The placenta: A multifaceted, transient organ

Philosophical Transactions of the Royal Society B: Biological Sciences

Volumn 370, Issue 1663, 2015, Pages

  Burton, Graham J ^a   Fowden, Abigail L ^a  

^a UNIVERSITY OF CAMBRIDGE   (United Kingdom)

Author keywords

Fetal growth; Placenta; Pregnancy

Indexed keywords

FUNCTIONAL ROLE; LACTATION; MATERNAL HEALTH; MEMBRANE; PREGNANCY;

PLACENTAL PEPTIDE HORMONE;

BODY POSTURE; FEMALE; FETUS; HUMAN; METABOLISM; PHYSIOLOGY; PLACENTA; PLACENTA CIRCULATION; PREGNANCY; VASCULAR REMODELING; VASCULARIZATION;

FEMALE; FETUS; HUMANS; PLACENTA; PLACENTAL CIRCULATION; PLACENTAL HORMONES; POSTURE; PREGNANCY; VASCULAR REMODELING;

EID: 84922326948     PISSN: 09628436     EISSN: 14712970     Source Type: Journal    
DOI: 10.1098/rstb.2014.0066     Document Type: Review

References (90)

1. Croft Long E. 1963 The placenta in lore and legend. Bull. Med. Libr. Assoc. 51, 233–241.
2. Yoshizawa RS. 2013 Review: Public perspectives on the utilization of human placentas in scientific research and medicine. Placenta 34, 9–13. (doi:10.1016/j.placenta.2012.10.014)
3. Mossman HW. 1937 Comparative morphogenesis of the fetal membranes and accessory uterine structures. Contrib. Embryol. 26, 129–246.
4. Burton GJ, Kaufmann P, Huppertz B. 2006 Anatomy and genesis of the placenta. In Knobil and Neill’s physiology of reproduction (ed. JD Neill), pp. 189–243, 3rd edn. Amsterdam, The Netherlands: Academic Press.
5. Benirschke K, Burton GJ, Baergen RN. 2012 Pathology of the human placenta, 6th edn. Heidelberg, Germany: Springer.
6. Simpson RA, Mayhew TM, Barnes PR. 1992 From 13 weeks to term, the trophoblast of human placenta grows by the continuous recruitment of new proliferative units: A study of nuclear number using the dissector. Placenta 13, 501–512. (doi:10.1016/0143-4004(92)90055-X)
7. Robbins JR, Skrzypczynska KM, Zeldovich VB, Kapidzic M, Bakardjiev AI. 2010 Placental syncytiotrophoblast constitutes a major barrier to vertical transmission of Listeria monocytogenes. PLoS Pathog. 6, e1000732. (doi:10.1371/journal.ppat.1000732)
8. Carter AM. 2000 Placental oxygen consumption. Part I: in vivo studies-a review. Placenta 21(Suppl. A), S31–S37. (doi:10.1053/plac.1999.0513)
9. Burton GJ, Tham SW. 1992 The formation of vasculo-syncytial membranes in the human placenta. J. Dev. Physiol. 18, 43–47.
10. Ockleford CD, Whyte A. 1977 Differeniated regions of human placental cell surface associated with exchange of materials between maternal and foetal blood: Coated vesicles. J. Cell Sci. 25, 293–312.
11. Gauster M, Huppertz B. 2010 The paradox of caspase 8 in human villous trophoblast fusion. Placenta 31, 82–88. (doi:10.1016/j.placenta.2009.12.007)
12. Rote NS, Wei BR, Xu C, Luo L. 2010 Caspase 8 and human villous cytotrophoblast differentiation. Placenta 31, 89–96. (doi:10.1016/j.placenta.2009.12.014)
13. Willis DM, O’Grady JP, Faber JJ, Thornburg KL. 1986 Diffusion permeability of cyanocobalamin in human placenta. Am. J. Physiol. 250, R459–R464.
14. Thornburg KL, Burry KJ, Adams AK, Kirk EP, Faber JJ. 1988 Permeability of placenta to inulin. Am. J. Obstet. Gynecol. 158, 1165–1169. (doi:10.1016/0002-9378(88)90246-3)
15. Bain MD, Copas DK, Taylor A, Landon MJ, Stacey TE. 1990 Permeability of the human placenta in vivo to four non-metabolized hydrophilic molecules. J. Physiol. 431, 505–513.
16. Kaufmann P, Schroder H, Leichtweiss HP. 1982 Fluid shift across the placenta: II. Fetomaternal transfer of horseradish peroxidase in the guinea pig. Placenta 3, 339–348. (doi:10.1016/S0143-4004(82)80027-1)
17. Burton GJ. 1987 The fine structure of the human placenta as revealed by scanning electron microscopy. Scan. Microsc. 1, 1811–1828.
18. Burton GJ, Watson AL. 1997 The structure of the human placenta: implications for initiating and defending against viral infections. Rev. Med. Virol. 7, 219–228. (doi:10.1002/(SICI)1099-1654(199712)7:4,219::AID-RMV205.3.0.CO;2-E)
19. Brownbill P, Edwards D, Jones C, Mahendran D, Owen D, Sibley C, Johnson R, Swanson P, Nelson DM. 1995 Mechanisms of alphafetoprotein transfer in the perfused human placental cotyledon from uncomplicated pregnancy. J. Clin. Invest. 96, 2220–2226. (doi:10.1172/JCI118277)
20. Mayhew TM, Jackson MR, Boyd PA. 1993 Changes in oxygen diffusive conductances of human placental during gestation (10–41 weeks) are commensurate with the gain in fetal weight. Placenta 14, 51–61. (doi:10.1016/S0143-4004(05)80248-6)
21. Reshetnikova OS, Burton GJ, Milovanov AP. 1994 Effects of hypobaric hypoxia on the feto-placental unit: The morphometric diffusing capacity of the villous membrane at high altitude. Am. J. Obstet. Gynecol. 171, 1560–1565. (doi:10.1016/0002-9378(94)90402-2)
22. Stulc J, Svihovec J, Drabkova J, Stribrny J, Kobilkova J, Vido I, Dolezal A. 1978 Electrical potential difference across the mid-term human placenta. Acta Obstet. Gynecol. Scand. 57, 125–126. (doi:10.3109/00016347809155889)
23. Mellor DJ, Cockburn F, Lees MM, Blagden A. 1969 Distribution of ions and electrical potential differences between mother and fetus in the human at term. J. Obstet. Gynaecol. Br. Commonw. 76, 993–998. (doi:10.1111/j.1471-0528.1969.tb09465.x)
24. Atkinson DE, Boyd RDH, Sibley CP. 2006 Placental transfer. In Knobil and Neill’s physiology of reproduction (ed. JD Neill), pp. 2787–2846. Amsterdam, The Netherlands: Elsevier.
25. Tessier DR, Ferraro ZM, Gruslin A. 2013 Role of leptin in pregnancy: consequences of maternal obesity. Placenta 34, 205–211. (doi:10.1016/j.placenta.2012.11.035)
26. Fowden AL, Sferruzzi-Perri AN, Coan PM, Constancia M, Burton GJ. 2009 Placental efficiency and adaptation: endocrine regulation. J. Physiol. 587, 3459–3472. (doi:10.1113/jphysiol.2009.173013)
27. Sibley CP et al. 2004 Placental-specific insulin-like growth factor 2 (Igf2) regulates the diffusional exchange characteristics of the mouse placenta. Proc. Natl Acad. Sci. USA 101, 8204–8208. (doi:10.1073/pnas.0402508101)
28. Coan PM, Vaughan OR, Sekita Y, Finn SL, Burton GJ, Constancia M, Fowden AL. 2010 Adaptations in placental phenotype support fetal growth during undernutrition of pregnant mice. J. Physiol. 588, 527–538. (doi:10.1113/jphysiol.2009.181214)
29. Sferruzzi-Perri AN, Vaughan OR, Coan PM, Suciu MC, Darbyshire R, Constancia M, Burton GJ, Fowden AL. 2011 Placental-specific Igf2 deficiency alters developmental adaptations to undernutrition in mice. Endocrinology 152, 3202–3212. (doi:10.1210/en.2011-0240)
30. King BF. 1982 Absorption of peroxidase-conjugated immunoglobulin G by human placenta: an in vitro study. Placenta 3, 395–406. (doi:10.1016/S0143-4004(82)80032-5)
31. Hempstock J, Cindrova-Davies T, Jauniaux E, Burton GJ. 2004 Endometrial glands as a source of nutrients, growth factors and cytokines during the first trimester of human pregnancy: a morphological and immunohistochemical study. Reprod. Biol. Endocrinol. 2, 58. (doi:10.1186/1477-7827-2-58)
32. Jauniaux E, Gulbis B. 2000 Fluid compartments of the embryonic environment. Hum. Reprod. Update 6, 268–278. (doi:10.1093/humupd/6.3.268)
33. Karimu AL, Burton GJ. 1994 The effects of maternal vascular pressure on the dimensions of the placental capillaries. Br. J. Obstet. Gynaecol. 101, 57–63. (doi:10.1111/j.1471-0528.1994.tb13011.x)
34. Hutchinson ES, Brownbill P, Jones NW, Abrahams VM, Baker PN, Sibley CP, Crocker IP. 2009 Uteroplacental haemodynamics in the pathogenesis of pre-eclampsia. Placenta 30, 634–641. (doi:10.1016/j.placenta.2009.04.011)
35. Burton GJ, Woods AW, Jauniaux E, Kingdom JC. 2009 Rheological and physiological consequences of conversion of the maternal spiral arteries for uteroplacental blood flow during human pregnancy. Placenta 30, 473–482. (doi:10.1016/j.placenta.2009.02.009)
36. Wooding FP, Burton GJ. 2008 Comparative placentation. Structures, functions and evolution. Berlin, Germany: Springer.
37. Harris JWS, Ramsey EM. 1966 The morphology of human uteroplacental vasculature. Contrib. Embryol. 38, 43–58.
38. Pijnenborg R, Vercruysse L, Hanssens M. 2006 The uterine spiral arteries in human pregnancy: facts and controversies. Placenta 27, 939–958. (doi:10.1016/j.placenta.2005.12.006)
39. Whitley GS, Cartwright JE. 2010 Cellular and molecular regulation of spiral artery remodelling: lessons from the cardiovascular field. Placenta 31, 465–474. (doi:10.1016/j.placenta.2010.03.002)
40. Kam EPY, Gardner L, Loke YW, King A. 1999 The role of trophoblast in the physiological change in decidual spiral arteries. Hum. Reprod. 14, 2131–2138. (doi:10.1093/humrep/14.8.2131)
41. Harris LK. 2010 Trophoblast-vascular cell interactions in early pregnancy: How to remodel a vessel. Placenta 31, S93–S98. (doi:10.1016/j.placenta.2009.12.012)
42. Hanna J et al. 2006 Decidual NK cells regulate key developmental processes at the human fetalmaternal interface. Nat. Med. 12, 1065–1074. (doi:10.1038/nm1452)
43. Xiong S et al. 2013 Maternal uterine NK cellactivating receptor KIR2DS1 enhances placentation. J. Clin. Invest. 123, 4264–4272. (doi:10.1172/JCI68991)
44. Moffett A, Colucci F. 2014 Uterine NK cells: active regulators at the maternal-fetal interface. J. Clin. Invest. 124, 1872–1879. (doi:10.1172/JCI68107)
45. Hiby SE et al. 2010 Maternal activating KIRs protect against human reproductive failure mediated by fetal HLA-C2. J. Clin. Invest. 120, 4102–4110. (doi:10.1172/JCI43998)
46. 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. (doi:10.1016/j.ajog.2010.08.009)
47. Redman CW, Sargent IL. 2005 Latest advances in understanding preeclampsia. Science 308, 1592–1594. (doi:10.1126/science.1111726)
48. Levine RJ et al. 2004 Circulating angiogenic factors and the risk of preeclampsia. N. Engl. J. Med. 350, 672–683. (doi:10.1056/NEJMoa031884)
49. Cindrova-Davies T, Spasic-Boskovic O, Jauniaux E, Charnock-Jones DS, Burton GJ. 2007 Nuclear factorkappa B, p38, and stress-activated protein kinase mitogen-activated protein kinase signaling pathways regulate proinflammatory cytokines and apoptosis in human placental explants in response to oxidative stress: effects of antioxidant vitamins. Am. J. Pathol. 170, 1511–1520. (doi:10.2353/ajpath.2007.061035)
50. Yung HW, Atkinson D, Campion-Smith T, Olovsson M, Charnock-Jones DS, Burton GJ. 2014 Differential activation of placental unfolded protein response pathways implies heterogeneity in causation of early- and late-onset pre-eclampsia. J. Pathol. 234, 262–276. (doi:10.1002/path.4394)
51. Yung HW, Calabrese S, Hynx D, Hemmings BA, Cetin I, Charnock-Jones DS, Burton GJ. 2008 Evidence of placental translation inhibition and endoplasmic reticulum stress in the etiology of human intrauterine growth restriction. Am. J. Pathol. 173, 451–462. (doi:10.2353/ajpath.2008.071193)
52. Burton GJ, Yung HW, Cindrova-Davies T, Charnock-Jones DS. 2009 Placental endoplasmic reticulum stress and oxidative stress in the pathophysiology of unexplained intrauterine growth restriction and early onset preeclampsia. Placenta 30(Suppl. A), S43–S48. (doi:10.1016/j.placenta.2008.11.003)
53. Zhang K, Kaufman RJ. 2008 From endoplasmicreticulum stress to the inflammatory response. Nature 454, 455–462. (doi:10.1038/nature07203)
54. Abitbol MM. 1993 Growth of the fetus in the abdominal cavity. Am. J. Phys. Anthropol. 91, 367–378. (doi:10.1002/ajpa.1330910309)
55. Kauppila A, Koskinen M, Puolakka J, Tuimala R, Kuikka J. 1980 Decreased intervillous and unchanged myometrial blood flow in supine recumbency. Obstet. Gynecol. 55, 203–205. (doi:10.1097/00006250-198003001-00050)
56. Hung TH, Burton GJ. 2006 Hypoxia and reoxygenation: a possible mechanism for placental oxidative stress in preeclampsia. Taiwan J. Obstet. Gynecol. 45, 189–200. (doi:10.1016/S1028-4559(09)60224-2)
57. Burton GJ, Charnock-Jones DS, Jauniaux E. 2009 Regulation of vascular growth and function in human placenta. Reproduction 138, 895–902. (doi:10.1530/REP-09-0092)
58. Lash GE, Naruse K, Innes BA, Robson SC, Searle RF, Bulmer JN. 2010 Secretion of angiogenic growth factors by villous cytotrophoblast and extravillous trophoblast in early human pregnancy. Placenta 31, 545–548. (doi:10.1016/j.placenta.2010.02.020)
59. Leach L, Babawale MO, Anderson M, Lammiman M. 2002 Vasculogenesis, angiogenesis and the molecular organisation of endothelial junctions in the early human placenta. J. Vasc. Res. 39, 246–259. (doi:10.1159/000063690)
60. Jirkovska M, Janacek J, Kalab J, Kubinova L. 2008 Three-dimensional arrangement of the capillary bed and its relationship to microrheology in the terminal villi of normal term placenta. Placenta 29, 892–897. (doi:10.1016/j.placenta.2008.07.004)
61. Myatt L. 1992 Control of vascular resistance in the human placenta. Placenta 13, 329–341. (doi:10.1016/0143-4004(92)90057-Z)
62. Barber A, Robson SC, Myatt L, Bulmer JN, Lyall F. 2001 Heme oxygenase expression in human placenta and placental bed: reduced expression of placenta endothelial HO-2 in preeclampsia and fetal growth restriction. FASEB J. 15, 1158–1168. (doi:10.1096/fj.00-0376com)
63. Cindrova-Davies T, Herrera EA, Niu Y, Kingdom J, Giussani DA, Burton GJ. 2013 Reduced cystathionine gamma-lyase and increased miR-21 expression are associated with increased vascular resistance in growth-restricted pregnancies: Hydrogen sulfide as a placental vasodilator. Am. J. Pathol. 182, 1448–1458. (doi:10.1016/j.ajpath.2013.01.001)
64. Petraglia F, Florio P, Torricelli M. 2006 Placental endocrine function. In Knobil and Neill’s physiology of reproduction (ed. JD Neill), pp. 2847–2897, 3rd edn. Amsterdam, The Netherlands: Elsevier.
65. Brunton PJ, Russell JA. 2010 Endocrine induced changes in brain function during pregnancy. Brain Res. 1364, 198–215. (doi:10.1016/j.brainres.2010.09.062)
66. Freemark M. 2006 Regulation of maternal metabolism by pituitary and placental hormones: Roles in fetal development and metabolic programming. Horm. Res. 65(Suppl. 3), 41–49. (doi:10.1159/000091505)
67. Newbern D, Freemark M. 2011 Placental hormones and the control of maternal metabolism and fetal growth. Curr. Opin. Endocrinol. Diabetes Obes. 18, 409–416. (doi:10.1097/MED.0b013e32834c800d)
68. Papper Z et al. 2009 Ancient origin of placental expression in the growth hormone genes of anthropoid primates. Proc. Natl Acad. Sci. USA 106, 17 083–17 088. (doi:10.1073/pnas.0908377106)
69. Cross JC, Baczyk D, Dobric N, Hemberger M, Hughes M, Simmons DG, Yamamoto H, Kingdom JCP. 2003 Genes, development and evolution of the placenta. Placenta 24, 123–130. (doi:10.1053/plac.2002.0887)
70. Ladyman SR, Augustine RA, Grattan DR. 2010 Hormone interactions regulating energy balance during pregnancy. J. Neuroendocrinol. 22, 805–817.
71. Barbour LA, Shao J, Qiao L, Leitner W, Anderson M, Friedman JE, Draznin B. 2004 Human placental growth hormone increases expression of the p85 regulatory unit of phosphatidylinositol 3-kinase and triggers severe insulin resistance in skeletal muscle. Endocrinology 145, 1144–1150. (doi:10.1210/en.2003-1297)
72. Caufriez A, Frankenne F, Hennen G, Copinschi G. 1993 Regulation of maternal IGF-I by placental GH in normal and abnormal human pregnancies. Am. J. Physiol. 265, E572–577.
73. Sferruzzi-Perri AN, Owens JA, Pringle KG, Roberts CT. 2011 The neglected role of insulin-like growth factors in the maternal circulation regulating fetal growth. J. Physiol. 589, 7–20. (doi:10.1113/jphysiol.2010.198622)
74. Bloxam DL. 1985 Human placental energy metabolism: its relevance to in vitro perfusion. Contrib. Gynecol. Obstet. 13, 59–69.
75. Jauniaux E, Jurkovic D, Gulbis B, Collin WP, Zaidi J, Campbell S. 1994 Investigation of the acid-base balance of coelomic and amniotic fluids in early human pregnancy. Am. J. Obstet. Gynecol. 170, 1359–1365. (doi:10.1016/S0002-9378(94)70156-3)
76. Schneider H. 2000 Placental oxygen consumption. Part II: in vitro studies-a review. Placenta 21(Suppl. A), S38–S44. (doi:10.1053/plac.1999.0512)
77. Jauniaux E, Hempstock J, Teng C, Battaglia F, 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, 1171–1175. (doi:10.1210/jc.2004-1513)
78. Coller HA. 2014 Is cancer a metabolic disease? Am. J. Pathol. 184, 4–17. (doi:10.1016/j.ajpath.2013.07.035)
79. Boyd JD. 1959 Glycogen in early human implantation sites. Memoirs Soc. Endocrinol. 6, 26–34.
80. Burton GJ, Watson AL, Hempstock J, Skepper JN, Jauniaux E. 2002 Uterine glands provide histiotrophic nutrition for the human fetus during the first trimester of pregnancy. J. Clin. Endocrinol. Metab. 87, 2954–2959. (doi:10.1210/jcem.87.6.8563)
81. McTernan CL, Draper N, Nicholson H, Chalder SM, Driver P, Hewison M, Kilby MD, Stewart PM. 2001 Reduced placental 11beta-hydroxysteroid dehydrogenase type 2 mRNA levels in human pregnancies complicated by intrauterine growth restriction: an analysis of possible mechanisms.J. Clin. Endocrinol. Metab. 86, 4979–4983.
82. Dy J, Guan H, Sampath-Kumar R, Richardson BS, Yang K. 2008 Placental 11beta-hydroxysteroid dehydrogenase type 2 is reduced in pregnancies complicated with idiopathic intrauterine growth restriction: evidence that this is associated with an attenuated ratio of cortisone to cortisol in the umbilical artery. Placenta 29, 193–200. (doi:10.1016/j.placenta.2007.10.010)
83. Baron-Cohen S et al. In press. Elevated fetal steroidogenic activity in autism. Mol. Psychiatry. (doi:10.1038/mp.2014.48)
84. Stark MJ, Wright IM, Clifton VL. 2009 Sex-specific alterations in placental 11beta-hydroxysteroid dehydrogenase 2 activity and early postnatal clinical course following antenatal betamethasone. Am. J. Physiol. Regul. Integr. Comp. Physiol. 297, R510–R514. (doi:10.1152/ajpregu.00175.2009)
85. St-Pierre MV, Serrano MA, Macias RI, Dubs U, Hoechli M, Lauper U, Meier PJ, Marin JJ. 2000 Expression of members of the multidrug resistance protein family in human term placenta. Am. J. Physiol. Regul. Integr. Comp. Physiol. 279, R1495–R1503.
86. Burton GJ, Fowden AL. 2012 Review: the placenta and developmental programming: balancing fetal nutrient demands with maternal resource allocation. Placenta 33, S23–S27. (doi:10.1016/j.placenta.2011.11.013)
87. Carter AM. 2011 Comparative studies of placentation and immunology in non-human primates suggest a scenario for the evolution of deep trophoblast invasion and an explanation for human pregnancy disorders. Reproduction 141, 391–396. (doi:10.1530/REP-10-0530)
88. Martin RD. 2007 The evolution of human reproduction: a primatological perspective. Am. J. Phys. Anthropol. 45, 59–84. (doi:10.1002/ajpa.20734)
89. Crosley EJ, Elliot MG, Christians JK, Crespi BJ. 2013 Placental invasion, preeclampsia risk and adaptive molecular evolution at the origin of the great apes: Evidence from genome-wide analyses. Placenta 34, 127–132. (doi:10.1016/j.placenta.2012.12.001)
90. Jauniaux E, Poston L, Burton GJ. 2006 Placentalrelateddiseases of pregnancy: involvement of oxidative stress and implications in human evolution. Hum. Reprod. Update 12, 747–755. (doi:10.1093/humupd/dml016)