期刊论文详细信息
BMC Developmental Biology
Changes in sub-cellular localisation of trophoblast and inner cell mass specific transcription factors during bovine preimplantation development
Dorota Lechniak1  Berenika Plusa2  Natalia Rozwadowska3  Piotr Pawlak1  Ewelina Warzych1  Kamila Hryniewicz1  Jaroslaw Sosnowski1  Zofia E Madeja1 
[1]Department of Genetics and Animal Breeding, Poznan University of Life Sciences, Wolynska 33, Poznan 60-673, Poland
[2]Faculty of Life Sciences, The University of Manchester, Manchester, UK
[3]Department of Reproduction and Stem Cells, Institute of Human Genetics, Polish Academy of Sciences, Poznan, Poland
关键词: Mitotic retention;    CDX2;    Gene expression patterns;    Cell fate;    ICM/TE lineage segregation;    Bovine blastocyst;   
Others  :  1085554
DOI  :  10.1186/1471-213X-13-32
 received in 2012-12-17, accepted in 2013-08-07,  发布年份 2013
PDF
【 摘 要 】

Background

Preimplantation bovine development is emerging as an attractive experimental model, yet little is known about the mechanisms underlying trophoblast (TE)/inner cell mass (ICM) segregation in cattle. To gain an insight into these processes we have studied protein and mRNA distribution during the crucial stages of bovine development. Protein distribution of lineage specific markers OCT4, NANOG, CDX2 were analysed in 5-cell, 8–16 cell, morula and blastocyst stage embryos. ICM/TE mRNA levels were compared in hatched blastocysts and included: OCT4, NANOG, FN-1, KLF4, c-MYC, REX1, CDX2, KRT-18 and GATA6.

Results

At the mRNA level the observed distribution patterns agree with the mouse model. CDX2 and OCT4 proteins were first detected in 5-cell stage embryos. NANOG appeared at the morula stage and was located in the cytoplasm forming characteristic rings around the nuclei. Changes in sub-cellular localisation of OCT4, NANOG and CDX2 were noted from the 8–16 cell onwards. CDX2 initially co-localised with OCT4, but at the blastocyst stage a clear lineage segregation could be observed. Interestingly, we have observed in a small proportion of embryos (2%) that CDX2 immunolabelling overlapped with mitotic chromosomes.

Conclusions

Cell fate specification in cattle become evident earlier than presently anticipated – around the time of bovine embryonic genome activation. There is an intriguing possibility that for proper lineage determination certain transcription factors (such as CDX2) may need to occupy specific regions of chromatin prior to its activation in the interphase nucleus. Our observation suggests a possible role of CDX2 in the process of epigenetic regulation of embryonic cell fate.

【 授权许可】

   
2013 Madeja et al.; licensee BioMed Central Ltd.

【 预 览 】
附件列表
Files Size Format View
20150113174408203.pdf 3150KB PDF download
Figure 9. 174KB Image download
Figure 8. 105KB Image download
Figure 7. 88KB Image download
Figure 6. 183KB Image download
Figure 5. 109KB Image download
Figure 4. 68KB Image download
Figure 3. 167KB Image download
Figure 2. 44KB Image download
Figure 1. 19KB Image download
【 图 表 】

Figure 1.

Figure 2.

Figure 3.

Figure 4.

Figure 5.

Figure 6.

Figure 7.

Figure 8.

Figure 9.

【 参考文献 】
  • [1]Adjaye J, Herwig R, Brink TC, Herrmann D, Greber B, Sudheer S, Groth D, Carnwath JW, Lehrach H, Niemann H: Conserved molecular portraits of bovine and human blastocysts as a consequence of the transition from maternal to embryonic control of gene expression. Physiol Genomics 2007, 31:315-327.
  • [2]Krischer RL: Utility of animal models for human embryo culture development: domestic species. Embryo cult: Methods Protoc, Methods Mol Bio 2012, 912:27-37.
  • [3]Oron E, Ivanova N: Cell fate regulation in early mammalian development. Phys Biol 2012, 9:1-17.
  • [4]Alexopoulos NI, Vajta G, Lewis I, Rogers P, Cann L, Callesen H, Tveden-Nyborg P, Trounson A: Immunohistochemical and ultrastructural characterization of the initial post-hatching development of bovine embryos. Reproduction 2003, 125:607-623.
  • [5]Aghion J, Gueth-Hallonet C, Antony C, Gros D, Maro B: Cell adhesion and gap junction formation in the early mouse embryo are induced prematurely by 6-DMAP in the absence of E cadherin phosphorylation. J Cell Sci 1994, 107:1369-1379.
  • [6]Pauken CM, Capco DG: The expression and stage-specific localization of protein kinase C isotypes during mouse preimplantation development. Dev Biol 2000, 223:411-412.
  • [7]Plusa B, Frankenberg S, Chalmers A, Hadjantonakis AK, Moore CA, Papalopulu N, Papaioannou VE, Glover DM, Zernicka-Goetz M: Downregulation of Par3 and aPKC function directs cells towards the ICM in the preimplantation mouse embryo. J Cell Sci 2005, 118:505-515.
  • [8]Louvet S, Aghion J, Santa-Maria A, Mangeat P, Maro B: Ezrin becomes restricted to outer cells following asymmetrical division in the preimplantation mouse embryo. Dev Biol 1996, 177:568-569.
  • [9]Johnson MH, Ziomek CA: Induction of polarity in mouse 8-cell blastomeres: specificity, geometry, and stability. J Cell Biol 1981, 91:303-308.
  • [10]Johnson MH, Ziomek CA: The foundation of two distinct cell lineages within the mouse morula. Cell 1981, 24:71-80.
  • [11]Yagi R, Kohn MJ, Karavanova I, Kaneko KJ, Vullhorst D, DePamphilis ML, Buonanno A: Transcription factor TEAD4 specifies the trophectoderm lineage at the beginning of mammalian development. Development 2007, 134:3827-3836.
  • [12]Nishioka N, Inoue K-I, Adachi K, Kiyonari H, Ota M, Ralston A, Yabuda N, Hirahara S, Stephenson RO, Ogonuki N: The Hippo signalling pathway components Lats and Yap pattern Tead4 activity to distinguish mouse trophectoderm from inner cells. Devel Cell 2009, 16:398-410.
  • [13]Home P, Ray S, Dutta D, Bronshteyn I, Larson M, Paul S: GATA3 is selectively expressed in the trophectoderm of peri-implantation embryo and directly regulates Cdx2 gene expression. J Biol Chem 2009, 284:28729-28737.
  • [14]Ralston A, Cox BJ, Nishioka N, Sasaki H, Chea E, Rugg-Gunn P, Guo G, Robson P, Draper JS, Rossant J: Gata3 regulates trophoblast development downstream of Tead4 and in parallel to Cdx2. Development 2010, 137:395-403.
  • [15]Ralston A, Rossant J: Cdx2 acts downstream of cell polarization to cell-autonomously promote trophectoderm fate in the early mouse embryo. Dev Biol 2008, 313:614-629.
  • [16]Strumpf D, Mao CA, Yamanaka Y, Ralston A, Chawengsaksophak K, Beck F, Rossant J: Cdx2 is required for correct cell fate specification and differentiation of trophectoderm in the mouse blastocyst. Development 2005, 132:2093-2102.
  • [17]Russ AP, Wattler S, Colledge WH, Aparicio SA, Carlton MB, Pearce JJ, Barton SC, Surani MA, Ryan K, Nehls MC, Wilson V, Evans MJ: Eomesodermin is required for mouse trophoblast development and mesoderm formation. Nature 2000, 404:95-99.
  • [18]Ng RK, Dean W, Dawson C, Lucifero D, Madeja Z, Reik W, Hemberger M: Epigenetic restriction of embryonic cell lineage fate by methylation of Elf5. Nat Cell Biol 2008, 10:1280-1290.
  • [19]Sasaki H: Mechanisms of trophectoderm fate specification in preimplantation mouse development. Dev Growth Diffr 2010, 52:263-273.
  • [20]Dietrich JE, Hiiragi T: Stochastic patterning in the mouse pre-implantation embryo. Development 2007, 134:4219-4231.
  • [21]Kondratiuk I, Bazydlo K, Maleszewski M, Szczepanska K: Delay of polarization event increases the number of Cdx2-positive blastomeres in mouse embryo. Dev Biol 2012, 368:54-62.
  • [22]Niwa H, Toyooka Y, Shimosato D, Strumpf D, Takahashi K, Yagi R, Rossant J: Interaction between Oct3/4 and Cdx2 determines trophectoderm differentiation. Cell 2005, 123:917-929.
  • [23]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.: Uncovering early response of gene regulatory networks in ESCs by systematic induction of transcription factors. Cell Stem Cell 2009, 5:420-433.
  • [24]Nichols J, Zevnik B, Anastassiadis K, Niwa H, Klewe-Nebenius D, Chambers I, Scholer H, Smith A: Formation of pluripotent stem cells in the mammalian embryo depends on the POU transcription factor Oct4. Cell 1998, 95:379-391.
  • [25]Mitsui K, Tokuzawa Y, Itoh H, Segawa K, Murakami M, Takahashi K, Maruyama M, Maeda M, Yamanaka S: The homeoprotein Nanog is required for maintenance of pluripotency in mouse epiblast and ES cells. Cell 2003, 113:631-642.
  • [26]Elling U, Klasen C, Eisenberger T, Anlag K, Treier M: Murine inner cell mass-derived lineages depend on Sall4 function. Proc Natl Acad Sci U S A 2006, 103:16319-16324.
  • [27]Avilion AA, Nicolis SK, Pevny LH, Perez L, Vivian N, Lovell-Badge R: Multipotent cell lineages in early mouse development depend on SOX2 function. Genes Dev 2003, 17:126-140.
  • [28]Roper S, Hemberger M: Defining pathways that enforce cell lineage specification in early development and stem cells. Cell Cycle 2009, 8:1515-1525.
  • [29]Masui S, Nakatake Y, Toyooka Y, Shimosato D, Yagi R, Takahashi K, Okochi H, Okuda A, Matoba R, Sharov AA, Ko MS, Niwa H: Pluripotency governed by Sox2 via regulation of Oct3/4 expression in mouse embryonic stem cells. Nat Cell Biol 2007, 9:625-635.
  • [30]Chambers I, Colby D, Robertson M, Nichols J, Lee S, Tweedie S, Smith A: Functional expression cloning of Nanog, a pluripotency sustaining factor in embryonic stem cells. Cell 2003, 113:643-655.
  • [31]Chen L, Yabuuchi A, Eminli S, Takeuchi A, Lu CW, Hochedlinger K, Daley GQ: Cross-regulation of the Nanog and Cdx2 promoters. Cell Res 2009, 19:1052-1061.
  • [32]Berg DK, Smith CS, Pearton DJ, Wells DN, Broadhurst R, Donnison M, Pfeffer PL: Trophectoderm lineage determination in cattle. Cell 2011, 20:244-255.
  • [33]De-Loos F, Van-Vliet C, Van-Maurik P, Kruip TA: Morphology of immature bovine oocytes. Gamete Res 1989, 24:197-204.
  • [34]Stinshoff H, Wilkening S, Hanstedt A, Brüning K, Wrenzycki C: Cryopreservation affects the quality of in vitro produced bovine embryos at the molecular level. Theriogenology 2011, 76:1433-1441.
  • [35]Parrish JJ, Susko-Parrish JL, Graham JK: In vitro capacitation of bovine spermatozoa: role of intracellular calcium. Theriogenology 1998, 51:461-472.
  • [36]Holm P, Booth PJ, Schmidt MH, Greve T, Callesen H: 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. Theriogenology 1999, 52:683-700.
  • [37]Livak KJ, Schmittgen TD: Analysis of relative gene expression data using real-time quantitative PCR and the 2(−Delta Delta C(T)). Methods 2001, 25:402-408.
  • [38]Schmittgen TD, Livak KJ: Analyzing real-time PCR data by the comparative C(T) method. Nat Protoc 2008, 3:1101-1108.
  • [39]Rekik W, Dufort I, Sirard MA: Analysis of the gene expression pattern of bovine blastocysts at three stages of development. Mol Reprod Dev 2011, 78:226-240.
  • [40]Madeja Z, Yadi H, Apps R, Boulenouar S, Roper SJ, Gardner L, Moffett A, Colucci F, Hemberger M: Paternal MHC expression on mouse trophoblast affects uterine vascularization and fetal growth. Proc Natl Acad Sci U S A 2011, 108:4012-4017.
  • [41]Plusa B, Piliszek A, Frankanberg S, Artus J, Hadjantonakis AK: Distinct sequential cell behaviours direct primitive endoderm formation in the mouse blastocyst. Development 2008, 135:3081-3091.
  • [42]Viebahn C: The anterior margin of the mammalian gastrula: comparative and phylogenetic aspects of its role in axis formation and head induction. Curr Top Dev Biol 1999, 46:63-103.
  • [43]Vejlsted M, Du Y, Vajta G, Maddox-Hyttel P: Post-hatching development of the porcine and bovine embryo–defining criteria for expected development in vivo and in vitro. Theriogenology 2006, 65:153-165.
  • [44]Peippo J, Machaty Z, Peter A: Terminologies for the pre-attachment bovine embryo. Theriogenology 2011, 76:1373-1379.
  • [45]Du-Puy L, Lopes SM, Haagsman HP, Roelen BA: Analysis of co-expression of OCT4, NANOG and SOX2 in pluripotent cells of the porcine embryo, in vivo and in vitro. Theriogenology 2011, 75:513-526.
  • [46]He S, Pant D, Schiffmacher A, Bischoff S, Melican D, Gavin W, Keefer C: Developmental expression of pluripotency determining factors in caprine embryos: novel pattern of NANOG protein localization in the nucleolus. Mol Reprod Dev 2006, 73:1512-1522.
  • [47]Zink D, Sadoni N, Ernst SE: Visualizing chromatin and chromosomes in living cells. Methods 2003, 29:42-50.
  • [48]Rossant J: A mouse is not a cow. Nature 2011, 471:457-458.
  • [49]Kurosaka S, Eckardt S, McLaughlin KJ: Pluripotent lineage definition in bovine embryos by Oct4 transcript localization. Biol Reprod 2004, 71:1578-1582.
  • [50]Degrelle SA, Campion E, Cabau C, Piumi F, Reinaud P, Richard C, Renard JP, Hue I: Molecular evidence for a critical period in mural trophoblast development in bovine blastocysts. Dev Biol 2005, 288:448-460.
  • [51]Maruotti J, Muñoz M, Degrelle SA, Gómez E, Louet C, Monforte CD, De-Longchamp PH, Brochard V, Hue I, Caamaño JN, Jouneau A: Efficient derivation of bovine embryonic stem cells needs more than active core pluripotency factors. Mol Reprod Dev 2012, 79:461-477.
  • [52]Cao S, Wang F, Chen Z, Liu Z, Mei C, Wu H, Huang J, Li C, Zhou L, Liu L: Isolation and culture of primary bovine embryonic stem cell colonies by a novel method. J Exp Zool A Ecol Genet Physiol 2009, 311:368-376.
  • [53]Wang L, Duan E, Sung LY, Jeong BS, Yang X, Tian XC: Generation and characterization of pluripotent stem cells from cloned bovine embryos. Biol Reprod 2005, 73:149-155.
  • [54]Khan DR, Dubé D, Gall L, Peynot N, Ruffini S, Laffont L, Le-Bourhis D, Degrelle S, Jouneau A, Duranthon V: Expression of pluripotency master regulators during two key developmental transitions: EGA and early lineage specification in the bovine embryo. PLoS One 2012, 7:1-11.
  • [55]Pant D, Keefer CL: Expression of pluripotency-related genes during bovine inner cell mass explant culture. Cloning Stem Cells 2009, 11:355-365.
  • [56]Kuijk EW, Du-Puy L, Van-Tol HT, Oei CH, Haagsman HP, Colenbrander B, Roelen BA: Differences in early lineage segregation between mammals. Dev Dyn 2008, 237:918-927.
  • [57]Kuijk EW, Van-Tol LTA, Van De-Velde H, Wobbolts R, Welling M, Geijsen N, Roelen B: The roles of FGF and MAP kinase signalling in the segregation of the epiblast and hypoblast cell lineages in bovine and human embryos. Development 2012, 139:871-882.
  • [58]Telford NA, Watson AJ, Schultz GA: Transition from maternal to embryonic control in early mammalian development: a comparison of several species. Mol Reprod Dev 1990, 26:90-100.
  • [59]Mamo S, Rizos D, Lonergan P: Transcriptomic changes in the bovine conceptus between the blastocyst stage and initiation of implantation. Anim Reprod Sci 2012, 134:56-63.
  • [60]Memili E, First NL: Control of gene expression at the onset of bovine embryonic development. Biol Reprod 1999, 61:1198-1207.
  • [61]Viuff D, Avery B, Greve T, King WA, Hyttel P: Transcriptional activity in in vitro produced bovine two- and four-cell embryos. Mol Reprod Dev 1996, 43:171-179.
  • [62]Hyttel P, Viuff D, Avery B, Laurincik J, Greve T: Transcription and cell cycle-dependent development of intranuclear bodies and granules in two-cell bovine embryos. J Reprod Fertil 1996, 108:263-270.
  • [63]Memili E, First NL: Developmental changes in RNA polymerase II in bovine oocytes, early embryos, and effect of alpha-amanitin on embryo development. Mol Reprod Dev 1998, 51:381-389.
  • [64]Natale DR, Kidder GM, Westhusin ME, Watson AJ: Assessment of differential display-RT-PCR of mRNA transcript transitions and alpha-amanitin sensitivity during bovine preattachment development. Mol Reprod Dev 2000, 55:152-163.
  • [65]Vigneault C, McGraw S, Massicotte L, Sirard MC: Transcription factor expression patterns in bovine in vitro-derived embryos prior to maternal-zygotic transition. Biol Reprod 2004, 70:1701-1709.
  • [66]Skamagki M, Wicher KB, Jedrusik A, Ganguly S, Zernicka-Goetz M: Asymmetric localization of Cdx2 mRNA during the first cell-fate decision in early mouse development. Cell Rep 2013, 3:442-457.
  • [67]Saiz N, Plusa B: Early cell fate decisions in the mouse embryo. Reproduction 2013, 145:R65-R80.
  • [68]Silva J, Nichols J, Theunissen TW, Guo G, Van-Oosten AL, Barrandon O, Wray J, Yamanaka S, Chambers I, Smith A: Nanog is the gateway to the pluripotent ground state. Cell 2009, 138:722-737.
  • [69]Rodda DJ, Chew JL, Lim LH, Loh YH, Wang B, Ng HH, Robson P: Transcriptional regulation of nanog by OCT4 and SOX2. J Biol Chem 2005, 280:24731-24737.
  • [70]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: The Oct4 and Nanog transcription network regulates pluripotency in mouse embryonic stem cells. Nat Genet 2006, 38:431-440.
  • [71]Chambers I, Tomlison SR: The transcriptional foundation of pluripotency. Development 2009, 136:2311-2322.
  • [72]Caufmann G, Van De-Velde H, Liebaers I, Van-Steirteghem A: Oct4 mRNA and preotein expression during human preimplantation development. Mol Hum Reprod 2005, 11:173-181.
  • [73]Sritanaudomachi H, Sparman M, Tachibana M, Cleper L, Woodward J, Gokhale S, Wolf D, Hennebold J, Hurlbut W, Grompe M, Mitalapov S: CDX2 in the formation of the trophectoderm lineage in primate embryos. Dev Biol 2009, 335:179-187.
  • [74]Guest DJ, Allen WR: Expression of cell-surface antigens and embryonic stem cell pluripotency genes in equine blastocysts. Stem Cells Dev 2007, 16:789-796.
  • [75]Kobolak J, Kiss K, Polgar Z, Mamo S, Rogel-Gaillard C, Tancos Z, Bock I, Baji AG, Tar K, Pirity MK: Promoter analysis of the rabbit POU5F1 gene and its expression in preimplantation stage embryos. BMC Mol Biol 2009, 10:88. BioMed Central Full Text
  • [76]Goosens K, Van-Soom A, Van-Poucke M, Vandaele L, Vandesompele J, Van-Zeveren A, Peelman LJ: Identification and expression analysis of genes associated with bovine blastocyst formation. BMC Dev Biol 2007, 7:64. BioMed Central Full Text
  • [77]Goosens K, Van-Soom A, Van-Zeveren A, Favoreel H, Peelman LJ: Quantification of Fibronectin 1 (FN1) splice variants, including two novel ones, and analysis of integrins as candidate FN1 receptors in bovine preimplantation embryos. BMC Dev Biol 2009, 9:1. BioMed Central Full Text
  • [78]Hesse M, Franz T, Tamai Y, Taketo MM, Magin TM: Targeted deletion of keratins 18 and 19 leads to trophoblast fragility and early embryonic lethality. EMBO J 2009, 19:5060-5070.
  • [79]Yang QE, Fields SD, Zhang K, Ozawa M, Johnson SE, Ealy AD: Fibroblast growth factor 2 promotes primitive endoderm development in bovine blastocyst outgrowths. Biol Reprod 2011, 85:946-953.
  • [80]Sumer H, Liu J, Malaver-Ortega LF, Lim ML, Khodadadi K, Verma PJ: NANOG is a key factor for induction of pluripotency in bovine adult fibroblasts. J Anim Sci 2011, 89:2708-2716.
  • [81]Rogers MB, Hosler BA, Gudas LJ: Specific expression of a retinoic acid-regulated, zinc-finger gene, Rex-1, in preimplantation embryos, trophoblast and spermatocytes. Development 1991, 113:815-824.
  • [82]Rugg-Gunn PJ, Cox BJ, Ralston A, Rossant J: Distinct histone modifications in stem cell lines and tissue lineages from the early mouse embryo. Proc Natl Acad Sci U S A 2010, 107:10783-10790.
  • [83]Hublitz P, Albert M, Peters AH: Mechanisms of transcriptional repression by histone lysine methylation. Int J Dev Biol 2009, 53:335-354.
  • [84]Pichugin A, Le-Bourhis D, Adenot P, Lehmann G, Audouard C, Renard JP, Vignon X, Beaujean N: Dynamics of constitutive heterochromatin: two contrasted kinetics of genome restructuring in early cloned bovine embryos. Reproduction 2010, 139:129-137.
  • [85]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: Mitotic retention of gene expression patterns by the cell fate-determining transcription factor Runx2. Proc Natl Acad Sci U S A 2004, 104:3189-3194.
  • [86]Zaidi SK, Young DW, Montecino M, Van-Wijnen AJ, Stein JL, Lian JB, Stein GS: Bookmarking the genome: maintenance of epigenetic information. J Biol Chem 2011, 286:18355-18361.
  文献评价指标  
  下载次数:0次 浏览次数:8次