CDX2 regulates multiple trophoblast genes in bovine trophectoderm CT-1 cells

Molecular Reproduction and Development

Volumn 80, Issue 10, 2013, Pages 826-839

  Schiffmacher, Andrew T ^a   Keefer, Carol L ^a  

^a UNIVERSITY OF MARYLAND   (United States)

Author keywords

[No Author keywords available]

Indexed keywords

INHIBITOR OF DIFFERENTIATION 2; NUCLEIC ACID BINDING PROTEIN; OCTAMER TRANSCRIPTION FACTOR 4; PROTEIN ERRB; SMALL INTERFERING RNA; TAU INTERFERON; TRANSCRIPTION FACTOR; TRANSCRIPTION FACTOR ASCL2; TRANSCRIPTION FACTOR CDX2; TRANSCRIPTION FACTOR ELF5; TRANSCRIPTION FACTOR ETS 2; TRANSCRIPTION FACTOR HAND1; TRANSCRIPTION FACTOR SOX15; UNCLASSIFIED DRUG;

AMINO ACID SEQUENCE; ANIMAL CELL; ARTICLE; CELL NUCLEUS; CELL PROLIFERATION; CELL STRUCTURE; COW; CYTOPLASM; GENE REGULATORY NETWORK; NONHUMAN; NUCLEOTIDE SEQUENCE; PLURIPOTENT STEM CELL; PRIORITY JOURNAL; PROTEIN EXPRESSION; PROTEIN FUNCTION; PROTEIN LOCALIZATION; TRANSCRIPTION REGULATION; TROPHECTODERM; TROPHOBLAST;

BOVINAE;

ANIMALS; CATTLE; CELL DIFFERENTIATION; CELL LINE; DOXYCYCLINE; ECTODERM; GENE EXPRESSION REGULATION, DEVELOPMENTAL; GENE REGULATORY NETWORKS; HEK293 CELLS; HUMANS; MICE; MODELS, GENETIC; OCTAMER TRANSCRIPTION FACTOR-3; RNA INTERFERENCE; RNA, MESSENGER; RNA, SMALL INTERFERING; TRANSCRIPTION FACTORS; TRANSCRIPTION, GENETIC; TRANSCRIPTIONAL ACTIVATION; TROPHOBLASTS;

EID: 84885838667     PISSN: 1040452X     EISSN: 10982795     Source Type: Journal    
DOI: 10.1002/mrd.22212     Document Type: Article

References (59)

1. Arnold DR, Bordignon V, Lefebvre R, Murphy BD, Smith LC. 2006. Somatic cell nuclear transfer alters peri-implantation trophoblast differentiation in bovine embryos. Reproduction 132:279-290.
2. Bai H, Sakurai T, Kim MS, Muroi Y, Ideta A, Aoyagi Y, Nakajima H, Takahashi M, Nagaoka K, Imakawa K. 2009. Involvement of GATA transcription factors in the regulation of endogenous bovine interferon-tau gene transcription. Mol Reprod Dev 76:1143-1152.
3. Bai H, Sakurai T, Someya Y, Konno T, Ideta A, Aoyagi Y, Imakawa K. 2011. Regulation of trophoblast-specific factors by GATA2 and GATA3 in bovine trophoblast CT-1 cells. J Reprod Dev 57:518-525.
4. Berg DK, Smith CS, Pearton DJ, Wells DN, Broadhurst R, Donnison M, Pfeffer PL. 2011. Trophectoderm lineage determination in cattle. Dev Cell 20:244-255.
5. Betteridge K, Fléchon J. 1988. The anatomy and physiology of pre-attachment bovine embryos. Theriogenology 29:155-187.
6. Cauffman G, Liebaers I, Van Steirteghem A, Van de Velde H. 2006. POU5F1 isoforms show different expression patterns in human embryonic stem cells and preimplantation embryos. Stem Cells 24:2685-2691.
7. Chen L, Yabuuchi A, Eminli S, Takeuchi A, Lu CW, Hochedlinger K, Daley GQ. 2009. Cross-regulation of the Nanog and Cdx2 promoters. Cell Res 19:1052-1061.
8. Cooke FN, Pennington KA, Yang Q, Ealy AD. 2009. Several fibroblast growth factors are expressed during pre-attachment bovine conceptus development and regulate interferon-tau expression from trophectoderm. Reproduction 137:259-269.
9. Degrelle SA, Campion E, Cabau C, Piumi F, Reinaud P, Richard C, Renard JP, Hue I. 2005. Molecular evidence for a critical period in mural trophoblast development in bovine blastocysts. Dev Biol 288:448-460.
10. Dietrich JE, Hiiragi T. 2007. Stochastic patterning in the mouse pre-implantation embryo. Development 134:4219-4231.
11. Donnison M, Beaton A, Davey HW, Broadhurst R, L'Huillier P, Pfeffer PL. 2005. Loss of the extraembryonic ectoderm in Elf5 mutants leads to defects in embryonic patterning. Development 132:2299-2308.
12. Douglas GC, VandeVoort CA, Kumar P, Chang TC, Golos TG. 2009. Trophoblast stem cells: Models for investigating trophectoderm differentiation and placental development. Endocr Rev 30:228-240.
13. Ezashi T, Das P, Gupta R, Walker A, Roberts RM. 2008. The role of homeobox protein distal-less 3 and its interaction with ETS2 in regulating bovine interferon-tau gene expression-synergistic transcriptional activation with ETS2. Biol Reprod 79:115-124.
14. Garbayo JM, Serrano B, Lopez-Gatius F. 2008. Identification of novel pregnancy-associated glycoproteins (PAG) expressed by the peri-implantation conceptus of domestic ruminants. Anim Reprod Sci 103:120-134.
15. Green JA, Xie S, Quan X, Bao B, Gan X, Mathialagan N, Beckers JF, Roberts RM. 2000. Pregnancy-associated bovine and ovine glycoproteins exhibit spatially and temporally distinct expression patterns during pregnancy. Biol Reprod 62:1624-1631.
16. Hall VJ, Ruddock NT, French AJ. 2005. Expression profiling of genes crucial for placental and preimplantation development in bovine in vivo, in vitro, and nuclear transfer blastocysts. Mol Reprod Dev 72:16-24.
17. Hay DC, Sutherland L, Clark J, Burdon T. 2004. Oct-4 knockdown induces similar patterns of endoderm and trophoblast differentiation markers in human and mouse embryonic stem cells. Stem Cells 22:225-235.
18. He S, Pant D, Schiffmacher A, Bischoff S, Melican D, Gavin W, Keefer C. 2006. Developmental expression of pluripotency determining factors in caprine embryos: Novel pattern of NANOG protein localization in the nucleolus. Mol Reprod Dev 73:1512-1522.
19. He S, Pant D, Schiffmacher A, Meece A, Keefer CL. 2008. Lymphoid enhancer factor 1-mediated Wnt signaling promotes the initiation of trophoblast lineage differentiation in mouse embryonic stem cells. Stem Cells 26:842-849.
20. Hemberger M, Dean W, Reik W. 2009. Epigenetic dynamics of stem cells and cell lineage commitment: Digging Waddington's canal. Nat Rev Mol Cell Biol 10:526-537.
21. Home P, Ray S, Dutta D, Bronshteyn I, Larson M, Paul S. 2009. GATA3 is selectively expressed in the trophectoderm of peri-implantation embryo and directly regulates Cdx2 gene expression. J Biol Chem 284:28729-28737.
22. Imakawa K, Kim MS, Matsuda-Minehata F, Ishida S, Iizuka M, Suzuki M, Chang KT, Echternkamp SE, Christenson RK. 2006. Regulation of the ovine interferon-tau gene by a blastocyst-specific transcription factor, Cdx2. Mol Reprod Dev 73:559-567.
23. Ivanova N, Dobrin R, Lu R, Kotenko I, Levorse J, DeCoste C, Schafer X, Lun Y, Lemischka IR. 2006. Dissecting self-renewal in stem cells with RNA interference. Nature 442:533-538.
24. Janatpour MJ, McMaster MT, Genbacev O, Zhou Y, Dong J, Cross JC, Israel MA, Fisher SJ. 2000. Id-2 regulates critical aspects of human cytotrophoblast differentiation, invasion and migration. Development 127:549-558.
25. Jiang W, Zhou L, Breyer B, Feng T, Cheng H, Haydon R, Ishikawa A, He TC. 2001. Tetracycline-regulated gene expression mediated by a novel chimeric repressor that recruits histone deacetylases in mammalian cells. J Biol Chem 276:45168-45174.
26. Keefer CL, Pant D, Blomberg L, Talbot NC. 2007. Challenges and prospects for the establishment of embryonic stem cell lines of domesticated ungulates. Anim Reprod Sci 98:147-168.
27. Kirchhof N, Carnwath JW, Lemme E, Anastassiadis K, Schöler H, Niemann H. 2000. Expression pattern of Oct-4 in preimplantation embryos of different species. Biol Reprod 63:1698-1705.
28. Kuijk EW, Du Puy L, Van Tol HT, Oei CH, Haagsman HP, Colenbrander B, Roelen BA. 2008. Differences in early lineage segregation between mammals. Dev Dyn 237:918-927.
29. Kurosaka S, Eckardt S, McLaughlin KJ. 2004. Pluripotent lineage definition in bovine embryos by Oct4 transcript localization. Biol Reprod 71:1578-1582.
30. Maruyama M, Ichisaka T, Nakagawa M, Yamanaka S. 2005. Differential roles for Sox15 and Sox2 in transcriptional control in mouse embryonic stem cells. J Biol Chem 280:24371-24379.
31. Mitalipov SM, Kuo HC, Hennebold JD, Wolf DP. 2003. Oct-4 expression in pluripotent cells of the rhesus monkey. Biol Reprod 69:1785-1792.
32. Nakano H, Shimada A, Imai K, Takahashi T, Hashizume K. 2005. The cytoplasmic expression of E-cadherin and beta-catenin in bovine trophoblasts during binucleate cell differentiation. Placenta 26:393-401.
33. Ng RK, Dean W, Dawson C, Lucifero D, Madeja Z, Reik W, Hemberger M. 2008. Epigenetic restriction of embryonic cell lineage fate by methylation of Elf5. Nat Cell Biol 10:1280-1290.
34. Nichols J, Zevnik B, Anastassiadis K, Niwa H, Klewe-Nebenius D, Chambers I, Schöler H, Smith A. 1998. Formation of pluripotent stem cells in the mammalian embryo depends on the POU transcription factor Oct4. Cell 95:379-391.
35. Niwa H, Miyazaki J, Smith AG. 2000. Quantitative expression of Oct-3/4 defines differentiation, dedifferentiation or self-renewal of ES cells. Nat Genet 24:372-376.
36. Niwa H, Toyooka Y, Shimosato D, Strumpf D, Takahashi K, Yagi R, Rossant J. 2005. Interaction between Oct3/4 and Cdx2 determines trophectoderm differentiation. Cell 123:917-929.
37. Pesce M, Schöler HR. 2001. Oct-4: Gatekeeper in the beginnings of mammalian development. Stem Cells 19:271-278.
38. Porter TE, Ellestad LE, Fay A, Stewart JL, Bossis I. 2006. Identification of the chicken growth hormone-releasing hormone receptor (GHRH-R) mRNA and gene: Regulation of anterior pituitary GHRH-R mRNA levels by homologous and heterologous hormones. Endocrinology 147:2535-2543.
39. Ralston A, Rossant J. 2008. Cdx2 acts downstream of cell polarization to cell-autonomously promote trophectoderm fate in the early mouse embryo. Dev Biol 313:614-629.
40. Ralston A, Cox BJ, Nishioka N, Sasaki H, Chea E, Rugg-Gunn P, Guo G, Robson P, Draper JS, Rossant J. 2010. Gata3 regulates trophoblast development downstream of Tead4 and in parallel to Cdx2. Development 137:395-403.
41. Roberts RM, Ezashi T, Das P. 2004. Trophoblast gene expression: Transcription factors in the specification of early trophoblast. Reprod Biol Endocrinol 2:47.
42. Rossant J, Cross JC. 2001. Placental development: Lessons from mouse mutants. Nat Rev Genet 2:538-548.
43. Rossant J, Tam PP. 2009. Blastocyst lineage formation, early embryonic asymmetries, and axis patterning in the mouse. Development 136:701-713.
44. Russ AP, Wattler S, Colledge WH, Aparicio SA, Carlton MB, Pearce JJ, Barton SC, Surani MA, Ryan K, Nehls MC, Wilson V, Evans MJ. 2000. Eomesodermin is required for mouse trophoblast development and mesoderm formation. Nature 404:95-99.
45. Sakurai T, Sakamoto A, Muroi Y, Bai H, Nagaoka K, Tamura K, Takahashi T, Hashizume K, Sakatani M, Takahashi M, Godkin JD, Imakawa K. 2009. Induction of endogenous interferon tau gene transcription by CDX2 and high acetylation in bovine nontrophoblast cells. Biol Reprod 80:1223-1231.
46. Schiffmacher AT, Keefer CL. 2012. Optimization of a lipitoid-based plasmid DNA transfection protocol for bovine trophectoderm CT-1 cells. In Vitro Cell Dev Biol Anim 48:403-406.
47. Scott IC, Anson-Cartwright L, Riley P, Reda D, Cross JC. 2000. The HAND1 basic helix-loop-helix transcription factor regulates trophoblast differentiation via multiple mechanisms. Mol Cell Biol 20:530-541.
48. Sritanaudomchai H, Sparman M, Tachibana M, Clepper L, Woodward J, Gokhale S, Wolf D, Hennebold J, Hurlbut W, Grompe M, Mitalipov S. 2009. CDX2 in the formation of the trophectoderm lineage in primate embryos. Dev Biol 335:179-187.
49. Strumpf D, Mao CA, Yamanaka Y, Ralston A, Chawengsaksophak K, Beck F, Rossant J. 2005. Cdx2 is required for correct cell fate specification and differentiation of trophectoderm in the mouse blastocyst. Development 132:2093-2102.
50. Talbot NC, Caperna TJ, Edwards JL, Garrett W, Wells KD, Ealy AD. 2000. Bovine blastocyst-derived trophectoderm and endoderm cell cultures: Interferon tau and transferrin expression as respective in vitro markers. Biol Reprod 62:235-247.
51. Ushizawa K, Takahashi T, Kaneyama K, Tokunaga T, Tsunoda Y, Hashizume K. 2005. Gene expression profiles of bovine trophoblastic cell line (BT-1) analyzed by a custom cDNA microarray. J Reprod Dev 51:211-220.
52. Ushizawa K, Takahashi T, Hosoe M, Kizaki K, Hashizume K. 2009. Characterization and expression analysis of SOLD1, a novel member of the retrotransposon-derived Ly-6 superfamily, in bovine placental villi. PLoS ONE 4:e5814.
53. Utku Y, Dehan E, Ouerfelli O, Piano F, Zuckermann RN, Pagano M, Kirshenbaum K. 2006. A peptidomimetic siRNA transfection reagent for highly effective gene silencing. Mol Biosyst 2:312-317.
54. van Eijk MJ, van Rooijen MA, Modina S, Scesi L, Folkers G, van Tol HT, Bevers MM, Fisher SR, Lewin HA, Rakacolli D, Galli C, de Vaureix C, Trounson AO, Mummery CL, Gandolfi F. 1999. Molecular cloning, genetic mapping, and developmental expression of bovine POU5F1. Biol Reprod 60:1093-1103.
55. Wang X, Dai J. 2010. Concise review: Isoforms of OCT4 contribute to the confusing diversity in stem cell biology. Stem Cells 28:885-893.
56. Wen F, Tynan JA, Cecena G, Williams R, Múnera J, Mavrothalassitis G, Oshima RG. 2007. Ets2 is required for trophoblast stem cell self-renewal. Dev Biol 312:284-299.
57. Xie, S, Low BG, Nagel RJ, Kramer KK, Anthony RV, Zoli AP, Beckers JF, Roberts RM. 1991. Identification of the major pregnancy-specific antigens of cattle and sheep as inactive members of the aspartic proteinase family. Proc Natl Acad Sci USA 88:10247-10251.
58. Xie S, Green J, Bixby JB, Szafranska B, DeMartini JC, Hecht S, Roberts RM. 1997. The diversity and evolutionary relationships of the pregnancy-associated glycoproteins, an aspartic proteinase subfamily consisting of many trophoblast-expressed genes. Proc Natl Acad Sci USA 94:12809-12816.
59. Yamada K, Kanda H, Tanaka S, Takamatsu N, Shiba T, Ito M. 2006. Sox15 enhances trophoblast giant cell differentiation induced by Hand1 in mouse placenta. Differentiation 74:212-221.