Skip to main content
Key Specialties
Cardiology Diabetology Endocrinology Gastroenterology Geriatrics and Gerontology Gynecology and Obstetrics Hematology Infectious Disease Internal Medicine Nephrology Neurology Oncology Pediatrics Respiratory Medicine Rheumatology Surgery
Congress Coverage
2024 ACC Congress 2023 ESMO Congress 2023 EASD Congress 2023 ERS Congress 2023 ESC Congress 2023 EHA Congress 2023 ASCO Annual Meeting
Clinical Collections
Advances in Alzheimer’s

At a glance: The ONWARDS insulin icodec trials

A round-up of the ONWARDS phase 3 clinical trials evaluating the novel weekly insulin icodec in people with diabetes.
ADVANCED SEARCH
Log in
Top
Reproductive Biology and Endocrinology
Published in: Reproductive Biology and Endocrinology 1/2018

Open Access 01-12-2018 | Review

Shifting perspectives from “oncogenic” to oncofetal proteins; how these factors drive placental development

Authors: Rachel C. West, Gerrit J. Bouma, Quinton A. Winger

Published in: Reproductive Biology and Endocrinology | Issue 1/2018

Login to get access

Abstract

Early human placental development strongly resembles carcinogenesis in otherwise healthy tissues. The progenitor cells of the placenta, the cytotrophoblast, rapidly proliferate to produce a sufficient number of cells to form an organ that will contribute to fetal development as early as the first trimester. The cytotrophoblast cells begin to differentiate, some towards the fused cells of the syncytiotrophoblast and some towards the highly invasive and migratory extravillous trophoblast. Invasion and migration of extravillous trophoblast cells mimics tumor metastasis. One key difference between cancer progression and placental development is the tight regulation of these oncogenes and oncogenic processes. Often, tumor suppressors and oncogenes work synergistically to regulate cell proliferation, differentiation, and invasion in a restrained manner compared to the uncontrollable growth in cancer. This review will compare and contrast the mechanisms that drive both cancer progression and placental development. Specifically, this review will focus on the molecular mechanisms that promote cell proliferation, evasion of apoptosis, cell invasion, and angiogenesis.
Literature
1.
Goplerud JM, Delivoria-Papadopoulos M. Physiology of the placenta--gas exchange. Ann Clin Lab Sci. 1985;15(4):270–8.PubMed
2.
Hay WW Jr. Placental transport of nutrients to the fetus. Horm Res. 1994;42(4–5):215–22.PubMed
3.
Freemark M. Placental hormones and the control of fetal growth. J Clin Endocrinol Metab. 2010;95(5):2054–7.PubMedCrossRef
4.
Ilekis JV, Reddy UM, Roberts JM. Preeclampsia--a pressing problem: an executive summary of a National Institute of Child Health and Human Development workshop. Reprod Sci. 2007;14(6):508–23.PubMedCrossRef
5.
Gude NM, et al. Growth and function of the normal human placenta. Thromb Res. 2004;114(5–6):397–407.PubMedCrossRef
6.
7.
Coolman M, et al. Medical record validation of maternally reported history of preeclampsia. J Clin Epidemiol. 2010;63(8):932–7.PubMedCrossRef
8.
Ergaz Z, Avgil M, Ornoy A. Intrauterine growth restriction-etiology and consequences: what do we know about the human situation and experimental animal models? Reprod Toxicol. 2005;20(3):301–22.PubMedCrossRef
9.
Ananth CV, Vintzileos AM. Epidemiology of preterm birth and its clinical subtypes. J Matern Fetal Neonatal Med. 2006;19(12):773–82.PubMedCrossRef
10.
Hutter D, Kingdom J, Jaeggi E. Causes and mechanisms of intrauterine hypoxia and its impact on the fetal cardiovascular system: a review. Int J Pediatr. 2010;2010:401323.PubMedPubMedCentralCrossRef
11.
12.
von Beckerath AK, et al. Perinatal complications and long-term neurodevelopmental outcome of infants with intrauterine growth restriction. Am J Obstet Gynecol. 2013;208(2):130 e1–6.CrossRef
13.
14.
Veerbeek JH, et al. Placental pathology in early intrauterine growth restriction associated with maternal hypertension. Placenta. 2014;35(9):696–701.PubMedCrossRef
15.
Huppertz B. Placental origins of preeclampsia: challenging the current hypothesis. Hypertension. 2008;51(4):970–5.PubMedCrossRef
16.
Dunn CL, Kelly RW, Critchley HO. Decidualization of the human endometrial stromal cell: an enigmatic transformation. Reprod BioMed Online. 2003;7(2):151–61.PubMedCrossRef
17.
18.
Gellersen B, Brosens JJ. Cyclic decidualization of the human endometrium in reproductive health and failure. Endocr Rev. 2014;35(6):851–905.PubMedCrossRef
19.
Brosens JJ, Pijnenborg R, Brosens IA. The myometrial junctional zone spiral arteries in normal and abnormal pregnancies: a review of the literature. Am J Obstet Gynecol. 2002;187(5):1416–23.PubMedCrossRef
20.
Cross JC, Werb Z, Fisher SJ. Implantation and the placenta: key pieces of the development puzzle. Science. 1994;266(5190):1508–18.PubMedCrossRef
21.
Croxatto HB, et al. Studies on the duration of egg transport in the human oviduct. I. the time interval between ovulation and egg recovery from the uterus in normal women. Fertil Steril. 1972;23(7):447–58.PubMedCrossRef
22.
Hardy K, Handyside AH, Winston RM. The human blastocyst: cell number, death and allocation during late preimplantation development in vitro. Development. 1989;107(3):597–604.PubMed
23.
James JL, Carter AM, Chamley LW. Human placentation from nidation to 5 weeks of gestation. Part II: tools to model the crucial first days. Placenta. 2012;33(5):335–42.PubMedCrossRef
24.
Hertig AT, Rock J, Adams EC. A description of 34 human ova within the first 17 days of development. Am J Anat. 1956;98(3):435–93.PubMedCrossRef
25.
26.
Yabe S, et al. Comparison of syncytiotrophoblast generated from human embryonic stem cells and from term placentas. Proc Natl Acad Sci U S A. 2016;113(19):E2598–607.PubMedPubMedCentralCrossRef
27.
Genbacev O, et al. Hypoxia alters early gestation human cytotrophoblast differentiation/invasion in vitro and models the placental defects that occur in preeclampsia. J Clin Invest. 1996;97(2):540–50.PubMedPubMedCentralCrossRef
28.
Lyall F, et al. Human trophoblast invasion and spiral artery transformation: the role of PECAM-1 in normal pregnancy, preeclampsia, and fetal growth restriction. Am J Pathol. 2001;158(5):1713–21.PubMedPubMedCentralCrossRef
29.
Ferretti C, et al. Molecular circuits shared by placental and cancer cells, and their implications in the proliferative, invasive and migratory capacities of trophoblasts. Hum Reprod Update. 2007;13(2):121–41.PubMedCrossRef
30.
Ladines-Llave CA, et al. Cytologic localization of epidermal growth factor and its receptor in developing human placenta varies over the course of pregnancy. Am J Obstet Gynecol. 1991;165(5 Pt 1):1377–82.PubMedCrossRef
31.
Horowitz GM, et al. Immunohistochemical localization of transforming growth factor-alpha in human endometrium, decidua, and trophoblast. J Clin Endocrinol Metab. 1993;76(3):786–92.PubMed
32.
Dungy LJ, Siddiqi TA, Khan S. Transforming growth factor-beta 1 expression during placental development. Am J Obstet Gynecol. 1991;165(4 Pt 1):853–7.PubMedCrossRef
33.
Maruo T, Mochizuki M. Immunohistochemical localization of epidermal growth factor receptor and myc oncogene product in human placenta: implication for trophoblast proliferation and differentiation. Am J Obstet Gynecol. 1987;156(3):721–7.PubMedCrossRef
34.
Clark DE, et al. Localization of VEGF and expression of its receptors flt and KDR in human placenta throughout pregnancy. Hum Reprod. 1996;11(5):1090–8.PubMedCrossRef
35.
Maglione D, et al. Isolation of a human placenta cDNA coding for a protein related to the vascular permeability factor. Proc Natl Acad Sci U S A. 1991;88(20):9267–71.PubMedPubMedCentralCrossRef
36.
Fant M, Munro H, Moses AC. An autocrine/paracrine role for insulin-like growth factors in the regulation of human placental growth. J Clin Endocrinol Metab. 1986;63(2):499–505.PubMedCrossRef
37.
Scaltriti M, Baselga J. The epidermal growth factor receptor pathway: a model for targeted therapy. Clin Cancer Res. 2006;12(18):5268–72.PubMedCrossRef
38.
Forbes K, et al. 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(6):C1313–22.PubMedCrossRef
39.
Hatano N, et al. Essential role for ERK2 mitogen-activated protein kinase in placental development. Genes Cells. 2003;8(11):847–56.PubMedCrossRef
40.
Simmons DG, Cross JC. Determinants of trophoblast lineage and cell subtype specification in the mouse placenta. Dev Biol. 2005;284(1):12–24.PubMedCrossRef
41.
Yang ZZ, et al. Protein kinase B alpha/Akt1 regulates placental development and fetal growth. J Biol Chem. 2003;278(34):32124–31.CrossRefPubMed
42.
Kita N, et al. Expression and activation of MAP kinases, ERK1/2, in the human villous trophoblasts. Placenta. 2003;24(2–3):164–72.PubMedCrossRef
43.
Dungy LJ, Siddiqi TA, Khan S. C-jun and jun-B oncogene expression during placental development. Am J Obstet Gynecol. 1991;165(6 Pt 1):1853–6.PubMedCrossRef
44.
Dakour J, et al. EGF promotes development of a differentiated trophoblast phenotype having c-myc and junB proto-oncogene activation. Placenta. 1999;20(1):119–26.PubMedCrossRef
45.
Chen H, et al. Adiponectin exerts antiproliferative effect on human placenta via modulation of the JNK/c-Jun pathway. Int J Clin Exp Pathol. 2014;7(6):2894–904.PubMedPubMedCentral
46.
Faas L, et al. Lin28 proteins are required for germ layer specification in Xenopus. Development. 2013;140(5):976–86.PubMedCrossRef
47.
Guo Y, et al. Identification and characterization of LIN-28 homolog B (LIN28B) in human hepatocellular carcinoma. Gene. 2006;384:51–61.PubMedCrossRef
48.
49.
Wang T, et al. Aberrant regulation of the LIN28A/LIN28B and let-7 loop in human malignant tumors and its effects on the hallmarks of cancer. Mol Cancer. 2015;14:125.PubMedPubMedCentralCrossRef
50.
51.
52.
Lotem J, Sachs L. Control of apoptosis in hematopoiesis and leukemia by cytokines, tumor suppressor and oncogenes. Leukemia. 1996;10(6):925–31.PubMed
53.
Gooch JL, Van Den Berg CL, Yee D. Insulin-like growth factor (IGF)-I rescues breast cancer cells from chemotherapy-induced cell death--proliferative and anti-apoptotic effects. Breast Cancer Res Treat. 1999;56(1):1–10.PubMedCrossRef
54.
Peruzzi F, et al. Multiple signaling pathways of the insulin-like growth factor 1 receptor in protection from apoptosis. Mol Cell Biol. 1999;19(10):7203–15.PubMedPubMedCentralCrossRef
55.
Kennedy SG, et al. The PI 3-kinase/Akt signaling pathway delivers an anti-apoptotic signal. Genes Dev. 1997;11(6):701–13.PubMedCrossRef
56.
Scotlandi K, et al. Expression of an IGF-I receptor dominant negative mutant induces apoptosis, inhibits tumorigenesis and enhances chemosensitivity in Ewing's sarcoma cells. Int J Cancer. 2002;101(1):11–6.PubMedCrossRef
57.
Harris LK, et al. 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. 2011;84(3):440–6.PubMedCrossRef
58.
Walenkamp MJ, et al. A variable degree of intrauterine and postnatal growth retardation in a family with a missense mutation in the insulin-like growth factor I receptor. J Clin Endocrinol Metab. 2006;91(8):3062–70.PubMedCrossRef
59.
Gibson JM, et al. Regulation of IGF bioavailability in pregnancy. Mol Hum Reprod. 2001;7(1):79–87.PubMedCrossRef
60.
61.
Reed JC, et al. Differential expression of bcl2 protooncogene in neuroblastoma and other human tumor cell lines of neural origin. Cancer Res. 1991;51(24):6529–38.PubMed
62.
Gala JL, et al. High expression of bcl-2 is the rule in acute lymphoblastic leukemia, except in Burkitt subtype at presentation, and is not correlated with the prognosis. Ann Hematol. 1994;69(1):17–24.CrossRefPubMed
63.
Chen-Levy Z, Nourse J, Cleary ML. The bcl-2 candidate proto-oncogene product is a 24-kilodalton integral-membrane protein highly expressed in lymphoid cell lines and lymphomas carrying the t(14,18) translocation. Mol Cell Biol. 1989;9(2):701–10.PubMedPubMedCentralCrossRef
64.
65.
van Golen CM, Castle VP, Feldman EL. IGF-I receptor activation and BCL-2 overexpression prevent early apoptotic events in human neuroblastoma. Cell Death Differ. 2000;7(7):654–65.PubMedCrossRef
66.
Ishihara N, et al. 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(3):317–27.PubMedCrossRef
67.
68.
Ratts VS, et al. Expression of BCL-2, BAX and BAK in the trophoblast layer of the term human placenta: a unique model of apoptosis within a syncytium. Placenta. 2000;21(4):361–6.PubMedCrossRef
69.
Soni S, et al. Apoptosis and Bcl-2 protein expression in human placenta over the course of normal pregnancy. Anat Histol Embryol. 2010;39(5):426–31.PubMed
70.
Singleton JR, Randolph AE, Feldman EL. Insulin-like growth factor I receptor prevents apoptosis and enhances neuroblastoma tumorigenesis. Cancer Res. 1996;56(19):4522–9.PubMed
71.
Cao Y, et al. Insulin-like growth factor (IGF)-1 suppresses oligodendrocyte caspase-3 activation and increases glial proliferation after ischemia in near-term fetal sheep. J Cereb Blood Flow Metab. 2003;23(6):739–47.PubMedCrossRef
72.
Longtine MS, et al. Caspase-mediated apoptosis of trophoblasts in term human placental villi is restricted to cytotrophoblasts and absent from the multinucleated syncytiotrophoblast. Reproduction. 2012;143(1):107–21.PubMedCrossRef
73.
74.
75.
76.
77.
Forbes K, Westwood M. Maternal growth factor regulation of human placental development and fetal growth. J Endocrinol. 2010;207(1):1–16.PubMedCrossRef
78.
Buckbinder L, et al. Induction of the growth inhibitor IGF-binding protein 3 by p53. Nature. 1995;377(6550):646–9.CrossRefPubMed
79.
Neuberg M, et al. The p53/IGF-1 receptor axis in the regulation of programmed cell death. Endocrine. 1997;7(1):107–9.PubMedCrossRef
80.
81.
82.
83.
84.
Vaira V, et al. Regulation of survivin expression by IGF-1/mTOR signaling. Oncogene. 2007;26(19):2678–84.PubMedCrossRef
85.
Lehner R, et al. Localization of telomerase hTERT protein and survivin in placenta: relation to placental development and hydatidiform mole. Obstet Gynecol. 2001;97(6):965–70.PubMed
86.
87.
Li CF, et al. Reduced expression of survivin, the inhibitor of apoptosis protein correlates with severity of preeclampsia. Placenta. 2012;33(1):47–51.PubMedCrossRef
88.
Pollheimer J, Knofler M. Signalling pathways regulating the invasive differentiation of human trophoblasts: a review. Placenta. 2005;26(Suppl A):S21–30.PubMedCrossRef
89.
Farahani E, et al. Cell adhesion molecules and their relation to (cancer) cell stemness. Carcinogenesis. 2014;35(4):747–59.PubMedCrossRef
90.
91.
Damsky CH, et al. Integrin switching regulates normal trophoblast invasion. Development. 1994;120(12):3657–66.PubMed
92.
Zhou Y, et al. Preeclampsia is associated with abnormal expression of adhesion molecules by invasive cytotrophoblasts. J Clin Invest. 1993;91(3):950–60.PubMedPubMedCentralCrossRef
93.
94.
Mise N, et al. Zyxin is a transforming growth factor-beta (TGF-beta)/Smad3 target gene that regulates lung cancer cell motility via integrin alpha5beta1. J Biol Chem. 2012;287(37):31393–405.PubMedPubMedCentralCrossRef
95.
Huang Z, et al. Transforming growth factor beta1 promotes invasion of human JEG-3 trophoblast cells via TGF-beta/Smad3 signaling pathway. Oncotarget. 2017;8(20):33560–70.PubMedPubMedCentral
96.
Cheng JC, Chang HM, Leung PC. Transforming growth factor-beta1 inhibits trophoblast cell invasion by inducing snail-mediated down-regulation of vascular endothelial-cadherin protein. J Biol Chem. 2013;288(46):33181–92.PubMedPubMedCentralCrossRef
97.
98.
Vleminckx K, et al. Genetic manipulation of E-cadherin expression by epithelial tumor cells reveals an invasion suppressor role. Cell. 1991;66(1):107–19.PubMedCrossRef
99.
Behrens J, et al. Dissecting tumor cell invasion: epithelial cells acquire invasive properties after the loss of uvomorulin-mediated cell-cell adhesion. J Cell Biol. 1989;108(6):2435–47.PubMedCrossRef
100.
Hay ED. An overview of epithelio-mesenchymal transformation. Acta Anat (Basel). 1995;154(1):8–20.CrossRef
101.
Zhou Y, et al. Human cytotrophoblasts adopt a vascular phenotype as they differentiate. A strategy for successful endovascular invasion? J Clin Invest. 1997;99(9):2139–51.PubMedPubMedCentralCrossRef
102.
Blechschmidt K, et al. Expression of E-cadherin and its repressor snail in placental tissue of normal, preeclamptic and HELLP pregnancies. Virchows Arch. 2007;450(2):195–202.PubMedCrossRef
103.
104.
Mehner C, et al. Tumor cell-produced matrix metalloproteinase 9 (MMP-9) drives malignant progression and metastasis of basal-like triple negative breast cancer. Oncotarget. 2014;5(9):2736–49.PubMedPubMedCentralCrossRef
105.
Cohen M, Meisser A, Bischof P. Metalloproteinases and human placental invasiveness. Placenta. 2006;27(8):783–93.PubMedCrossRef
106.
Demir-Weusten AY, et al. Matrix metalloproteinases-2, −3 and −9 in human term placenta. Acta Histochem. 2007;109(5):403–12.PubMedCrossRef
107.
Onogi A, et al. Hypoxia inhibits invasion of extravillous trophoblast cells through reduction of matrix metalloproteinase (MMP)-2 activation in the early first trimester of human pregnancy. Placenta. 2011;32(9):665–70.PubMedCrossRef
108.
Cohen M, et al. Role of decidua in trophoblastic invasion. Neuro Endocrinol Lett. 2010;31(2):193–7.PubMed
109.
Tapia-Pizarro A, et al. Human chorionic gonadotropin (hCG) modulation of TIMP1 secretion by human endometrial stromal cells facilitates extravillous trophoblast invasion in vitro. Hum Reprod. 2013;28(8):2215–27.PubMedCrossRef
110.
Zygmunt M, et al. Invasion of cytotrophoblastic JEG-3 cells is stimulated by hCG in vitro. Placenta. 1998;19(8):587–93.PubMedCrossRef
111.
Prast J, et al. Human chorionic gonadotropin stimulates trophoblast invasion through extracellularly regulated kinase and AKT signaling. Endocrinology. 2008;149(3):979–87.PubMedCrossRef
112.
Geva E, et al. Human placental vascular development: vasculogenic and angiogenic (branching and nonbranching) transformation is regulated by vascular endothelial growth factor-a, angiopoietin-1, and angiopoietin-2. J Clin Endocrinol Metab. 2002;87(9):4213–24.PubMedCrossRef
113.
Carmeliet P, et al. Synergism between vascular endothelial growth factor and placental growth factor contributes to angiogenesis and plasma extravasation in pathological conditions. Nat Med. 2001;7(5):575–83.PubMedCrossRef
114.
Demir R, Seval Y, Huppertz B. Vasculogenesis and angiogenesis in the early human placenta. Acta Histochem. 2007;109(4):257–65.PubMedCrossRef
115.
Arroyo JA, Winn VD. Vasculogenesis and angiogenesis in the IUGR placenta. Semin Perinatol. 2008;32(3):172–7.PubMedCrossRef
116.
Wang, Y. and S. Zhao, in Vascular Biology of the Placenta. San Rafael (CA). Morgan and Claypool Publishers; 2010.
117.
Vuorela P, et al. Expression of vascular endothelial growth factor and placenta growth factor in human placenta. Biol Reprod. 1997;56(2):489–94.PubMedCrossRef
118.
Gourvas V, et al. Angiogenic factors in placentas from pregnancies complicated by fetal growth restriction (review). Mol Med Rep. 2012;6(1):23–7.PubMed
119.
Kingdom J, et al. Development of the placental villous tree and its consequences for fetal growth. Eur J Obstet Gynecol Reprod Biol. 2000;92(1):35–43.PubMedCrossRef
120.
Charnock-Jones DS, Kaufmann P, Mayhew TM. Aspects of human fetoplacental vasculogenesis and angiogenesis. I Molecular regulation. Placenta. 2004;25(2–3):103–13.PubMedCrossRef
121.
Ahmed A, et al. Regulation of placental vascular endothelial growth factor (VEGF) and placenta growth factor (PIGF) and soluble Flt-1 by oxygen--a review. Placenta. 2000;21(Suppl A):S16–24.PubMedCrossRef
122.
123.
Saffer C, et al. Determination of placental growth factor (PlGF) levels in healthy pregnant women without signs or symptoms of preeclampsia. Pregnancy Hypertens. 2013;3(2):124–32.PubMedCrossRef
124.
Eriksson A, et al. Placenta growth factor-1 antagonizes VEGF-induced angiogenesis and tumor growth by the formation of functionally inactive PlGF-1/VEGF heterodimers. Cancer Cell. 2002;1(1):99–108.CrossRefPubMed
125.
Kaufmann P, et al. The fetal vascularisation of term human placental villi. II. Intermediate and terminal villi. Anat Embryol (Berl). 1985;173(2):203–14.CrossRef
126.
Shweiki D, et al. Vascular endothelial growth factor induced by hypoxia may mediate hypoxia-initiated angiogenesis. Nature. 1992;359(6398):843–5.CrossRefPubMed
127.
Plate KH, et al. Vascular endothelial growth factor is a potential tumour angiogenesis factor in human gliomas in vivo. Nature. 1992;359(6398):845–8.CrossRefPubMed
128.
Tuder RM, Flook BE, Voelkel NF. Increased gene expression for VEGF and the VEGF receptors KDR/Flk and Flt in lungs exposed to acute or to chronic hypoxia. Modulation of gene expression by nitric oxide. J Clin Invest. 1995;95(4):1798–807.PubMedPubMedCentralCrossRef
129.
Jauniaux E, et al. Trophoblastic oxidative stress in relation to temporal and regional differences in maternal placental blood flow in normal and abnormal early pregnancies. Am J Pathol. 2003;162(1):115–25.PubMedPubMedCentralCrossRef
130.
Wheeler T, Elcock CL, Anthony FW. Angiogenesis and the placental environment. Placenta. 1995;16(3):289–96.PubMedCrossRef
131.
Kim S, et al. Regulation of angiogenesis in vivo by ligation of integrin alpha5beta1 with the central cell-binding domain of fibronectin. Am J Pathol. 2000;156(4):1345–62.PubMedPubMedCentralCrossRef
132.
Parsons-Wingerter P, et al. Uniform overexpression and rapid accessibility of alpha5beta1 integrin on blood vessels in tumors. Am J Pathol. 2005;167(1):193–211.PubMedPubMedCentralCrossRef
133.
Goerges AL, Nugent MA. pH regulates vascular endothelial growth factor binding to fibronectin: a mechanism for control of extracellular matrix storage and release. J Biol Chem. 2004;279(3):2307–15.PubMedCrossRef
134.
Gaus G, et al. Extracellular pH modulates the secretion of fibronectin isoforms by human trophoblast. Acta Histochem. 2002;104(1):51–63.PubMedCrossRef
135.
Lee MY, et al. Angiogenesis in differentiated placental multipotent mesenchymal stromal cells is dependent on integrin alpha5beta1. PLoS One. 2009;4(10):e6913.PubMedPubMedCentralCrossRef
136.
Krebs C, Longo LD, Leiser R. Term ovine placental vasculature: comparison of sea level and high altitude conditions by corrosion cast and histomorphometry. Placenta. 1997;18(1):43–51.PubMedCrossRef
137.
Kiserud T, et al. Estimation of the pressure gradient across the fetal ductus venosus based on Doppler velocimetry. Ultrasound Med Biol. 1994;20(3):225–32.PubMedCrossRef
138.
Macara L, et al. Structural analysis of placental terminal villi from growth-restricted pregnancies with abnormal umbilical artery Doppler waveforms. Placenta. 1996;17(1):37–48.PubMedCrossRef
139.
140.
Vanneste E, et al. Chromosome instability is common in human cleavage-stage embryos. Nat Med. 2009;15(5):577–83.PubMedCrossRef
141.
Fragouli E, et al. The origin and impact of embryonic aneuploidy. Hum Genet. 2013;132(9):1001–13.PubMedCrossRef
142.
Farquharson RG, Stephenson MD, editors. Early pregnancy. Second edition. Cambridge: Cambridge University Press; 2017. pages cm
143.
Cross JC. Genetic insights into trophoblast differentiation and placental morphogenesis. Semin Cell Dev Biol. 2000;11(2):105–13.PubMedCrossRef
144.
145.
146.
147.
Velicky P, Knofler M, Pollheimer J. Function and control of human invasive trophoblast subtypes: intrinsic vs. maternal control. Cell Adhes Migr. 2016;10(1–2):154–62.CrossRef
148.
149.
150.
West SC. Molecular views of recombination proteins and their control. Nat Rev Mol Cell Biol. 2003;4(6):435–45.PubMedCrossRef
151.
Ahmed KM, Tsai CY, Lee WH. Derepression of HMGA2 via removal of ZBRK1/BRCA1/CtIP complex enhances mammary tumorigenesis. J Biol Chem. 2010;285(7):4464–71.PubMedCrossRef
152.
153.
Hakem R, et al. The tumor suppressor gene Brca1 is required for embryonic cellular proliferation in the mouse. Cell. 1996;85(7):1009–23.CrossRefPubMed
Metadata
Title
Shifting perspectives from “oncogenic” to oncofetal proteins; how these factors drive placental development
Authors
Rachel C. West
Gerrit J. Bouma
Quinton A. Winger
Publication date
01-12-2018
Publisher
BioMed Central
Published in
Reproductive Biology and Endocrinology / Issue 1/2018
Electronic ISSN: 1477-7827
DOI
https://doi.org/10.1186/s12958-018-0421-3

Other articles of this Issue 1/2018

Reproductive Biology and Endocrinology 1/2018 Go to the issue

Research

Influencing factors of pregnancy loss and survival probability of clinical pregnancies conceived through assisted reproductive technology

Research

Meta-analysis of ART outcomes in women with different preconception TSH levels

Review

Smoke, alcohol and drug addiction and male fertility

Short communication

Follicle-stimulating hormone (FSH) promotes retinol uptake and metabolism in the mouse ovary

Research

Regulation by FSH of the dynamic expression of retinol-binding protein 4 in the mouse ovary

Short communication

Live birth after Laser Assisted Viability Assessment (LAVA) to detect pentoxifylline resistant ejaculated immotile spermatozoa during ICSI in a couple with male Kartagener’s syndrome