An integrative view on the physiology of human early placental villi

Progress in Biophysics and Molecular Biology

Volumn 114, Issue 1, 2014, Pages 33-48

  Huppertz, Berthold ^a   Ghosh, Debabrata ^b   Sengupta, Jayasree ^c  

^a MEDICAL UNIVERSITY OF GRAZ   (Austria)

^b ALL INDIA INSTITUTE OF MEDICAL SCIENCES   (India)

^c HINDU RAO HOSPITAL   (India)

Author keywords

Early pregnancy loss; IUGR; Placenta; Pre eclampsia; Transcriptomics; Trophoblast

Indexed keywords

APOPTOSIS; CHORION VILLUS; CYTOLOGY; ENDOCRINE GLAND; FEMALE; HUMAN; IMMUNOLOGY; METABOLISM; PATHOLOGY; PATHOPHYSIOLOGY; PHYSIOLOGICAL PROCESS; PHYSIOLOGY; PREGNANCY; PREGNANCY COMPLICATION; SIGNAL TRANSDUCTION;

APOPTOSIS; CHORIONIC VILLI; ENDOCRINE GLANDS; FEMALE; HUMANS; PHYSIOLOGICAL PROCESSES; PREGNANCY; PREGNANCY COMPLICATIONS; SIGNAL TRANSDUCTION;

EID: 84897959955     PISSN: 00796107     EISSN: None     Source Type: Journal    
DOI: 10.1016/j.pbiomolbio.2013.11.007     Document Type: Review

References (183)

1. Allikmets R., Schriml L.M., Hutchinson A., Romano-Spica V., Dean M. Ahuman placenta-specific ATP-binding cassette gene (ABCP) on chromosome 4q22 that is involved in multidrug resistance. Cancer Res. 1998, 58:5337-5339.
2. Aplin J.D., Jones C.J., Harris L.K. Adhesion molecules in human trophoblast - a review. I. Villous trophoblast. Placenta 2009, 30:293-298.
3. Apps R., Sharkey A., Gardner L., Male V., Trotter M., Miller N., North R., Founds S., Moffet A. Genome-wide expression profile of first trimester villous and extravillous human trophoblast cells. Placenta 2011, 32:33-43.
4. Arimoto-Ishida E., Sakata M., Sawada K., Nakayama M., Nishimoto F., Mabuchi S., Takeda T., Yamamoto T., Isobe A., Okamoto Y., Lengyel E., Suehara N., Morishige K., Kimura T. Up-regulation of alpha5-integrin by E-cadherin loss in hypoxia and its key role in the migration of extravillous trophoblast cells during early implantation. Endocrinology 2009, 150:4306-4315.
5. Atkinson D.E., Boyd R.D.H., Sibley C.P. Placental transfer. Knobil and Neill's Physiology of Reproduction 2005, 2787-2846. Elsevier Academic Press, London. third ed. P. Wassarman, J.D. Neill (Eds.).
6. Baczyk D., Drewlo S., Proctor L., Dunk C., Lye S., Kingdom J. Glial cell missing-1 transcription factor is required for the differentiation of the human trophoblast. Cell Death Differ. 2009, 16:719-727.
7. Baczyk D., Satkunaratnam A., Nait-Oumesmar B., Huppertz B., Cross J.C. Complex patterns of GCM1 mRNA and protein in villous and extravillous trophoblast cells of the human placenta. Placenta 2004, 25:553-559.
8. Baek K.H., Lee E.J., Kim Y.S. Recurrent pregnancy loss: the key potential mechanisms. Trends Mol. Med. 2007, 13:310-317.
9. Ball E., Robson S.C., Ayis S., Lyall F., Bulmer J.N. Early embryonic demise: no evidence of abnormal spiral artery transformation or trophoblast invasion. J.Pathol. 2006, 208:528-534.
10. Barber A., Robson S.C., Myatt L., Bulmer J.N., Lyall F. Heme oxygenase expression in human placenta and placental bed: reduced expression of placenta endothelial HO-2 in preeclampsia and fetal growth restriction. FASEB J. 2001, 15:1158-1168.
11. Barrera D., Noyola-Martinez N., Avila E., Halhali A., Larrea F., Diaz L. Calcitriol inhibits interleukin-10 expression in cultured human trophoblasts under normal and inflammatory conditions. Cytokine 2012, 57:316-327.
12. Bernirschke K., Kaufmann P., Baergen R.N. Pathology of the Human Placenta 2006, Springer, New York. fifth ed.
13. Bilic I., Ellmeier W. The role of BTB domain-containing zinc finger proteins in T cell development and function. Immunol. Lett. 2007, 108:1-9.
14. Black S., Kadyrov M., Kaufman P., Ugele B., Emans N., Huppertz B. Syncytial fusion of human trophoblast depends on caspase 8. Cell Death Differ. 2004, 11:90-98.
15. Borges T.J., Wieten L., van Herwijnen M.J., Broere F., van der Zee R., Bonorino C., van Eden W. The anti-inflammatory mechanisms of Hsp70. Front. Immunol. 2012, 3:95. 10.3389/fimmu.2012.00095.
16. Bostrom N., Sandberg A. The wisdom of nature: an evolutionary heuristic for human enhancement. Human Enhancement 2009, 375-416. Oxford University Press, Oxford. J. Savulescu, N. Bostrom (Eds.).
17. Brosens I.A. Morphological changes in the utero-placental bed in pregnancy hypertension. Clin. Obstet. Gynaecol. 1977, 4:573-593.
18. Brown L.M., Lacey H.A., Baker P.N., Crocker I.P. E-cadherin in the assessment of aberrant placental cytotrophoblast turnover in pregnancies complicated by pre-eclampsia. Histochem. Cell. Biol. 2005, 124:499-506.
19. Bulmer J.N., Williams P.J., Lash G.E. Immune cells in the placental bed. Int. J. Dev. Biol. 2010, 54:281-294.
20. Burton G.J., Jauniaux E. Maternal vascularisation of the human placenta: does the embryo develop in a hypoxic environment?. Gynecol. Obstet. Fertil. 2001, 29:503-508.
21. Burton G.J., Jauniaux E., Watson A.L. Maternal arterial connections to the placental intervillous space during the first trimester of human pregnancy: the Boyd collection revisited. Am. J. Obstet. Gynecol. 1999, 181:718-724.
22. Burton G.J., Skepper J.N., Hempstock J., Cindrova T., Jones C.J., Jauniaux E. Areappraisal of the contrasting morphological appearances of villous cytotrophoblast cells during early human pregnancy; evidence for both apoptosis and primary necrosis. Placenta 2003, 24:297-305.
23. Burton G.J., Woods A.W., Jauniaux E., Kingdom J.C. Rheological and physiological consequences of conversion of the maternal spiral arteries for uteroplacental blood flow during human pregnancy. Placenta 2009, 30:473-482.
24. Calleja-Agius J., Jauniaux E., Muttukrishna S. Placental villous expression of TNFα and IL-10 and effect of oxygen tension in euploid early pregnancy failure. Am. J. Reprod. Immunol. 2012, 67:515-525.
25. Canonici A., Steelant W., Rigot V., Khomitch-Baud A., Boutaghou-Cherid H., Bruyneel E., Van Roy F., Garrouste F., Pommier G., André F. Insulin-like growth factor-I receptor, E-cadherin and alpha v integrin form a dynamic complex under the control of alpha-catenin. Int. J. Cancer 2008, 122:572-582.
26. Carter A.M. Evolution of placental function in mammals: the molecular basis of gas and nutrient transfer, hormone secretion, and immune responses. Physiol. Rev. 2012, 92:1543-1576.
27. Carter A.M. Comparative studies of placentation and immunology in non-human primates suggest a scenario for the evolution of deep trophoblast invasion and an explantation for human pregnancy disorders. Reproduction 2011, 141:391-396.
28. Castellucci M., Celona A., Bartels H., Steininger B., Benedetto V., Kaufmann P. Mitosis of the Hofbauer cell: possible implications for a fetal macrophage. Placenta 1987, 8:65-76.
29. Centlow M., Wingren C., Borrebaeck C., Brownstein M.J., Hansson S.R. Differential gene expression analysis of placentas with increased vascular resistance and pre-eclampsia using whole-genome microarrays. J.Pregnancy 2011, 10.1155/2011/472354.
30. Cetin I. Placental transport of amino acids in normal and growth-restricted pregnancies. Eur. J. Obstet. Gynecol. Reprod. Biol. 2003, 110(Suppl.1):S50-S54.
31. Chen H.W., Chen J.J., Tzeng C.R., Li H.N., Chang S.J., Cheng Y.F., Chang C.W., Wang R.S., Yang P.C., Lee Y.T. Global analysis of differentially expressed genes in early gestational decidua and chorionic villi using a 9600 human cDNA microarray. Mol. Hum. Reprod. 2002, 8:475-484.
32. Chen E.Y., Liao Y.C., Smith D.H., Barrera-Saldana H.A., Gelinas R.E., Seeburg P.H. The human growth hormone locus: nucleotide sequence, biology, and evolution. Genomics 1989, 4:479-497.
33. Cochery-Nouvellon E., Nguyen P., Attaoua R., Cornillet-Lefebvre P., Mercier E., Vitry F., Gris J.C. Interleukin 10 gene promoter polymorphisms in women with pregnancy loss: preferential association with embryonic wastage. Biol. Reprod. 2009, 80:1115-1120.
34. Cocquebert M., Berndt S., Segond N., Guibourdenche J., Murthi P., Aldaz-Carroll L., Evain-Brion D., Fournier T. Comparative expression of hCG β-genes in human trophoblast from early and late first-trimester placentas. Am. J. Physiol. Endocrinol. Metab. 2012, 303:950-958.
35. Constância M., Hemberger M., Hughes J., Dean W., Ferguson-Smith A., Fundele R., Stewart F., Kelsey G., Fowden A., Sibley C., Reik W. Placental-specific IGF-II is a major modulator of placental and fetal growth. Nature 2002, 417:945-948.
36. Crespi B., Semeniuk C. Parent-offspring conflict in the evolution of vertebrate reproductive mode. Am. Nat. 2004, 163:635-653.
37. Crick F. Of Molecules and Men 1966, University of Washington Press, Seattle.
38. Cudmore M.J., Ahmad S., Sissaoui S., Ramma W., Ma B., Fujisawa T., Al-Ani B., Wang K., Cai M., Crispi F., Hewett P.W., Gratacós E., Egginton S., Ahmed A. Loss of Akt activity increases circulating soluble endoglin release in preeclampsia: identification of inter-dependency between Akt-1 and heme oxygenase-1. Eur. Heart J. 2012, 33:1150-1158.
39. Demir R., Seval Y., Huppertz B. Vasculogenesis and angiogenesis in the early human placenta. Acta Histochem. 2007, 109:257-265.
40. Demir R., Kaufmann P., Castellucci M., Erbengi T., Kotowski A. Fetal vasculogenesis and angiogenesis in human placental villi. Acta. Anat. 1989, 136:190-203.
41. Demir R., Kayisli U.A., Seval Y., Celik-Ozenci C., Korgun E.T., Demir-Weusten A.Y., Huppertz B. Sequential expression of VEGF and its receptors in human placental villi during very early pregnancy: differences between placental vasculogenesis and angiogenesis. Placenta 2004, 25:560-572.
42. Desforges M., Lacey H.A., Glazier J.D., Greenwood S.L., Mynett K.J., Speake P.F., Sibley C.P. SNAT4 isoform of system A amino acid transporter is expressed in human placenta. Am. J. Physiol. Cell Physiol. 2006, 290:305-312.
43. Desforges M., Sibley C.P. Placental nutrient supply and fetal growth. Int. J. Dev. Biol. 2010, 54:377-390.
44. Dhara S., Lalitkumar P.G., Sengupta J., Ghosh D. Immunohistochemical localization of insulin-like growth factors I and II at the primary implantation site in the Rhesus monkey. Mol. Hum. Reprod. 2001, 7:365-371.
45. Dizon-Townson D.S., Lu J., Morgan T.K., Ward K.J. Genetic expression by fetal chorionic villi during the first trimester of human gestation. Am. J. Obstet. Gynecol. 2000, 183:706-711.
46. Drewlo S., Czikk M., Baczyk D., Lye S., Kingdom J. Glial cell missing-1 mediates over-expression of tissue inhibitor of metalloproteinase-4 in severe pre-eclamptic placental villi. Hum. Reprod. 2011, 26:1025-1034.
47. Ellery P.M., Cindrova-Davies T., Jauniaux E., Ferguson-Smith A.C., Burton G.J. Evidence for transcriptional activity in the syncytiotrophoblast of the human placenta. Placenta 2009, 30:329-334.
48. Everett C. Incidence and outcome of bleeding before the 20th week of pregnancy: prospective study from general practice. Br. Med. J. 1997, 315:32-34.
49. Evseenko D.A., Paxton J.W., Keelan J.A. ABC drug transporter expression and functional activity in trophoblast-like cell lines and differentiating primary trophoblast. Am. J. Physiol. Regul. Integr. Comp. Physiol. 2006, 290:1357-1365.
50. Faridi R.M., Agarwal S. Killer immunoglobulin-like receptors (KIRs) and HLA-C allorecognition patterns implicative of dominant activation of natural killer cells contribute to recurrent miscarriages. Hum. Reprod. 2011, 26:491-497.
51. Farina A., Zucchini C., De Sanctis P., Morano D., Sekizawa A., Purwosunu Y., Okai T., Rizzo N. Gene expression in chorionic villous samples at 11 weeks of gestation in women who develop pre-eclampsia later in pregnancy: implications for screening. Prenat. Diagn. 2011, 31:181-185.
52. Farquharson R.G., Jauniaux E., Exalto N., ESHRE Special Interest Group for Early Pregnancy (SIGEP) Updated and revised nomenclature for description of early pregnancy events. Hum. Reprod. 2005, 20:3008-3011.
53. Fedorova L., Gatto-Weis C., Smaili S., Khurshid N., Shapiro J.I., Malhotra D., Horrigan T. Down-regulation of the transcription factor snail in the placentas of patients with preeclampsia and in a rat model of preeclampsia. Reprod. Biol. Endocrinol 2012, 10:15. 10.1186/1477-7827-10-15.
54. Fingar D.C., Richardson C.J., Tee A.R., Cheatham L., Tsou C., Blenis J. mTOR controls cell cycle progression through its growth effectors S6K1 and 4E-BP1/eukaryotic translation initiation factor 4E. Mol. Cell. Biol. 2004, 24:200-216.
55. Florey E. Fads and fallacies in contemporary physiology. Advances in Physiological Research 1987, 91-110. Plenum Press, New York. H. McLennan, J.R. Ledsome, C.H.S. McIntosh, D.R. Jones (Eds.).
56. Floridon C., Nielsen O., Holund B., Sunde L., Westergaard J.G., Thomsen S.G., Teisner B. Localization of E-cadherin in villous, extravillous and vascular trophoblasts during intrauterine, ectopic and molar pregnancy. Mol. Hum. Reprod. 2000, 6:943-950.
57. Foltran F., Berchialla P., Bernasconi S., Grossi E., Gregori D., Street M.E. Asystems biology approach: new insights into fetal growth restriction using Bayesian Networks. J.Biol. Regul. Homeost. Agents 2011, 25:269-277.
58. Forbes K., Westwood M., Baker P.N., Aplin J.D. Insulin-like growth factor I and II regulate the life cycle of trophoblast in the developing human placenta. Am. J. Physiol. Cell Physiol. 2008, 294:1313-1322.
59. Founds S.A., Conley Y.P., Lyons-Weiler J.F., Jeyabalan A., Hogge W.A., Conrad K.P. Altered global gene expression in first trimester placentas of women destined to develop preeclampsia. Placenta 2009, 30:15-24.
60. Founds S.A., Fallert-Junecko B., Reinhart T.A., Conley Y.P., Parks W.T. LAIR2 localizes specifically to sites of extravillous trophoblast invasion. Placenta 2010, 31:880-885.
61. Fowden A.L. The insulin-like growth factors and feto-placental growth. Placenta 2003, 24:803-812.
62. Frost M., Moore G.E. The importance of imprinting in the human placenta. Plos Genet. 2010, 6:e1001015. 10.1371/journal.pgen.1001015.
63. Fu J., Lv X., Lin H., Wu L., Wang R., Zhou Z., Zhang B., Wang Y.L., Tsang B.K., Zhu C., Wang H. Ubiquitin ligase cullin 7 induces epithelial-mesenchymal transition in human choriocarcinoma cells. J.Biol. Chem. 2010, 285:10870-10879.
64. Gauster M., Moser G., Orendi K., Huppertz B. Factors involved in regulating trophoblast fusion: potential role in the development of preeclampsia. Placenta 2009, 30:S49-S54.
65. Ghosh D., Najwa A.R., Khan M.A., Sengupta J. IGF2, IGF binding protein 1, and matrix metalloproteinases 2 and 9 in implantation-stage endometrium following immunoneutralization of vascular endothelial growth factor in the rhesus monkey. Reproduction 2011, 141:501-509.
66. Gill P.S., Rosenblum N.D. Control of murine kidney development by sonic hedgehog and its GLI effectors. Cell Cycle 2006, 5:1426-1430.
67. Greenwold N., Jauniaux E., Gulbis B., Hempstock J., Gervy C., Burton G.J. Relationship among maternal serum endocrinology, placental karyotype, and intervillous circulation in early pregnancy failure. Fertil. Steril. 2003, 79:1373-1379.
68. Gundogan F., Elwood G., Longato L., Tong M., Feijoo A., Carlson R.I., Wands J.R., De la Monte S.M. Impaired placentation in fetal alcohol syndrome. Placenta 2008, 29:148-157.
69. Handschuh K., Guibourdenche J., Tsatsaris V., Guesnon M., Laurendeau I., Evain-Brion D., Fournier T. Human chorionic gonadotropin produced by the invasive trophoblast but not the villous trophoblast promotes cell invasion and is down-regulated by peroxisome proliferator-activated receptor-gamma. Endocrinology 2007, 148:5011-5019.
70. Hay W.W. Placental-fetal glucose exchange and fetal glucose metabolism. Trans. Am. Clin. Climatol. Assoc. 2006, 117:321-340.
71. Hay N., Sonenberg N. Upstream and downstream of mTOR. Genes Dev. 2004, 18:1926-1945.
72. Hempstock J., Jauniaux E., Greenwold N., Burton G.J. The contribution of placental oxidative stress to early pregnancy failure. Hum. Pathol. 2003, 34:1265-1275.
73. Hill D.J., Clemmons D.R., Riley S.C., Bassett N., Challis J.R. Immunohistochemical localization of insulin-like growth factors (IGFs) and IGF binding proteins -1, -2 and -3 in human placenta and fetal membranes. Placenta 1993, 14:1-12.
74. Hirt H., Kimelman J., Birnbaum M.J., Chen E.Y., Seeburg P.H., Eberhardt N.L., Barta A. The human growth hormone gene locus: structure, evolution and allelic variations. DNA 1987, 6:59-70.
75. Hollemann T., Bellefroid E., Stick R., Pieler T. Zinc finger proteins in early Xenopus development. Int. J. Dev. Biol. 1996, 40:291-295.
76. Hu L., Lytras A., Bock M.E., Yuen C.K., Dodd J.G., Cattini P.A. Detection of placental growth hormone variant and chorionic somatomammotropin-L-RNA expression in normal and diabetic pregnancy by reverse transcriptase-polymerase chain reaction. Mol. Cell. Endocrinol. 1999, 157:131-142.
77. Hung T.H., Skepper J.N., Burton G.J. Invitro ischemia-reperfusion injury in term human placenta as a model for oxidative stress in pathological pregnancies. Am. J. Pathol. 2001, 159:1031-1043.
78. Hunt J.S. Stranger in a strange land. Immunol. Rev. 2006, 213:36-47.
79. Huppertz B. IFPA award in placentology lecture: biology of the placental syncytiotrophoblast - myths and facts. Placenta 2010, 31:75-81.
80. Huppertz B. The anatomy of the normal placenta. J.Clin. Pathol. 2008, 61:1296-1302.
81. Huppertz B. Placental origins of preeclampsia: challenging the current hypothesis. Hypertension 2008, 51:970-975.
82. Huppertz B., Bartz C., Kokozidou M. Trophoblast fusion: fusogenic proteins, syncytins and ADAMs, and other prerequisites for syncytial fusion. Micron 2006, 37:509-517.
83. Huppertz B., Frank H.G., Reister F., Kingdom J., Korr H., Kaufmann P. Apoptosis cascade progresses during turnover of human trophoblast: analysis of villous cytotrophoblast and syncytial fragments invitro. Lab. Invest. 1999, 79:1687-1702.
84. Huppertz B., Kadyrov M., Kingdom J.C. Apoptosis and its role in the trophoblast. Am. J. Obstet. Gynecol. 2006, 195:29-39.
85. Huppertz B., Kingdom J.C. Apoptosis in the trophoblast - role of apoptosis in placental morphogenesis. J.Soc. Gynecol. Invest. 2004, 11:353-362.
86. Huppertz B., Tews D.S., Kaufmann P. Apoptosis and syncytial fusion in human placental trophoblast and skeletal muscle. Int. Rev. Cytol. 2001, 205:215-253.
87. Ishihara N., Matsuo H., Murakoshi H., Laoag-Fernandez J., Samoto T., Maruo T. Changes in proliferative potential, apoptosis and Bcl-2 protein expression in cytotrophoblasts and syncytiotrophoblast in human placenta over the course of pregnancy. Endocr. J. 2000, 47:317-327.
88. Ishii T., Warabi E., Yanagawa T. Novel roles of peroxiredoxins in inflammation, cancer and innate immunity. J.Clin. Biochem. Nutr. 2012, 50:91-105.
89. James J.L., Stone P.R., Chamley L.W. Cytotrophoblast differentiation in the first trimester of pregnancy: evidence for separate progenitors of extravillous trophoblasts and syncytiotrophoblast. Reproduction 2005, 130:95-103.
90. Jauniaux E., Burton G.J. Pathophysiology of histological changes in early pregnancy loss. Placenta 2005, 26:114-123.
91. Jauniaux E., Farquharson R.G., Christiansen O.B., Exalto N. Evidence-based guidelines for the investigation and medical treatment of recurrent miscarriage. Hum. Reprod. 2006, 21:2216-2222.
92. Jauniaux E., Gulbis B., Burton G.J. Physiological implications of the materno-fetal oxygen gradient in human early pregnancy. Reprod. Biomed. Online 2003, 7:250-253.
93. Jauniaux E., Poston L., Burton G.J. Placental-related diseases of pregnancy: involvement of oxidative stress and implications in human evolution. Hum. Reprod. Update 2006, 12:747-755.
94. Jauniaux E., Watson A.L., Hempstock J., Bao Y.P., Skepper J.N., Burton G.J. Onset of maternal arterial blood flow and placental oxidative stress. A possible factor in human early pregnancy failure. Am. J. Pathol. 2000, 157:2111-2122.
95. Jerzak M., Bischof P. Apoptosis in the first trimester human placenta: the role in maintaining immune privilege at the maternal-foetal interface and in the trophoblast remodeling. Eur. J. Obstet. Gynecol. Reprod. Biol. 2002, 100:138-142.
96. Kadyrov M., Schmitz C., Black S., Kaufmann P., Huppertz B. Pre-eclampsia and maternal anaemia display reduced apoptosis and opposite invasive phenotypes of extravillous trophoblast. Placenta 2003, 24:540-548.
97. Kar M., Ghosh D., Sengupta J. Histochemical and morphological examination of proliferation and apoptosis in human first trimester villous trophoblast. Hum. Reprod. 2007, 22:2814-2823.
98. Kaufmann P., Black S., Huppertz B. Endovascular trophoblast invasion: implications for the pathogenesis of intrauterine growth retardation and preeclampsia. Biol. Reprod. 2003, 69:1-7.
99. Khan M.A., Kar M., Mittal S., Kumar S., Bharagava V.L., Sengupta J., Ghosh D. Small scale transcript expression profile of Human first trimester placental villi analyzed by a custom-tailored cDNA array. Indian J. Physiol. Pharmacol. 2010, 54:235-254.
100. Khan M.A., Mittal S., Kumar S., Sengupta J., Ghosh D. Quantitative analysis of six gene products as candidate markers of early placental villi development in the human. Indian J. Physiol. Pharmacol. 2010, 54:299-308.
101. Khan M.A., Manna S., Malhotra N., Sengupta J., Ghosh D. Genome-wide transcript profiles reveal that the expressional regulation of the genes linked to immunity and programmed development is operative in human first trimester placental villi. Indian J. Med. Res. 2013, (in press).
102. Kim Y.S., Kang H.S., Jetten A.M. The Kruppel-like zinc finger protein Glis2 functions as a negative modulator of the Wnt/β-catenin signaling pathway. FEBS Lett. 2007, 581:858-864.
103. Knofler M. Critical growth factors and signaling pathways controlling trophoblast invasion. Int. J. Dev. Biol. 2010, 54:269-280.
104. Kudaka W., Oda T., Jinno Y., Yoshimi N., Aoki Y. Cellular localization of placenta-specific human endogenous retrovirus (HERV) transcripts and their possible implication in pregnancy-induced hypertension. Placenta 2008, 29:282-289.
105. Kurjak A., Kupesic S. Doppler assessment of the intervillous blood flow in normal and abnormal early pregnancy. Obstet. Gynecol. 1997, 89:252-256.
106. Laity J.H., Lee B.M., Wright P.E. Zinc finger proteins: new insights into structural and functional diversity. Curr. Opin. Struct. Biol. 2001, 11:39-46.
107. Laresgoiti-Servitje E., Gómez-López N., Olson D.M. An immunological insight into the origins of pre-eclampsia. Hum. Reprod. Update 2010, 16:510-524.
108. Lau M.M., Stewart C.E., Liu Z., Bhatt H., Rotwein P., Stewart C.L. Loss of the imprinted IGF2/cation-independent mannose 6-phosphate receptor results in fetal overgrowth and perinatal lethality. Genes Dev. 1994, 8:2953-2963.
109. Leach L., Eaton B.M., Firth J.A., Contractor S.F. Immunogold localisation of endogenous immunoglobulin-G in ultrathin frozen sections of the human placenta. Cell Tissue Res. 1989, 257:603-607.
110. Lee C.L., Lam K.K., Koistinen H., Seppala M., Kurpisz M., Fernandez N., Pang R.T., Yeung W.S., Chiu P.C. Glycodelin-A as a paracrine regulator in early pregnancy. J.Reprod. Immunol. 2011, 90:29-34.
111. Levine B., Yuan J. Autophagy in cell death: an innocent convict?. J.Clin. Invest. 2005, 115:2679-2688.
112. Li L., Obinata M., Hori K. Role of peroxiredoxin III in the pathogenesis of pre-eclampsia as evidenced in mice. Oxid. Med. Cell. Longev. 2010, 3:71-73.
113. Li W., Zhu S., Li J., Huang Y., Rongrong Z. Ahepatic protein, fetuin-A, occupies a protective role in lethal systemic inflammation. PLoS One 2011, 6:e16945. 10.1371/journal.pone.0016945.
114. Lin C., Lin M., Chen H. Biochemical characterization of the human placental transcription factor GCma/1. Biochem. Cell. Biol. 2005, 83:188-195.
115. Liu J.P., Barker J., Perkins A.S., Robertson E.J., Efstratiadis A. Mice carrying null mutations of the genes encoding insulin-like growth factor I (IGF-I) and type 1 IGF receptor (IGFIR). Cell 1993, 75:59-72.
116. Liu A.X., Jin F., Zhang W.W., Zhou T.H., Zhou C.Y., Yao W.M., Qian Y.L., Huang H.F. Proteomic analysis on the alteration of protein expression in the placental villous tissue of early pregnancy loss. Biol. Reprod. 2006, 75:414-420.
117. Ljunger E., Cnattingius S., Lundin C., Annerén G. Chromosomal anomalies in first-trimester miscarriages. Acta. Obstet. Gynecol. Scand. 2005, 84:1103-1107.
118. Lockshin R.A., Zakeri Z. Programmed cell death and apoptosis: origins of the theory. Nat. Rev. Mol. Cell Biol. 2001, 2:545-550.
119. Lorenzi T., Turi A., Lorenzi M., Paolinelli F., Mancioli F., La Sala L., Morroni M., Ciarmela P., Mantovani A., Tranquilli A.L., Castellucci M., Marzioni D. Placental expression of CD100, CD72 and CD45 is dysregulated in human miscarriage. PLoS One 2012, 7:e35232. 10.1371/journal.pone.0035232.
120. Lorkowski S., Cullen P. ABCG subfamily of human ATP-binding cassette proteins. Pure Appl. Chem. 2002, 74:2057-2081.
121. MacLeod J.N., Lee A.K., Liebhaber S.A., Cooke N.E. Developmental control and alternative splicing of the placentally expressed transcripts from the human growth hormone cluster. J.Biol. Chem. 1992, 267:14219-14226.
122. Maiuri M.C., Zalckvar E., Kimchi A., Kroemer G. Self-eating and self-killing: crosstalk between autophagy and apoptosis. Nat. Rev. Mol. Cell Biol. 2007, 8:741-752.
123. Makris A., Thornton C., Thompson J., Thomson S., Martin R., Ogle R., Waugh R., McKenzie P., Kirwan P., Hennessy A. Uteroplacental ischemia results in proteinuric hypertension and elevated sFLT-1. Kidney Int. 2007, 71:977-984.
124. Mandò C., Tabano S., Colapietro P., Pileri P., Colleoni F., Avagliano L., Doi P., Bulfamante G., Miozzo M., Cetin I. Transferrin receptor gene and protein expression and localization in human IUGR and normal term placentas. Placenta 2011, 32:44-50.
125. Mannik J., Vaas P., Rull K., Teesalu P., Rebane T., Laan M. Differential expression profile of growth hormone/chorionic somatomammotropin genes in placenta of small- and large-for-gestational-age newborns. J.Clin. Endocrinol. Metabol. 2010, 95:2433-2442.
126. McNab F.W., Rajsbaum R., Stoye J.P., O'Garra A. Tripartite-motif proteins and innate immune regulation. Curr. Opin. Immunol. 2011, 23:46-56.
127. Medawar P. Some immunological and endocrinological problems raised by evolution of viviparity in vertebrates. Symp. Exp. Biol. 1953, 44:320-338.
128. Mercé L.T., Barco M.J., Alcázar J.L., Sabatel R., Troyano J. Intervillous and uteroplacental circulation in normal early pregnancy and early pregnancy loss assessed by 3-dimensional power Doppler angiography. Am. J. Obstet. Gynecol. 2009, 200:315.e1-315.e8.
129. Mikheev A.M., Nabekura T., Kaddoumi A., Bammler T.K., Govindarajan R., Hebert M.F., Unadkat J.D. Profiling gene expression in human placentae of different gestational ages: an OPRU Network and UW SCOR. Study. Reprod. Sci. 2008, 15:866-877.
130. Monk D., Arnaud P., Apostolidou S., Hills F.A., Kelsey G., Stanier P., Feil R., Moore G.E. Limited evolutionary conservation of imprinting in the human placenta. Proc. Natl. Acad. Sci. U. S. A. 2006, 103:6623-6628.
131. Moser G., Gauster M., Orendi K., Glasner A., Theuerkauf R., Huppertz B. Endoglandular trophoblast, an alternative route of trophoblast invasion? Analysis with novel confrontation co-culture models. Hum. Reprod. 2010, 25:1127-1136.
132. Murakami M., Ichisaka T., Maeda M., Oshiro N., Hara K., Edenhofer F., Kiyama H., Yonezawa K., Yamanaka S. mTOR is essential for growth and proliferation in early mouse embryos and embryonic stem cells. Mol. Cell. Biol. 2004, 24:6710-6718.
133. Myatt L. Control of vascular resistance in the human placenta. Placenta 1992, 13:329-341.
134. Myatt L., Eis A.L., Brockman D.E., Kossenjans W., Greer I.A., Lyall F. Differential localization of superoxide dismutase isoforms in placental villous tissue of normotensive, pre-eclamptic, and intrauterine growth-restricted pregnancies. J.Histochem. Cytochem. 1997, 45:1433-1438.
135. Nelissen E.C.M., Van Montfoort A.P.A., Dumoulin C.M., Evers J.L.H. Epigenetics and the placenta. Hum. Reprod. Update 2011, 17:397-417.
136. Ni Z., Mao Q. ATP-binding cassette efflux transporters in human placenta. Curr. Pharm. Biotechnol. 2011, 12:674-685.
137. Ochanuna Z., Geiger-Maor A., Dembinsky-Vaknin A., Karussis D., Tykocinski M.L., Rachmilewitz J. Inhibition of effector function but not T cell activation and increase in FoxP3 expression in T cells differentiated in the presence of PP14. PLoS One 2010, 23(5):e12868. 10.1371/journal.pone.0012868.
138. Pardi G., Marconi A.M., Cetin I. Placental-fetal interrelationship in IUGR fetuses - a review. Placenta 2002, 23(Suppl.A):136-141.
139. Parry S., Strauss J.F. Placental Hormones. Endocrinology 2005, 3353-3367. Elsevier Saunders, Philadelphia. fifth ed. L.J. DeGroot, L. Jameson (Eds.).
140. Pennington K.A., Schlitt J.M., Jackson D.L., Schulz L.C., Schust D.J. Preeclampsia: multiple approaches for a multifactorial disease. Dis. Model Mech. 2012, 5:9-18.
141. Petraglia F., Florio P., Torricelli M. Placental endocrine function. Knobil and Neill's Physiology of Reproduction 2005, 2747-2897. Elsevier Academic Press, London, UK. fifth ed. J.D. James (Ed.).
142. Prouillac C., Lecoeur S. The role of the placenta in fetal exposure to xenobiotics: importance of membrane transporters and human models for transfer studies. Drug Metab. Dispos. 2010, 38:1623-1635.
143. Rahanama F., Shafiei F., Gluckman P.D., Mitchell M.D., Lobie P.E. Epigenetic regulation of human trophoblastic cell migration and invasion. Endocrinology 2006, 147:5275-5283.
144. Reddy A., Suri S., Sargent I.L., Redman C.W., Muttukrishna S. Maternal circulating levels of activin A, inhibin A, sFlt-1 and endoglin at parturition in normal pregnancy and pre-eclampsia. PLoS One 2009, 4:e4453. 10.1371/journal.pone.0004453.
145. Regan L., Braude P.R., Trembath P.L. Influence of past reproductive performance on risk of spontaneous abortion. BMJ 1989, 299:541-545.
146. Robertson W.B., Brosens I., Pijnenborg R., De Wolf F. The making of the placental bed. Eur. J. Obstet. Gynecol. Reprod. Biol. 1984, 18:255-266.
147. Roos S., Jansson N., Palmberg I., Säljö K., Powell T.L., Jansson T. Mammalian target of rapamycin in the human placenta regulates leucine transport and is down-regulated in restricted fetal growth. J.Physiol. 2007, 582:449-459.
148. Roos S., Powell T.L., Jansson T. Placental mTOR links maternal nutrient availability to fetal growth. Biochem. Soc. Trans. 2009, 37:295-298.
149. Rull K., Laan M. Expression of beta-subunit of human chorionic gonadotropin genes during the normal and failed pregnancies. Hum. Reprod. 2005, 20:3360-3368.
150. Schanz A., Winn V.D., Fisher S.J., Blumenstein M., Heiss C., Hess A.P., Kruessel J.S., Mcmaster M., North R.A. Pre-eclampsia is associated with elevated CXCL12 levels in placental syncytiotrophoblasts and maternal blood. Eur. J. Obstet. Gynecol. Reprod. Biol. 2011, 157:32-37.
151. Sharp A.N., Heazell A.E., Crocker I.P., Mor G. Placental apoptosis in health and disease. Am. J. Reprod. Immunol. 2010, 64:159-169.
152. Sheikh S., Satoskar P., Bhartiya D. Expression of insulin-like growth factor-I and placental growth hormone mRNA in placentae: a comparison between normal and intrauterine growth retardation pregnancies. Mol. Hum. Reprod. 2001, 7:287-292.
153. Shichita T., Hasegawa E., Kimura A., Morita R., Sakaguchi R., Takada I., Sekiya T., Ooboshi H., Kitazono T., Yanagawa T., Ishii T., Takahashi H., Mori S., Nishibori M., Kuroda K., Akira S., Miyake K., Yoshimura A. Peroxiredoxin family proteins are key initiators of post-ischemic inflammation in the brain. Nat. Med. 2012, 18:911-917.
154. Sibley C.P., Turner M.A., Cetin I., Ayuk P., Boyd C.A., D'Souza S.W., Glazier J.D., Greenwood S.L., Jansson T., Powell T. Placental phenotypes of intrauterine growth. Pediatr. Res. 2005, 58:827-832.
155. Soleymanlou N., Jurisica I., Nevo O., Ietta F., Zhang X., Zamudio S., Post M., Cannigia I. Molecular evidence of placental hypoxia in preeclampsia. J.Clin. Endcrinol. Metab. 2006, 90:4299-4308.
156. Soni C., Karande A.A. Glycodelin A suppresses the cytolytic activity of CD8+ T lymphocytes. Mol. Immunol. 2010, 47:2458-2466.
157. Srinivas S.K., Edlow A.G., Neff P.M., Sammel M.D., Andrela C.M., Elovitz M.A. Rethinking IUGR in preeclampsia: dependent or independent of maternal hypertension?. J.Perinatol. 2009, 29:680-684.
158. Street M.E., Grossi E., Volta C., Faleschini E., Bernasconi S. Placental determinants of fetal growth: identification of key factors in the insulin-like growth factor and cytokine systems using artificial neural networks. B.M.C. Pediatr. 2008, 8:24. 10.1186/1471-2431-8-24.
159. Stortoni P., Cecati M., Giannubilo S.R., Sartini D., Turi A., Emanuelli M., Tranquilli A.L. Placental thrombomodulin expression in recurrent miscarriage. Reprod. Biol. Endocrinol. 2010, 8:1. 10.1186/1477-7827-8-1.
160. Struyf S., Proost P., Vandercappellen J., Dempe S., Noyens B., Nelissen S., Gouwy M., Locati M., Opdenakker G., Dinsart C., Van Damme J. Synergistic up-regulation of MCP-2/CCL8 activity is counteracted by chemokine cleavage, limiting its inflammatory and anti-tumoral effects. Eur. J. Immunol. 2009, 39:843-857.
161. Stulc J. Placental transfer of inorganic ions and water. Physiol. Rev. 1997, 77:805-836.
162. Su M.T., Lin S.H., Chen Y.C. Genetic association studies of angiogenesis- and vasoconstriction-related genes in women with recurrent pregnancy loss: a systematic review and meta-analysis. Hum. Reprod. Update 2011, 17:803-812.
163. Su M.T., Lin S.H., Lee I.W., Chen Y.C., Kuo P.L. Association of polymorphisms/haplotypes of the genes encoding vascular endothelial growth factor and its KDR receptor with recurrent pregnancy loss. Hum. Reprod. 2011, 26:758-764.
164. Svensson A.M., Waters B.L., Laszik Z.G., Simmons-Arnold L., Goodwin A., Beatty B.G., Bovill E.G. The protein C system in placental massive perivillous fibrin deposition. Blood Coagul. Fibrinolysis 2004, 15:491-495.
165. Tirado-González I., Muñoz-Fernández R., Prados A., Leno-Durán E., Martin F., Abadía-Molina A.C., Olivares E.G. Apoptotic DC-SIGN+ cells in normal human decidua. Placenta 2012, 33:257-263.
166. Toft J.H., Lian I.A., Tarca A.L., Erez O., Espinoza J., Eide I.P., Bjørge L., Draghici S., Romero R., Austgulen R. Whole-genome microarray and targeted analysis of angiogenesis-regulating gene expression (ENG, FLT1, VEGF, PlGF) in placentas from pre-eclamptic and small-for-gestational-age pregnancies. J.Matern. Fetal Neonatal Med. 2008, 21:267-273.
167. Tokunaga C., Yoshino K., Yonezawa K. mTOR integrates amino acid- and energy-sensing pathways. Biochem. Biophys. Res. Commun. 2004, 313:443-446.
168. Van den Brink G.R., Bleuming S.A., Hardwick J.C., Schepman B.L., Offerhaus G.J., Keller J.J., Nielsen C., Gaffield W., van Deventer S.J., Roberts D.J., Peppelenbosch M.P. Indian Hedgehog is an antagonist of Wnt signaling in colonic epithelial cell differentiation. Nat. Genet. 2004, 36:277-282.
169. Wang Y., Walsh S.W. TNF alpha concentrations and mRNA expression are increased in preeclamptic placentas. J.Reprod. Immunol. 1996, 32:157-169.
170. Wang Y., Walsh S.W. Antioxidant activities and mRNA expression of superoxide dismutase, catalase, and glutathione peroxidase in normal and preeclamptic placentas. J.Soc. Gynecol. Invest. 1996, 3:179-184.
171. Wang S., Kallichanda N., Song W., Ramirez B.A., Ross M.G. Expression of aquaporin-8 in human placenta and chorioamniotic membranes: evidence of molecular mechanism for intramembranous amniotic fluid resorption. Am. J. Obstet. Gynecol. 2001, 185:1226-1231.
172. Warning J.C., McCracken S.A., Morris J.M. Abalancing act: mechanisms by which the fetus avoids rejection by the maternal immune system. Reproduction 2011, 141:715-724.
173. Webster R.P., Brockman D., Myatt L. Nitration of p38 MAPK in the placenta: association of nitration with reduced catalytic activity of p38 MAPK in pre-eclampsia. Mol. Hum. Reprod. 2006, 12:677-685.
174. Wen H.Y., Abbasi S., Kellems R.E., Xia Y. mTOR: a placental growth signaling sensor. Placenta 2005, 26(Suppl.A):63-69.
175. Wilkins J.F., Haig D. Parental modifiers, antisense transcripts and loss of imprinting. Proc. Biol. Sci. 2002, 269:1841-1846.
176. Yamada K., Ogawa H., Honda S.I., Harada N., Okazaki T. AGCM motif protein is involved in placenta-specific expression of human aromatase gene. J.Biol. Chem. 1999, 274:32279-32286.
177. Yin K., Chen W.J., Zhou Z.G., Zhao G.J., Lv Y.C., Ouyang X.P., Yu X.H., Fu Y., Jiang Z.S., Tang C.K. Apolipoprotein A-I inhibits CD40 proinflammatory signaling via ATP-binding cassette transporter A1-mediated modulation of lipid raft in macrophages. J.Atheroscler. Thromb. 2012, 19:823-836.
178. Yurdakan G., Ekem T.E., Bahadir B., Gun B.D., Kuzey G.M., Ozdamar S.O. Expression of adhesion molecules in first trimester spontaneous abortions and their role in abortion pathogenesis. Acta. Obstet. Gynecol. Scand. 2008, 87:775-782.
179. Zhang E.G., Burton G.J., Smith S.K., Charnock-Jones D.S. Placental vessel adaptation during gestation and to high altitude: changes in diameter and perivascular cell coverage. Placenta 2002, 23:751-762.
180. Zhou Y., Damsky C.H., Fisher S.J. Preeclampsia is associated with failure of human cytotrophoblasts to mimic a vascular adhesion phenotype. One cause of defective endovascular invasion in this syndrome?. J.Clin. Invest. 1997, 99:2152-2164.
181. Zhou Y., Fisher S.J., Janatpour M., Genbacev O., Dejana E., Wheelock M., Damsky C.H. Human cytotrophoblasts adopt a vascular phenotype as they differentiate. A strategy for successful endovascular invasion?. J.Clin. Invest. 1997, 99:2139-2151.
182. Zhou H., Huang S. Role of mtOR signaling in tumor cell motility, invasion and metastasis. Curr. Protein Pept. Sci. 2011, 12:30-42.
183. Zhou Y., McMaster M., Woo K., Janatpour M., Perry J., Karpanen T., Alitalo K., Damsky C., Fisher S.J. Vascular endothelial growth factor ligands and receptors that regulate human cytotrophoblast survival are dysregulated in severe preeclampsia and hemolysis, elevated liver enzymes, and low platelets syndrome. Am. J. Pathol. 2002, 160:1405-1423.