y, Ezashi T, Walker AM. Interferons and the maternal-conceptus dialog in mammals. Semin Cell Dev Biol 2008; 19:170-177.
201. Bazer FW, Thatcher WW. Chronicling the discovery of interferon tau. Reproduction 2017; 154:F11-F20.
202. Ross GT. Clinical relevance of research on the structure of human chorionic gonadotropin. Am J Obstet Gynecol 1977; 129:795-808.
203. Henke A, Gromoll J. New insights into the evolution of chorionic gonadotrophin. Mol Cell Endocrinol 2008; 291:11-19.
204. Cooke NE, Liebhaber SA. Molecular biology of the growth hormoneprolactin gene system. Vitam Horm 1995; 50:385-459.
205. Soares MJ, Konno T, Alam SM. The prolactin family: effectors of pregnancy-dependent adaptations. Trends Endocrinol Metab 2007; 18:114-121.
206. Wiemers DO, Shao LJ, Ain R, Dai G, Soares MJ. The mouse prolactin gene family locus. Endocrinology 2003; 144:313-325.
207. Alam SM, Ain R, Konno T, Ho-Chen JK, Soares MJ. The rat prolactin gene family locus: species-specific gene family expansion. Mamm Genome 2006; 17:858-877.
208. Martal J, Lacroix MC, Loudes C, Saunier M, Wintenberger-Torrès S. Trophoblastin, an antiluteolytic protein present in early pregnancy in sheep. Reproduction 1979; 56:63-73.
209. Godkin JD, Bazer FW, Moffatt J, Sessions F, Roberts RM. Purification and properties of a major, low molecular weight protein released by the trophoblast of sheep blastocysts at Day 13-21. Reproduction 1982; 65:141-150.
210. Godkin JD, Bazer FW, Thatcher WW, Roberts RM. Proteins released by cultured Day 15-16 conceptuses prolong luteal maintenance when introduced into the uterine lumen of cyclic ewes. Reproduction 1984; 71:57-64.
211. Imakawa K, Anthony RV, Kazemi M, Marotti KR, Polites HG, Roberts RM. Interferon-like sequence of ovine trophoblast protein secreted by embryonic trophectoderm. Nature 1987; 330:377-379.
212. Stewart HJ, McCann SH, Barker PJ, Lee KE, Lamming GE, Flint AP. Interferon sequence homology and receptor binding activity of ovine trophoblast antiluteolytic protein. J Endocrinol 1987; 115:R13-R15.
213. Gibori G, Khan I, Warshaw ML, McLean MP, Puryear TK, Nelson S, Durkee TJ, Azhar S, Steinschneider A, Rao MC. Placental-derived regulators and the complex control of luteal cell function. Recent Prog Horm Res 1988; 44:377-429.
214. Yamamoto T, Chapman BM, Johnson DC, Givens CR, Mellon SH, Soares MJ. Cytochrome P450 17 alpha-hydroxylase gene expression in differentiating rat trophoblast cells. J Endocrinol 1996; 150:161-168.
215. Waterman MR, Simpson ER. Regulation of steroid hydroxylase gene expression is multifactorial in nature. Recent Prog Horm Res 1989; 45:533-563.
216. Escobar JC, Patel SS, Beshay VE, Suzuki T, Carr BR. TheHuman Placenta Expresses CYP17 and Generates Androgens De Novo. J Clin Endocrinol Metab 2011; 96:1385-1392.
217. Simpson ER, Zhao Y, Agarwal VR, Michael MD, Bulun SE, Hinshelwood MM, Graham-Lorence S, Sun T, Fisher CR, Qin K, Mendelson CR. Aromatase expression in health and disease. Recent Prog Horm Res 1997; 52:185-213.
218. Kamat A, Hinshelwood MM, Murry BA, Mendelson CR. Mechanisms in tissue-specific regulation of estrogen biosynthesis in humans. Trends Endocrinol Metab 2002; 13:122-128.
219. Francino MP. An adaptive radiation model for the origin of new gene functions. Nat Genet 2005; 37:573-578.
220. Kidwell MG, Lisch DR. Perspective: transposable elements, parasitic DNA, and genome evolution. Evolution 2001; 55:1-24.
221. Feschotte C, Gilbert C. Endogenous viruses: insights into viral evolution and impact on host biology. Nat Rev Genet 2012; 13:283-296.
222. Rebollo R, Romanish MT, Mager DL. Transposable elements: an abundant and natural source of regulatory sequences for host genes. Annu Rev Genet 2012; 46:21-42.
223. Chuong EB, Elde NC, Feschotte C. Regulatory activities of transposable elements: from conflicts to benefits. Nat Rev Genet 2017; 18:71-86.
224. Frank JA, Feschotte C. Co-option of endogenous viral sequences for host cell function. Curr Opin Virol 2017; 25:81-89.
225. Dupressoir A, Lavialle C, Heidmann T. From ancestral infectious retroviruses to bona fide cellular genes: role of the captured syncytins in placentation. Placenta 2012;33:663-671.
226. Lavialle C, Cornelis G, Dupressoir A, Esnault C, Heidmann O, Vernochet C, Heidmann T. Paleovirology of 'syncytins', retroviral env genes exapted for a role in placentation. Philos Trans R Soc Lond B Biol Sci 2013; 368:20120507.
227. Dupressoir A, Vernochet C, Harper F, Guégan J, Dessen P, Pierron G, Heidmann T. 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 2011; 108:E1164-E1173.
228. Dunlap KA, Palmarini M, Varela M, Burghardt RC, Hayashi K, Farmer JL, Spencer TE. Endogenous retroviruses regulate periimplantation placental growth and differentiation. Proc Natl Acad Sci USA 2006; 103:14390-14395.
229. Chuong EB, Rumi MA, Soares MJ, Baker JC. Endogenous retroviruses function as species-specific enhancer elements in the placenta. Nat Genet 2013; 45:325-329.
230. Chapman V, Forrester L, Sanford J, Hastie N, Rossant J. Cell lineagespecific undermethylation of mouse repetitive DNA. Nature 1984; 307:284-286.
231. Rossant J, Sanford JP, Chapman VM, Andrews GK. Undermethylation of structural gene sequences in extraembryonic lineages of the mouse. Dev Biol 1986; 117:567-573.
232. Novakovic B, Saffery R. Placental pseudo-malignancy from a DNA methylation perspective: unanswered questions and future directions. Front Genet 2013; 4:285.
233. Macaulay EC, Chatterjee A, Cheng X, Baguley BC, Eccles MR, Morison IM. The genes of life and death: a potential role for placental-specific genes in cancer. Bioessays. 2017; 39:11.
234. Wilson SL, Robinson WP. Utility of DNA methylation to assess placental health. Placenta. 2017. DOI: 10.1016/j.placenta.2017.12.013.
235. Rosario GX, Konno T, Soares MJ. Maternal hypoxia activates endovascular trophoblast cell invasion. Dev Biol 2008; 314:362-375.
236. Genbacev O, Joslin R, Damsky CH, Polliotti BM, Fisher SJ. Hypoxia alters early gestation human cytotrophoblast differentiation/invasion in vitro and models the placental defects that occur in preeclampsia. J Clin Invest 1996; 97:540-550.
237. Genbacev O, Zhou Y, Ludlow JW, Fisher SJ. Regulation of human placental development by oxygen tension. Science 1997; 277:1669-1672.
238. Bu P, Alam SM, Dhakal P, Vivian JL, Soares MJ. A prolactin family paralog regulates placental adaptations to a physiological stressor. Biol Reprod 2016; 94:107.
239. Bronson SL, Bale TL. The placenta as a mediator of stress effects on neurodevelopmental reprogramming. Neuropsychopharmacol 2016;41:207-218.
240. Vrooman LA, Xin F, Bartolomei MS. Morphologic and molecular changes in the placenta: what we can learn from environmental exposures. Fertil Steril 2016; 106:930-940.
241. Soares MJ, Iqbal K, Kozai K. Hypoxia and placental development. Birth Defects Res 2017; 109:1309-1329.
242. Wakeland AK, Soncin F, Moretto-ZitaM, Chang CW, Horii M, Pizzo D, Nelson KK, Laurent LC, Parast MM. Hypoxia directs human extravillous trophoblast differentiation in a hypoxia-inducible factor-dependent manner. Am J Pathol 2017; 187:767-780.
243. Chang CW, Wakeland AK, Parast MM. Trophoblast lineage specification, differentiation and their regulation by oxygen tension. J Endocrinol 2018; 236:R43-R56.
244. Clifton VL. Review: sex and the human placenta: mediating differential strategies of fetal growth and survival. Placenta 2010; 31(Suppl):S33-S39.
245. Nugent BM, Bale TL. The omniscient placenta: metabolic and epigenetic regulation of fetal programming. Front Neuroendocrinol 2015; 39:28-37.
246. Rosenfeld CS. Sex-specific placental responses in fetal development. Endocrinology 2015; 156:3422-3434.
247. Kalisch-Smith JI, Simmons DG, Dickinson H, Moritz KM. Review: sexual dimorphism in the formation, function and adaptation of the placenta. Placenta 2017; 54:10-16.
248. Gallou-Kabani C, Gabory A, Tost J, Karimi M, Mayeur S, Lesage J, Boudadi E, Gross MS, Taurelle J, Vigé A, Breton C, Reusens B et al. Sex-and diet-specific changes of imprinted gene expression and DNA methylation in mouse placenta under a high-fat diet. PLoS One 2010; 5:e14398.
249. Gabory A, Ferry L, Fajardy I, Jouneau L, Gothié JD, Vigé A, Fleur C, Mayeur S, Gallou-Kabani C, Gross MS, Attig L, Vambergue A et al. Maternal diets trigger sex-specific divergent trajectories of gene expression and epigenetic systems in mouse placenta. PLoS One 2012; 7:e47986.
250. Cleaton MA, Edwards CA, Ferguson-Smith AC. Phenotypic outcomes of imprinted gene models in mice: elucidation of pre-and postnatal functions of imprinted genes. Annu Rev Genom Hum Genet 2014; 15:93-126.
251. Marsit CJ. Placental epigenetics in children's environmental health. Semin Reprod Med 2016; 34:36-41.
252. Eakin GS, Behringer RR. Tetraploid development in the mouse. Dev Dyn 2003; 228:751-766.
253. Weier JF, Weier HU, Jung CJ, Gormley M, Zhou Y, Chu LW, Genbacev O, Wright AA, Fisher SJ. Human cytotrophoblasts acquire aneuploidies as they differentiate to an invasive phenotype. Dev Biol 2005; 279:420-432.
254. Yuen RK, Robinson WP. Review: a high capacity of the human placenta for genetic and epigenetic variation: implications for assessing pregnancy outcome. Placenta 2011; 32(Suppl 2):S136-S141.
255. Kasak L, Rull K, Sober S, Laan M. Copy number variation profile in the placental and parental genomes of recurrent pregnancy loss families. Sci Rep 2017; 7:45327.
256. Guttmacher AE, Maddox YT, Spong CY. The human placenta project: placental structure, development, and function in real time. Placenta 2014; 35:303-304.
257. Barker DJ, Bull AR, Osmond C, Simmonds SJ. Fetal and placental size and risk of hypertension in adult life. BMJ 1990; 301:259-262.
258. Barker DJ, Thornburg KL. Placental programming of chronic diseases, cancer and lifespan: a review. Placenta 2013; 34:841-845.
259. Rubens CE, Sadovsky Y, Muglia L, Gravett MG, Lackritz E, Gravett C. Prevention of preterm birth: harnessing science to address the global epidemic. Sci Transl Med 2014; 6:262sr5-262sr5.
260. Partridge EA, Davey MG, Hornick MA, McGovern PE, Mejaddam AY, Vrecenak JD, Mesas-Burgos C, Olive A, Caskey RC, Weiland TR, Han J, Schupper AJ et al. An extra-uterine system to physiologically support the extreme premature lamb. Nat Commun 2017; 8:15112.