Changes in sub-cellular localisation of trophoblast and inner cell mass specific transcription factors during bovine preimplantation development

BMC Developmental Biology

Volumn 13, Issue 1, 2013, Pages

  Madeja, Zofia E ^a   Sosnowski, Jaroslaw ^a   Hryniewicz, Kamila ^a   Warzych, Ewelina ^a   Pawlak, Piotr ^a   Rozwadowska, Natalia ^b   Plusa, Berenika ^c   Lechniak, Dorota ^a  

^a POZNA UNIVERSITY OF LIFE SCIENCES   (Poland)

^b INSTITUTE OF HUMAN GENETICS   (Poland)

^c UNIVERSITY OF MANCHESTER   (United Kingdom)

Author keywords

Bovine blastocyst; CDX2; Cell fate; Gene expression patterns; ICM TE lineage segregation; Mitotic retention

Indexed keywords

ANIMALIA; BOS; BOVINAE;

PRIMER DNA; TRANSCRIPTION FACTOR;

ANIMAL; ARTICLE; BLASTOCYST; CATTLE; CELL FRACTIONATION; GENE EXPRESSION REGULATION; METABOLISM; NUCLEOTIDE SEQUENCE; REAL TIME POLYMERASE CHAIN REACTION; TROPHOBLAST;

ANIMALS; BASE SEQUENCE; BLASTOCYST; CATTLE; DNA PRIMERS; GENE EXPRESSION REGULATION, DEVELOPMENTAL; REAL-TIME POLYMERASE CHAIN REACTION; SUBCELLULAR FRACTIONS; TRANSCRIPTION FACTORS; TROPHOBLASTS;

EID: 84881295587     PISSN: None     EISSN: 1471213X     Source Type: Journal    
DOI: 10.1186/1471-213X-13-32     Document Type: Article

References (86)

1. Conserved molecular portraits of bovine and human blastocysts as a consequence of the transition from maternal to embryonic control of gene expression. Adjaye J, Herwig R, Brink TC, Herrmann D, Greber B, Sudheer S, Groth D, Carnwath JW, Lehrach H, Niemann H, Physiol Genomics 2007 31 315 327 10.1152/physiolgenomics.00041.2007 17595343
2. Utility of animal models for human embryo culture development: domestic species. Krischer RL, Embryo cult: Methods Protoc, Methods Mol Bio 2012 912 27 37
3. Cell fate regulation in early mammalian development. Oron E, Ivanova N, Phys Biol 2012 9 1 17
4. Immunohistochemical and ultrastructural characterization of the initial post-hatching development of bovine embryos. Alexopoulos NI, Vajta G, Lewis I, Rogers P, Cann L, Callesen H, Tveden-Nyborg P, Trounson A, Reproduction 2003 125 607 623 10.1530/rep.0.1250607 12683931
5. Cell adhesion and gap junction formation in the early mouse embryo are induced prematurely by 6-DMAP in the absence of E cadherin phosphorylation. Aghion J, Gueth-Hallonet C, Antony C, Gros D, Maro B, J Cell Sci 1994 107 1369 1379 7929642
6. The expression and stage-specific localization of protein kinase C isotypes during mouse preimplantation development. Pauken CM, Capco DG, Dev Biol 2000 223 411 412 10.1006/dbio.2000.9763 10882525
7. Downregulation of Par3 and aPKC function directs cells towards the ICM in the preimplantation mouse embryo. Plusa B, Frankenberg S, Chalmers A, Hadjantonakis AK, Moore CA, Papalopulu N, Papaioannou VE, Glover DM, Zernicka-Goetz M, J Cell Sci 2005 118 505 515 10.1242/jcs.01666 15657073
8. Ezrin becomes restricted to outer cells following asymmetrical division in the preimplantation mouse embryo. Louvet S, Aghion J, Santa-Maria A, Mangeat P, Maro B, Dev Biol 1996 177 568 569 10.1006/dbio.1996.0186 8806832
9. Induction of polarity in mouse 8-cell blastomeres: specificity, geometry, and stability. Johnson MH, Ziomek CA, J Cell Biol 1981 91 303 308 10.1083/jcb.91.1.303 7298724
10. The foundation of two distinct cell lineages within the mouse morula. Johnson MH, Ziomek CA, Cell 1981 24 71 80 10.1016/0092-8674(81)90502-X 7237545
11. Transcription factor TEAD4 specifies the trophectoderm lineage at the beginning of mammalian development. Yagi R, Kohn MJ, Karavanova I, Kaneko KJ, Vullhorst D, DePamphilis ML, Buonanno A, Development 2007 134 3827 3836 10.1242/dev.010223 17913785
12. The Hippo signalling pathway components Lats and Yap pattern Tead4 activity to distinguish mouse trophectoderm from inner cells. Nishioka N, Inoue K-I, Adachi K, Kiyonari H, Ota M, Ralston A, Yabuda N, Hirahara S, Stephenson RO, Ogonuki N, Devel Cell 2009 16 398 410 10.1016/j.devcel.2009.02.003
13. GATA3 is selectively expressed in the trophectoderm of peri-implantation embryo and directly regulates Cdx2 gene expression. Home P, Ray S, Dutta D, Bronshteyn I, Larson M, Paul S, J Biol Chem 2009 284 28729 28737 10.1074/jbc.M109.016840 19700764
14. Gata3 regulates trophoblast development downstream of Tead4 and in parallel to Cdx2. Ralston A, Cox BJ, Nishioka N, Sasaki H, Chea E, Rugg-Gunn P, Guo G, Robson P, Draper JS, Rossant J, Development 2010 137 395 403 10.1242/dev.038828 20081188
15. Cdx2 acts downstream of cell polarization to cell-autonomously promote trophectoderm fate in the early mouse embryo. Ralston A, Rossant J, Dev Biol 2008 313 614 629 10.1016/j.ydbio.2007.10.054 18067887
16. Cdx2 is required for correct cell fate specification and differentiation of trophectoderm in the mouse blastocyst. Strumpf D, Mao CA, Yamanaka Y, Ralston A, Chawengsaksophak K, Beck F, Rossant J, Development 2005 132 2093 2102 10.1242/dev.01801 15788452
17. Eomesodermin is required for mouse trophoblast development and mesoderm formation. Russ AP, Wattler S, Colledge WH, Aparicio SA, Carlton MB, Pearce JJ, Barton SC, Surani MA, Ryan K, Nehls MC, Wilson V, Evans MJ, Nature 2000 404 95 99 10.1038/35003601 10716450
18. Epigenetic restriction of embryonic cell lineage fate by methylation of Elf5. Ng RK, Dean W, Dawson C, Lucifero D, Madeja Z, Reik W, Hemberger M, Nat Cell Biol 2008 10 1280 1290 10.1038/ncb1786 18836439
19. Mechanisms of trophectoderm fate specification in preimplantation mouse development. Sasaki H, Dev Growth Diffr 2010 52 263 273 10.1111/j.1440-169X. 2009.01158.x
20. Stochastic patterning in the mouse pre-implantation embryo. Dietrich JE, Hiiragi T, Development 2007 134 4219 4231 10.1242/dev.003798 17978007
21. Delay of polarization event increases the number of Cdx2-positive blastomeres in mouse embryo. Kondratiuk I, Bazydlo K, Maleszewski M, Szczepanska K, Dev Biol 2012 368 54 62 10.1016/j.ydbio.2012.05.013 22609553
22. Interaction between Oct3/4 and Cdx2 determines trophectoderm differentiation. Niwa H, Toyooka Y, Shimosato D, Strumpf D, Takahashi K, Yagi R, Rossant J, Cell 2005 123 917 929 10.1016/j.cell.2005.08.040 16325584
23. Uncovering early response of gene regulatory networks in ESCs by systematic induction of transcription factors. Nishiyama A, Xin L, Sharov AA, Thomas M, Mowrer G, Meyers E, Piao Y, Mehta S, Yee S, Nakatake Y, Stagg C, Sharova L, Correa-Cerro LS, Bassey U, Hoang H, Kim E, Tapnio R, Qian Y, Dudekula D, Zalzman M, Li M, Falco G, Yang HT, Lee SL, Monti M, Stanghellini I, Islam MN, Nagaraja R, Goldberg I, Wang W, et al. Cell Stem Cell 2009 5 420 433 19796622
24. Formation of pluripotent stem cells in the mammalian embryo depends on the POU transcription factor Oct4. Nichols J, Zevnik B, Anastassiadis K, Niwa H, Klewe-Nebenius D, Chambers I, Scholer H, Smith A, Cell 1998 95 379 391 10.1016/S0092-8674(00)81769-9 9814708
25. The homeoprotein Nanog is required for maintenance of pluripotency in mouse epiblast and ES cells. Mitsui K, Tokuzawa Y, Itoh H, Segawa K, Murakami M, Takahashi K, Maruyama M, Maeda M, Yamanaka S, Cell 2003 113 631 642 10.1016/S0092-8674(03)00393-3 12787504
26. Murine inner cell mass-derived lineages depend on Sall4 function. Elling U, Klasen C, Eisenberger T, Anlag K, Treier M, Proc Natl Acad Sci U S A 2006 103 16319 16324 10.1073/pnas.0607884103 17060609
27. Multipotent cell lineages in early mouse development depend on SOX2 function. Avilion AA, Nicolis SK, Pevny LH, Perez L, Vivian N, Lovell-Badge R, Genes Dev 2003 17 126 140 10.1101/gad.224503 12514105
28. Defining pathways that enforce cell lineage specification in early development and stem cells. Roper S, Hemberger M, Cell Cycle 2009 8 1515 1525 10.4161/cc.8.10.8381 19377304
29. Pluripotency governed by Sox2 via regulation of Oct3/4 expression in mouse embryonic stem cells. Masui S, Nakatake Y, Toyooka Y, Shimosato D, Yagi R, Takahashi K, Okochi H, Okuda A, Matoba R, Sharov AA, Ko MS, Niwa H, Nat Cell Biol 2007 9 625 635 10.1038/ncb1589 17515932
30. Functional expression cloning of Nanog, a pluripotency sustaining factor in embryonic stem cells. Chambers I, Colby D, Robertson M, Nichols J, Lee S, Tweedie S, Smith A, Cell 2003 113 643 655 10.1016/S0092-8674(03)00392-1 12787505
31. Cross-regulation of the Nanog and Cdx2 promoters. Chen L, Yabuuchi A, Eminli S, Takeuchi A, Lu CW, Hochedlinger K, Daley GQ, Cell Res 2009 19 1052 1061 10.1038/cr.2009.79 19564890
32. Trophectoderm lineage determination in cattle. Berg DK, Smith CS, Pearton DJ, Wells DN, Broadhurst R, Donnison M, Pfeffer PL, Cell 2011 20 244 255
33. Morphology of immature bovine oocytes. De-Loos F, Van-Vliet C, Van-Maurik P, Kruip TA, Gamete Res 1989 24 197 204 10.1002/mrd.1120240207 2793058
34. Cryopreservation affects the quality of in vitro produced bovine embryos at the molecular level. Stinshoff H, Wilkening S, Hanstedt A, Brüning K, Wrenzycki C, Theriogenology 2011 76 1433 1441 10.1016/j.theriogenology.2011.06. 013 21835456
35. In vitro capacitation of bovine spermatozoa: role of intracellular calcium. Parrish JJ, Susko-Parrish JL, Graham JK, Theriogenology 1998 51 461 472
36. High bovine blastocyst development in a static in vitro production system using SOFaa medium supplemented with sodium citrate and myo-inositol with or without serum-proteins. Holm P, Booth PJ, Schmidt MH, Greve T, Callesen H, Theriogenology 1999 52 683 700 10.1016/S0093-691X(99)00162-4 10734366
37. Analysis of relative gene expression data using real-time quantitative PCR and the 2(-Delta Delta C(T)). Livak KJ, Schmittgen TD, Methods 2001 25 402 408 10.1006/meth.2001.1262 11846609
38. Analyzing real-time PCR data by the comparative C(T) method. Schmittgen TD, Livak KJ, Nat Protoc 2008 3 1101 1108 10.1038/nprot.2008.73 18546601
39. Analysis of the gene expression pattern of bovine blastocysts at three stages of development. Rekik W, Dufort I, Sirard MA, Mol Reprod Dev 2011 78 226 240 10.1002/mrd.21286 21509852
40. Paternal MHC expression on mouse trophoblast affects uterine vascularization and fetal growth. Madeja Z, Yadi H, Apps R, Boulenouar S, Roper SJ, Gardner L, Moffett A, Colucci F, Hemberger M, Proc Natl Acad Sci U S A 2011 108 4012 4017 10.1073/pnas.1005342108 21300875
41. Distinct sequential cell behaviours direct primitive endoderm formation in the mouse blastocyst. Plusa B, Piliszek A, Frankanberg S, Artus J, Hadjantonakis AK, Development 2008 135 3081 3091 10.1242/dev.021519 18725515
42. The anterior margin of the mammalian gastrula: comparative and phylogenetic aspects of its role in axis formation and head induction. Viebahn C, Curr Top Dev Biol 1999 46 63 103 10417877
43. Post-hatching development of the porcine and bovine embryo-defining criteria for expected development in vivo and in vitro. Vejlsted M, Du Y, Vajta G, Maddox-Hyttel P, Theriogenology 2006 65 153 165 10.1016/j.theriogenology. 2005.09.021 16257443
44. Terminologies for the pre-attachment bovine embryo. Peippo J, Machaty Z, Peter A, Theriogenology 2011 76 1373 1379 10.1016/j.theriogenology.2011.06.018 21855984
45. Analysis of co-expression of OCT4, NANOG and SOX2 in pluripotent cells of the porcine embryo, in vivo and in vitro. Du-Puy L, Lopes SM, Haagsman HP, Roelen BA, Theriogenology 2011 75 513 526 10.1016/j.theriogenology.2010.09.019 21074831
46. Developmental expression of pluripotency determining factors in caprine embryos: novel pattern of NANOG protein localization in the nucleolus. He S, Pant D, Schiffmacher A, Bischoff S, Melican D, Gavin W, Keefer C, Mol Reprod Dev 2006 73 1512 1522 10.1002/mrd.20525 16894532
47. Visualizing chromatin and chromosomes in living cells. Zink D, Sadoni N, Ernst SE, Methods 2003 29 42 50 10.1016/S1046-2023(02)00289-X 12543070
48. A mouse is not a cow. Rossant J, Nature 2011 471 457 458 10.1038/471457a 21430771
49. Pluripotent lineage definition in bovine embryos by Oct4 transcript localization. Kurosaka S, Eckardt S, McLaughlin KJ, Biol Reprod 2004 71 1578 1582 10.1095/biolreprod.104.029322 15229144
50. Molecular evidence for a critical period in mural trophoblast development in bovine blastocysts. Degrelle SA, Campion E, Cabau C, Piumi F, Reinaud P, Richard C, Renard JP, Hue I, Dev Biol 2005 288 448 460 10.1016/j.ydbio.2005.09. 043 16289134
51. Efficient derivation of bovine embryonic stem cells needs more than active core pluripotency factors. Maruotti J, Muñoz M, Degrelle SA, Gómez E, Louet C, Monforte CD, De-Longchamp PH, Brochard V, Hue I, Caamaño JN, Jouneau A, Mol Reprod Dev 2012 79 461 477 10.1002/mrd.22051 22573702
52. Isolation and culture of primary bovine embryonic stem cell colonies by a novel method. Cao S, Wang F, Chen Z, Liu Z, Mei C, Wu H, Huang J, Li C, Zhou L, Liu L, J Exp Zool A Ecol Genet Physiol 2009 311 368 376 19340839
53. Generation and characterization of pluripotent stem cells from cloned bovine embryos. Wang L, Duan E, Sung LY, Jeong BS, Yang X, Tian XC, Biol Reprod 2005 73 149 155 10.1095/biolreprod.104.037150 15744021
54. Expression of pluripotency master regulators during two key developmental transitions: EGA and early lineage specification in the bovine embryo. Khan DR, Dubé D, Gall L, Peynot N, Ruffini S, Laffont L, Le-Bourhis D, Degrelle S, Jouneau A, Duranthon V, PLoS One 2012 7 1 11
55. Expression of pluripotency-related genes during bovine inner cell mass explant culture. Pant D, Keefer CL, Cloning Stem Cells 2009 11 355 365 10.1089/clo.2008.0078 19594391
56. Differences in early lineage segregation between mammals. Kuijk EW, Du-Puy L, Van-Tol HT, Oei CH, Haagsman HP, Colenbrander B, Roelen BA, Dev Dyn 2008 237 918 927 10.1002/dvdy.21480 18330925
57. The roles of FGF and MAP kinase signalling in the segregation of the epiblast and hypoblast cell lineages in bovine and human embryos. Kuijk EW, Van-Tol LTA, Van De-Velde H, Wobbolts R, Welling M, Geijsen N, Roelen B, Development 2012 139 871 882 10.1242/dev.071688 22278923
58. Transition from maternal to embryonic control in early mammalian development: a comparison of several species. Telford NA, Watson AJ, Schultz GA, Mol Reprod Dev 1990 26 90 100 10.1002/mrd.1080260113 2189447
59. Transcriptomic changes in the bovine conceptus between the blastocyst stage and initiation of implantation. Mamo S, Rizos D, Lonergan P, Anim Reprod Sci 2012 134 56 63 10.1016/j.anireprosci.2012.08.011 22944169
60. Control of gene expression at the onset of bovine embryonic development. Memili E, First NL, Biol Reprod 1999 61 1198 1207 10.1095/biolreprod61.5.1198 10529265
61. Transcriptional activity in in vitro produced bovine two- and four-cell embryos. Viuff D, Avery B, Greve T, King WA, Hyttel P, Mol Reprod Dev 1996 43 171 179 10.1002/(SICI)1098-2795(199602)43:2<171::AID-MRD6>3.0.CO;2-O 8824915
62. Transcription and cell cycle-dependent development of intranuclear bodies and granules in two-cell bovine embryos. Hyttel P, Viuff D, Avery B, Laurincik J, Greve T, J Reprod Fertil 1996 108 263 270 10.1530/jrf.0.1080263 9038785
63. Developmental changes in RNA polymerase II in bovine oocytes, early embryos, and effect of alpha-amanitin on embryo development. Memili E, First NL, Mol Reprod Dev 1998 51 381 389 10.1002/(SICI)1098-2795(199812)51:4<381::AID- MRD4>3.0.CO;2-G 9820196
64. Assessment of differential display-RT-PCR of mRNA transcript transitions and alpha-amanitin sensitivity during bovine preattachment development. Natale DR, Kidder GM, Westhusin ME, Watson AJ, Mol Reprod Dev 2000 55 152 163 10.1002/(SICI)1098-2795(200002)55:2<152::AID-MRD4>3.0.CO;2-N 10618654
65. Transcription factor expression patterns in bovine in vitro-derived embryos prior to maternal-zygotic transition. Vigneault C, McGraw S, Massicotte L, Sirard MC, Biol Reprod 2004 70 1701 1709 10.1095/biolreprod.103.022970 14960490
66. Asymmetric localization of Cdx2 mRNA during the first cell-fate decision in early mouse development. Skamagki M, Wicher KB, Jedrusik A, Ganguly S, Zernicka-Goetz M, Cell Rep 2013 3 442 457 10.1016/j.celrep.2013.01.006 23375373
67. Early cell fate decisions in the mouse embryo. Saiz N, Plusa B, Reproduction 2013 145 65 R80 10.1530/REP-12-0381 23221010
68. Nanog is the gateway to the pluripotent ground state. Silva J, Nichols J, Theunissen TW, Guo G, Van-Oosten AL, Barrandon O, Wray J, Yamanaka S, Chambers I, Smith A, Cell 2009 138 722 737 10.1016/j.cell.2009.07.039 19703398
69. Transcriptional regulation of nanog by OCT4 and SOX2. Rodda DJ, Chew JL, Lim LH, Loh YH, Wang B, Ng HH, Robson P, J Biol Chem 2005 280 24731 24737 10.1074/jbc.M502573200 15860457
70. The Oct4 and Nanog transcription network regulates pluripotency in mouse embryonic stem cells. Loh YH, Wu Q, Chew JL, Vega VB, Zhang W, Chen X, Bourque G, George J, Leong B, Liu J, Wong KY, Sung KW, Lee CW, Zhao XD, Chiu KP, Lipovich L, Kuznetsov VA, Robson P, Stanton LW, Wei CL, Ruan Y, Lim B, Ng HH, Nat Genet 2006 38 431 440 10.1038/ng1760 16518401
71. The transcriptional foundation of pluripotency. Chambers I, Tomlison SR, Development 2009 136 2311 2322 10.1242/dev.024398 19542351
72. Oct4 mRNA and preotein expression during human preimplantation development. Caufmann G, Van De-Velde H, Liebaers I, Van-Steirteghem A, Mol Hum Reprod 2005 11 173 181 10.1093/molehr/gah155 15695770
73. CDX2 in the formation of the trophectoderm lineage in primate embryos. Sritanaudomachi H, Sparman M, Tachibana M, Cleper L, Woodward J, Gokhale S, Wolf D, Hennebold J, Hurlbut W, Grompe M, Mitalapov S, Dev Biol 2009 335 179 187 10.1016/j.ydbio.2009.08.025 19733166
74. Expression of cell-surface antigens and embryonic stem cell pluripotency genes in equine blastocysts. Guest DJ, Allen WR, Stem Cells Dev 2007 16 789 796 10.1089/scd.2007.0032 17999600
75. Promoter analysis of the rabbit POU5F1 gene and its expression in preimplantation stage embryos. Kobolak J, Kiss K, Polgar Z, Mamo S, Rogel-Gaillard C, Tancos Z, Bock I, Baji AG, Tar K, Pirity MK, BMC Mol Biol 2009 10 88 10.1186/1471-2199-10-88 19732419
76. Identification and expression analysis of genes associated with bovine blastocyst formation. Goosens K, Van-Soom A, Van-Poucke M, Vandaele L, Vandesompele J, Van-Zeveren A, Peelman LJ, BMC Dev Biol 2007 7 64 10.1186/1471-213X-7-64 17559642
77. Quantification of Fibronectin 1 (FN1) splice variants, including two novel ones, and analysis of integrins as candidate FN1 receptors in bovine preimplantation embryos. Goosens K, Van-Soom A, Van-Zeveren A, Favoreel H, Peelman LJ, BMC Dev Biol 2009 9 1 10.1186/1471-213X-9-1 19126199
78. Targeted deletion of keratins 18 and 19 leads to trophoblast fragility and early embryonic lethality. Hesse M, Franz T, Tamai Y, Taketo MM, Magin TM, EMBO J 2009 19 5060 5070
79. Fibroblast growth factor 2 promotes primitive endoderm development in bovine blastocyst outgrowths. Yang QE, Fields SD, Zhang K, Ozawa M, Johnson SE, Ealy AD, Biol Reprod 2011 85 946 953 10.1095/biolreprod.111.093203 21778141
80. NANOG is a key factor for induction of pluripotency in bovine adult fibroblasts. Sumer H, Liu J, Malaver-Ortega LF, Lim ML, Khodadadi K, Verma PJ, J Anim Sci 2011 89 2708 2716 10.2527/jas.2010-3666 21478453
81. Specific expression of a retinoic acid-regulated, zinc-finger gene, Rex-1, in preimplantation embryos, trophoblast and spermatocytes. Rogers MB, Hosler BA, Gudas LJ, Development 1991 113 815 824 1821852
82. Distinct histone modifications in stem cell lines and tissue lineages from the early mouse embryo. Rugg-Gunn PJ, Cox BJ, Ralston A, Rossant J, Proc Natl Acad Sci U S A 2010 107 10783 10790 10.1073/pnas.0914507107 20479220
83. Mechanisms of transcriptional repression by histone lysine methylation. Hublitz P, Albert M, Peters AH, Int J Dev Biol 2009 53 335 354 10.1387/ijdb.082717ph 19412890
84. Dynamics of constitutive heterochromatin: two contrasted kinetics of genome restructuring in early cloned bovine embryos. Pichugin A, Le-Bourhis D, Adenot P, Lehmann G, Audouard C, Renard JP, Vignon X, Beaujean N, Reproduction 2010 139 129 137 10.1530/REP-08-0435 19778997
85. Mitotic retention of gene expression patterns by the cell fate-determining transcription factor Runx2. Young DW, Hassan MQ, Yang XQ, Galindo M, Javed A, Zaidi SK, Furcinitti P, Lapointe D, Montecino M, Lian JB, Stein JL, Van-Wijnen AJ, Stein GS, Proc Natl Acad Sci U S A 2004 104 3189 3194
86. Bookmarking the genome: maintenance of epigenetic information. Zaidi SK, Young DW, Montecino M, Van-Wijnen AJ, Stein JL, Lian JB, Stein GS, J Biol Chem 2011 286 18355 18361 10.1074/jbc.R110.197061 21454629