Activation of the Canonical Wingless/T-Cell Factor Signaling Pathway Promotes Invasive Differentiation of Human Trophoblast

The American Journal of Pathology - Tập 168 Số 4 - Trang 1134-1147 - 2006
Jürgen Pollheimer1, Thomas Loregger1, Stefan Sonderegger1, Leila Saleh1, Sandra Bauer1, Martin Bilban2, K. Czerwenka3, Peter Husslein1, Martin Knöfler1
1Departments of Obstetrics and Gynecology, Medical University of Vienna, Vienna, Austria
2Medical and Chemical Laboratory Diagnostics, Medical University of Vienna, Vienna, Austria
3Clinical Pathology, Medical University of Vienna, Vienna, Austria

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Pijnenborg, 1983, Uteroplacental arterial changes related to interstitial trophoblast migration in early human pregnancy, Placenta, 4, 397, 10.1016/S0143-4004(83)80043-5

Zhou, 1997, Human cytotrophoblasts adopt a vascular phenotype as they differentiate. A strategy for successful endovascular invasion?, J Clin Invest, 99, 2139, 10.1172/JCI119387

Librach, 1991, 92-kD type IV collagenase mediates invasion of human cytotrophoblasts, J Cell Biol, 113, 437, 10.1083/jcb.113.2.437

Damsky, 1992, Distribution patterns of extracellular matrix components and adhesion receptors are intricately modulated during first trimester cytotrophoblast differentiation along the invasive pathway, in vivo, J Clin Invest, 89, 210, 10.1172/JCI115565

Vicovac, 1995, Trophoblast differentiation during formation of anchoring villi in a model of the early human placenta in vitro, Placenta, 16, 41, 10.1016/0143-4004(95)90080-2

Bischof, 2000, Paracrine and autocrine regulators of trophoblast invasion—a review, Placenta, 21, S55, 10.1053/plac.2000.0521

Lala, 1996, Growth factors, proteases and protease inhibitors in the maternal-fetal dialogue, Placenta, 17, 545, 10.1016/S0143-4004(96)80071-3

Khong, 1986, Inadequate maternal vascular response to placentation in pregnancies complicated by pre-eclampsia and by small-for-gestational age infants, Br J Obstet Gynaecol, 93, 1049, 10.1111/j.1471-0528.1986.tb07830.x

Zhou, 1997, 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, 99, 2152, 10.1172/JCI119388

Li, 2002, Current understandings of the molecular genetics of gestational trophoblastic diseases, Placenta, 23, 20, 10.1053/plac.2001.0744

Hui, 2005, Gestational trophoblastic diseases: recent advances in histopathologic diagnosis and related genetic aspects, Adv Anat Pathol, 12, 116, 10.1097/01.pap.0000163960.11107.73

Loregger, 2003, Regulatory transcription factors controlling function and differentiation of human trophoblast—a review, Placenta, 24, S104, 10.1053/plac.2002.0929

Cadigan, 1997, Wnt signaling: a common theme in animal development, Genes Dev, 11, 3286, 10.1101/gad.11.24.3286

Nusse, 1992, Wnt genes, Cell, 69, 1073, 10.1016/0092-8674(92)90630-U

He, 2004, LDL receptor-related proteins 5 and 6 in Wnt/beta-catenin signaling: arrows point the way, Development, 131, 1663, 10.1242/dev.01117

Wharton, 2003, Runnin' with the Dvl: proteins that associate with Dsh/Dvl and their significance to Wnt signal transduction, Dev Biol, 253, 1, 10.1006/dbio.2002.0869

Willert, 1998, Beta-catenin: a key mediator of Wnt signaling, Curr Opin Genet Dev, 8, 95, 10.1016/S0959-437X(98)80068-3

Polakis, 2000, Wnt signaling and cancer, Genes Dev, 14, 1837, 10.1101/gad.14.15.1837

Bienz, 2000, Linking colorectal cancer to Wnt signaling, Cell, 103, 311, 10.1016/S0092-8674(00)00122-7

Eastman, 1999, Regulation of LEF-1/TCF transcription factors by Wnt and other signals, Curr Opin Cell Biol, 11, 233, 10.1016/S0955-0674(99)80031-3

Tetsu, 1999, Beta-catenin regulates expression of cyclin D1 in colon carcinoma cells, Nature, 398, 422, 10.1038/18884

He, 1998, Identification of c-MYC as a target of the APC pathway, Science, 281, 1509, 10.1126/science.281.5382.1509

Brabletz, 1999, Beta-catenin regulates the expression of the matrix metalloproteinase-7 in human colorectal cancer, Am J Pathol, 155, 1033, 10.1016/S0002-9440(10)65204-2

Takahashi, 2002, Identification of membrane-type matrix metalloproteinase-1 as a target of the beta-catenin/Tcf4 complex in human colorectal cancers, Oncogene, 21, 5861, 10.1038/sj.onc.1205755

Hurlstone, 2002, T-cell factors: turn-ons and turn-offs, EMBO J, 21, 2303, 10.1093/emboj/21.10.2303

Barker, 2000, Catenins, Wnt signaling and cancer, Bioessays, 22, 961, 10.1002/1521-1878(200011)22:11<961::AID-BIES1>3.0.CO;2-T

Hovanes, 2001, Beta-catenin-sensitive isoforms of lymphoid enhancer factor-1 are selectively expressed in colon cancer, Nat Genet, 28, 53, 10.1038/ng0501-53

Parr, 2001, Wnt7b regulates placental development in mice, Dev Biol, 237, 324, 10.1006/dbio.2001.0373

Monkley, 1996, Targeted disruption of the Wnt2 gene results in placentation defects, Development, 122, 3343, 10.1242/dev.122.11.3343

Galceran, 1999, Wnt3a−/−-like phenotype and limb deficiency in Lef1(−/−)Tcf1(−/−) mice, Genes Dev, 13, 709, 10.1101/gad.13.6.709

Paria, 2001, Cellular and molecular responses of the uterus to embryo implantation can be elicited by locally applied growth factors, Proc Natl Acad Sci USA, 98, 1047, 10.1073/pnas.98.3.1047

Glinka, 1998, Dickkopf-1 is a member of a new family of secreted proteins and functions in head induction, Nature, 391, 357, 10.1038/34848

Kawano, 2003, Secreted antagonists of the Wnt signalling pathway, J Cell Sci, 116, 2627, 10.1242/jcs.00623

Tulac, 2003, Identification, characterization, and regulation of the canonical Wnt signaling pathway in human endometrium, J Clin Endocrinol Metab, 88, 3860, 10.1210/jc.2003-030494

Ikegawa, 1996, Isolation, characterization and chromosomal assignment of the human WNT7A gene, Cytogenet Cell Genet, 74, 149, 10.1159/000134404

Katoh, 2001, Frequent up-regulation of WNT2 in primary gastric cancer and colorectal cancer, Int J Oncol, 19, 1003

Katoh, 1996, Cloning, expression and chromosomal localization of Wnt-13, a novel member of the Wnt gene family, Oncogene, 13, 873

Saitoh, 2001, Molecular cloning and characterization of WNT3A and WNT14 clustered in human chromosome 1q42 region, Biochem Biophys Res Commun, 284, 1168, 10.1006/bbrc.2001.5105

Saitoh, 2002, Frequent up-regulation of WNT5A mRNA in primary gastric cancer, Int J Mol Med, 9, 515

Jun, 2003, p57kip2 is useful in the classification and differential diagnosis of complete and partial hydatidiform moles, Histopathology, 43, 17, 10.1046/j.1365-2559.2003.01667.x

Fukunaga, 2002, Immunohistochemical characterization of p57(KIP2) expression in early hydatidiform moles, Hum Pathol, 33, 1188, 10.1053/hupa.2002.129421

Knofler, 2002, Human hand1 basic helix-loop-helix (bHLH) protein: extra-embryonic expression pattern, interaction partners and identification of its transcriptional repressor domains, Biochem J, 361, 641, 10.1042/bj3610641

Pollheimer, 2004, Expression pattern of collagen XVIII and its cleavage product, the angiogenesis inhibitor endostatin, at the fetal-maternal interface, Placenta, 25, 770, 10.1016/j.placenta.2004.03.003

Choy, 1998, The phagocytic activity of human first trimester extravillous trophoblast, Hum Reprod, 13, 2941, 10.1093/humrep/13.10.2941

Genbacev, 1992, Villous culture of first trimester human placenta—model to study extravillous trophoblast (EVT) differentiation, Placenta, 13, 439, 10.1016/0143-4004(92)90051-T

Bauer, 2004, TNF inhibits trophoblast migration through elevation of PAI-1 in first trimester villous explant cultures, J Clin Endocrinol Metab, 89, 812, 10.1210/jc.2003-031351

Knofler, 2004, Transcriptional regulation of the human chorionic gonadotropin β gene during villous trophoblast differentiation, Endocrinology, 145, 1685, 10.1210/en.2003-0954

Kliman, 1986, Purification, characterization, and in vitro differentiation of cytotrophoblasts from human term placentae, Endocrinology, 118, 1567, 10.1210/endo-118-4-1567

Fisher, 1989, Adhesive and degradative properties of human placental cytotrophoblast cells in vitro, J Cell Biol, 109, 891, 10.1083/jcb.109.2.891

Blaschitz, 2000, Antibody reaction patterns in first trimester placenta: implications for trophoblast isolation and purity screening, Placenta, 21, 733, 10.1053/plac.2000.0559

Knofler, 2000, TNF-alpha/TNFRI in primary and immortalized first trimester cytotrophoblasts, Placenta, 21, 525, 10.1053/plac.1999.0501

Van de Wetering, 1996, Extensive alternative splicing and dual promoter usage generate Tcf-1 protein isoforms with differential transcription control properties, Mol Cell Biol, 16, 745, 10.1128/MCB.16.3.745

Eustice, 1991, A sensitive method for the detection of beta-galactosidase in transfected mammalian cells, Biotechniques, 11, 733

Korinek, 1997, Constitutive transcriptional activation by a beta-catenin-Tcf complex in APC−/− colon carcinoma, Science, 275, 1784, 10.1126/science.275.5307.1784

Barker, 1999, Restricted high level expression of Tcf-4 protein in intestinal and mammary gland epithelium, Am J Pathol, 154, 29, 10.1016/S0002-9440(10)65247-9

Klein, 1996, A molecular mechanism for the effect of lithium on development, Proc Natl Acad Sci USA, 93, 8455, 10.1073/pnas.93.16.8455

Saegusa, 2005, Upregulation of TCF4 expression as a transcriptional target of beta-catenin/p300 complexes during trans-differentiation of endometrial carcinoma cells, Lab Invest, 85, 768, 10.1038/labinvest.3700273

Yun, 2005, Both ERK and Wnt/beta-catenin pathways are involved in Wnt3a-induced proliferation, J Cell Sci, 118, 313, 10.1242/jcs.01601

Pollheimer, 2005, Signalling pathways regulating the invasive differentiation of human trophoblasts: a review, Placenta, 26, S21, 10.1016/j.placenta.2004.11.013

Cross, 2003, Genes, development and evolution of the placenta, Placenta, 24, 123, 10.1053/plac.2002.0887

Cross, 2002, Transcription factors underlying the development and endocrine functions of the placenta, Recent Prog Horm Res, 57, 221, 10.1210/rp.57.1.221

Meinhardt, 2005, Tissue-specific and ubiquitous basic helix-loop-helix transcription factors in human placental trophoblasts, Placenta, 26, 527, 10.1016/j.placenta.2004.09.005

Gotzmann, 2004, Molecular aspects of epithelial cell plasticity: implications for local tumor invasion and metastasis, Mutat Res, 566, 9, 10.1016/S1383-5742(03)00033-4

Kang, 2004, Epithelial-mesenchymal transitions: twist in development and metastasis, Cell, 118, 277, 10.1016/j.cell.2004.07.011

Haigh, 1999, Studies of mesenchymal cells from 1st trimester human placenta: expression of cytokeratin outside the trophoblast lineage, Placenta, 20, 615, 10.1053/plac.1999.0441

Floridon, 2000, Localization of E-cadherin in villous, extravillous and vascular trophoblasts during intrauterine, ectopic and molar pregnancy, Mol Hum Reprod, 6, 943, 10.1093/molehr/6.10.943

Zhou, 2005, Wnt, Hedgehog and Snail: sister pathways that control by GSK-3beta and beta-Trcp in the regulation of metastasis, Cell Cycle, 4, 772, 10.4161/cc.4.6.1744

Nusse, 2005, Wnt signaling in disease and in development, Cell Res, 15, 28, 10.1038/sj.cr.7290260

Eger, 2004, Beta-catenin and TGFbeta signalling cooperate to maintain a mesenchymal phenotype after FosER-induced epithelial to mesenchymal transition, Oncogene, 23, 2672, 10.1038/sj.onc.1207416

Morali, 2001, IGF-II induces rapid beta-catenin relocation to the nucleus during epithelium to mesenchyme transition, Oncogene, 20, 4942, 10.1038/sj.onc.1204660

Li, 2003, Expression of e-cadherin and beta-catenin in trophoblastic tissue in normal and pathological pregnancies, Int J Gynecol Pathol, 22, 63, 10.1097/00004347-200301000-00013

Getsios, 2000, Regulation of beta-catenin mRNA and protein levels in human villous cytotrophoblasts undergoing aggregation and fusion in vitro: correlation with E-cadherin expression, J Reprod Fertil, 119, 59, 10.1530/jrf.0.1190059

Eberhart, 2001, Wnt signaling in human development: beta-catenin nuclear translocation in fetal lung, kidney, placenta, capillaries, adrenal, and cartilage, Pediatr Dev Pathol, 4, 351, 10.1007/s10024001-0037-y

Jope, 2004, The glamour and gloom of glycogen synthase kinase-3, Trends Biochem Sci, 29, 95, 10.1016/j.tibs.2003.12.004

Vettraino, 1996, Collagenase-I, stromelysin-I, and matrilysin are expressed within the placenta during multiple stages of human pregnancy, Placenta, 17, 557, 10.1016/S0143-4004(96)80072-5

Bjorn, 1997, Co-ordinated expression of MMP-2 and its putative activator, MT1-MMP, in human placentation, Mol Hum Reprod, 3, 713, 10.1093/molehr/3.8.713

Aihara, 2005, Clinical significance of mucin phenotype, beta-catenin and matrix metalloproteinase 7 in early undifferentiated gastric carcinoma, Br J Surg, 92, 454, 10.1002/bjs.4868

Gamallo, 1999, Beta-catenin expression pattern in stage I and II ovarian carcinomas: relationship with beta-catenin gene mutations, clinicopathological features, and clinical outcome, Am J Pathol, 155, 527, 10.1016/S0002-9440(10)65148-6

Wong, 2003, Nuclear beta catenin as a potential prognostic and diagnostic marker in patients with colorectal cancer from Hong Kong, Mol Pathol, 56, 347, 10.1136/mp.56.6.347

Morin, 1997, Activation of beta-catenin-Tcf signaling in colon cancer by mutations in beta-catenin or APC, Science, 275, 1787, 10.1126/science.275.5307.1787

Cross, 1995, Inhibition of glycogen synthase kinase-3 by insulin mediated by protein kinase B, Nature, 378, 785, 10.1038/378785a0

Eldar-Finkelman, 1995, Inactivation of glycogen synthase kinase-3 by epidermal growth factor is mediated by mitogen-activated protein kinase/p90 ribosomal protein S6 kinase signaling pathway in NIH/3T3 cells, J Biol Chem, 270, 987, 10.1074/jbc.270.3.987

Novak, 1998, Cell adhesion and the integrin-linked kinase regulate the LEF-1 and beta-catenin signaling pathways, Proc Natl Acad Sci USA, 95, 4374, 10.1073/pnas.95.8.4374

Kato, 2002, Growth-associated gene expression profiles by microarray analysis of trophoblast of molar pregnancies and normal villi, Int J Gynecol Pathol, 21, 255, 10.1097/00004347-200207000-00008

Nakano, 2005, The cytoplasmic expression of E-cadherin and beta-catenin in bovine trophoblasts during binucleate cell differentiation, Placenta, 26, 393, 10.1016/j.placenta.2004.08.002

Zybina, 2002, Genome multiplication of extravillous trophoblast cells in human placenta in the course of differentiation and invasion into endometrium and myometrium. I. Dynamics of polyploidization, Tsitologiia, 44, 1058

Weier, 2005, Human cytotrophoblasts acquire aneuploidies as they differentiate to an invasive phenotype, Dev Biol, 279, 420, 10.1016/j.ydbio.2004.12.035