1932

Abstract

The placenta sits at the interface between the maternal and fetal vascular beds where it mediates nutrient and waste exchange to enable in utero existence. Placental cells (trophoblasts) accomplish this via invading and remodeling the uterine vasculature. Amazingly, despite being of fetal origin, trophoblasts do not trigger a significant maternal immune response. Additionally, they maintain a highly reliable hemostasis in this extremely vascular interface. Decades of research into how the placenta differentiates itself from embryonic tissues to accomplish these and other feats have revealed a previously unappreciated level of complexity with respect to the placenta's cellular composition. Additionally, novel insights with respect to roles played by the placenta in guiding fetal development and metabolism have sparked a renewed interest in understanding the interrelationship between fetal and placental well-being. Here, we present an overview of emerging research in placental biology that highlights these themes and the importance of the placenta to fetal and adult health.

Loading

Article metrics loading...

/content/journals/10.1146/annurev-cellbio-100814-125620
2015-11-13
2024-12-13
Loading full text...

Full text loading...

/deliver/fulltext/cellbio/31/1/annurev-cellbio-100814-125620.html?itemId=/content/journals/10.1146/annurev-cellbio-100814-125620&mimeType=html&fmt=ahah

Literature Cited

  1. Abbott BD, Buckalew AR. 2000. Placental defects in ARNT-knockout conceptus correlate with localized decreases in VEGF-R2, Ang-1, and Tie-2. Dev. Dyn. 219:526–38 [Google Scholar]
  2. Achen MG, Gad JM, Stacker SA, Wilks AF. 1997. Placenta growth factor and vascular endothelial growth factor are co-expressed during early embryonic development. Growth Factors 15:69–80 [Google Scholar]
  3. Adelman DM, Gertsenstein M, Nagy A, Simon MC, Maltepe E. 2000. Placental cell fates are regulated in vivo by HIF-mediated hypoxia responses. Genes Dev. 14:3191–203 [Google Scholar]
  4. Aguilar PS, Baylies MK, Fleissner A, Helming L, Inoue N. et al. 2013. Genetic basis of cell-cell fusion mechanisms. Trends Genet. 29:427–37 [Google Scholar]
  5. Alavi MV, Bette S, Schimpf S, Schuettauf F, Schraermeyer U. et al. 2007. A splice site mutation in the murine Opa1 gene features pathology of autosomal dominant optic atrophy. Brain 130:1029–42 [Google Scholar]
  6. Alwasel SH, Abotalib Z, Aljarallah JS, Osmond C, Al Omar SY. et al. 2012. The breadth of the placental surface but not the length is associated with body size at birth. Placenta 33:619–22 [Google Scholar]
  7. Alwasel SH, Harrath AH, Aljarallah JS, Abotalib Z, Osmond C. et al. 2013. The velocity of fetal growth is associated with the breadth of the placental surface, but not with the length. Am. J. Hum. Biol. 25:534–37 [Google Scholar]
  8. Amelio I, Cutruzzola F, Antonov A, Agostini M, Melino G. 2014. Serine and glycine metabolism in cancer. Trends Biochem. Sci. 39:191–98 [Google Scholar]
  9. Amoroso EC. 1968. The evolution of viviparity. Proc. R. Soc. Med. 61:1188–200 [Google Scholar]
  10. Ananth CV. 2014. Ischemic placental disease: a unifying concept for preeclampsia, intrauterine growth restriction, and placental abruption. Semin. Perinatol. 38:131–32 [Google Scholar]
  11. Ananth CV, Kinzler WL. 2011. Placental abruption. . In Bleeding During Pregnancy: A Comprehensive Guide, ed. EK Sheiner 119–33 New York: Springer [Google Scholar]
  12. Ananth CV, Williams MA. 2013. Placental abruption and placental weight—implications for fetal growth. Acta Obstet. Gynecol. Scand. 92:1143–50 [Google Scholar]
  13. Andraweera PH, Dekker GA, Roberts CT. 2012. The vascular endothelial growth factor family in adverse pregnancy outcomes. Hum. Reprod. Update 18:436–57 [Google Scholar]
  14. Anson-Cartwright L, Dawson K, Holmyard D, Fisher SJ, Lazzarini RA, Cross JC. 2000. The glial cells missing-1 protein is essential for branching morphogenesis in the chorioallantoic placenta. Nat. Genet. 25:311–14 [Google Scholar]
  15. Arkwright PD, Rademacher TW, Dwek RA, Redman CW. 1993. Pre-eclampsia is associated with an increase in trophoblast glycogen content and glycogen synthase activity, similar to that found in hydatidiform moles. J. Clin. Investig. 91:2744–53 [Google Scholar]
  16. Auman HJ, Nottoli T, Lakiza O, Winger Q, Donaldson S, Williams T. 2002. Transcription factor AP-2γ is essential in the extra-embryonic lineages for early postimplantation development. Development 129:2733–47 [Google Scholar]
  17. Bagner DM, Sheinkopf SJ, Vohr BR, Lester BM. 2010. A preliminary study of cortisol reactivity and behavior problems in young children born premature. Dev. Psychobiol. 52:574–82 [Google Scholar]
  18. Barker DJ, Thornburg KL. 2013. Placental programming of chronic diseases, cancer and lifespan: a review. Placenta 34:841–45 [Google Scholar]
  19. Bartlett RH, Gazzaniga AB, Jefferies MR, Huxtable RF, Haiduc NJ, Fong SW. 1976. Extracorporeal membrane oxygenation (ECMO) cardiopulmonary support in infancy. Trans. Am. Soc. Artif. Intern. Organs 22:80–93 [Google Scholar]
  20. Basyuk E, Cross JC, Corbin J, Nakayama H, Hunter P. et al. 1999. Murine Gcm1 gene is expressed in a subset of placental trophoblast cells. Dev. Dyn. 214:303–11 [Google Scholar]
  21. Battaglia FC. 2007. Placental transport: a function of permeability and perfusion. Am. J. Clin. Nutr. 85:591S–97S [Google Scholar]
  22. Bax BE, Bloxam DL. 1997. Energy metabolism and glycolysis in human placental trophoblast cells during differentiation. Biochim. Biophys. Acta 1319:283–92 [Google Scholar]
  23. Baylis JR. 1981. The evolution of parental care in fishes, with reference to Darwin's rule of male sexual selection. Environ. Biol. Fishes 6:223–51 [Google Scholar]
  24. Belkacemi L, Bedard I, Simoneau L, Lafond J. 2005. Calcium channels, transporters and exchangers in placenta: a review. Cell Calcium 37:1–8 [Google Scholar]
  25. Bell AW, Kennaugh JM, Battaglia FC, Makowski EL, Meschia G. 1986. Metabolic and circulatory studies of fetal lamb at midgestation. Am. J. Physiol. Endocrinol. Metab. 250:E538–44 [Google Scholar]
  26. Benirschke K, Kaufmann P. 1995. Pathology of the Human Placenta New York: Springer-Verlag [Google Scholar]
  27. Berg DK, Smith CS, Pearton DJ, Wells DN, Broadhurst R. et al. 2011. Trophectoderm lineage determination in cattle. Dev. Cell 20:244–55 [Google Scholar]
  28. Blond JL, Lavillette D, Cheynet V, Bouton O, Oriol G. 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. 74:3321–29 [Google Scholar]
  29. Boehlert GW, Kusakari M, Yamada J. 1991. Oxygen consumption of gestating female Sebastes schlegeli: estimating the reproductive costs of livebearing. Environ. Biol. Fishes 30:81–89 [Google Scholar]
  30. Bonnin A, Goeden N, Chen K, Wilson ML, King J. et al. 2011. A transient placental source of serotonin for the fetal forebrain. Nature 472:347–50 [Google Scholar]
  31. Bonnin A, Levitt P. 2011. Fetal, maternal, and placental sources of serotonin and new implications for developmental programming of the brain. Neuroscience 197:1–7 [Google Scholar]
  32. Bonnin A, Torii M, Wang L, Rakic P, Levitt P. 2007. Serotonin modulates the response of embryonic thalamocortical axons to netrin-1. Nat. Neurosci. 10:588–97 [Google Scholar]
  33. Brosens I, Pijnenborg R, Vercruysse L, Romero R. 2011. The “Great Obstetrical Syndromes” are associated with disorders of deep placentation. Am. J. Obstet. Gynecol. 204:193–201 [Google Scholar]
  34. Brosens IA, Robertson WB, Dixon HG. 1972. The role of the spiral arteries in the pathogenesis of preeclampsia. Obstet. Gynecol. Annu. 1:177–91 [Google Scholar]
  35. Brunton PJ, Russell JA. 2008. The expectant brain: adapting for motherhood. Nat. Rev. Neurosci. 9:11–25 [Google Scholar]
  36. Bryner BS, Mychaliska GB. 2014. ECLS for preemies: the artificial placenta. Semin. Perinatol. 38:122–29 [Google Scholar]
  37. Burton GJ. 2009. Oxygen, the Janus gas; its effects on human placental development and function. J. Anat. 215:27–35 [Google Scholar]
  38. Burton GJ, Charnock-Jones DS, Jauniaux E. 2009. Regulation of vascular growth and function in the human placenta. Reproduction 138:895–902 [Google Scholar]
  39. Caniggia I, Mostachfi H, Winter J, Gassmann M, Lye SJ. et al. 2000. Hypoxia-inducible factor-1 mediates the biological effects of oxygen on human trophoblast differentiation through TGFβ3. J. Clin. Investig. 105:577–87 [Google Scholar]
  40. Cantor JM, Ginsberg MH. 2012. CD98 at the crossroads of adaptive immunity and cancer. J. Cell Sci. 125:1373–82 [Google Scholar]
  41. Carter AM. 2000. Placental oxygen consumption. Part I: In vivo studies—a review. Placenta 21:Suppl. AS31–37 [Google Scholar]
  42. Carter BS, Moores RR Jr, Battaglia FC, Meschia G. 1993. Ovine fetal placental lactate exchange and decarboxylation at midgestation. Am. J. Physiol. Endocrinol. Metab. 264:E221–25 [Google Scholar]
  43. Carvalho L, Heisenberg CP. 2010. The yolk syncytial layer in early zebrafish development. Trends Cell Biol. 20:586–92 [Google Scholar]
  44. Catalano PM, McIntyre HD, Cruickshank JK, McCance DR, Dyer AR. et al. 2012. The hyperglycemia and adverse pregnancy outcome study: associations of GDM and obesity with pregnancy outcomes. Diabetes Care 35:780–86 [Google Scholar]
  45. Cerdeira AS, Karumanchi SA. 2012. Angiogenic factors in preeclampsia and related disorders. Cold Spring Harb. Perspect. Med. 2:11a006585 [Google Scholar]
  46. Cetin I. 2001. Amino acid interconversions in the fetal-placental unit: the animal model and human studies in vivo. Pediatr. Res. 49:148–54 [Google Scholar]
  47. Cetin I, Fennessey PV, Sparks JW, Meschia G, Battaglia FC. 1992. Fetal serine fluxes across fetal liver, hindlimb, and placenta in late gestation. Am. J. Physiol. Endocrinol. Metab. 263:E786–93 [Google Scholar]
  48. Cha J, Sun X, Dey SK. 2012. Mechanisms of implantation: strategies for successful pregnancy. Nat. Med. 18:1754–67 [Google Scholar]
  49. Chauhan M, Yallampalli U, Dong YL, Hankins GD, Yallampalli C. 2009. Expression of adrenomedullin 2 (ADM2)/intermedin (IMD) in human placenta: role in trophoblast invasion and migration. Biol. Reprod. 81:777–83 [Google Scholar]
  50. Chen CP, Chen LF, Yang SR, Chen CY, Ko CC. et al. 2008. Functional characterization of the human placental fusogenic membrane protein syncytin 2. Biol. Reprod. 79:815–23 [Google Scholar]
  51. Chen DB, Zheng J. 2014. Regulation of placental angiogenesis. Microcirculation 21:15–25 [Google Scholar]
  52. Chen H, Detmer SA, Ewald AJ, Griffin EE, Fraser SE, Chan DC. 2003. Mitofusins Mfn1 and Mfn2 coordinately regulate mitochondrial fusion and are essential for embryonic development. J. Cell Biol. 160:189–200 [Google Scholar]
  53. Choi HJ, Sanders TA, Tormos KV, Ameri K, Tsai JD. et al. 2013. ECM-dependent HIF induction directs trophoblast stem cell fate via LIMK1-mediated cytoskeletal rearrangement. PLOS ONE 8:e56949 [Google Scholar]
  54. Choi KS, Bae MK, Jeong JW, Moon HE, Kim KW. 2003. Hypoxia-induced angiogenesis during carcinogenesis. J. Biochem. Mol. Biol. 36:120–27 [Google Scholar]
  55. Chung M, Teng C, Timmerman M, Meschia G, Battaglia FC. 1998. Production and utilization of amino acids by ovine placenta in vivo. Am. J. Physiol. Endocrinol. Metab. 274:E13–22 [Google Scholar]
  56. Chuong EB, Rumi MA, Soares MJ, Baker JC. 2013. Endogenous retroviruses function as species-specific enhancer elements in the placenta. Nat. Genet. 45:325–29 [Google Scholar]
  57. Cilley RE, Zwischenberger JB, Andrews AF, Bowerman RA, Roloff DW, Bartlett RH. 1986. Intracranial hemorrhage during extracorporeal membrane oxygenation in neonates. Pediatrics 78:699–704 [Google Scholar]
  58. Clutton-Brock TH. 1991. The Evolution of Parental Care Princeton, NJ: Princeton Univ. Press [Google Scholar]
  59. Coan PM, Vaughan OR, Sekita Y, Finn SL, Burton GJ. et al. 2010. Adaptations in placental phenotype support fetal growth during undernutrition of pregnant mice. J. Physiol. 588:527–38 [Google Scholar]
  60. Cornelis G, Heidmann O, Bernard-Stoecklin S, Reynaud K, Veron G. et al. 2012. Ancestral capture of syncytin-Car1, a fusogenic endogenous retroviral envelope gene involved in placentation and conserved in Carnivora. PNAS 109:E432–41 [Google Scholar]
  61. Cowden Dahl KD, Fryer BH, Mack FA, Compernolle V, Maltepe E. et al. 2005. Hypoxia-inducible factors 1α and 2α regulate trophoblast differentiation. Mol. Cell. Biol. 25:10479–91 [Google Scholar]
  62. Crossley KJ, Walker DW, Beart PM, Hirst JJ. 2000. Characterisation of GABAA receptors in fetal, neonatal and adult ovine brain: region and age related changes and the effects of allopregnanolone. Neuropharmacology 39:1514–22 [Google Scholar]
  63. Cunningham FG, Williams JW. 2010. Williams Obstetrics New York: McGraw-Hill Medical [Google Scholar]
  64. Dalton P, Christian HC, Redman CW, Sargent IL, Boyd CA. 2007. Membrane trafficking of CD98 and its ligand galectin 3 in BeWo cells—implication for placental cell fusion. FEBS J. 274:2715–27 [Google Scholar]
  65. Desforges M, Sibley CP. 2010. Placental nutrient supply and fetal growth. Int. J. Dev. Biol. 54:377–90 [Google Scholar]
  66. Dietrich JE, Hiiragi T. 2008. Stochastic processes during mouse blastocyst patterning. Cells Tissues Organs 188:46–51 [Google Scholar]
  67. Dilworth MR, Kusinski LC, Cowley E, Ward BS, Husain SM. et al. 2010. Placental-specific Igf2 knockout mice exhibit hypocalcemia and adaptive changes in placental calcium transport. PNAS 107:3894–99 [Google Scholar]
  68. Dilworth MR, Sibley CP. 2013. Review: transport across the placenta of mice and women. Placenta 34:Suppl.S34–39 [Google Scholar]
  69. Donnison M, Beaton A, Davey HW, Broadhurst R, L'Huillier P, Pfeffer PL. 2005. Loss of the extraembryonic ectoderm in Elf5 mutants leads to defects in embryonic patterning. Development 132:2299–308 [Google Scholar]
  70. Drake PM, Red-Horse K, Fisher SJ. 2004. Reciprocal chemokine receptor and ligand expression in the human placenta: implications for cytotrophoblast differentiation. Dev. Dyn. 229:877–85 [Google Scholar]
  71. Dulvy NK, Ellis JR, Goodwin NB, Grant A, Reynolds JD, Jennings S. 2004. Methods of assessing extinction risk in marine fishes. Fish Fisheries 5:255–76 [Google Scholar]
  72. Dulvy NK, Reynolds JD. 1997. Evolutionary transitions among egg-laying, live-bearing and maternal inputs in sharks and rays. Proc. R. Soc. B 264:1309–15 [Google Scholar]
  73. Dupressoir A, Vernochet C, Bawa O, Harper F, Pierron G. et al. 2009. Syncytin-A knockout mice demonstrate the critical role in placentation of a fusogenic, endogenous retrovirus-derived, envelope gene. PNAS 106:12127–32 [Google Scholar]
  74. Dupressoir A, Vernochet C, Harper F, Guegan J, Dessen P. et al. 2011. A pair of co-opted retroviral envelope syncytin genes is required for formation of the two-layered murine placental syncytiotrophoblast. PNAS 108:E1164–73 [Google Scholar]
  75. Edgar BA, Zielke N, Gutierrez C. 2014. Endocycles: a recurrent evolutionary innovation for post-mitotic cell growth. Nat. Rev. Mol. Cell Biol. 15:197–210 [Google Scholar]
  76. Erlebacher A, Price KA, Glimcher LH. 2004. Maintenance of mouse trophoblast stem cell proliferation by TGF-β/activin. Dev. Biol. 275:158–69 [Google Scholar]
  77. Erlich J, Parry GC, Fearns C, Muller M, Carmeliet P. et al. 1999. Tissue factor is required for uterine homeostasis and maintenance of the placental labyrinth during gestation. PNAS 96:8138–43 [Google Scholar]
  78. Escuin D, Kline ER, Giannakakou P. 2005. Both microtubule-stabilizing and microtubule-destabilizing drugs inhibit hypoxia-inducible factor-1α accumulation and activity by disrupting microtubule function. Cancer Res. 65:9021–28 [Google Scholar]
  79. Esnault C, Priet S, Ribet D, Vernochet C, Bruls T. et al. 2008. A placenta-specific receptor for the fusogenic, endogenous retrovirus-derived, human syncytin-2. PNAS 105:17532–37 [Google Scholar]
  80. Ezashi T, Matsuyama H, Telugu BP, Roberts RM. 2011. Generation of colonies of induced trophoblast cells during standard reprogramming of porcine fibroblasts to induced pluripotent stem cells. Biol. Reprod. 85:779–87 [Google Scholar]
  81. Gaspar P, Cases O, Maroteaux L. 2003. The developmental role of serotonin: news from mouse molecular genetics. Nat. Rev. Neurosci. 4:1002–12 [Google Scholar]
  82. Gasperowicz M, Rai A, Cross JC. 2013. Spatiotemporal expression of Notch receptors and ligands in developing mouse placenta. Gene Expr. Patterns 13:249–54 [Google Scholar]
  83. Gauster M, Siwetz M, Orendi K, Moser G, Desoye G, Huppertz B. 2010. Caspases rather than calpains mediate remodelling of the fodrin skeleton during human placental trophoblast fusion. Cell Death Differ. 17:336–45 [Google Scholar]
  84. Genbacev O, Donne M, Kapidzic M, Gormley M, Lamb J. et al. 2011. Establishment of human trophoblast progenitor cell lines from the chorion. Stem Cells 29:1427–36 [Google Scholar]
  85. Genbacev O, Joslin R, Damsky CH, Polliotti BM, Fisher SJ. 1996. Hypoxia alters early gestation human cytotrophoblast differentiation/invasion in vitro and models the placental defects that occur in preeclampsia. J. Clin. Investig. 97:540–50 [Google Scholar]
  86. Genbacev O, Zhou Y, Ludlow JW, Fisher SJ. 1997. Regulation of human placental development by oxygen tension. Science 277:1669–72 [Google Scholar]
  87. Geng Y, Yu Q, Sicinska E, Das M, Schneider JE. et al. 2003. Cyclin E ablation in the mouse. Cell 114:431–43 [Google Scholar]
  88. Georgiades P, Rossant J. 2006. Ets2 is necessary in trophoblast for normal embryonic anteroposterior axis development. Development 133:1059–68 [Google Scholar]
  89. Gilmore RG. 1993. Reproductive biology of lamnoid sharks. Environ. Biol. Fishes 38:95–114 [Google Scholar]
  90. Gilmore RG, Dodrill JW, Linley PA. 1983. Reproduction and embryonic development of the sand tiger shark, Odontaspis taurus (Rafinesque). Fish. Bull. 81:201–25 [Google Scholar]
  91. Gnarra JR, Ward JM, Porter FD, Wagner JR, Devor DE. et al. 1997. Defective placental vasculogenesis causes embryonic lethality in VHL-deficient mice. PNAS 94:9102–7 [Google Scholar]
  92. Gonzalez MA, Tachibana KE, Adams DJ, van der Weyden L, Hemberger M. et al. 2006. Geminin is essential to prevent endoreduplication and to form pluripotent cells during mammalian development. Genes Dev. 20:1880–84 [Google Scholar]
  93. Goodwin NB, Dulvy NK, Reynolds JD. 2002. Life-history correlates of the evolution of live bearing in fishes. Philos. Trans. R. Soc. B 357:259–67 [Google Scholar]
  94. Gray BW, Shaffer AW, Mychaliska GB. 2012. Advances in neonatal extracorporeal support: the role of extracorporeal membrane oxygenation and the artificial placenta. Clin. Perinataol. 39:311–29 [Google Scholar]
  95. Griffin LD, Gong W, Verot L, Mellon SH. 2004. Niemann-Pick type C disease involves disrupted neurosteroidogenesis and responds to allopregnanolone. Nat. Med. 10:704–11 [Google Scholar]
  96. Guzman-Ayala M, Ben-Haim N, Beck S, Constam DB. 2004. Nodal protein processing and fibroblast growth factor 4 synergize to maintain a trophoblast stem cell microenvironment. PNAS 101:15656–60 [Google Scholar]
  97. Hannibal RL, Chuong EB, Rivera-Mulia JC, Gilbert DM, Valouev A, Baker JC. 2014. Copy number variation is a fundamental aspect of the placental genome. PLOS Genet. 10:e1004290 [Google Scholar]
  98. Hardham AR. 2013. Microtubules and biotic interactions. Plant J. 75:278–89 [Google Scholar]
  99. Harrington K, Cooper D, Lees C, Hecher K, Campbell S. 1996. Doppler ultrasound of the uterine arteries: the importance of bilateral notching in the prediction of pre-eclampsia, placental abruption or delivery of a small-for-gestational-age baby. Ultrasound Obstet. Gynecol. 7:182–88 [Google Scholar]
  100. He J, Evans CO, Hoffman SW, Oyesiku NM, Stein DG. 2004. Progesterone and allopregnanolone reduce inflammatory cytokines after traumatic brain injury. Exp. Neurol. 189:404–12 [Google Scholar]
  101. 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 [Google Scholar]
  102. Hirashima M, Lu Y, Byers L, Rossant J. 2003. Trophoblast expression of fms-like tyrosine kinase 1 is not required for the establishment of the maternal-fetal interface in the mouse placenta. PNAS 100:15637–42 [Google Scholar]
  103. Hirate Y, Hirahara S, Inoue K, Suzuki A, Alarcon VB. et al. 2013. Polarity-dependent distribution of angiomotin localizes Hippo signaling in preimplantation embryos. Curr. Biol. 23:1181–94 [Google Scholar]
  104. Ho-Chen JK, Bustamante JJ, Soares MJ. 2007. Prolactin-like protein-F subfamily of placental hormones/cytokines: responsiveness to maternal hypoxia. Endocrinology 148:559–65 [Google Scholar]
  105. Hu D, Cross JC. 2010. Development and function of trophoblast giant cells in the rodent placenta. Int. J. Dev. Biol. 54:341–54 [Google Scholar]
  106. Hubel CA, McLaughlin MK, Evans RW, Hauth BA, Sims CJ, Roberts JM. 1996. Fasting serum triglycerides, free fatty acids, and malondialdehyde are increased in preeclampsia, are positively correlated, and decrease within 48 hours post partum. Am. J. Obstet. Gynecol. 174:975–82 [Google Scholar]
  107. Hughes RL, Hall LS. 1998. Early development and embryology of the platypus. Philos. Trans. R. Soc. B 353:1101–14 [Google Scholar]
  108. Hunkapiller NM, Gasperowicz M, Kapidzic M, Plaks V, Maltepe E. et al. 2011. A role for Notch signaling in trophoblast endovascular invasion and in the pathogenesis of pre-eclampsia. Development 138:2987–98 [Google Scholar]
  109. Huppertz B, Frank HG, Reister F, Kingdom J, Korr H, Kaufmann P. 1999. Apoptosis cascade progresses during turnover of human trophoblast: analysis of villous cytotrophoblast and syncytial fragments in vitro. Lab. Investig. 79:1687–702 [Google Scholar]
  110. Huppertz B, Gauster M. 2011. Trophoblast fusion. Adv. Exp. Med. Biol. 713:81–95 [Google Scholar]
  111. Iams JD. 2014. Clinical practice: prevention of preterm parturition. N. Engl. J. Med. 370:254–61 [Google Scholar]
  112. Ietta F, Wu Y, Romagnoli R, Soleymanlou N, Orsini B. et al. 2007. Oxygen regulation of macrophage migration inhibitory factor in human placenta. Am. J. Physiol. Endocrinol. Metab. 292:E272–80 [Google Scholar]
  113. Illsley NP, Caniggia I, Zamudio S. 2010. Placental metabolic reprogramming: Do changes in the mix of energy-generating substrates modulate fetal growth?. Int. J. Dev. Biol. 54:409–19 [Google Scholar]
  114. Jansson T, Wennergren M, Illsley NP. 1993. Glucose transporter protein expression in human placenta throughout gestation and in intrauterine growth retardation. J. Clin. Endocrinol. Metab. 77:1554–62 [Google Scholar]
  115. Jauniaux E, Hempstock J, Teng C, Battaglia FC, Burton GJ. 2005. Polyol concentrations in the fluid compartments of the human conceptus during the first trimester of pregnancy: maintenance of redox potential in a low oxygen environment. J. Clin. Endocrinol. Metab. 90:1171–75 [Google Scholar]
  116. Jensen GM, Moore LG. 1997. The effect of high altitude and other risk factors on birthweight: independent or interactive effects?. Am. J. Public Health 87:1003–7 [Google Scholar]
  117. Johnson S, Hollis C, Kochhar P, Hennessy E, Wolke D, Marlow N. 2010a. Autism spectrum disorders in extremely preterm children. J. Pediatr. 156:525–31 [Google Scholar]
  118. Johnson S, Hollis C, Kochhar P, Hennessy E, Wolke D, Marlow N. 2010b. Psychiatric disorders in extremely preterm children: longitudinal finding at age 11 years in the EPICure study. J. Am. Acad. Child Adolesc. Psychiatry 49:453–63 [Google Scholar]
  119. Juul SE, Ferriero DM. 2014. Pharmacologic neuroprotective strategies in neonatal brain injury. Clin. Perinatol. 41:119–31 [Google Scholar]
  120. Kaelin WG Jr, Ratcliffe PJ. 2008. Oxygen sensing by metazoans: the central role of the HIF hydroxylase pathway. Mol. Cell 30:393–402 [Google Scholar]
  121. Kasahara A, Cipolat S, Chen Y, Dorn GW Jr, Scorrano L. 2013. Mitochondrial fusion directs cardiomyocyte differentiation via calcineurin and Notch signaling. Science 342:734–37 [Google Scholar]
  122. Kenny LC, Black MA, Poston L, Taylor R, Myers JE. et al. 2014. Early pregnancy prediction of preeclampsia in nulliparous women, combining clinical risk and biomarkers: the Screening for Pregnancy Endpoints (SCOPE) international cohort study. Hypertension 64:644–52 [Google Scholar]
  123. Keyes LE, Armaza JF, Niermeyer S, Vargas E, Young DA, Moore LG. 2003. Intrauterine growth restriction, preeclampsia, and intrauterine mortality at high altitude in Bolivia. Pediatr. Res. 54:20–25 [Google Scholar]
  124. Kibschull M, Gellhaus A, Winterhager E. 2008. Analogous and unique functions of connexins in mouse and human placental development. Placenta 29:848–54 [Google Scholar]
  125. Kibschull M, Winterhager E. 2006. Connexins and trophoblast cell lineage development. Methods Mol. Med. 121:149–58 [Google Scholar]
  126. Kim YM, Bujold E, Chaiworapongsa T, Gomez R, Yoon BH. et al. 2003. Failure of physiologic transformation of the spiral arteries in patients with preterm labor and intact membranes. Am. J. Obstet. Gynecol. 189:1063–69 [Google Scholar]
  127. Kim YM, Chaiworapongsa T, Gomez R, Bujold E, Yoon BH. et al. 2002. Failure of physiologic transformation of the spiral arteries in the placental bed in preterm premature rupture of membranes. Am. J. Obstet. Gynecol. 187:1137–42 [Google Scholar]
  128. Kleinrouweler CE, Wiegerinck MM, Ris-Stalpers C, Bossuyt PM, van der Post JA. et al. 2012. Accuracy of circulating placental growth factor, vascular endothelial growth factor, soluble fms-like tyrosine kinase 1 and soluble endoglin in the prediction of pre-eclampsia: a systematic review and meta-analysis. BJOG 119:778–87 [Google Scholar]
  129. Knofler M, Pollheimer J. 2013. Human placental trophoblast invasion and differentiation: a particular focus on Wnt signaling. Front. Genet. 4:190 [Google Scholar]
  130. Knott JG, Paul S. 2014. Transcriptional regulators of the trophoblast lineage in mammals with hemochorial placentation. Reproduction 148:R121–36 [Google Scholar]
  131. Kudo Y, Boyd CA. 2004. RNA interference–induced reduction in CD98 expression suppresses cell fusion during syncytialization of human placental BeWo cells. FEBS Lett. 577:473–77 [Google Scholar]
  132. Kudo Y, Boyd CA, Sargent IL, Redman CW. 2003a. Hypoxia alters expression and function of syncytin and its receptor during trophoblast cell fusion of human placental BeWo cells: implications for impaired trophoblast syncytialisation in pre-eclampsia. Biochim. Biophys. Acta 1638:63–71 [Google Scholar]
  133. Kudo Y, Boyd CA, Millo J, Sargent IL, Redman CW. 2003b. Manipulation of CD98 expression affects both trophoblast cell fusion and amino acid transport activity during syncytialization of human placental BeWo cells. J. Physiol. 550:3–9 [Google Scholar]
  134. Kuwabara Y, Okai T, Imanishi Y, Muronosono E, Kozuma S. et al. 1987. Development of extrauterine fetal incubation system using extracorporeal membrane oxygenator. Artif. Organs 11:224–27 [Google Scholar]
  135. Kuwabara Y, Okai T, Kozuma S, Unno N, Akiba K. et al. 1989. Artificial placenta: long-term extrauterine incubation of isolated goat fetuses. Artif. Organs 13:527–31 [Google Scholar]
  136. Lanir N, Aharon A, Brenner B. 2003. Procoagulant and anticoagulant mechanisms in human placenta. Semin. Thromb. Hemost. 29:175–84 [Google Scholar]
  137. Latos PA, Hemberger M. 2014. Review: the transcriptional and signalling networks of mouse trophoblast stem cells. Placenta 35:Suppl.S81–85 [Google Scholar]
  138. Lee Y, Voogt JL. 1999. Feedback effects of placental lactogens on prolactin levels and Fos-related antigen immunoreactivity of tuberoinfundibular dopaminergic neurons in the arcuate nucleus during pregnancy in the rat. Endocrinology 140:2159–66 [Google Scholar]
  139. Li M, Yee D, Magnuson TR, Smithies O, Caron KM. 2006. Reduced maternal expression of adrenomedullin disrupts fertility, placentation, and fetal growth in mice. J. Clin. Investig. 116:2653–62 [Google Scholar]
  140. Long JA, Trinajstic K, Young GC, Senden T. 2008. Live birth in the Devonian period. Nature 453:650–52 [Google Scholar]
  141. Lorenzo FR, Huff C, Myllymaki M, Olenchock B, Swierczek S. et al. 2014. A genetic mechanism for Tibetan high-altitude adaptation. Nat. Genet. 46:951–56 [Google Scholar]
  142. Lyden TW, Ng AK, Rote NS. 1993. Modulation of phosphatidylserine epitope expression by BeWo cells during forskolin treatment. Placenta 14:177–86 [Google Scholar]
  143. Lynch VJ, Leclerc RD, May G, Wagner GP. 2011. Transposon-mediated rewiring of gene regulatory networks contributed to the evolution of pregnancy in mammals. Nat. Genet. 43:1154–59 [Google Scholar]
  144. Lynch VJ, Nnamani MC, Kapusta A, Brayer K, Plaza SL. et al. 2015. Ancient transposable elements transformed the uterine regulatory landscape and transcriptome during the evolution of mammalian pregnancy. Cell Rep. 10:4551–61 [Google Scholar]
  145. Mabjeesh NJ, Escuin D, LaVallee TM, Pribluda VS, Swartz GM. et al. 2003. 2ME2 inhibits tumor growth and angiogenesis by disrupting microtubules and dysregulating HIF. Cancer Cell 3:363–75 [Google Scholar]
  146. Malassine A, Blaise S, Handschuh K, Lalucque H, Dupressoir A. et al. 2007. Expression of the fusogenic HERV-FRD Env glycoprotein (syncytin 2) in human placenta is restricted to villous cytotrophoblastic cells. Placenta 28:185–91 [Google Scholar]
  147. Maltepe E, Bakardjiev AI, Fisher SJ. 2010. The placenta: transcriptional, epigenetic, and physiological integration during development. J. Clin. Investig. 120:1016–25 [Google Scholar]
  148. Maltepe E, Krampitz GW, Okazaki KM, Red-Horse K, Mak W. et al. 2005. Hypoxia-inducible factor–dependent histone deacetylase activity determines stem cell fate in the placenta. Development 132:3393–403 [Google Scholar]
  149. Mann PE, Bridges RS. 2001. Lactogenic hormone regulation of maternal behavior. Prog. Brain Res. 133:251–62 [Google Scholar]
  150. Markow TA, Beall S, Matzkin LM. 2009. Egg size, embryonic development time and ovoviviparity in Drosophila species. J. Evol. Biol. 22:430–34 [Google Scholar]
  151. Maynard SE, Min JY, Merchan J, Lim KH, Li J. et al. 2003. Excess placental soluble fms-like tyrosine kinase 1 (sFlt1) may contribute to endothelial dysfunction, hypertension, and proteinuria in preeclampsia. J. Clin. Investig. 111:649–58 [Google Scholar]
  152. Mi S, Lee X, Li X, Veldman GM, Finnerty H. et al. 2000. Syncytin is a captive retroviral envelope protein involved in human placental morphogenesis. Nature 403:785–89 [Google Scholar]
  153. Miura Y, Matsuda T, Funakubo A, Watanabe S, Kitanishi R. et al. 2012. Novel modification of an artificial placenta: pumpless arteriovenous extracorporeal life support in a premature lamb model. Pediatr. Res. 72:490–94 [Google Scholar]
  154. Mould A, Morgan MA, Li L, Bikoff EK, Robertson EJ. 2012. Blimp1/Prdm1 governs terminal differentiation of endovascular trophoblast giant cells and defines multipotent progenitors in the developing placenta. Genes Dev. 26:2063–74 [Google Scholar]
  155. Nevo O, Soleymanlou N, Wu Y, Xu J, Kingdom J. et al. 2006. Increased expression of sFlt-1 in in vivo and in vitro models of human placental hypoxia is mediated by HIF-1. Am. J. Physiol. Regul. Integr. Comp. Physiol. 291:R1085–93 [Google Scholar]
  156. Newstead J, von Dadelszen P, Magee LA. 2007. Preeclampsia and future cardiovascular risk. Expert Rev. Cardiovasc. Ther. 5:283–94 [Google Scholar]
  157. Ng RK, Dean W, Dawson C, Lucifero D, Madeja Z. et al. 2008. Epigenetic restriction of embryonic cell lineage fate by methylation of Elf5. Nat. Cell Biol. 10:1280–90 [Google Scholar]
  158. Niakan KK, Eggan K. 2013. Analysis of human embryos from zygote to blastocyst reveals distinct gene expression patterns relative to the mouse. Dev. Biol. 375:54–64 [Google Scholar]
  159. Nishioka N, Inoue K, Adachi K, Kiyonari H, Ota M. et al. 2009. The Hippo signaling pathway components Lats and Yap pattern Tead4 activity to distinguish mouse trophectoderm from inner cell mass. Dev. Cell 16:398–410 [Google Scholar]
  160. Nishioka N, Yamamoto S, Kiyonari H, Sato H, Sawada A. et al. 2008. Tead4 is required for specification of trophectoderm in pre-implantation mouse embryos. Mech. Dev. 125:270–83 [Google Scholar]
  161. Niwa H, Toyooka Y, Shimosato D, Strumpf D, Takahashi K. et al. 2005. Interaction between Oct3/4 and Cdx2 determines trophectoderm differentiation. Cell 123:917–29 [Google Scholar]
  162. Packard GC, Elinson RP, Gavaud J, Guillette LJ, Lombardi J. et al. 1989. How are reproductive systems integrated and how has viviparity evolved?. In Complex Organismal Functions: Integration and Evolution in Vertebrates, ed. DB Wake, G Roth 281–93 Chichester, UK: Wiley [Google Scholar]
  163. Parast MM, Aeder S, Sutherland AE. 2001. Trophoblast giant-cell differentiation involves changes in cytoskeleton and cell motility. Dev. Biol. 230:43–60 [Google Scholar]
  164. Partridge C, Shardo J, Boettcher A. 2007. Osmoregulatory role of the brood pouch in the euryhaline Gulf pipefish, Syngnathus scovelli. Comp. Biochem. Physiol. A 147:556–61 [Google Scholar]
  165. Pfeffer PL, Pearton DJ. 2012. Trophoblast development. Reproduction 143:231–46 [Google Scholar]
  166. Pijnenborg R, Bland JM, Robertson WB, Brosens I. 1983. Uteroplacental arterial changes related to interstitial trophoblast migration in early human pregnancy. Placenta 4:397–413 [Google Scholar]
  167. Pijnenborg R, Bland JM, Robertson WB, Dixon G, Brosens I. 1981. The pattern of interstitial trophoblastic invasion of the myometrium in early human pregnancy. Placenta 2:303–16 [Google Scholar]
  168. Pijnenborg R, Vercruysse L, Brosens I. 2011. Deep placentation. Best Pract. Res. Clin. Obstet. Gynaecol. 25:273–85 [Google Scholar]
  169. Pijnenborg R, Vercruysse L, Hanssens M. 2006. The uterine spiral arteries in human pregnancy: facts and controversies. Placenta 27:939–58 [Google Scholar]
  170. Piotrowska-Nitsche K, Perea-Gomez A, Haraguchi S, Zernicka-Goetz M. 2005. Four-cell stage mouse blastomeres have different developmental properties. Development 132:479–90 [Google Scholar]
  171. Piotrowska-Nitsche K, Zernicka-Goetz M. 2005. Spatial arrangement of individual 4-cell stage blastomeres and the order in which they are generated correlate with blastocyst pattern in the mouse embryo. Mech. Dev. 122:487–500 [Google Scholar]
  172. Postigo L, Heredia G, Illsley NP, Torricos T, Dolan C. et al. 2009. Where the O2 goes to: preservation of human fetal oxygen delivery and consumption at high altitude. J. Physiol. 587:693–708 [Google Scholar]
  173. Potter JM, Nestel PJ. 1979. The hyperlipidemia of pregnancy in normal and complicated pregnancies. Am. J. Obstet. Gynecol. 133:165–70 [Google Scholar]
  174. Power ML, Schulkin J. 2012. The Evolution of the Human Placenta Baltimore: Johns Hopkins Univ. Press [Google Scholar]
  175. Pringle KG, Kind KL, Thompson JG, Roberts CT. 2007. Complex interactions between hypoxia inducible factors, insulin-like growth factor-II and oxygen in early murine trophoblasts. Placenta 28:1147–57 [Google Scholar]
  176. Qualls CP, Shine R. 1995. Maternal body–volume as a constraint on reproductive output in lizards: evidence from the evolution of viviparity. Oecologia 103:73–78 [Google Scholar]
  177. Rai A, Cross JC. 2014. Development of the hemochorial maternal vascular spaces in the placenta through endothelial and vasculogenic mimicry. Dev. Biol. 387:131–41 [Google Scholar]
  178. Raval Z, Losordo DW. 2013. Cell therapy of peripheral arterial disease: from experimental findings to clinical trials. Circ. Res. 112:1288–302 [Google Scholar]
  179. Rayon T, Menchero S, Nieto A, Xenopoulos P, Crespo M. et al. 2014. Notch and Hippo converge on Cdx2 to specify the trophectoderm lineage in the mouse blastocyst. Dev. Cell 30:410–22 [Google Scholar]
  180. Red-Horse K, Kapidzic M, Zhou Y, Feng KT, Singh H, Fisher SJ. 2005. EPHB4 regulates chemokine-evoked trophoblast responses: a mechanism for incorporating the human placenta into the maternal circulation. Development 132:4097–106 [Google Scholar]
  181. Red-Horse K, Rivera J, Schanz A, Zhou Y, Winn V. et al. 2006. Cytotrophoblast induction of arterial apoptosis and lymphangiogenesis in an in vivo model of human placentation. J. Clin. Investig. 116:2643–52 [Google Scholar]
  182. Red-Horse K, Zhou Y, Genbacev O, Prakobphol A, Foulk R. et al. 2004. Trophoblast differentiation during embryo implantation and formation of the maternal-fetal interface. J. Clin. Investig. 114:744–54 [Google Scholar]
  183. Reis FM, Florio P, Cobellis L, Luisi S, Severi FM. et al. 2001. Human placenta as a source of neuroendocrine factors. Biol. Neonate 79:150–56 [Google Scholar]
  184. Renfree MB. 2010. Review: marsupials: placental mammals with a difference. Placenta 31:Suppl.S21–26 [Google Scholar]
  185. Roberts JM. 2014. Pathophysiology of ischemic placental disease. Semin. Perinatol. 38:139–45 [Google Scholar]
  186. Roberts JM, Gammill H. 2005. Pre-eclampsia and cardiovascular disease in later life. Lancet 366:961–62 [Google Scholar]
  187. Roberts RM, Fisher SJ. 2011. Trophoblast stem cells. Biol. Reprod. 84:412–21 [Google Scholar]
  188. Romero R, Dey SK, Fisher SJ. 2014. Preterm labor: one syndrome, many causes. Science 345:760–65 [Google Scholar]
  189. Rosario GX, Konno T, Soares MJ. 2008. Maternal hypoxia activates endovascular trophoblast cell invasion. Dev. Biol. 314:362–75 [Google Scholar]
  190. Rossant J, Cross JC. 2001. Placental development: lessons from mouse mutants. Nat. Rev. Genet. 2:538–48 [Google Scholar]
  191. Rossant J, Tam PP. 2009. Blastocyst lineage formation, early embryonic asymmetries and axis patterning in the mouse. Development 136:701–13 [Google Scholar]
  192. Rubens CE, Sadovsky Y, Muglia L, Gravett MG, Lackritz E, Gravett C. 2014. Prevention of preterm birth: harnessing science to address the global epidemic. Sci. Transl. Med. 6:262sr5 [Google Scholar]
  193. Russ AP, Wattler S, Colledge WH, Aparicio SA, Carlton MB. et al. 2000. Eomesodermin is required for mouse trophoblast development and mesoderm formation. Nature 404:95–99 [Google Scholar]
  194. Saji F, Samejima Y, Kamiura S, Koyama M. 1999. Dynamics of immunoglobulins at the feto-maternal interface. Rev. Reprod. 4:81–89 [Google Scholar]
  195. Sandovici I, Hoelle K, Angiolini E, Constancia M. 2012. Placental adaptations to the maternal-fetal environment: implications for fetal growth and developmental programming. Reprod. Biomed. Online 25:68–89 [Google Scholar]
  196. Sasaki H. 2010. Mechanisms of trophectoderm fate specification in preimplantation mouse development. Dev. Growth Differ. 52:263–73 [Google Scholar]
  197. Savasan ZA, Goncalves LF, Bahado-Singh RO. 2014. Second- and third-trimester biochemical and ultrasound markers predictive of ischemic placental disease. Semin. Perinatol. 38:167–76 [Google Scholar]
  198. Schaffer L, Vogel J, Breymann C, Gassmann M, Marti HH. 2006. Preserved placental oxygenation and development during severe systemic hypoxia. Am. J. Physiol. Regul. Integr. Comp. Physiol. 290:R844–51 [Google Scholar]
  199. Schnakenberg SL, Matias WR, Siegal ML. 2011. Sperm-storage defects and live birth in Drosophila females lacking spermathecal secretory cells. PLOS Biol. 9:e1001192 [Google Scholar]
  200. Schneider H, Miller RK. 2010. Receptor-mediated uptake and transport of macromolecules in the human placenta. Int. J. Dev. Biol. 54:367–75 [Google Scholar]
  201. Selwood L, Johnson MH. 2006. Trophoblast and hypoblast in the monotreme, marsupial and eutherian mammal: evolution and origins. BioEssays 28:128–45 [Google Scholar]
  202. Semenza GL. 2009. Regulation of oxygen homeostasis by hypoxia-inducible factor 1. Physiology 24:97–106 [Google Scholar]
  203. Semenza GL. 2010. HIF-1: upstream and downstream of cancer metabolism. Curr. Opin. Genet. Dev. 20:51–56 [Google Scholar]
  204. Severa M, Islam SA, Waggoner SN, Jiang Z, Kim ND. et al. 2014. The transcriptional repressor BLIMP1 curbs host defenses by suppressing expression of the chemokine CCL8. J. Immunol. 192:2291–304 [Google Scholar]
  205. Shaw GM, Wise PH, Mayo J, Carmichael SL, Ley C. et al. 2014. Maternal prepregnancy body mass index and risk of spontaneous preterm birth. Paediatr. Perinat. Epidemiol. 28:302–11 [Google Scholar]
  206. Shibukawa Y, Yamazaki N, Kumasawa K, Daimon E, Tajiri M. et al. 2010. Calponin 3 regulates actin cytoskeleton rearrangement in trophoblastic cell fusion. Mol. Biol. Cell 21:223973–84 [Google Scholar]
  207. Shine R. 1983. Reptilian reproductive modes: the oviparity-viviparity continuum. Herpetologica 39:1–8 [Google Scholar]
  208. Shine R. 1989. Ecological influences on the evolution of vertebrate viviparity. . In Complex Organismal Functions: Integration and Evolution in Vertebrates, ed. DB Wake, G Roth 263–78 Chichester, UK: Wiley [Google Scholar]
  209. Shine R, Bull JJ. 1979. Evolution of live-bearing in lizards and snakes. Am. Nat. 113:905–23 [Google Scholar]
  210. Sibley CP, Boyd RD. 1988. Control of transfer across the mature placenta. Oxf. Rev. Reprod. Biol. 10:382–435 [Google Scholar]
  211. Simmons DG, Fortier AL, Cross JC. 2007. Diverse subtypes and developmental origins of trophoblast giant cells in the mouse placenta. Dev. Biol. 304:567–78 [Google Scholar]
  212. Simmons DG, Natale DR, Begay V, Hughes M, Leutz A, Cross JC. 2008. Early patterning of the chorion leads to the trilaminar trophoblast cell structure in the placental labyrinth. Development 135:2083–91 [Google Scholar]
  213. Soares MJ, Chakraborty D, Renaud SJ, Kubota K, Bu P. et al. 2012. Regulatory pathways controlling the endovascular invasive trophoblast cell lineage. J. Reprod. Dev. 58:283–87 [Google Scholar]
  214. Soares MJ, Konno T, Alam SM. 2007. The prolactin family: effectors of pregnancy-dependent adaptations. Trends Endocrinol. Metab. 18:114–21 [Google Scholar]
  215. Soncin F, Natale D, Parast MM. 2014. Signaling pathways in mouse and human trophoblast differentiation: a comparative review. Cell. Mol. Life Sci. 72:71291–302 [Google Scholar]
  216. Sood R, Kalloway S, Mast AE, Hillard CJ, Weiler H. 2006. Fetomaternal cross talk in the placental vascular bed: control of coagulation by trophoblast cells. Blood 107:3173–80 [Google Scholar]
  217. Staff AC, Dechend R, Pijnenborg R. 2010. Learning from the placenta: acute atherosis and vascular remodeling in preeclampsia—novel aspects for atherosclerosis and future cardiovascular health. Hypertension 56:1026–34 [Google Scholar]
  218. Stein DG. 2008. Progesterone exerts neuroprotective effects after brain injury. Brain Res. Rev. 57:386–97 [Google Scholar]
  219. Strumpf D, Mao CA, Yamanaka Y, Ralston A, Chawengsaksophak K. et al. 2005. Cdx2 is required for correct cell fate specification and differentiation of trophectoderm in the mouse blastocyst. Development 132:2093–102 [Google Scholar]
  220. Tabansky I, Lenarcic A, Draft RW, Loulier K, Keskin DB. et al. 2013. Developmental bias in cleavage-stage mouse blastomeres. Curr. Biol. 23:21–31 [Google Scholar]
  221. Takeda K, Ho VC, Takeda H, Duan LJ, Nagy A, Fong GH. 2006. Placental but not heart defects are associated with elevated hypoxia-inducible factor α levels in mice lacking prolyl hydroxylase domain protein 2. Mol. Cell. Biol. 26:8336–46 [Google Scholar]
  222. Tanaka S, Kunath T, Hadjantonakis AK, Nagy A, Rossant J. 1998. Promotion of trophoblast stem cell proliferation by FGF4. Science 282:2072–75 [Google Scholar]
  223. Tesser RB, Scherholz PL, do Nascimento L, Katz SG. 2010. Trophoblast glycogen cells differentiate early in the mouse ectoplacental cone: putative role during placentation. Histochem. Cell Biol. 134:83–92 [Google Scholar]
  224. Than NG, Pick E, Bellyei S, Szigeti A, Burger O. et al. 2004. Functional analyses of placental protein 13/galectin-13. Eur. J. Biochem. 271:1065–78 [Google Scholar]
  225. Thibault RE, Schultz RJ. 1978. Reproductive adaptations among viviparous fishes (Cyprinodontiformes poeciliidae). Evolution 32:320–33 [Google Scholar]
  226. Tsurudome M, Ito Y. 2000. Function of fusion regulatory proteins (FRPs) in immune cells and virus-infected cells. Crit. Rev. Immunol. 20:167–96 [Google Scholar]
  227. Ueno M, Lee LK, Chhabra A, Kim YJ, Sasidharan R. et al. 2013. c-Met–dependent multipotent labyrinth trophoblast progenitors establish placental exchange interface. Dev. Cell 27:373–86 [Google Scholar]
  228. Uy GD, Downs KM, Gardner RL. 2002. Inhibition of trophoblast stem cell potential in chorionic ectoderm coincides with occlusion of the ectoplacental cavity in the mouse. Development 129:3913–24 [Google Scholar]
  229. Villar J, Carroli G, Wojdyla D, Abalos E, Giordano D. et al. 2006. Preeclampsia, gestational hypertension and intrauterine growth restriction, related or independent conditions?. Am. J. Obstet. Gynecol. 194:921–31 [Google Scholar]
  230. Wang GL, Jiang BH, Rue EA, Semenza GL. 1995. Hypoxia-inducible factor 1 is a basic-helix-loop-helix-PAS heterodimer regulated by cellular O2 tension. PNAS 92:5510–14 [Google Scholar]
  231. Wang X, Campos B, Kaetzel MA, Dedman JR. 1999. Annexin V is critical in the maintenance of murine placental integrity. Am. J. Obstet. Gynecol. 180:1008–16 [Google Scholar]
  232. Weber S, Eckert D, Nettersheim D, Gillis AJ, Schafer S. et al. 2010. Critical function of AP-2γ/TCFAP2C in mouse embryonic germ cell maintenance. Biol. Reprod. 82:214–23 [Google Scholar]
  233. Weier JF, Weier HU, Jung CJ, Gormley M, Zhou Y. et al. 2005. Human cytotrophoblasts acquire aneuploidies as they differentiate to an invasive phenotype. Dev. Biol. 279:420–32 [Google Scholar]
  234. Werling U, Schorle H. 2002. Transcription factor gene AP-2γ essential for early murine development. Mol. Cell. Biol. 22:3149–56 [Google Scholar]
  235. Wildman DE, Chen C, Erez O, Grossman LI, Goodman M, Romero R. 2006. Evolution of the mammalian placenta revealed by phylogenetic analysis. PNAS 103:3203–8 [Google Scholar]
  236. Williams D. 2003. Pregnancy: a stress test for life. Curr. Opin. Obstet. Gynecol. 15:465–71 [Google Scholar]
  237. Wilson C, Nikitenko LL, Sargent IL, Rees MC. 2004. Adrenomedullin: multiple functions in human pregnancy. Angiogenesis 7:203–12 [Google Scholar]
  238. Wourms JP. 1981. Viviparity: the maternal-fetal relationship in fishes. Am. Zool. 21:473–515 [Google Scholar]
  239. Wourms JP. 1994. The challenges of piscine viviparity. Israel J. Zool. 40:551–68 [Google Scholar]
  240. Wourms JP, Lombardi J. 1992. Reflections on the evolution of piscine viviparity. Am. Zool. 32:276–93 [Google Scholar]
  241. Yamamoto H, Flannery ML, Kupriyanov S, Pearce J, McKercher SR. et al. 1998. Defective trophoblast function in mice with a targeted mutation of Ets2. Genes Dev. 12:1315–26 [Google Scholar]
  242. Yang CJ, Tan HP, Du YJ. 2014. The developmental disruptions of serotonin signaling may be involved in autism during early brain development. Neuroscience 267:1–10 [Google Scholar]
  243. Yang VS, Carter SA, Hyland SJ, Tachibana-Konwalski K, Laskey RA, Gonzalez MA. 2011. Geminin escapes degradation in G1 of mouse pluripotent cells and mediates the expression of Oct4, Sox2, and Nanog. Curr. Biol. 21:692–99 [Google Scholar]
  244. York TP, Eaves LJ, Neale MC, Strauss JF III. 2014. The contribution of genetic and environmental factors to the duration of pregnancy. Am. J. Obstet. Gynecol. 210:398–405 [Google Scholar]
  245. Yoshie M, Kashima H, Bessho T, Takeichi M, Isaka K, Tamura K. 2008. Expression of stathmin, a microtubule regulatory protein, is associated with the migration and differentiation of cultured early trophoblasts. Hum. Reprod. 23:2766–74 [Google Scholar]
  246. Yu Y, Zhang Y, Martin JA, Ozbolat IT. 2013. Evaluation of cell viability and functionality in vessel-like bioprintable cell-laden tubular channels. J. Biomech. Eng. 135:91011 [Google Scholar]
  247. Zamudio S, Wu Y, Ietta F, Rolfo A, Cross A. et al. 2007. Human placental hypoxia-inducible factor-1α expression correlates with clinical outcomes in chronic hypoxia in vivo. Am. J. Pathol. 170:2171–79 [Google Scholar]
  248. Zeldovich VB, Clausen CH, Bradford E, Fletcher DA, Maltepe E. et al. 2013. Placental syncytium forms a biophysical barrier against pathogen invasion. PLOS Pathog. 9:e1003821 [Google Scholar]
  249. Zhang X, Green KE, Yallampalli C, Dong YL. 2005. Adrenomedullin enhances invasion by trophoblast cell lines. Biol. Reprod. 73:619–26 [Google Scholar]
  250. Zhou Y, Bellingard V, Feng KT, McMaster M, Fisher SJ. 2003a. Human cytotrophoblasts promote endothelial survival and vascular remodeling through secretion of Ang2, PlGF, and VEGF-C. Dev. Biol. 263:114–25 [Google Scholar]
  251. Zhou Y, Chiu K, Brescia RJ, Combs CA, Katz MA. et al. 1993. Increased depth of trophoblast invasion after chronic constriction of the lower aorta in rhesus monkeys. Am. J. Obstet. Gynecol. 169:224–29 [Google Scholar]
  252. Zhou Y, Genbacev O, Fisher SJ. 2003b. The human placenta remodels the uterus by using a combination of molecules that govern vasculogenesis or leukocyte extravasation. Ann. N. Y. Acad. Sci. 995:73–83 [Google Scholar]
  253. Zhou Y, McMaster M, Woo K, Janatpour M, Perry J. et al. 2002. Vascular endothelial growth factor ligands and receptors that regulate human cytotrophoblast survival are dysregulated in severe preeclampsia and hemolysis, elevated liver enzymes, and low platelets syndrome. Am. J. Pathol. 160:1405–23 [Google Scholar]
  254. Zhou Y, Yuge A, Rajah AM, Unek G, Rinaudo PF, Maltepe E. 2014. LIMK1 regulates human trophoblast invasion/differentiation and is down-regulated in preeclampsia. Am. J. Pathol. 184:123321–31 [Google Scholar]
/content/journals/10.1146/annurev-cellbio-100814-125620
Loading
/content/journals/10.1146/annurev-cellbio-100814-125620
Loading

Data & Media loading...

  • Article Type: Review Article
This is a required field
Please enter a valid email address
Approval was a Success
Invalid data
An Error Occurred
Approval was partially successful, following selected items could not be processed due to error