What Is Trophoblast? A Combination of Criteria Define Human First-Trimester Trophoblast

Stem Cell Reports

Volumn 6, Issue 2, 2016, Pages 257-272

  Lee, Cheryl Q E ^a,b   Gardner, Lucy ^a   Turco, Margherita ^a   Zhao, Nancy ^a   Murray, Matthew J ^a   Coleman, Nicholas ^a   Rossant, Janet ^b,c   Hemberger, Myriam ^a,d   Moffett, Ashley ^a  

^a UNIVERSITY OF CAMBRIDGE   (United Kingdom)

^b HOSPITAL FOR SICK CHILDREN   (Canada)

^c UNIVERSITY OF TORONTO   (Canada)

^d BABRAHAM INSTITUTE   (United Kingdom)

Author keywords

[No Author keywords available]

Indexed keywords

BONE MORPHOGENETIC PROTEIN; HLA ANTIGEN CLASS 1; MICRORNA; TRANSCRIPTION FACTOR GATA 3; 1 TERT BUTYL 3 [6 (3,5 DIMETHOXYPHENYL) 2 (4 DIETHYLAMINOBUTYLAMINO)PYRIDO[2,3 D]PYRIMIDIN 7 YL]UREA; BIOLOGICAL MARKER; ELF5 PROTEIN, HUMAN; FIBROBLAST GROWTH FACTOR; PYRIMIDINE DERIVATIVE; TRANSCRIPTION FACTOR ETS;

ARTICLE; CHROMOSOME 19; CONSENSUS; DNA METHYLATION; EMBRYO; EMBRYONAL CARCINOMA CELL LINE; FIRST TRIMESTER PREGNANCY; GENE EXPRESSION; HUMAN; HUMAN CELL; PHENOTYPE; PLACENTA; PRIORITY JOURNAL; PROMOTER REGION; TROPHOBLAST; CELL CULTURE; CYTOLOGY; DRUG EFFECTS; FEMALE; GENETICS; HUMAN EMBRYONIC STEM CELL; METABOLISM; NOMENCLATURE; PREGNANCY;

BIOMARKERS; CELLS, CULTURED; CHROMOSOMES, HUMAN, PAIR 19; DNA METHYLATION; FEMALE; FIBROBLAST GROWTH FACTORS; HISTOCOMPATIBILITY ANTIGENS CLASS I; HUMAN EMBRYONIC STEM CELLS; HUMANS; MICRORNAS; PREGNANCY; PREGNANCY TRIMESTER, FIRST; PROMOTER REGIONS, GENETIC; PROTO-ONCOGENE PROTEINS C-ETS; PYRIMIDINES; TERMINOLOGY AS TOPIC; TROPHOBLASTS;

EID: 84957799858     PISSN: 22136711     EISSN: None     Source Type: Journal    
DOI: 10.1016/j.stemcr.2016.01.006     Document Type: Article

References (81)

1. R.S. Al-Lamki, J.N. Skepper, and G.J. Burton Are human placental bed giant cells merely aggregates of small mononuclear trophoblast cells? An ultrastructural and immunocytochemical study Hum. Reprod. 14 1999 496 504
2. M. Amita, K. Adachi, A.P. Alexenko, S. Sinha, D.J. Schust, and L.C. Schulz Complete and unidirectional conversion of human embryonic stem cells to trophoblast by BMP4 Proc. Natl. Acad. Sci. USA 110 2013 E1212 E1221
3. D.J. Anderson, P. Narayan, and W.C. DeWolf Major histocompatibility antigens are not detectable on post-meiotic human testicular germ cells J. Immunol. 133 1984 1962 1965
4. R. Apps, L. Gardner, and A. Moffett A critical look at HLA-G Trends Immunol. 29 2008 313 321
5. R. Apps, S.P. Murphy, R. Fernando, L. Gardner, T. Ahad, and A. Moffett Human leucocyte antigen (HLA) expression of primary trophoblast cells and placental cell lines, determined using single antigen beads to characterize allotype specificities of anti-HLA antibodies Immunology 127 2009 26 39
6. R. Apps, A. Sharkey, L. Gardner, V. Male, M. Trotter, N. Miller, R. North, S. Founds, and A. Moffett Genome-wide expression profile of first trimester villous and extravillous human trophoblast cells Placenta 32 2011 33 43
7. M. Bar, S.K. Wyman, B.R. Fritz, J. Qi, K.S. Garg, R.K. Parkin, E.M. Kroh, A. Bendoraite, P.S. Mitchell, A.M. Nelson, and et al. MicroRNA discovery and profiling in human embryonic stem cells by deep sequencing of small RNA libraries Stem Cells 26 2008 2496 2505
8. T. Beck, G. Schweikhart, and E. Stolz Immunohistochemical location of HPL, SP1 and β-HCG in normal placentas of varying gestational age Arch. Gynecol. 239 1986 63 74
9. I. Bentwich, A. Avniel, Y. Karov, R. Aharonov, S. Gilad, O. Barad, A. Barzilai, P. Einat, U. Einav, E. Meiri, and et al. Identification of hundreds of conserved and nonconserved human microRNAs Nat. Genet. 37 2005 766 770
10. A.S. Bernardo, T. Faial, L. Gardner, K.K. Niakan, D. Ortmann, C.E. Senner, E.M. Callery, M.W. Trotter, M. Hemberger, J.C. Smith, and et al. BRACHYURY and CDX2 mediate BMP-induced differentiation of human and mouse pluripotent stem cells into embryonic and extraembryonic lineages Cell Stem Cell 9 2011 144 155
11. K. Biadasiewicz, S. Sonderegger, P. Haslinger, S. Haider, L. Saleh, C. Fiala, J. Pollheimer, and M. Knöfler Transcription factor AP-2α promotes EGF-dependent invasion of human trophoblast Endocrinology 152 2011 1458 1469
12. A. Blaschitz, U. Weiss, G. Dohr, and G. Desoye Antibody reaction patterns in first trimester placenta: implications for trophoblast isolation and purity screening Placenta 21 2000 733 741
13. M.-L. Bortolin-Cavaillé, M. Dance, M. Weber, and J. Cavaillé C19MC microRNAs are processed from introns of large Pol-II, non-protein-coding transcripts Nucleic Acids Res. 37 2009 3464 3473
14. F.M. Brodsky, P. Parham, C.J. Barnstable, M.J. Crumpton, and W.F. Bodmer Monoclonal antibodies for analysis of the HLA system Immunol. Rev. 47 1979 3 61
15. F. Cambuli, A. Murray, W. Dean, D. Dudzinska, F. Krueger, S. Andrews, C.E. Senner, S.J. Cook, and M. Hemberger Epigenetic memory of the first cell fate decision prevents complete ES cell reprogramming into trophoblast Nat. Commun. 5 2014 5538
16. H. Cao, C. Yang, and T.M. Rana Evolutionary emergence of microRNAs in human embryonic stem cells PLoS One 3 2008 e2820
17. C. Chen, D.A. Ridzon, A.J. Broomer, Z. Zhou, D.H. Lee, J.T. Nguyen, M. Barbisin, N.L. Xu, V.R. Mahuvakar, M.R. Andersen, and et al. Real-time quantification of microRNAs by stem-loop RT-PCR Nucleic Acids Res. 33 2005 e179
18. Y. Chen, K. Wang, Y.G. Gong, S.K. Khoo, and R. Leach Roles of CDX2 and EOMES in human induced trophoblast progenitor cells Biochem. Biophys. Res. Commun. 431 2013 197 202
19. Y. Chen, K. Wang, G.V.R. Chandramouli, J.G. Knott, and R. Leach Trophoblast lineage cells derived from human induced pluripotent stem cells Biochem. Biophys. Res. Commun. 436 2013 677 684
20. L.A. Cole Hyperglycosylated hCG, a review Placenta 31 2010 653 664
21. L.A. Cole hCG, the wonder of today's science Reprod. Biol. Endocrinol. 10 2012 24
22. Z. Czimmerer, J. Hulvely, Z. Simandi, E. Varallyay, Z. Havelda, E. Szabo, A. Varga, B. Dezso, M. Balogh, A. Horvath, and et al. A versatile method to design stem-loop primer-based quantitative PCR assays for detecting small regulatory RNA molecules PLoS One 8 2013 e55168
23. I. Damjanov, and P.W. Andrews Ultrastructural differentiation of a clonal human embryonal carcinoma cell line in vitro Cancer Res. 43 1983 2190 2198
24. A.M. Deaton, and A. Bird CpG islands and the regulation of transcription Genes Dev. 25 2011 1010 1022
25. R. Donker, J. Mouillet, T. Chu, C. Hubel, D. Stolz, A. Morelli, and Y. Sadovsky The expression profile of C19MC microRNAs in primary human trophoblast cells and exosomes MHR Basic Sci. Reprod. Med. 18 2012 417 424
26. M. Donnison, A. Beaton, H.W. Davey, R. Broadhurst, P. L'Huillier, and P.L. Pfeffer Loss of the extraembryonic ectoderm in Elf5 mutants leads to defects in embryonic patterning Development 132 2005 2299 2308
27. R.J. Duquesnoy, M. Marrari, L. Jelenik, A. Zeevi, F.H.J. Claas, and A. Mulder Structural aspects of HLA class I epitopes reacting with human monoclonal antibodies in Ig-binding, C1q-binding and lymphocytotoxicity assays Hum. Immunol. 74 2013 1271 1279
28. K.A. Fleming, A. McMichael, J.A. Morton, J. Woods, and J.O. McGee Distribution of HLA class 1 antigens in normal human tissue and in mammary cancer J. Clin. Pathol. 34 1981 779 784
29. O. Genbacev, M. Donne, M. Kapidzic, M. Gormley, J. Lamb, J. Gilmore, N. Larocque, G. Goldfien, T. Zdravkovic, M.T. McMaster, and et al. Establishment of human trophoblast progenitor cell lines from the chorion Stem Cells 29 2011 1427 1436
30. Y. Hariyama, A. Itakura, M. Okamura, M. Ito, Y. Murata, T. Nagasaka, H. Nakazato, and S. Mizutani Placental aminopeptidase A as a possible barrier of angiotensin II between mother and fetus Placenta 21 2000 621 627
31. R. Harun, L. Ruban, M. Matin, J. Draper, N.M. Jenkins, G.C. Liew, P.W. Andrews, T.C. Li, S.M. Laird, and H.D.M. Moore Cytotrophoblast stem cell lines derived from human embryonic stem cells and their capacity to mimic invasive implantation events Hum. Reprod. 21 2006 1349 1358
32. M. Hemberger, R. Udayashankar, P. Tesar, H. Moore, and G.J. Burton ELF5-enforced transcriptional networks define an epigenetically regulated trophoblast stem cell compartment in the human placenta Hum. Mol. Genet. 19 2010 2456 2467
33. U. Hiden, C. Wadsack, N. Prutsch, M. Gauster, U. Weiss, H.-G. Frank, U. Schmitz, C. Fast-Hirsch, M. Hengstschläger, A. Pötgens, and et al. The first trimester human trophoblast cell line ACH-3P: a novel tool to study autocrine/paracrine regulatory loops of human trophoblast subpopulations - TNF-alpha stimulates MMP15 expression BMC Dev. Biol. 7 2007 137 150
34. C.E. Hoei-Hansen, J.E. Nielsen, K. Almstrup, S.B. Sonne, N. Graem, N.E. Skakkebaek, H. Leffers, and E.R.-D. Meyts Transcription factor AP-2gamma is a developmentally regulated marker of testicular carcinoma in situ and germ cell tumors Clin. Cancer Res. 10 2004 8521 8530
35. K. Ino, F. Kikkawa, T. Suzuki, H. Kajiyama, K. Shibata, S. Nomura, A. Itakura, M. Ito, T. Nagasaka, A. Hattori, and et al. Expression of placental leucine aminopeptidase and adipocyte-derived leucine aminopeptidase in human normal and malignant invasive trophoblastic cells Lab. Investig. 83 2003 1799 1809
36. N. Ito, S. Nomura, A. Iwase, T. Ito, K. Ino, T. Nagasaka, M. Tsujimoto, M. Kobayashi, and S. Mizutani Ultrastructural localization of aminopeptidase A/angiotensinase and placental leucine aminopeptidase/oxytocinase in chorionic villi of human placenta Early Hum. Dev. 71 2003 29 37
37. R. Jalleh, J. Gilbertson, R. Williamson, S. Slater, and C. Foster Expression of major histocompatibility antigens in human chronic pancreatitis Gut 34 1993 1452 1457
38. J.L. James, P.R. Stone, and L.W. Chamley The isolation and characterization of a population of extravillous trophoblast progenitors from first trimester human placenta Hum. Reprod. 22 2007 2111 2119
39. R. Josephson, C.J. Ording, Y. Liu, S. Shin, U. Lakshmipathy, A. Toumadje, B. Love, J.D. Chesnut, P.W. Andrews, M.S. Rao, and et al. Qualification of embryonal carcinoma 2102Ep as a reference for human embryonic stem cell research Stem Cells 25 2007 437 446
40. A. King, L. Thomas, and P. Bischof Cell culture models of trophoblast II: trophoblast cell lines - a workshop report Placenta 21 2000 S113 S119
41. G. Koene, A. Mulder, K. van der Ven, C. Eijsink, M. Franke, P. Slootweg, F. Claas, and M. Tilanus Human monoclonal antibodies as a tool for the detection of HLA class I allele-specific expression loss in head-and-neck squamous cell carcinoma and corresponding lymph node metastases Hum. Immunol. 67 2006 692 699
42. P. Kuckenberg, S. Buhl, T. Woynecki, B. van Fürden, E. Tolkunova, F. Seiffe, M. Moser, A. Tomilin, E. Winterhager, and H. Schorle The transcription factor TCFAP2C/AP-2gamma cooperates with CDX2 to maintain trophectoderm formation Mol. Cell. Biol. 30 2010 3310 3320
43. P. Kuckenberg, C. Kubaczka, and H. Schorle The role of transcription factor Tcfap2c/TFAP2C in trophectoderm development Reprod. Biomed. Online 25 2012 12 20
44. L.A. Lampson, and W.F. Hickey Monoclonal antibody analysis of MHC expression in human brain biopsies: tissue ranging from "histologically normal" to that showing different levels of glial tumor involvement J. Immunol. 136 1986 4054 4062
45. L.C. Laurent, J. Chen, I. Ulitsky, F.-J. Mueller, C. Lu, R. Shamir, J.-B. Fan, and J.F. Loring Comprehensive microRNA profiling reveals a unique human embryonic stem cell signature dominated by a single seed sequence Stem Cells 26 2008 1506 1516
46. M.J. Lee, A.P. Vogt, W. Hsiao, and A.O. Osunkoya CDX-2 expression in malignant germ cell tumors of the testes, intratubular germ cell neoplasia, and normal seminiferous tubules Tumour Biol. 33 2012 2185 2188
47. S.S.-L. Li, S.-L. Yu, L.-P. Kao, Z.Y. Tsai, S. Singh, B.Z. Chen, B.-C. Ho, Y.-H. Liu, and P.-C. Yang Target identification of microRNAs expressed highly in human embryonic stem cells J. Cell. Biochem. 106 2009 1020 1030
48. V. Male, A. Trundley, L. Gardner, J. Northfield, C. Chang, R. Apps, and A. Moffett Natural killer cells in human pregnancy K.S. Campbell, Natural Killer Cell Protocols, Methods in Molecular Biology 2010 Humana Press 447 463
49. M. Marchand, J.A. Horcajadas, F.J. Esteban, S.L. McElroy, S.J. Fisher, and L.C. Giudice Transcriptomic signature of trophoblast differentiation in a human embryonic stem cell model Biol. Reprod. 84 2011 1258 1271
50. D.M. Morales-Prieto, W. Chaiwangyen, S. Ospina-Prieto, U. Schneider, J. Herrmann, B. Gruhn, and U.R. Markert MicroRNA expression profiles of trophoblastic cells Placenta 33 2012 725 734
51. J. Muhlhauser, C. Crescimanno, M. Kasper, D. Zaccheo, and M. Castellucci Differentiation of human trophoblast populations involves alterations in cytokeratin patterns J. Histochem. Cytochem. 43 1995 579 589
52. T. Nagamatsu, T. Fujii, T. Ishikawa, T. Kanai, H. Hyodo, T. Yamashita, Y. Osuga, M. Momoeda, S. Kozuma, and Y. Taketani A primary cell culture system for human cytotrophoblasts of proximal cytotrophoblast cell columns enabling in vitro acquisition of the extra-villous phenotype Placenta 25 2004 153 165
53. R.K. Ng, W. Dean, C. Dawson, D. Lucifero, Z. Madeja, W. Reik, and M. Hemberger Epigenetic restriction of embryonic cell lineage fate by methylation of Elf5 Nat. Cell Biol. 10 2008 1280 1290
54. NIH (2009). HLA Typing. In Stem Cell Information, http://stemcells.nih.gov/research/nihresearch/scunit/Pages/hla.aspx.
55. M. Noguer-Dance, S. Abu-Amero, M. Al-Khtib, A. Lefèvre, P. Coullin, G.E. Moore, and J. Cavaillé The primate-specific microRNA gene cluster (C19MC) is imprinted in the placenta Hum. Mol. Genet. 19 2010 3566 3582
56. B. Novakovic, L. Gordon, N.C. Wong, A. Moffett, U. Manuelpillai, J.M. Craig, A. Sharkey, and R. Saffery Wide-ranging DNA methylation differences of primary trophoblast cell populations and derived cell lines: implications and opportunities for understanding trophoblast function Mol. Hum. Reprod. 17 2011 344 353
57. G.W. Novotny, K. Belling, J.B. Bramsen, J.E. Nielsen, J. Bork-Jensen, K. Almstrup, S.B. Sonne, J. Kjems, E. Rajpert-De Meyts, and H. Leffers MicroRNA expression profiling of carcinoma in situ (CIS) cells of the testis Endocr. Relat. Cancer 19 2012 365 379
58. H. Omi, A. Okamoto, T. Nikaido, M. Urashima, R. Kawaguchi, N. Umehara, K. Sugiura, M. Saito, T. Kiyono, and T. Tanaka Establishment of an immortalized human extravillous trophoblast cell line by retroviral infection of E6/E7/hTERT and its transcriptional profile during hypoxia and reoxygenation Int. J. Mol. Med. 23 2009 229 236
59. R.D. Palmer, M.J. Murray, H.K. Saini, S. van Dongen, C. Abreu-Goodger, B. Muralidhar, M.R. Pett, C.M. Thornton, J.C. Nicholson, A.J. Enright, and et al. Malignant germ cell tumors display common microRNA profiles resulting in global changes in expression of messenger RNA targets Cancer Res. 70 2010 2911 2923
60. P. Parham, and F.M. Brodsky Partial purification and some properties of BB7.2 a cytotoxic monoclonal antibody with specificity for HLA-A2 and a variant of HLA-A28 Hum. Immunol. 3 1981 277 299
61. H.J. Peltier, and G.J. Latham Normalization of microRNA expression levels in quantitative RT-PCR assays: identification of suitable reference RNA targets in normal and cancerous human solid tissues RNA 14 2008 844 852
62. S. Przyborski, V.B. Christie, M.W. Hayman, R. Stewart, and G.M. Horrocks Human embryonal carcinoma stem cells: models of embryonic development in humans Stem Cells Dev. 13 2004 400 408
63. F. Ramaekers, A. Huysmans, G. Schaart, O. Moesker, and P. Vooijs Tissue distribution of keratin 7 as monitored by a monoclonal antibody Exp. Cell Res. 170 1987 235 249
64. J. Ren, P. Jin, E. Wang, F.M. Marincola, and D.F. Stroncek MicroRNA and gene expression patterns in the differentiation of human embryonic stem cells J. Transl. Med. 7 2009 20
65. R.M. Roberts, K.M. Loh, M. Amita, A.S. Bernardo, K. Adachi, A.P. Alexenko, D.J. Schust, L.C. Schulz, B.P.V.L. Telugu, T. Ezashi, and et al. Differentiation of trophoblast cells from human embryonic stem cells: to be or not to be? Reproduction 147 2014 D1 D12
66. J. Rossant Stem cells from the mammalian blastocyst Stem Cells 19 2001 477 482
67. P. Sarkar, S.M. Randall, S. Timothy, A. Nero, T.A. Russell, C. Muddiman, and B.M. Rao Activin/Nodal signaling switches the terminal fate of human embryonic stem cell-derived trophoblasts J. Biol. Chem. 290 2015 8834 8848
68. M. Schumm, T. Feuchtinger, M. Pfeiffer, W. Hoelle, W. Bethge, M. Ebinger, S. Kuci, R. Handgretinger, and P. Lang Flow cytometry with anti HLA-antibodies: a simple but highly sensitive method for monitoring chimerism and minimal residual disease after HLA-mismatched stem cell transplantation Bone Marrow Transpl. 39 2007 767 773
69. C.E. Senner, and M. Hemberger Regulation of early trophoblast differentiation - lessons from the mouse Placenta 31 2010 944 950
70. G.C.S. Smith First-trimester determination of complications of late pregnancy J. Am. Med. Assoc. 303 2010 561 562
71. S.L. Straszewski-Chavez, V.M. Abrahams, A.B. Alvero, B.A. Paulomi, Y. Ma, S. Guller, R. Romero, and G. Mor The isolation and characterization of a novel telomerase immortalized first trimester trophoblast cell line, Swan 71 Placenta 30 2009 939 948
72. T. Takao, K. Asanoma, K. Kato, K. Fukushima, R. Tsunematsu, T. Hirakawa, S. Matsumura, H. Seki, S. Takeda, and N. Wake Isolation and characterization of human trophoblast side-population (SP) cells in primary villous cytotrophoblasts and HTR-8/SVneo cell line PLoS One 6 2011 e21990
73. M. Takayama, K. Isaka, Y. Suzuki, H. Funayama, K. Akiya, and H. Bohn Comparative study of placental protein 19, human chorionic gonadotrophin and pregnancy-specific beta 1-glycoprotein as immunohistochemical markers for extravillous trophoblast in pregnancy and trophoblastic disease Histochemistry 93 1989 167 173
74. B.P. Telugu, K. Adachi, J.M. Schlitt, T. Ezashi, D.J. Schust, R.M. Roberts, and L.C. Schulz Comparison of extravillous trophoblast cells derived from human embryonic stem cells and from first trimester human placentas Placenta 34 2013 1 8
75. R. Udayashankar, D. Baker, E. Tuckerman, S. Laird, T.C. Li, and H.D. Moore Characterization of invasive trophoblasts generated from human embryonic stem cells Hum. Reprod. 26 2011 398 406
76. Y. Wang, W. Qiu, H. Feng, Y. Li, L. Zhuang, Z. Wang, Y. Liu, J. Zhou, D. Zhang, and G.S.W. Tsao Immortalization of normal human cytotrophoblast cells by reconstitution of telomeric reverse transcriptase activity Mol. Hum. Reprod. 12 2006 451 460
77. X. Wei, and H.T. Orr Differential expression of HLA-E, HLA-F, and HLA-G transcripts in human tissue Hum. Immunol. 29 1990 131 142
78. R.-H. Xu, X. Chen, D.S. Li, R. Li, G.C. Addicks, C. Glennon, T.P. Zwaka, and J.A. Thomson BMP4 initiates human embryonic stem cell differentiation to trophoblast Nat. Biotechnol. 20 2002 1261 1264
79. N. Yamahara, S. Nomura, T. Suzuki, A. Itakura, M. Ito, T. Okamoto, M. Tsujimoto, H. Nakazato, and S. Mizutani Placental leucine aminopeptidase/oxytocinase in maternal serum and placenta during normal pregnancy Life Sci. 66 2000 1401 1410
80. L. Zhang, W. Zhang, C. Shao, J. Zhang, K. Men, Z. Shao, Y. Yan, and D. Xu Establishment and characterization of a spontaneously immortalized trophoblast cell line (HPT-8) and its hepatitis B virus-expressing clone Hum. Reprod. 26 2011 2146 2156
81. G.Q. Zhou, V. Baranov, W. Zimmermann, F. Grunert, B. Erhard, L. Mincheva-Nilsson, S. Hammarström, and J. Thompson Highly specific monoclonal antibody demonstrates that pregnancy-specific glycoprotein (PSG) is limited to syncytiotrophoblast in human early and term placenta Placenta 18 1997 491 501