Abstract
Throughout placental development, different types of villi are formed that have differing structural and functional specializations. Despite this diversification, all villi exhibit the same basic structure (Fig. 6.1).
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References
Adler RR, Ng AK, Rote NS (1995) Monoclonal antiphosphatidylserine antibody inhibits intercellular fusion of the choriocarcinoma line, JAR. Biol Reprod 53:905–910
Ahmed A, Li XF, Dunk C, Whittle MJ, Rushton DI, Rollason T (1995) Colocalisation of vascular endothelial growth factor and its Flt-1 receptor in human placenta. Growth Factors 12:235–243
Aladjem S (1967) The syncytial knot: a sign of active syncytial proliferation. Am J Obstet Gynecol 99:350–358
Al-Husaini AM (2009) Role of placenta in the vertical transmission of human immunodeficiency virus. J Perinatol 29:331–336
Ali KZM, Burton GJ, Morad N, Ali ME (1996) Does hypercapillarization influence the branching pattern of terminal villi in the human placenta at high altitude? Placenta 17:677–682
Allaire AD, Ballenger KA, Wells SR, McMahon MJ, Lessey BA (2000) Placental apoptosis in preeclampsia. Obstet Gynecol 96:271–276
Alvarez H, Benedetti WL, De Leonis VK (1967) Syncytial proliferation in normal and toxemic pregnancies. Obstet Gynecol 29:637–643
Alvarez H, Benedetti WL, Morel RL, Scavarelli M (1970) Trophoblast development gradient and its relationship to placental hemodynamics. Am J Obstet Gynecol 106:416–420
Amarnani S, Sangrat B, Chaudhuri G (1999) Effects of selected endothelium-dependent vasodilators on fetoplacental vasculature: physiological implications. Am J Physiol 277:H842–H847
Amenta PS, Gay S, Vaheri A, Martinez-Hernandez A (1986) The extracellular matrix is an integrated unit: ultrastructural localization of collagen types I, III, IV, V, VI, fibronectin, and laminin in human term placenta. Coll Relat Res 6:125–152
Amstutz E (1960) Observations on the maturation of chroionic villi in the human placenta with special reference to epithelial plates. Acta Anat (Basel) 42:12–30
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 25:311–314
Anteby EY, Natanson-Yaron S, Greenfield C, Goldman-Wohl D, Haimov-Kochman R, Holzer H, Yagel S (2005) Human placental Hofbauer cells express sprouty proteins: a possible modulating mechanism of villous branching. Placenta 26:476–483
Aplin JD, Jones CJ, Harris LK (2009) Adhesion molecules in human trophoblast – a review. I. Villous trophoblast. Placenta 30:293–298
Apps R, Gardner L, Moffett A (2008) A critical look at HLA-G. Trends Immunol 29:313–321
Arkwright PD, Redman CW, Williams PJ, Dwek RA, Rademacher TW (1991) Syncytiotrophoblast membrane protein glycosylation patterns in normal human pregnancy and changes with gestational age and parturition. Placenta 12:637–651
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 Invest 91:2744–2753
Austgulen R, Isaksen CV, Chedwick L, Romundstad P, Vatten L, Craven C (2004) Pre-eclampsia: associated with increased syncytial apoptosis when the infant is small-for-gestational-age. J Reprod Immunol 61:39–50
Autio-Harmainen H, Sandberg M, Pihlajaniemi T, Vuorio E (1991) Synthesis of laminin and type IV collagen by trophoblastic cells and fibroblastic stromal cells in the early human placenta. Lab Invest 64:483–491
Baczyk D, Satkunaratnam A, Nait-Oumesmar B, Huppertz B, Cross JC, Kingdom JC (2004) Complex patterns of GCM1 mRNA and protein in villous and extravillous trophoblast cells of the human placenta. Placenta 25:553–559
Baczyk D, Dunk C, Huppertz B, Maxwell C, Reister F, Giannoulias D, Kingdom JC (2006) Bi-potential behaviour of cytotrophoblasts in first trimester chorionic villi. Placenta 27:367–374
Baczyk D, Drewlo S, Proctor L, Dunk C, Lye S, Kingdom J (2009) Glial cell missing-1 transcription factor is required for the differentiation of the human trophoblast. Cell Death Differ 16:719–727
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
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
Beham A, Denk H, Desoye G (1988) The distribution of intermediate filament proteins, actin and desmoplakins in human placental tissue as revealed by polyclonal and monoclonal antibodies. Placenta 9:479–492
Benirschke K, Willes L (2010) Deportation of trophoblastic emboli to maternal lung. A source of cell-free DNA in maternal blood? Chimerism 1:15–18
Berryman M, Gary R, Bretscher A (1995) Ezrin oligomers are major cytoskeletal components of placental microvilli: a proposal for their involvement in cortical morphogenesis. J Cell Biol 131:1231–1242
Bianco P, Fisher LW, Young MF, Termine JD, Robey PG (1990) Expression and localization of the two small proteoglycans biglycan and decorin in developing human skeletal and non-skeletal tissues. J Histochem Cytochem 38:1549–1563
Birdsey TJ, Boyd RD, Sibley CP, Greenwood SL (1997) Microvillous membrane potential (Em) in villi from first trimester human placenta: comparison to Em at term. Am J Physiol 273:R1519–R1528
Bisseling TM, Steegers EAP, van den Heuvel JJM, Siero HLM, van de Water FM, Walker AJ, Steegers-Theunissen RPM, Smits P, Russel FGM (2004) Placental folate transport and binding are not impaired in pregnancies complicated by fetal growth restriction. Placenta 25:588–593
Black S, Kadyrov M, Kaufmann P, Ugele B, Emans N, Huppertz B (2004) Syncytial fusion of human trophoblast depends on caspase 8. Cell Death Differ 11:90–98
Blaise S, de Parseval N, Benit L, Heidmann T (2003) Genomewide screening for fusogenic human endogenous retrovirus envelopes identifies syncytin 2, a gene conserved on primate evolution. Proc Natl Acad Sci USA 100:13013–13018
Blond JL, Lavillette D, Cheynet V, Bouton O, Oriol G, Chapel-Fernandes S, Mandrand B, Mallet F, Cosset FL (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 74:3321–3329
Bockle BC, Solder E, Kind S, Romani N, Sepp NT (2008) DC-sign+ CD163+ macrophages expressing hyaluronan receptor LYVE-1 are located within chorion villi of the placenta. Placenta 29:187–192
Boehm KD, Kelley MF, Ilan J (1989) The interleukin 2 gene is expressed in the syncytiotrophoblast of the human placenta. Proc Natl Acad Sci USA 86:656–660
Boura ALA, Walter WAW (1991) Autocoids and the control of vascular tone in the human umbilical-placental circulation. Placenta 12:453–477
Bourgeois C, Robert B, Rebourcet R, Mondon F, Mignot TM, Duc-Goiran P, Ferre F (1997) Endothelin-1 and ETA receptor expression in vascular smooth muscle cells from human placenta: a new ETA receptor messenger ribonucleic acid is generated by alternative splicing of exon 3. J Clin Endocrinol Metab 82:3116–3123
Boyd JD (1959) Some aspects of the relationship between mother and child. Ulster Med J 28:35–46
Boyd JD, Hamilton WJ (1966) Electron microscopic observations on the cytotrophoblast contribution to the syncytium in the human placenta. J Anat 100:535–548
Boyd JD, Hamilton WJ (1970) The human placenta. Heffer and Sons, Cambridge
Boyd MT, Bax CM, Bax BE, Bloxam DL, Weiss RA (1993) The human endogenous retrovirus ERV-3 is upregulated in differentiating placental trophoblast cells. Virology 196:905–909
Bracero LA, Beneck D, Kirshenbaum N, Peiffer M, Stalter P, Schulman H (1989) Doppler velocimetry and placental disease. Am J Obstet Gynecol 161:388–393
Bradbury FM, Ockleford CD (1990) A confocal and conventional epifluorescence microscope study of the intermediate filaments in chorionic villi. J Anat 169:173–187
Bright NA, Ockleford CD, Anwar M (1994) Ontogeny and distribution of Fcg receptors in the human placenta. Transport or immune surveillance? J Anat 184:297–308
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
Bulmer JN, Johnson PM (1984) Macrophage populations in the human placenta and amniochorion. Clin Exp Immunol 57:393–403
Bulmer JN, Morrison L, Johnson PM, Meager A (1990) Immunohistochemical localization of interferons in human placental tissues in normal, ectopic, and molar pregnancy. Am J Reprod Immunol 22:109–116
Burgos MH, Rodriguez EM (1966) Specialized zones in the trophoblast of the human term placenta. Am J Obstet Gynecol 96:342–356
Burrows TD, King A, Loke YW (1993) Expression of integrins by human trophoblast and differential adhesion to laminin or fibronectin. Hum Reprod 8:475–484
Burton GJ (1986a) Intervillous bridges in the mature human placenta; syncytial fusion or section artifacts? J Anat 145:12–23
Burton GJ (1986b) Scanning electron microscopy of intervillous connections in the mature human placenta. J Anat 147:245–254
Burton GJ (1987) The fine structure of the human placenta as revealed by scanning electron microscopy. Scanning Microsc 1:1811–1828
Burton GJ (1990) On the varied appearances of the human placental villous surface visualised by scanning electron microscopy. Scanning Microsc 4:501–507
Burton GJ, Feneley MR (1992) Capillary volume fraction is the principal determinant of villous membrane thickness in the human placenta at term. J Dev Physiol 17:39–45
Burton GJ, Jauniaux E (1995) Sonographic, stereological and Doppler flow velocimetric assessments of placental maturity. Br J Obstet Gynaecol 102:818–825
Burton GJ, Jauniaux E (2004) Placental oxidative stress; from miscarriage to preeclampsia. J Soc Gynecol Invest 11:342–352
Burton GJ, Jones CJ (2009) Syncytial knots, sprouts, apoptosis, and trophoblast deportation from the human placenta. Taiwan J Obstet Gynecol 48:28–37
Burton GJ, Tham SW (1992) The formation of vasculo-syncytial membranes in the human placenta. J Dev Physiol 18:43–47
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
Burton GJ, Ingram SC, Palmer ME (1987) The influence of the mode of fixation on morphometrical data derived from terminal villi in the human placenta at term: a comparison of immersion and perfusion fixation. Placenta 8:37–51
Burton GJ, Thurley KW, Skepper JN (1991) A technique for correlative scanning and transmission electron microscopy of individual human placental villi: an example demonstrating syncytial sprouts in early gestation. Scanning Microsc 5:451–458; discussion 458–459
Burton GJ, O’Shea S, Rostron T, Mullen JE, Aiyer S, Skepper JN, Smith R, Banatvala JE (1996) Significance of placental damage in vertical transmission of human immunodeficiency virus. J Med Virol 50:237–243
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
Burton GJ, Skepper JN, Hempstock J, Cindrova T, Jones CJP, Jauniaux E (2003) A reappraisal of the contrasting morphological appearances of villous cytotrophoblast cells during early human pregnancy; evidence for both apoptosis and primary necrosis. Placenta 24:297–305
Burton GJ, Charnock-Jones DS, Jauniaux E (2009) Regulation of vascular growth and function in human placenta. Reproduction 138:895–902
Cantle SJ, Kaufmann P, Luckhardt M, Schweikhart G (1987) Interpretation of syncytial sprouts and bridges in the human placenta. Placenta 8:221–234
Castellucci M, Kaufmann P (1982) A three-dimensional study of the normal human placental villous core: II. Stromal architecture. Placenta 3:269–286
Castellucci M, Zaccheo D (1989) The Hofbauer cells of the human placenta: morphological and immunological aspects. Prog Clin Biol Res 296:443–451
Castellucci M, Zaccheo D, Pescetto G (1980) A three-dimensional study of the normal human placental villous core. I. The Hofbauer cells. Cell Tissue Res 210:235–247
Castellucci M, Celona A, Bartels H, Steininger B, Benedetto V, Kaufmann P (1987) Mitosis of the Hofbauer cell: possible implications for a fetal macrophage. Placenta 8:65–76
Castellucci M, Classen-Linke I, Muhlhauser J, Kaufmann P, Zardi L, Chiquet-Ehrismann R (1991) The human placenta: a model for tenascin expression. Histochemistry 95:449–458
Castellucci M, Theelen T, Pompili E, Fumagalli L, De Renzis G, Muhlhauser J (1994) Immunohistochemical localization of serine-protease inhibitors in the human placenta. Cell Tissue Res 278:283–289
Castro E, Parks EA, Galambos C (2011) Neither normal nor diseased placentas contain lymphatic vessels. Placenta 32:310–316
Cavicchia JC (1971) Junctional complexes in the trophoblast of the human full term placenta. J Anat 108:339–346
Cetin I, Alvino G (2009) Intrauterine growth restriction: implications for placental metabolism and transport. A review. Placenta 30 Suppl A:S77–S82
Challier JC, Galtier M, Kacemi A, Guillaumin D (1999) Pericytes of term human foeto-placental microvessels: ultrastructure and visualization. Cell Mol Biol (Noisy-le-Grand) 45:89–100
Challier JC, Basu S, Bintein T, Minium J, Hotmire K, Catalano PM, Hauguel-de Mouzon S (2008) Obesity in pregnancy stimulates macrophage accumulation and inflammation in the placenta. Placenta 29:274–281
Charnock Jones DS, Kaufmann P, Mayhew TM (2004) Aspects of human fetoplacental vasculogenesis and angiogenesis. I. Molecular recognition. Placenta 25:103–113
Chen C-P, Aplin JD (2003) Placental extracellular matrix: gene expression, deposition by placental fibroblasts and the effect of oxygen. Placenta 24:316–325
Chen K, Thomas SR, Keaney JF (2003) Beyond LDL oxidation: ROS in vascular signal transduction. Free Radic Biol Med 35:117–132
Chen CP, Chen CY, Yang YC, Su TH, Chen H (2004) Decreased placental GCM1 (glial cells missing) gene expression in pre-eclampsia. Placenta 25:413–421
Chen CP, Wang KG, Chen CY, Yu C, Chuang HC, Chen H (2006) Altered placental syncytin and its receptor ASCT2 expression in placental development and pre-eclampsia. BJOG 113:152–158
Chen CP, Liu SH, Lee MY, Chen YY (2008) Heparan sulfate proteoglycans in the basement membranes of the human placenta and decidua. Placenta 29:309–316
Cheng HM, Johnson PM (1985) A description of human placental syncytiotrophoblast membrane glycosphingolipids. Placenta 6: 229–238
Chiang MH, Liang FY, Chen CP, Chang CW, Cheong ML, Wang LJ, Liang CY, Lin FY, Chou CC, Chen H (2009) Mechanism of hypoxia-induced GCM1 degradation: implications for the pathogenesis of preeclampsia. J Biol Chem 284:17411–17419
Clark DE, Smith SK, Sharkey AM, Charnock-Jones DS (1996) Localization of VEGF and expression of its receptors flt and KDR in human placenta throughout pregnancy. Hum Reprod 11:1090–1098
Cindrova-Davies T, Herrera E, Niu YG, Giussani DA, Burton GJ (2011) Vasodilator effect of hydrogen sulphide (H2S) in the perfused human placenta. Placenta 32:A38
Cleal JK, Lewis RM (2008) The mechanisms and regulation of placental amino acid transport to the human foetus. J Neuroendocrinol 20:419–426
Coan PM, Angiolini E, Sandovici I, Burton GJ, Constancia M, Fowden AL (2008) Adaptations in placental nutrient transfer capacity to meet fetal growth demands depend on placental size in mice. J Physiol 586:4567–4576
Contractor SF, Banks RW, Jones CJ, Fox H (1977) A possible role for placental lysosomes in the formation of villous syncytiotrophoblast. Cell Tissue Res 178:411–419
Critchley GR, Burton GJ (1987) Intralobular variations in barrier thickness in the mature human placenta. Placenta 8:185–194
Cronier L, Herve JC, Deleze J, Malassine A (1997) Regulation of gap junctional communication during human trophoblast differentiation. Microsc Res Tech 38:21–28
Cronier L, Alsat E, Herve JC, Deleze J, Malassine A (1998) Dexamethasone stimulates gap junctional communication, peptide hormone production and differentiation of human term trophoblast. Trophoblast Res 11:35–49
Cronier L, Dubut A, Guibourdenche J, Malassine A (1999) Effects of endothelin on villous trophoblast differentiation and free intracellular calcium. Trophoblast Res 13:69–86
Cronier L, Defamie N, Dupays L, Theveniau-Ruissy M, Goffin F, Pointis G, Malassine A (2002) Connexin expression and gap junctional intercellular communication in human first trimester trophoblast. Mol Hum Reprod 8:1005–1013
Cronier L, Frendo J-L, Defamie N, Pidoux G, Bertin G, Guibourdenche J, Pointis G, Malassine A (2003) Requirement of gap junctional intercellular communication for human villous trophoblast differentiation. Biol Reprod 69:1472–1480
Dakour J, Li H, Chen H, Morrish DW (1999) EGF promotes development of a differentiated trophoblast phenotype having c-myc and junB proto-oncogene activation. Placenta 20:119–126
Daleke DL (2007) Phospholipid flippases. J Biol Chem 282:821–825
Damiano A, Zotta E, Goldstein J, Reisin I, Ibarra C (2001) Water channel proteins AQP3 and AQP9 are present in syncytiotrophoblast of human term placenta. Placenta 22:776–781
Damiano AE, Zotta E, Ibarra C (2006) Functional and molecular expression of AQP9 channel and UT-A transporter in normal and preeclamptic human placentas. Placenta 27:1073–1081
Dave-Sharma S, Wilson RC, Harbison MD, Newfield R, Azar MR, Krozowski ZS, Funder JW, Shackleton CH, Bradlow HL, Wei JQ, Hertecant J, Moran A, Neiberger RE, Balfe JW, Fattah A, Daneman D, Akkurt HI, De Santis C, New MI (1998) Examination of genotype and phenotype relationships in 14 patients with apparent mineralocorticoid excess. J Clin Endocrinol Metab 83:2244–2254
Demir R (1979) Scanning electron-microscopic observations on the surfaces of chorionic villi of young and mature placentas. Acta Anat (Basel) 105:226–232
Demir R, Kaufmann P, Castellucci M, Erbengi T, Kotowski A (1989) Fetal vasculogenesis and angiogenesis in human placental villi. Acta Anat 136:190–203
Demir R, Kosanke G, Kohnen G, Kertschanska S, Kaufmann P (1997) Classification of human placental stem villi: review of structural and functional aspects. Microsc Res Tech 38:29–41
Desoye G, Hauguel-de Mouzon S (2007) The human placenta in gestational diabetes mellitus. The insulin and cytokine network. Diabetes Care 30 Suppl 2:S120–S126
Desoye G, Hartmann M, Jones CJ, Wolf HJ, Kohnen G, Kosanke G, Kaufmann P (1997) Location of insulin receptors in the placenta and its progenitor tissues. Microsc Res Tech 38:63–75
Di Iorio R, Marinoni E, Letizia C, Villaccio B, Alberini A, Cosmi EV (1999) Adrenomedullin production is increased in normal human pregnancy. Eur J Endocrinol 140:201–206
Di Simone N, Luigi MP, Marco D, Fiorella DN, Silvia D, Clara DM, Alessandro C (2007) Pregnancies complicated with antiphospholipid syndrome: the pathogenic mechanism of antiphospholipid antibodies: a review of the literature. Ann N Y Acad Sci 1108:505–514
Doherty KR, Cave A, Davis DB, Delmonte AJ, Posey A, Earley JU, Hadhazy M, McNally EM (2005) Normal myoblast fusion requires myoferlin. Development 132:5565–5575
Dong YL, Chauhan M, Green KE, Vegiraju S, Wang HQ, Hankins GD, Yallampalli C (2006) Circulating calcitonin gene-related peptide and its placental origins in normotensive and preeclamptic pregnancies. Am J Obstet Gynecol 195:1657–1667
Droge W (2002) Free radicals in the physiological control of cell function. Physiol Rev 82:47–95
Dupressoir A, Vernochet C, Bawa O, Harper F, Pierron G, Opolon P, Heidmann T (2009) Syncytin-A knockout mice demonstrate the critical role in placentation of a fusogenic, endogenous retrovirus-derived, envelope gene. Proc Natl Acad Sci USA 106:12127–12132
Durst-Zivkovic B (1973) Occurence of mast cells in the placenta. Anat Anz 134:225–229
Edwards HC, Booth AG (1987) Calcium-sensitive, lipid-binding cytoskeletal proteins of the human placental microvillar region. J Cell Biol 105:303–311
Ellery PM, Cindrova-Davies T, Jauniaux E, Ferguson-Smith AC, Burton GJ (2009) Evidence for transcriptional activity in the syncytiotrophoblast of the human placenta. Placenta 30:329–334
Enders AC (1965) Formation of syncytium from cytotrophoblast in the human placenta. Obstet Gynecol 25:378–386
Erel CT, Dane B, Calay Z, Kaleli S, Aydinli K (2001) Apoptosis in the placenta of pregnancies complicated with IUGR. Int J Gynaecol Obstet 73:229–235
Ericsson A, Hamark B, Powell TL, Jansson T (2005) Glucose transporter isoform 4 is expressed in the syncytiotrophoblast of first trimester human placenta. Hum Reprod 20:521–530
Esnault C, Priet S, Ribet D, Vernochet C, Bruls T, Lavialle C, Weissenbach J, Heidmann T (2008) A placenta-specific receptor for the fusogenic, endogenous retrovirus-derived, human syncytin-2. Proc Natl Acad Sci USA 105:17532–17537
Ezashi T, Das P, Roberts RM (2005) Low O2 tensions and the prevention of differentiation of hES cells. Proc Natl Acad Sci USA 102:4783–4788
Fadok VA, Voelker DR, Campbell PA, Cohen JJ, Bratton DL, Henson PM (1992) Exposure of phosphatidylserine on the surface of apoptotic lymphocytes triggers specific recognition and removal by macrophages. J Immunol 148:2207–2216
Farley AE, Graham CH, Smith GN (2004) Contractile properties of human placental anchoring villi. Am J Physiol Regul Integr Comp Physiol 287:R680–R685
Fedoroff N (2006) Redox regulatory mechanisms in cellular stress responses. Ann Bot (Lond) 98:289–300
Firth KF, Broughton Pipkin F (1989) Human alpha- and beta-calcitonin gene-related peptides are vasodilators in human chorionic plate vasculature. Am J Obstet Gynecol 161:1318–1319
Fogarty NME, Mayhew TM, Ferguson-Smith AC, Burton GJ (2011) A quantitative analysis of transcriptionally active syncytiotrophoblastic nuclei across human gestation. J Anat 219(5):601–610
Forbes K, Westwood M (2010) Maternal growth factor regulation of human placental development and fetal growth. J Endocrinol 207:1–16
Forbes K, Westwood M, Baker PN, Aplin JD (2008) Insulin-like growth factor I and II regulate the life cycle of trophoblast in the developing human placenta. Am J Physiol Cell Physiol 294:C1313–C1322
Fowden AL, Sferruzzi-Perri AN, Coan PM, Constancia M, Burton GJ (2009) Placental efficiency and adaptation: endocrine regulation. J Physiol 587:3459–3472
Fox H (1964) The pattern of villous variability in the normal placenta. J Obstet Gynaecol Br Commonw 71:749–758
Fox H (1965) The significance of villous syncytial knots in the human placenta. J Obstet Gynaecol Br Commonw 72:347–355
Fox H (1967a) Perivillous fibrin deposition in the human placenta. Am J Obstet Gynecol 98:245–251
Fox H (1967b) The incidence and significance of vasculo-syncytial membranes in the human placenta. J Obstet Gynaecol Br Commonw 47:28–33
Fox H (1968) Fibrinoid necrosis of placental villi. J Obstet Gynaecol Br Commonw 75:448–452
Fox H (1970) Effect of hypoxia on trophoblast in organ culture. A morphologic and autoradiographic study. Am J Obstet Gynecol 107:1058–1064
Fox H, Agrafojo-Blanco A (1974) Scanning electron microscopy of the human placenta in normal and abnormal pregnancies. Eur J Obstet Gynecol Reprod Biol 4:45–50
Frank HG, Malekzadeh F, Kertschanska S, Crescimanno C, Castellucci M, Lang I, Desoye G, Kaufmann P (1994) Immunohistochemistry of two different types of placental fibrinoid. Acta Anat 150:55–68
Frendo JL, Cronier L, Bertin G, Guibourdenche J, Vidaud M, Evain-Brion D, Malassine A (2003a) Involvement of connexin 43 in human trophoblast cell fusion and differentiation. J Cell Sci 116:3413–3421
Frendo JL, Olivier D, Cheynet V, Blond JL, Bouton O, Vidaud M, Rabreau M, Evain-Brion D, Mallet F (2003b) Direct involvement of HERV-W Env glycoprotein in human trophoblast cell fusion and differentiation. Mol Cell Biol 23:3566–3574
Fukuchi Y, Nakajima H, Sugiyama D, Hirose I, Kitamura T, Tsuji K (2004) Human placenta-derived cells have mesenchymal stem/progenitor cell potential. Stem Cells 22:649–658
Furugori K, Kurauchi O, Itakura A, Kanou Y, Murata Y, Mizutani S, Seo H, Tomoda Y, Nakamura T (1997) Levels of hepatocyte growth factor and its messenger ribonucleic acid in uncomplicated pregnancies and those complicated by preeclampsia. J Clin Endocrinol Metab 82:2726–2730
Gadella BM, Harrison RA (2002) Capacitation induces cyclic adenosine 3′,5′-monophosphate-dependent, but apoptosis-unrelated, exposure of aminophospholipids at the apical head plasma membrane of boar sperm cells. Biol Reprod 67:340–350
Garcia-Lloret MI, Morrish DW, Wegmann TG, Honore L, Turner AR, Guilbert LJ (1994) Demonstration of functional cytokine-placental interactions: CSF-1 and GM-CSF stimulate human cytotrophoblast differentiation and peptide hormone secretion. Exp Cell Res 214:46–54
Garcia-Lloret MI, Winkler-Lowen B, Guilbert LJ (2000) Monocytes adhering by LFA-1 to placental syncytiotrophoblasts induce local apoptosis via release of TNF-alpha. A model for hematogenous initiation of placental inflammations. J Leukoc Biol 68:903–908
Gaunt M, Ockleford CD (1986) Microinjection of human placenta. II: biological application. Placenta 7:325–331
Gauster M, Huppertz B (2010) The paradox of caspase 8 in human villous trophoblast fusion. Placenta 31:82–88
Gauster M, Siwetz M, Huppertz B (2009a) Fusion of villous trophoblast can be visualized by localizing active caspase 8. Placenta 30:547–550
Gauster M, Moser G, Orendi K, Huppertz B (2009b) Factors involved in regulating trophoblast fusion: potential role in the development of preeclampsia. Placenta 30 Suppl A:S49–S54
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 17:336–345
Georgieff MK, Wobken JK, Welle J, Burdo JR, Connor JR (2000) Identification and localization of divalent metal transporter-1 (DMT-1) in term human placenta. Placenta 21:799–804
Giles WB, Trudinger BJ, Baird PJ (1985) Fetal umbilical artery flow velocity waveforms and placental resistance: pathological correlation. Br J Obstet Gynaecol 92:31–38
Glazier JD, Cetin I, Perugino G, Ronzoni S, Grey AM, Mahendran D, Marconi AM, Pardi G, Sibley CP (1997) Association between the activity of the system A amino acid transporter in the microvillous plasma membrane of the human placenta and severity of fetal compromise in intrauterine growth restriction. Pediatr Res 42:514–519
Glover DM, Brownstein D, Burchett S, Larsen A, Wilson CB (1987) Expression of HLA class II antigens and secretion of interleukin-1 by monocytes and macrophages from adults and neonates. Immunology 61:195–201
Godfrey KM, Matthews N, Glazier J, Jackson A, Wilman C, Sibley CP (1998) Neutral amino acid uptake by the microvillous plasma membrane of the human placenta is inversely related to fetal size at birth in normal pregnancy. J Clin Endocrinol Metab 83:3320–3326
Godoy V, Riquelme G (2008) Distinct lipid rafts in subdomains from human placental apical syncytiotrophoblast membranes. J Membr Biol 224:21–31
Goldstein J, Braverman M, Salafia C, Buckley P (1988) The phenotype of human placental macrophages and its variation with gestational age. Am J Pathol 133:648–659
Gordon Z, Eytan O, Jaffa AJ, Elad D (2007) Fetal blood flow in branching models of the chorionic arterial vasculature. Ann N Y Acad Sci 1101:250–265
Gude NM, Stevenson JL, Rogers S, Best JD, Kalionis B, Huisman MA, Erwich JJ, Timmer A, King RG (2003) GLUT12 expression in human placenta in first trimester and term. Placenta 24:566–570
Guilbert LJ, Riddell M, Winkler-Lowen B (2010) Caspase activation is not required for villous cytotrophoblast fusion into syncytiotrophoblasts. Placenta 31:982–988
Halliwell B, Gutteridge JMC (1999) Free radicals in biology and medicine. Oxford Science Publications, Oxford
Han R, Campbell KP (2007) Dysferlin and muscle membrane repair. Curr Opin Cell Biol 19:409–416
Harris LK, Crocker IP, Baker PN, Aplin JD, Westwood M (2011) IGF2 actions on trophoblast in human placenta are regulated by the insulin-like growth factor 2 receptor, which can function as both a signaling and clearance receptor. Biol Reprod 84(3):440–446
Heazell AE, Crocker IP (2008) Live and let die – regulation of villous trophoblast apoptosis in normal and abnormal pregnancies. Placenta 29:772–783
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
Heinrich D, Metz J, Raviola E, Forssmann WG (1976) Ultrastructure of perfusion-fixed fetal capillaries in the human placenta. Cell Tissue Res 172:157–169
Hemberger M, Udayashankar R, Tesar P, Moore H, Burton GJ (2010) ELF5-enforced transcriptonal networks define an epigentically regulated trophoblast stem cell compartment in the human placenta. Hum Mol Genet 19:2456–2467
Hempstock J, Jauniaux E, Greenwold N, Burton GJ (2003) The contribution of placental oxidative stress to early pregnancy failure. Hum Pathol 34:1265–1275
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
Ho HC (2010) Redistribution of nuclear pores during formation of the redundant nuclear envelope in mouse spermatids. J Anat 216:525–532
Hoeldtke NJ, Wagner RK, Calhoun BC, Hume RF Jr (2000) Vasodilatory response of fetoplacental vasculature to adrenomedullin after constriction with the thromboxane sympathomimetic U46619. Am J Obstet Gynecol 183:1573–1578
Holcberg G, Kossenjans W, Brewer A, Miodovnik M, Myatt L (1995) Selective vasodilator effects of atrial natriuretic peptide in the human placental vasculature. J Soc Gynecol Investig 2:1–5
Hoshina M, Boothby M, Boime I (1982) Cytological localization of chorionic gonadotropin alpha and placental lactogen mRNAs during development of the human placenta. J Cell Biol 93:190–198
Hoshina M, Boothby M, Hussa R, Pattillo R, Camel HM, Boime I (1985) Linkage of human chorionic gonadotrophin and placental-lactogen biosynthesis to trophoblast differentiation and tumorigenesis. Placenta 6:163–172
Huang SA, Dorfman DM, Genest DR, Salvatore D, Larsen PR (2003) Type 3 iodothyronine deiodinase is highly expressed in the human uteroplacental unit and in fetal epithelium. J Clin Endocrinol Metab 88:1384–1388
Hughes M, Dobric N, Scott IC, Su L, Starovic M, St-Pierre B, Egan SE, Kingdom JC, Cross JC (2004) The Hand1, Stra13 and Gcm1 transcription factors override FGF signaling to promote terminal differentiation of trophoblast stem cells. Dev Biol 271:26–37
Humphrey RG, Smith SD, Pang L, Sadovsky Y, Nelson DM (2005) Fibrin enhances differentiation, but not apoptosis, and limits hypoxic injury of cultured term human trophoblasts. Placenta 26:491–497
Hung TH, Skepper JN, Burton GJ (2001) In vitro ischemia-reperfusion injury in term human placenta as a model for oxidative stress in pathological pregnancies. Am J Pathol 159:1031–1043
Hung T-H, Skepper JN, Charnock-Jones DS, Burton GJ (2002) Hypoxia/reoxygenation: a potent inducer of apoptotic changes in the human placenta and possible etiological factor in preeclampsia. Circ Res 90:1274–1281
Huppertz B, Kaufmann P (1999) The apoptosis cascade in human villous trophoblast. Trophoblast Res 13:215–242
Huppertz B, Frank H-G, Kingdom JCP, Reister F, Kaufmann P (1998) Villous cytotrophoblastic regulation of the syncytial apoptotic cascade in the human placenta. Histochem Cell Biol 110:495–508
Huppertz B, Frank H-G, Reister F, Kingdom J, Korr H, Kaufmann P (1999a) Apoptosis cascade progresses during turnover of human trophoblast: analysis of villous cytotrophoblast and syncytial fragments in vitro. Lab Invest 79:1687–1702
Huppertz B, Frank HG, Kaufmann P (1999b) The apoptosis cascade-morphological and immunohistochemical methods for its visualization. Anat Embryol (Berl) 200:1–18
Huppertz B, Kingdom J, Caniggia I, Desoye G, Black S, Korr H, Kaufmann P (2003) Hypoxia favours necrotic versus apoptotic shedding of placental syncytiotrophoblast into the maternal circulation. Placenta 24:181–190
Huppertz B, Kadyrov M, Kingdom JC (2006) Apoptosis and its role in the trophoblast. Am J Obstet Gynecol 195:29–39
Iklé FA (1961) Trophoblastzellen im strömenden Blut. Schweiz Med Wochenschr 91:934–945
Iklé FA (1964) Dissemination of syncytial trophoblastic cells in the maternal blood stream during pregnancy. Bull Schweiz Akad Med Wiss 20:62–72
Ingman K, Cookson VJ, Jones CJ, Aplin JD (2010) Characterisation of Hofbauer cells in first and second trimester placenta: incidence, phenotype, survival in vitro and motility. Placenta 31:535–544
Ishihara N, Matsuo H, Murakoshi H, Laoag-fernandez J, Samoto T, Maruo T (2000) Changes in proliferative potential, apoptosis and Bcl-2 protein expression in cytotrophoblasts and syncytiotrophoblast in human placenta over the course of pregnancy. Endocr J 47:317–327
Ishihara N, Matsuo H, Murakoshi H, Laoag-Fernandez J, Samoto T, Maruo T (2002) Increased apoptosis in the syncytiotrophoblast in human term placentas complicated by either preeclampsia or intrauterine growth retardation. Am J Obstet Gynecol 186:158–166
Jackson MR, Mayhew TM, Boyd PA (1992) Quantitative description of the elaboration and maturation of villi from 10 weeks of gestation to term. Placenta 13:357–370
Jackson MR, Walsh AJ, Morrow RJ, Mullen JBM, Lye SJ, Ritchie JWK (1995) Reduced placental villous tree elaboration in small-for-gestational-age pregnancies: relationship with umbilical artery Doppler waveforms. Am J Obstet Gynecol 172:518–525
Jansson T, Powell TL (2006) IFPA 2005 award in placentology lecture. Human placental transport in altered fetal growth: does the placenta function as a nutrient sensor? - a review. Placenta 27 Suppl A:S91–S97
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 77:1554–1562
Jansson N, Pettersson J, Haafiz A, Ericsson A, Palmberg I, Tranberg M, Ganapathy V, Powell TL, Jansson T (2006) Down-regulation of placental transport of amino acids precedes the development of intrauterine growth restriction in rats fed a low protein diet. J Physiol 576:935–946
Jauniaux E, Gulbis B (2000) Fluid compartments of the embryonic environment. Hum Reprod Update 6:268–278
Jauniaux E, Watson AL, Burton GJ (2001) Evaluation of respiratory gases and acid-base gradients in fetal fluids and uteroplacental tissue between 7 and 16 weeks. Am J Obstet Gynecol 184:998–1003
Jauniaux E, Hempstock J, Greenwold N, Burton GJ (2003) Trophoblastic oxidative stress in relation to temporal and regional differences in maternal placental blood flow in normal and abnormal early pregnancies. Am J Pathol 162:115–125
Jerat S, DiMarzo L, Morrish DW, Kaufman S (2008) Adrenomedullin-induced dilation of human placental arteries is modulated by an endothelium-derived constricting factor. Regul Pept 146:183–188
Jokhi PP, King A, Loke YW (1994) Reciprocal expression of epidermal growth factor receptor (EGF-R) and c-erbB2 by non-invasive and invasive human trophoblast populations. Cytokine 6:433–442
Jokimaa VI, Kujari HP, Ekholm EM, Inki PL, Anttila L (2000) Placental expression of syndecan 1 is diminished in preeclampsia. Am J Obstet Gynecol 183:1495–1498
Jones CJP, Fox H (1977) Syncytial knots and intervillous bridges in the human placenta: an ultrastructural study. J Anat 124:275–286
Jones CJP, Fox H (1980) An ultrastructural and ultrahistochemical study of the human placenta in maternal pre-eclampsia. Placenta 1:61–76
Jones CJP, Fox H (1991) Ultrastructure of the normal human placenta. Electron Microsc Rev 4:129–178
Jones HN, Powell TL, Jansson T (2007) Regulation of placental nutrient transport – a review. Placenta 28:763–774
Jones CJP, Owens S, Senga E, Van Rheenen P, Faragher B, Denton J, Brabin BJ (2008a) Placental expression of α2,6-linked sialic acid is upregulated in malaria. Placenta 29:300–304
Jones CJ, Harris LK, Whittingham J, Aplin JD, Mayhew TM (2008b) A re-appraisal of the morphophenotype and basal lamina coverage of cytotrophoblasts in human term placenta. Placenta 29:215–219
Kadyrov M, Kaufmann P, Huppertz B (2001) Expression of a cytokeratin 18 neo-epitope is a specific marker for trophoblast apoptosis in human placenta. Placenta 22:44–48
Kalter SS, Helmke RJ, Heberling RL, Panigel M, Fowler AK, Strickland JE, Hellman A (1973) Brief communication: C-type particles in normal human placentas. J Natl Cancer Inst 50:1081–1084
Kar M, Ghosh D, Sengupta J (2007) Histochemical and morphological examination of proliferation and apoptosis in human first trimester villous trophoblast. Hum Reprod 22:2814–2823
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
Karimu AL, Burton GJ (1995a) Human term placental capillary endothelial cell specialization: a morphometric study. Placenta 16:93–99
Karimu AL, Burton GJ (1995b) The distribution of microvilli over the villous surface of the normal human term placenta is homogenous. Reprod Fertil Dev 7:1269–1273
Kataoka H, Shimomura T, Kawaguchi T, Hamasuna R, Itoh H, Kitamura N, Miyazawa K, Koono M (2000) Hepatocyte growth factor activator inhibitor type 1 is a specific cell surface binding protein of hepatocyte growth factor activator (HGFA) and regulates HGFA activity in the pericellular microenvironment. J Biol Chem 275:40453–40462
Kaufmann P (1972) Observations on the Langhans cells in the human placenta. Z Zellforsch Mikrosk Anat 128:283–302
Kaufmann P (1983) Vergleichend-anatomische und funktionelle Aspekte des Placenta-Baues. Funkt Biol Med 2:71–79
Kaufmann P (1985) Influence of ischemia and artificial perfusion on placental ultrastructure and morphometry. Contrib Gynecol Obstet 13:18–26
Kaufmann P, Stark J (1972) Enzyme-histochemical studies on mature human placental villi. I. Differentiation and degeneration of the trophoblast. Histochemie 29:65–82
Kaufmann P, Stark J, Stegner HE (1977) The villous stroma of the human placenta. 1. The ultrastructure of fixed connective tissue cells. Cell Tissue Res 177:105–121
Kaufmann P, Luckhardt M, Schweikhart G, Cantle SJ (1987) Cross-sectional features and three-dimensional structure of human placental villi. Placenta 8:235–247
Kaufmann P, Huppertz B, Frank H-G (1996) The fibrinoids of the human placenta: origin, composition and functional relevance. Ann Anat 178:485–501
Kertschanska S, Kosanke G, Kaufmann P (1997) Pressure dependence of so-called transtrophoblastic channels during fetal perfusion of human placental villi. Microsc Res Tech 38:52–62
Khaliq A, Li XF, Shams M, Sisi P, Acevedo CA, Whittle MJ, Weich H, Ahmed A (1996) Localisation of placenta growth factor (PIGF) in human term placenta. Growth Factors 13:243–250
Khong TY, Lane EB, Robertson WB (1986) An immunocytochemical study of fetal cells at the maternal-placental interface using monoclonal antibodies to keratins, vimentin and desmin. Cell Tissue Res 246:189–195
Kilby MD, Afford S, Li XF, Strain AJ, Ahmed A, Whittle MJ (1996) Localisation of hepatocyte growth factor and its receptor (c-met) protein and mRNA in human term placenta. Growth Factors 13:133–139
Kim JS, Romero R, Kim MR, Kim YM, Friel L, Espinoza J, Kim CJ (2008) Involvement of Hofbauer cells and maternal T cells in villitis of unknown aetiology. Histopathology 52:457–464
King BF (1983) The organization of actin filaments in human placental villi. J Ultrastruct Res 85:320–328
King BF, Menton DN (1975) Scanning electron microscopy of human placental villi from early and late in gestation. Am J Obstet Gynecol 122:824–828
King RG, Gude NM, Di Iulio JL, Brennecke SP (1995) Regulation of human placental fetal vessel tone: role of nitric oxide. Reprod Fertil Dev 7:1407–1411
Kippler M, Hoque AM, Raqib R, Ohrvik H, Ekstrom EC, Vahter M (2010) Accumulation of cadmium in human placenta interacts with the transport of micronutrients to the fetus. Toxicol Lett 192:162–168
Kliman HJ, Feinman MA, Strauss JF (1987) Differentiation of human cytotrophoblast into syncytiotrophoblast in culture. Trophoblast Res 2:407–421
Knerr I, Schubert SW, Wich C, Amann K, Aigner T, Vogler T, Jung R, Dotsch J, Rascher W, Hashemolhosseini S (2005) Stimulation of GCMa and syncytin via cAMP mediated PKA signaling in human trophoblastic cells under normoxic and hypoxic conditions. FEBS Lett 579:3991–3998
Knofler M, Saleh L, Bauer S, Vasicek R, Griesinger G, Strohmer H, Helmer H, Husslein P (2000) Promoter elements and transcription factors involved in differentiation-dependent human chorionic gonadotrophin-alpha messenger ribonucleic acid expression of term villous trophoblasts. Endocrinology 141:3737–3748
Kohnen G, Kertschanska S, Demir R, Kaufmann P (1996) Placental villous stroma as a model system for myofibroblast differentiation. Histochem Cell Biol 105:415–429
Kokawa K, Shikone T, Nakano R (1998) Apoptosis in human chorionic villi and decidua during normal embryonic development and spontaneous abortion in the first trimester. Placenta 19:21–26
Korhonen M, Virtanen I (2001) Immunohistochemical localization of laminin and fibronectin isoforms in human placental villi. J Histochem Cytochem 49:313–322
Krozowski Z, MaGuire JA, Stein-Oakley AN, Dowling J, Smith RE, Andrews RK (1995) Immunohistochemical localization of the 11 beta-hydroxysteroid dehydrogenase type II enzyme in human kidney and placenta. J Clin Endocrinol Metab 80:2203–2209
Kudaka W, Oda T, Jinno Y, Yoshimi N, Aoki Y (2008) Cellular localization of placenta-specific human endogenous retrovirus (HERV) transcripts and their possible implication in pregnancy-induced hypertension. Placenta 29:282–289
Kudo Y, Boyd CA (1990) Characterization of amino acid transport systems in human placental basal membrane vesicles. Biochim Biophys Acta 1021:169–174
Kudo Y, Boyd CA, Sargent IL, Redman CW (2003) 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
Kumazaki K, Nakayama M, Yanagihara I, Suehara N, Wada Y (2004) Immunohistochemical distribution of Toll-like receptor 4 in term and preterm human placentas from normal and complicated pregnancy including chorioamnionitis. Hum Pathol 35:47–54
Küstermann W (1981) Über ‘Proliferationsknoten’ und ‘Syncytialbrücken’ der menschlichen Plazenta. Anat Anz 150:144–157
Lairmore MD, Cuthbert PS, Utley LL, Morgan CJ, Dezzutti CS, Anderson CL, Sedmak DD (1993) Cellular localization of CD4 in the human placenta. Implications for maternal-to-fetal transmission of HIV. J Immunol 151:1673–1681
Lamkanfi M, Festjens N, Declercq W, Vanden Berghe T, Vandenabeele P (2007) Caspases in cell survival, proliferation and differentiation. Cell Death Differ 14:44–55
Lang CT, Markham KB, Behrendt NJ, Suarez AA, Samuels P, Vandre DD, Robinson JM, Ackerman WE (2009) Placental dysferlin expression is reduced in severe preeclampsia. Placenta 30:711–718
Leach L (2002) The phenotype of the human materno-fetal endothelial barrier: molecular occupancy of paracellular junctions dictate permeability and angiogenic plasticity. J Anat 200:599–606
Leach RE, Khalifa R, Ramirez ND, Das SK, Wang J, Dey SK, Romero R, Armant DR (1999) Multiple roles for heparin-binding epidermal growth factor-like growth factor are suggested by its cell-specific expression during the human endometrial cycle and early placentation. J Clin Endocrinol Metab 84:3355–3363
Leach L, Lammiman MJ, Babawale MO, Hobson SA, Bromilou B, Lovat S, Simmonds MJ (2000) Molecular organization of tight and adherens junctions in the human placental vascular tree. Placenta 21:547–557
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
Leach RE, Kilburn BA, Petkova A, Romero R, Armant DR (2008) Diminished survival of human cytotrophoblast cells exposed to hypoxia/reoxygenation injury and associated reduction of heparin-binding epidermal growth factor-like growth factor. Am J Obstet Gynecol 198:471 e1–471 e7; discussion 471 e7–471 e8
Learmont JG, Poston L (1996) Nitric oxide is involved in flow-induced dilation of isolated human small fetoplacental arteries. Am J Obstet Gynecol 174:583–588
Lee X, Keith JC Jr, Stumm N, Moutsatsos I, McCoy JM, Crum CP, Genest D, Chin D, Ehrenfels C, Pijnenborg R, van Assche FA, Mi S (2001) Downregulation of placental syncytin expression and abnormal protein localization in pre-eclampsia. Placenta 22:808–812
Lee MY, Huang JP, Chen YY, Aplin JD, Wu YH, Chen CY, Chen PC, Chen CP (2009) Angiogenesis in differentiated placental multipotent mesenchymal stromal cells is dependent on integrin alpha5beta1. PLoS One 4:e6913
Leibl W, Kerjaschki D, Horandner H (1975) Microvilli-free areas of human placentas. Gegenbaurs Morphol Jahrb 121:26–28
Leung DN, Smith SC, To KF, Sahota DS, Baker PN (2001) Increased placental apoptosis in pregnancies complicated by preeclampsia. Am J Obstet Gynecol 184:1249–1250
Liang CY, Wang LJ, Chen CP, Chen LF, Chen YH, Chen H (2010) GCM1 regulation of the expression of syncytin 2 and its cognate receptor MFSD2A in human placenta. Biol Reprod 83:387–395
Lievano S, Alarcon L, Chavez-Munguia B, Gonzalez-Mariscal L (2006) Endothelia of term human placentae display diminished expression of tight junction proteins during preeclampsia. Cell Tissue Res 324:433–448
Linton EA, Rodriguez-Linares B, Rashid-Doubell F, Ferguson DJ, Redman CW (2003) Caveolae and caveolin-1 in human term villous trophoblast. Placenta 24:745–757
Lo YM, Corbetta N, Chamberlain PF, Rai V, Sargent IL, Redman CW, Wainscoat JS (1997) Presence of fetal DNA in maternal plasma and serum. Lancet 350:485–487
Lo YM, Leung TN, Tein MS, Sargent IL, Zhang J, Lau TK, Haines CJ, Redman CW (1999) Quantitative abnormalities of fetal DNA in maternal serum in preeclampsia. Clin Chem 45:184–188
Loke YW (1982) Transmission of parasites across the placenta. Adv Parasitol 21:155–228
Loke YW, Eremin O, Ashby J, Day S (1982) Characterization of the phagocytic cells isolated from the human placenta. J Reticuloendothel Soc 31:317–324
Longtine MS, Chen B, Odibo AO, Zhong Y, Nelson DM (2012) Villous trophoblast apoptosis is elevated and restricted to cytotrophoblasts in pregnancies complicated by preeclampsia, IUGR, or preeclampsia with IUGR. Placenta. 33(5), Epub Feb 15
Luo SS, Ishibashi O, Ishikawa G, Ishikawa T, Katayama A, Mishima T, Takizawa T, Shigihara T, Goto T, Izumi A, Ohkuchi A, Matsubara S, Takeshita T (2009) Human villous trophoblasts express and secrete placenta-specific microRNAs into maternal circulation via exosomes. Biol Reprod 81:717–729
Lyall F, Barber A, Myatt L, Bulmer JN, Robson SC (2000) Hemeoxygenase expression in human placenta and placental bed implies a role in regulation of trophoblast invasion and placental function. FASEB J 14:208–219
Lyden TW, Vogt E, Ng AK, Johnson PM, Rote NS (1992) Monoclonal antiphospholipid antibody reactivity against human placental trophoblast. J Reprod Immunol 22:1–14
Lyden TW, Johnson PM, Mwenda JM, Rote NS (1994) Ultrastructural characterization of endogenous retroviral particles isolated from normal human placentas. Biol Reprod 51:152–157
Lyden TW, Anderson CL, Robinson JM (2002) The endothelium but not the syncytiotrophoblast of human placenta expresses caveolae. Placenta 23:640–652
Macara LM, Kingdom JCP, Kaufmann P (1993) Control of the fetoplacental circulation. Fetal Matern Med Rev 5:167–179
Maelfait J, Beyaert R (2008) Non-apoptotic functions of caspase-8. Biochem Pharmacol 76:1365–1373
Malassine A, Handschuh K, Tsatsaris V, Gerbaud P, Cheynet V, Oriol G, Mallet F, Evain-Brion D (2005) Expression of HERV-W Env glycoprotein (syncytin) in the extravillous trophoblast of first trimester human placenta. Placenta 26:556–562
Malassine A, Blaise S, Handschuh K, Lalucque H, Dupressoir A, Evain-Brion D, Heidmann T (2007) Expression of the fusogenic HERV-FRD Env glycoprotein (syncytin 2) in human placenta is restricted to villous cytotrophoblastic cells. Placenta 28:185–191
Malassine A, Frendo JL, Evain-Brion D (2010) Trisomy 21- affected placentas highlight prerequisite factors for human trophoblast fusion and differentiation. Int J Dev Biol 54:475–482
Mangeney M, Renard M, Schlecht-Louf G, Bouallaga I, Heidmann O, Letzelter C, Richaud A, Ducos B, Heidmann T (2007) Placental syncytins: genetic disjunction between the fusogenic and immunosuppressive activity of retroviral envelope proteins. Proc Natl Acad Sci USA 104:20534–20539
Many A, Westerhausen-Larson A, Kanbour-Shakir A, Roberts JM (1996) Xanthine oxidase/dehydrogenase is present in human placenta. Placenta 17:361–365
Marinoni E, Picca A, Scucchi L, Cosmi EV, Di Iorio R (1995) Immunohistochemical localization of endothelin-1 in placenta and fetal membranes in term and preterm human pregnancy. Am J Reprod Immunol 34:213–218
Martin BJ, Spicer SS (1973) Ultrastructural features of cellular maturation and aging in human trophoblast. J Ultrastruct Res 43:133–149
Martinez F, Kiriakidou M, Strauss JF (1997) Structural and functional changes in mitochondria associated with trophoblast differentiation: methods to isolate enriched preparations of syncytiotrophoblast mitochondria. Endocrinology 138:2172–2183
Martinoli C, Castellucci M, Zaccheo D, Kaufmann P (1984) Scanning electron microscopy of stromal cells of human placental villi throughout pregnancy. Cell Tissue Res 235:647–655
Maruo T, Matsuo H, Murata K, Mochizuki M (1992) Gestational age-dependent dual action of epidermal growth factor on human placenta early in gestation. J Clin Endocrinol Metab 75:1362–1367
Marzioni D, Crescimanno C, Zaccheo D, Coppari R, Underhill CB, Castellucci M (2001) Hyaluronate and CD44 expression patterns in the human placenta throughout pregnancy. Eur J Histochem 45:131–140
Matejevic D, Neudeck H, Graf R, Muller T, Dietl J (2001) Localization of hyaluronan with a hyaluronan-specific hyaluronic acid binding protein in the placenta in pre-eclampsia. Gynecol Obstet Invest 52:257–259
Mayhew TM (2001) Villous trophoblast of human placenta: a coherent view of its turnover, repair and contributions to villous development and maturation. Histol Histopathol 16:1213–1224
Mayhew TM, Barker BL (2001) Villous trophoblast: morphometric perspectives on growth, differentiation, turnover and deposition of fibrin-type fibrinoid during gestation. Placenta 22:628–638
Mayhew TM, Wadrop E, Simpson RA (1994) Proliferative versus hypertrophic growth in tissue subcompartments of human placental villi during gestation. J Anat 184:535–543
Mayhew TM, Leach L, McGee R, Ismail WW, Myklebust R, Lammiman MJ (1999) Proliferation, differentiation and apoptosis in villous trophoblast at 13–41 weeks of gestation (including observations on annulate lamellae and nuclear pore complexes). Placenta 20:407–422
Maymo JL, Perez Perez A, Gambino Y, Calvo JC, Sanchez-Margalet V, Varone CL (2011) Review: leptin gene expression in the placenta – regulation of a key hormone in trophoblast proliferation and survival. Placenta 32 Suppl 2:S146–S153
McArdle HJ, Andersen HS, Jones H, Gambling L (2008) Copper and iron transport across the placenta: regulation and interactions. J Neuroendocrinol 20:427–431
McCarthy AL, Woolfson RG, Evans BJ, Davies DR, Raju SK, Poston L (1994) Functional characteristics of small placental arteries. Am J Obstet Gynecol 170:945–951
Metz J, Weihe E (1980) Intercellular junctions in the full term human placenta. II. Cytotrophoblast cells, intravillous stroma cells and blood vessels. Anat Embryol (Berl) 158:167–178
Mi S, Lee X, Li X, Veldman GM, Finnerty H, Racie L, LaVallie E, Tang XY, Edouard P, Howes S, Keith JC Jr, McCoy JM (2000) Syncytin is a captive retroviral envelope protein involved in human placental morphogenesis. Nature 403:785–789
Midgley AR, Pierce GB Jr, Deneau GA, Gosling JR (1963) Morphogenesis of syncytiotrophoblast in vivo: an autoradiographic demonstration. Science 141:349–350
Mincheva-Nilsson L, Baranov V (2010) The role of placental exosomes in reproduction. Am J Reprod Immunol 63:520–533
Moffett A, Loke C (2006) Immunology of placentation in eutherian mammals. Nat Rev Immunol 6:584–594
Moll UM, Lane BL (1990) Proteolytic activity of first trimester human placenta: localization of interstitial collagenase in villous and extravillous trophoblast. Histochemistry 94:555–560
Mori M, Ishikawa G, Luo SS, Mishima T, Goto T, Robinson JM, Matsubara S, Takeshita T, Kataoka H, Takizawa T (2007) The cytotrophoblast layer of human chorionic villi becomes thinner but maintains its structural integrity during gestation. Biol Reprod 76:164–172
Morrish DW, Marusyk H (1997) Localization of human chorionic gonadoptropin and placental lactogen by immunogold labeling for electron microscopy: technique and limitations. Microsc Res Tech 38:176–187
Morrish DW, Bhardwaj D, Paras MT (1991) Transforming growth factor beta 1 inhibits placental differentiation and human chorionic gonadotropin and human placental lactogen secretion. Endocrinology 129:22–26
Morrish DW, Dakour J, Li H (1998) Functional regulation of human trophoblast differentiation. J Reprod Immunol 39:179–195
Muhlhauser J, Crescimanno C, Kasper M, Zaccheo D, Castellucci M (1995) Differentiation of human trophoblast populations involves alterations in cytokeratin patterns. J Histochem Cytochem 43:579–589
Muhlhauser J, Marzioni D, Morroni M, Vuckovic M, Crescimanno C, Castellucci M (1996) Codistribution of basic fibroblast growth factor and heparan sulfate proteoglycan in the growth zones of the human placenta. Cell Tissue Res 285:101–107
Muir A, Lever AM, Moffett A (2006) Human endogenous retrovirus-W envelope (syncytin) is expressed in both villous and extravillous trophoblast populations. J Gen Virol 87:2067–2071
Murphy VE, Zakar T, Smith R, Giles WB, Gibson PG, Clifton VL (2002) Reduced 11beta-hydroxysteroid dehydrogenase type 2 activity is associated with decreased birth weight centile in pregnancies complicated by asthma. J Clin Endocrinol Metab 87:1660–1668
Myatt L, Brewer A, Brockman DE (1991) The action of nitric oxide in the perfused human fetal-placental circulation. Am J Obstet Gynecol 164:687–692
Myatt L, Rosenfield RB, Eis ALW, Brockman DE, Greer I, Lyall F (1996) Nitrotyrosine residues in placenta. Evidence of peroxynitrite formation and action. Hypertension 28:488–493
Myatt L, Eis ALW, Brockman DE, Kossenjans W, Greer I, Lyall F (1997a) Inducible (Type II) nitric oxide synthase in human placental villous tissue of normotensive, pre-eclamptic and intrauterine growth-restricted pregnancies. Placenta 18:261–268
Myatt L, Eis ALW, Brockman DE, Kossenjans W, Greer IA, Lyall F (1997b) Differential localization of superoxide dismutase isoforms in placental villous tissue of normotensive, pre-eclamptic, and intrauterine growth-restricted pregnancies. J Histochem Cytochem 45:1433–1438
Myllynen P, Pasanen M, Pelkonen O (2005) Human placenta: a human organ for developmental toxicology research and biomonitoring. Placenta 26:361–371
Nachtigall MJ, Kliman HJ, Feinberg RF, Olive DL, Engin O, Arici A (1996) The effect of leukemia inhibitory factor (LIF) on trophoblast differentiation: a potential role in human implantation. J Clin Endocrinol Metab 81:801–806
Naderi S, Blomhoff HK (2008) Activation of cAMP signaling enhances Fas-mediated apoptosis and activation-induced cell death through potentiation of caspase 8 activation. Hum Immunol 69:833–836
Nait-Oumesmar B, Copperman AB, Lazzarini RA (2000) Placental expression and chromosomal localization of the human Gcm 1 gene. J Histochem Cytochem 48:915–922
Nanaev AK, Rukosuev VS, Shirinsky VP, Milovanov AP, Domogatsky SP, Duance VC, Bradbury FM, Yarrow P, Gardiner L, D’Lacey C et al (1991) Confocal and conventional immunofluorescent and immunogold electron microscopic localization of collagen types III and IV in human placenta. Placenta 12:573–595
Nelson DM (1996) Apoptotic changes occur in syncytiotrophoblast of human placental villi where fibrin type fibrinoid is deposited at discontinuities in the villous trophoblast. Placenta 17:387–391
Ng RK, Dean W, Dawson C, Lucifero D, Madeja Z, Reik W, Hemberger M (2008) Epigenetic restriction of embryonic cell lineage fate by methylation of Elf5. Nat Cell Biol 10:1280–1290
Ni XT, Duan T, Yang Z, Guo CM, Li JN, Sun K (2009) Role of human chorionic gonadotropin in maintaining 11beta-hydroxysteroid dehydrogenase type 2 expression in human placental syncytiotrophoblasts. Placenta 30:1023–1028
Nikolov SD, Schiebler TH (1981) Über Endothelzellen in Zottengefäben der reifen menschilchen placenta. Acta Anat 110:338–344
Nozawa S, Arai H, Jeng C, Itakura M, Ohta H, Suzuki K, Tamura S, Kurihara S (1984) Shift of placental alkaline phosphatase isoenzymes in the course of pregnancy. Nippon Sanka Fujinka Gakkai Zasshi 36:1145–1154
Ockleford CD, Wakely J (1981) The skeleton of the placenta. In: Harrison RJ, Holmes RL (eds) Progress in anatomy. Cambridge University Press, London, pp 19–48
Ockleford CD, Whyte A (1977) Differentiated regions of human placental cell surface associated with exchange of materials between maternal and foetal blood: coated vesicles. J Cell Sci 25:293–312
Ockleford CD, Wakely J, Badley RA (1981) Morphogenesis of human placental chorionic villi: cytoskeletal, syncytioskeletal and extracellular matrix proteins. Proc R Soc Lond B Biol Sci 212:305–316
Ockleford CD, Nevard CH, Indans I, Jones CJ (1987) Structure and function of the nematosome. J Cell Sci 87(Pt 1):27–44
Palmer ME, Watson AL, Burton GJ (1997) Morphological analysis of degeneration and regeneration of syncytiotrophoblast in first trimester villi during organ culture. Hum Reprod 12:379–382
Panem S (1979) C-type virus expression in the placenta. Curr Top Pathol 66:175–189
Paradela A, Bravo SB, Henriquez M, Riquelme G, Gavilanes F, Gonzalez-Ros JM, Albar JP (2005) Proteomic analysis of apical microvillous membranes of syncytiotrophoblast cells reveals a high degree of similarity with lipid rafts. J Proteome Res 4:2435–2441
Parmley RT, Takagi M, Denys FR (1984) Ultrastructural localization of glycosaminoglycans in human term placenta. Anat Rec 210:477–484
Paul S, Jailkhani BL (1982) Lysis of placental syncytiotrophoblast by allogenic leukocytes in vitro: effects of neuraminidase and chorionic gonadotropin. Am J Reprod Immunol 2:204–207
Perkins AV, Di Trapani G, McKay MS, Clarke FM (1995) Immunocytochemical localization of thioredoxin in human trophoblast and decidua. Placenta 16:635–642
Pidoux G, Gerbaud P, Marpeau O, Guibourdenche J, Ferreira F, Badet J, Evain-Brion D, Frendo JL (2007) Human placental development is impaired by abnormal human chorionic gonadotropin signaling in trisomy 21 pregnancies. Endocrinology 148:5403–5413
Pidoux G, Gerbaud P, Gnidehou S, Grynberg M, Geneau G, Guibourdenche J, Carette D, Cronier L, Evain-Brion D, Malassine A, Frendo JL (2010) ZO-1 is involved in trophoblastic cells differentiation in human placenta. Am J Physiol Cell Physiol 298(6):C1517–C1526
Pidoux G, Gerbaud P, Cocquebert M, Segond N, Badet J, Fournier T, Guibourdenche J and Evain-Brion D (2012) Review: Human trophoblast fusion and differentiation: Lessons from trisomy 21 placenta. Placenta 33 Suppl:S81–6
Pietryga M, Biczysko W, Wender-Ozegowska E, Brazert J, Bieganska E, Biczysko R (2004) Ultrastructural examination of the placenta in pregnancy complicated by diabetes mellitus. Ginekol Pol 75:111–118
Ponting JM, Kumar S (1995) Isolation and characterisation of a hyaluronan binding protein, hyaluronectin, from human placenta and its colocalisation with hyaluronan. J Anat 186:131–142
Portmann-Lanz CB, Schoeberlein A, Huber A, Sager R, Malek A, Holzgreve W, Surbek DV (2006) Placental mesenchymal stem cells as potential autologous graft for pre- and perinatal neuroregeneration. Am J Obstet Gynecol 194:664–673
Qiao S, Nagasaka T, Harada T, Nakashima N (1998) p53, Bax and Bcl-2 expression, and apoptosis in gestational trophoblast of complete hydatidiform mole. Placenta 19:361–369
Rahi M, Heikkinen T, Hakkola J, Hakala K, Wallerman O, Wadelius M, Wadelius C, Laine K (2008) Influence of adenosine triphosphate and ABCB1 (MDR1) genotype on the P-glycoprotein-dependent transfer of saquinavir in the dually perfused human placenta. Hum Exp Toxicol 27:65–71
Raijmakers MT, Burton GJ, Jauniaux E, Seed PT, Peters WH, Steegers EA, Poston L (2006) Placental NAD(P)H oxidase mediated superoxide generation in early pregnancy. Placenta 27:158–163
Ramsay B, Sooranna SR, Johnson MR (1996) Nitric oxide synthase activities in human myometrium and villous trophoblast throughout pregnancy. Obstet Gynecol 87:249–253
Redman CWG, Sargent IL (2000) Placental debris, oxidative stress and pre-eclampsia. Placenta 21:597–602
Rindsjo E, Joerink M, Papadogiannakis N, Scheynius A (2010) IgE in the human placenta: why there? Allergy 65:554–560
Riquelme G (2009) Placental chloride channels: a review. Placenta 30:659–669
Robaut C, Mondon F, Bandet J, Ferre F, Cavero I (1991) Regional distribution and pharmacological characterization of [125I]endothelin-1 binding sites in human fetal placental vessels. Placenta 12:55–67
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
Robin C, Bollerot K, Mendes S, Haak E, Crisan M, Cerisoli F, Lauw I, Kaimakis P, Jorna R, Vermeulen M, Kayser M, van der Linden R, Imanirad P, Verstegen M, Nawaz-Yousaf H, Papazian N, Steegers E, Cupedo T, Dzierzak E (2009) Human placenta is a potent hematopoietic niche containing hematopoietic stem and progenitor cells throughout development. Cell Stem Cell 5:385–395
Robinson JM, Ackerman WE, Behrendt NJ, Vandre DD (2009a) While dysferlin and myoferlin are coexpressed in the human placenta, only dysferlin expression is responsive to trophoblast fusion in model systems. Biol Reprod 81:33–39
Robinson JM, Ackerman WE, Tewari AK, Kniss DA, Vandre DD (2009b) Isolation of highly enriched apical plasma membranes of the placental syncytiotrophoblast. Anal Biochem 387:87–94
Ronco AM, Arguello G, Suazo M, Llanos MN (2005) Increased levels of metallothionein in placenta of smokers. Toxicology 208:133–139
Rote NS, Chang J, Katsuragawa H, Ng AK, Lyden TW, Mori T (1995) Expression of phosphatidylserine-dependent antigens on the surface of differentiating BeWo human choriocarcinoma cells. Am J Reprod Immunol 33:114–121
Rote NS, Chakrabarti S, Stetzer BP (2004) The role of human endogenous retroviruses in trophoblast differentiation and placental development. Placenta 25:673–683
Rote NS, Wei BR, Xu C, Luo L (2010) Caspase 8 and human villous cytotrophoblast differentiation. Placenta 31:89–96
Roulier S, Rochette-Egly C, Rebut-Bonneton C, Porquet D, Evain-Brion D (1994) Nuclear retinoic acid receptor characterization in cultured human trophoblast cells: effect of retinoic acid on epidermal growth factor receptor expression. Mol Cell Endocrinol 105:165–173
Rukosuev VS (1992) Immunofluorescent localization of collagen types I, III, IV, V, fibronectin, laminin, entactin, and heparan sulphate proteoglycan in human immature placenta. Experientia 48:285–287
Sahu SK, Gummadi SN, Manoj N, Aradhyam GK (2007) Phospholipid scramblases: an overview. Arch Biochem Biophys 462:103–114
Salas SP, Power RF, Singleton A, Wharton J, Polak JM, Brown J (1991) Heterogeneous binding sites for alpha-atrial natriuretic peptide in human umbilical cord and placenta. Am J Physiol 261:R633–638
Salmon JE, Girardi G (2008) Antiphospholipid antibodies and pregnancy loss: a disorder of inflammation. J Reprod Immunol 77:51–56
Sati L, Seval Y, Yasemin Demir A, Kosanke G, Kohnen G, Demir R (2007) Cellular diversity of human placental stem villi: an ultrastructural and immunohistochemical study. Acta Histochem 109:468–479
Sati L, Demir AY, Sarikcioglu L, Demir R (2008) Arrangement of collagen fibers in human placental stem villi. Acta Histochem 110:371–379
Schaaps JP, Tsatsaris V, Goffin F, Brichant JF, Delbecque K, Tebache M, Collignon L, Retz MC, Foidart JM (2005) Shunting the intervillous space: new concepts in human uteroplacental vascularization. Am J Obstet Gynecol 192:323–332
Schiebler TH, Kaufmann P (1969) Zonal differences in the human placenta. Z Zellforsch Mikrosk Anat 102:242–265
Schneider H, Miller RK (2010) Receptor-mediated uptake and transport of macromolecules in the human placenta. Int J Dev Biol 54:367–375
Schweikhart G, Kaufmann P (1977) Zur Abgrenzung normaler, artefizieller und pathologischer Strukturen in reifen menschlichen Plazentazotten. I. Ultrastruktur des Syncytiotrophoblasten. Arch Gynakol 222:213–230
Scioscia M, Gumaa K, Kunjara S, Paine MA, Selvaggi LE, Rodeck CH, Rademacher TW (2006) Insulin resistance in human preeclamptic placenta is mediated by serine phosphorylation of insulin receptor substrate-1 and -2. J Clin Endocrinol Metab 91:709–717
Scioscia M, Greco P, Selvaggi LE, Rademacher TW (2009) Is there a link between insulin resistance and inflammatory activation in preeclampsia? Med Hypotheses 73:813–817
Sheikh AU, Polliotti BM, Miller RK (2000) Human immunodeficiency virus infection: in situ polymerase chain reaction localization in human placentas after in utero and in vitro infection. Am J Obstet Gynecol 182:207–213
Shiverick K, Ino K, Harada T, Keelan J, Kikkawa F (2007) Placental enzymes and transporters: new functions and genetic polymorphisms-a workshop report. Placenta 28 Suppl A:S125–S128
Sibley CP (2009) Understanding placental nutrient transfer – why bother? New biomarkers of fetal growth. J Physiol 587:3431–3440
Siman CM, Sibley CP, Jones CJ, Turner MA, Greenwood SL (2001) The functional regeneration of syncytiotrophoblast in cultured explants of term placenta. Am J Physiol Regul Integr Comp Physiol 280:R1116–R1122
Simister NE (1998) Human placental Fc receptors and the trapping of immune complexes. Vaccine 16:1451–1455
Simister NE, Story CM (1997) Human placental Fc receptors and the transmission of antibodies from mother to fetus. J Reprod Immunol 37:1–23
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 disector. Placenta 13:501–512
Smallwood A, Papageorghiou A, Nicolaides K, Alley MK, Jim A, Nargund G, Ojha K, Campbell S, Banerjee S (2003) Temporal regulation of the expression of syncytin (HERV-W), maternally imprinted PEG10, and SGCE in human placenta. Biol Reprod 69:286–293
Smith SC, Baker PN, Symonds EM (1997a) Increased placental apoptosis in intrauterine growth restriction. Am J Obstet Gynecol 177:1395–1401
Smith SC, Baker PN, Symonds EM (1997b) Placental apoptosis in normal human pregnancy. Am J Obstet Gynecol 177:57–65
Snir A, Brenner B, Paz B, Lanir N (2010) Presence of integrin alpha(IIb)beta 3 in early gestation human trophoblasts: possible involvement of fibrin as a matrix ligand. Thromb Res 125:253–256
Soilleux EJ, Morris LS, Lee B, Pohlmann S, Trowsdale J, Doms RW, Coleman N (2001) Placental expression of DC-SIGN may mediate intrauterine vertical transmission of HIV. J Pathol 195:586–592
Sonderegger S, Pollheimer J, Knofler M (2010) Wnt signalling in implantation, decidualisation and placental differentiation – review. Placenta 31:839–847
Sooranna SR, Oteng-Ntim E, Meah R, Ryder TA, Bajoria R (1999) Characterization of human placental explants: morphological, biochemical and physiological studies using first and third trimester placenta. Hum Reprod 14:536–541
Stasenko S, Bradford EM, Piasek M, Henson MC, Varnai VM, Jurasovic J, Kusec V (2010) Metals in human placenta: focus on the effects of cadmium on steroid hormones and leptin. J Appl Toxicol 30:242–253
Stebbing PN, Gude NM, King RG, Brennecke SP (1996) Alpha-atrial natriuretic peptide-induced attenuation of vasoconstriction in the fetal circulation of the human isolated perfused placenta. J Perinat Med 24:253–260
Szukiewicz D, Szewczyk G, Watroba M, Kurowska E, Maslinski S (2005) Isolated placental vessel response to vascular endothelial growth factor and placenta growth factor in normal and growth-restricted pregnancy. Gynecol Obstet Invest 59:102–107
Tailor CS, Nouri A, Zhao Y, Takeuchi Y, Kabat D (1999) A sodium-dependent neutral-amino-acid transporter mediates infections of feline and baboon endogenous retroviruses and simian type D retroviruses. J Virol 73:4470–4474
Tanaka S, Kunath T, Hadjantonakis AK, Nagy A, Rossant J (1998) Promotion of trophoblast stem cell proliferation by FGF4. Science 282:2072–2075
Taylor DD, Akyol S, Gercel-Taylor C (2006) Pregnancy-associated exosomes and their modulation of T cell signaling. J Immunol 176:1534–1542
Teasdale F (1978) Functional significance of the zonal morphologic differences in the normal human placenta. A morphometric study. Am J Obstet Gynecol 130:773–781
Teasdale F, Jean-Jacques G (1985) Morphometric evaluation of the microvillus enlargement factor in the human placenta from midgestation to term. Placenta 6:375–381
Toth FD, Norskov-Lauritsen N, Juhl C, Ebbesen P (1991) Human trophoblast interferon: pattern of response to priming and superinduction of purified term trophoblast and choriocarcinoma cells. J Reprod Immunol 19:55–67
Turkewitz AP, Harrison SC (1989) Concentration of transferrin receptor in human placental coated vesicles. J Cell Biol 108:2127–2135
Uehara Y, Minowa O, Mori C, Shiota K, Kuno J, Noda T, Kitamura N (1995) Placental defect and embryonic lethality in mice lacking hepatocyte growth factor/scatter factor. Nature 373:702–705
Uzun H, Konukoglu D, Albayrak M, Benian A, Madazli R, Aydin S, Gelisgen R, Uludag S (2010) Increased maternal serum and cord blood fibronectin concentrations in preeclampsia are associated with higher placental hyaluronic acid and hydroxyproline content. Hypertens Pregnancy 29:153–162
Vahakangas K, Myllynen P (2009) Drug transporters in the human blood-placental barrier. Br J Pharmacol 158:665–678
Valadi H, Ekstrom K, Bossios A, Sjostrand M, Lee JJ, Lotvall JO (2007) Exosome-mediated transfer of mRNAs and microRNAs is a novel mechanism of genetic exchange between cells. Nat Cell Biol 9:654–659
van den Eijnde SM, van den Hoff MJ, Reutelingsperger CP, van Heerde WL, Henfling ME, Vermeij-Keers C, Schutte B, Borgers M, Ramaekers FC (2001) Transient expression of phosphatidylserine at cell-cell contact areas is required for myotube formation. J Cell Sci 114:3631–3642
van der Velde WJ, Peereboom-Stegeman JH, Treffers PE, James J (1985) Basal lamina thickening in the placentae of smoking mothers. Placenta 6:329–340
Vanderpuye OA, Edwards HC, Booth AG (1986) Proteins of the human placental microvillar cytoskeleton. alpha-Actinin. Biochem J 233:351–356
Vandre DD, Ackerman WE, Kniss DA, Tewari AK, Mori M, Takizawa T, Robinson JM (2007) Dysferlin is expressed in human placenta but does not associate with caveolin. Biol Reprod 77:533–542
Vargas A, Moreau J, Landry S, LeBellego F, Toufaily C, Rassart E, Lafond J, Barbeau B (2009) Syncytin-2 plays an important role in the fusion of human trophoblast cells. J Mol Biol 392:301–318
Venables PJ, Brookes SM, Griffiths D, Weiss RA, Boyd MT (1995) Abundance of an endogenous retroviral envelope protein in placental trophoblasts suggests a biological function. Virology 211:589–592
Viebig NK, Gamain B, Scheidig C, Lepolard C, Przyborski J, Lanzer M, Gysin J, Scherf A (2005) A single member of the Plasmodium falciparum var multigene family determines cytoadhesion to the placental receptor chondroitin sulphate A. EMBO Rep 6:775–781
Virtanen I, Laitinen L, Vartio T (1988) Differential expression of the extra domain-containing form of cellular fibronectin in human placentas at different stages of maturation. Histochemistry 90:25–30
Vizza E, Correr S, Barberini F, Heyn R, Bianchi S, Macchiarelli G (2005) 3-D ultrastructural distribution of collagen in human placental villi at term in relation to vascular tree. J Reprod Dev 51:433–443
Voigt S, Kaufmann P, Schweikhart G (1978) Problems of distinction of normal, artificial, and pathological structures in mature human placental villi. II. Morphometrical studies on the influence of the mode of fixation (author’s transl). Arch Gynecol 226:347–362
Wang Y, Walsh SW (1998) Placental mitochondria as a source of oxidative stress in pre-eclampsia. Placenta 19:581–586
Watson AL, Palmer ME, Burton GJ (1996) An in vitro model for the study of wound healing in first trimester human placenta. Cell Tissue Res 286:431–438
Watson AL, Palmer ME, Jauniaux E, Burton GJ (1997) Variations in expression of copper/zinc superoxide dismutase in villous trophoblast of the human placenta with gestational age. Placenta 18:295–299
Watson AL, Skepper JN, Jauniaux E, Burton GJ (1998a) Changes in the concentration, localisation and activity of catalase within the human placenta during early gestation. Placenta 19:27–34
Watson AL, Skepper JN, Jauniaux E, Burton GJ (1998b) Susceptibility of human placental syncytiotrophoblastic mitochondria to oxygen-mediated damage in relation to gestational age. J Clin Endocrinol Metab 83:1697–1705
Webb PD, Todd J (1988) Attachment of human placental-type alkaline phosphatase via phosphatidylinositol to syncytiotrophoblast and tumour cell plasma membranes. Eur J Biochem 172:647–652
Wetzka B, Clark DE, Charnock-Jones DS, Zahradnik HP, Smith SK (1997) Isolation of macrophages (Hofbauer cells) from human term placenta and their prostaglandin E2 and thromboxane production. Hum Reprod 12:847–852
Wide M, Persson H, Lundkvist O, Wide L (1988) Localization of mRNA for the beta-subunit of placental hCG by in situ hybridization. Acta Endocrinol (Copenh) 119:69–74
Wood GW, King CR Jr (1982) Trapping antigen-antibody complexes within the human placenta. Cell Immunol 69:347–362
Yamada T, Isemura M, Yamaguchi Y, Munakata H, Hayashi N, Kyogoku M (1987) Immunohistochemical localization of fibronectin in the human placentas at their different stages of maturation. Histochemistry 86:579–584
Yang M, Lei ZM, Rao CV (2003) The central role of human chorionic gonadotropin in the formation of human placental syncytium. Endocrinology 144:1108–1120
Yang K, Julan L, Rubio F, Sharma A, Guan H (2006) Cadmium reduces 11 beta-hydroxysteroid dehydrogenase type 2 activity and expression in human placental trophoblast cells. Am J Physiol Endocrinol Metab 290:E135–E142
Yen BL, Huang HI, Chien CC, Jui HY, Ko BS, Yao M, Shun CT, Yen ML, Lee MC, Chen YC (2005) Isolation of multipotent cells from human term placenta. Stem Cells 23:3–9
Yu C, Shen K, Lin M, Chen P, Lin C, Chang GD, Chen H (2002) GCMa regulates the syncytin-mediated trophoblastic fusion. J Biol Chem 277:50062–50068
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
Zhang EC, Burton GJ, Smith SK, Charnock-Jones DS (2002) Placental vessel adaptation during gestation and to high altitude: changes in diameter and perivascular cell coverage. Placenta 23:751–762
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Benirschke, K., Burton, G.J., Baergen, R.N. (2012). Basic Structure of the Villous Trees. In: Pathology of the Human Placenta. Springer, Berlin, Heidelberg. https://doi.org/10.1007/978-3-642-23941-0_6
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