Transcriptional Wiring for Establishing Cell Lineage Specification at the Blastocyst Stage in Cattle1

Biology of Reproduction

Volumn 88, Issue 6, 2013, Pages

  Nagatomo, Hiroaki ^a   Kagawa, Shinjiro ^a   Kishi, Yasunori ^b   Takuma, Tetsuya ^c   Sada, Ayari ^a   Yamanaka, Ken ichi ^d   Abe, Yasuyuki ^e   Wada, Yasuhiko ^d   Takahashi, Masashi ^a   Kono, Tomohiro ^b   Kawahara, Manabu ^a  

^a HOKKAIDO UNIVERSITY   (Japan)

^b TOKYO UNIVERSITY OF AGRICULTURE   (Japan)

^c Saga Prefectural Livestock Experiment Station   (Japan)

^d SAGA UNIVERSITY   (Japan)

^e YAMAGATA UNIVERSITY   (Japan)

Author keywords

Blastocyst; Bovine; Cell lineage specification; Gene expression

Indexed keywords

ANIMAL CELL; ARTICLE; BLASTOCYST; CATTLE; CELL FATE; CELL LINEAGE; ECTODERM; EMBRYO; EMBRYO DEVELOPMENT; FEMALE; GENE EXPRESSION; IN SITU HYBRIDIZATION; INNER CELL MASS; MALE; NONHUMAN; PREIMPLANTATION EMBRYO; PRIORITY JOURNAL; REAL TIME POLYMERASE CHAIN REACTION; TRANSCRIPTOMICS; TROPHECTODERM;

BLASTOCYST; BOVINE; CELL LINEAGE SPECIFICATION; GENE EXPRESSION;

ANIMALS; BLASTOCYST; BLASTOCYST INNER CELL MASS; CATTLE; CELL DIFFERENTIATION; CELL LINEAGE; EMBRYO CULTURE TECHNIQUES; EMBRYONIC DEVELOPMENT; FEMALE; FERTILIZATION IN VITRO; GENE EXPRESSION REGULATION, DEVELOPMENTAL; GENE REGULATORY NETWORKS;

EID: 84882279742     PISSN: 00063363     EISSN: 15297268     Source Type: Journal    
DOI: 10.1095/biolreprod.113.108993     Document Type: Article

References (60)

1. Palmieri SL, Peter W, Hess H, Scholer HR. Oct-4 transcription factor is differentially expressed in the mouse embryo during establishment of the first two extraembryonic cell lineages involved in implantation. Dev Biol 1994; 166:259-267.
2. Rossant J, Chazaud C, Yamanaka Y. Lineage allocation and asymmetries in the early mouse embryo. Philos Trans R Soc Lond B Biol Sci 2003; 358:1341-1348. Discussion 1349.
3. 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.
4. 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.
5. 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.
6. 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.
7. 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.
8. 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.
9. 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.
10. Chazaud C, Yamanaka Y, Pawson T, Rossant J. Early lineage segregation between epiblast and primitive endoderm in mouse blastocysts through the Grb2-MAPK pathway. Dev Cell 2006; 10:615-624.
11. 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.
12. Jedrusik A, Parfitt DE, Guo G, Skamagki M, Grabarek JB, Johnson MH, Robson P, Zernicka-Goetz M. Role of Cdx2 and cell polarity in cell allocation and specification of trophectoderm and inner cell mass in the mouse embryo. Genes Dev 2008; 22:2692-2706.
13. Tanaka SS, Matsui Y. Developmentally regulated expression of mil-1 and mil-2, mouse interferon-induced transmembrane protein like genes, during formation and differentiation of primordial germ cells. Mech Dev 2002; 119(suppl 1):S261-S267.
14. Winger Q, Huang J, Auman HJ, Lewandoski M, Williams T. Analysis of transcription factor AP-2 expression and function during mouse preimplantation development. Biol Reprod 2006; 75:324-333.
15. Yoshikawa T, Piao Y, Zhong J, Matoba R, Carter MG, Wang Y, Goldberg I, Ko MS. High-throughput screen for genes predominantly expressed in the ICM of mouse blastocysts by whole mount in situ hybridization. Gene Expr Patterns 2006; 6:213-224.
16. Berg DK, Smith CS, Pearton DJ, Wells DN, Broadhurst R, Donnison M, Pfeffer PL. Trophectoderm lineage determination in cattle. Dev Cell 2011; 20:244-255.
17. Aksu DA, Agca C, Aksu S, Bagis H, Akkoc T, Caputcu AT, Arat S, Taskin AC, Kizil SH, Karasahin T, Akyol N, Satilmis M, et al. Gene expression profiles of vitrified in vitro- and in vivo-derived bovine blastocysts. Mol Reprod Dev 2012; 79:613-625.
18. Ozawa M, Sakatani M, Yao J, Shanker S, Yu F, Yamashita R, Wakabayashi S, Nakai K, Dobbs KB, Sudano MJ, Farmerie WG, Hansen PJ. Global gene expression of the inner cell mass and trophectoderm of the bovine blastocyst. BMC Dev Biol 2012; 12:33.
19. Aono A, Nagatomo H, Takuma T, Nonaka R, Ono Y, Wada Y, Abe Y, Takahashi M, Watanabe T, Kawahara M. Dynamics of intracellular phospholipid membrane organization during oocyte maturation and successful vitrification of immature oocytes retrieved by ovum pick-up in cattle. Theriogenology 2013; 79:1146-1152. e1.
20. Brackett BG, Oliphant G. Capacitation of rabbit spermatozoa in vitro. Biol Reprod 1975; 12:260-274.
21. Thouas GA, Korfiatis NA, French AJ, Jones GM, Trounson AO. Simplified technique for differential staining of inner cell mass and trophectoderm cells of mouse and bovine blastocysts. Reprod Biomed Online 2001; 3:25-29.
22. Fukuda A, Cao F, Morita S, Yamada K, Jincho Y, Tane S, Sotomaru Y, Kono T. Identification of inappropriately reprogrammed genes by largescale transcriptome analysis of individual cloned mouse blastocysts. PLoS One 2010; 5:e11274.
23. Al-Shahrour F, Diaz-Uriarte R, Dopazo J. FatiGO: a web tool for finding significant associations of Gene Ontology terms with groups of genes. Bioinformatics 2004; 20:578-580.
24. Fujii T, Moriyasu S, Hirayama H, Hashizume T, Sawai K. Aberrant expression patterns of genes involved in segregation of inner cell mass and trophectoderm lineages in bovine embryos derived from somatic cell nuclear transfer. Cell Reprogram 2010; 12:617-625.
25. 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.
26. Cauffman G, Van de Velde H, Liebaers I, Van Steirteghem A. Oct-4 mRNA and protein expression during human preimplantation development. Mol Hum Reprod 2005; 11:173-181.
27. 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.
28. Kuijk EW, van Tol LT, Van de Velde H, Wubbolts R, Welling M, Geijsen N, Roelen BA. The roles of FGF and MAP kinase signaling in the segregation of the epiblast and hypoblast cell lineages in bovine and human embryos. Development 2012; 139:871-882.
29. Munoz M, Rodriguez A, De Frutos C, Caamano JN, Diez C, Facal N, Gomez E. Conventional pluripotency markers are unspecific for bovine embryonic-derived cell-lines. Theriogenology 2008; 69:1159-1164.
30. 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.
31. Kirchhof N, Carnwath JW, Lemme E, Anastassiadis K, Scholer H, Niemann H. Expression pattern of Oct-4 in preimplantation embryos of different species. Biol Reprod 2000; 63:1698-1705.
32. 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, et al. Molecular cloning, genetic mapping, and developmental expression of bovine POU5F1. Biol Reprod 1999; 60:1093-1103.
33. Khan DR, Dube 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:e34110.
34. Duncan SA, Manova K, Chen WS, Hoodless P, Weinstein DC, Bachvarova RF, Darnell JE Jr. Expression of transcription factor HNF-4 in the extraembryonic endoderm, gut, and nephrogenic tissue of the developing mouse embryo: HNF-4 is a marker for primary endoderm in the implanting blastocyst. Proc Natl Acad Sci U S A 1994; 91:7598-7602.
35. LeGouy E, Thompson EM, Muchardt C, Renard JP. Differential preimplantation regulation of two mouse homologues of the yeast SWI2 protein. Dev Dyn 1998; 212:38-48.
36. Morrisey EE, Tang Z, Sigrist K, Lu MM, Jiang F, Ip HS, Parmacek MS. GATA6 regulates HNF4 and is required for differentiation of visceral endoderm in the mouse embryo. Genes Dev 1998; 12:3579-3590.
37. Keramari M, Razavi J, Ingman KA, Patsch C, Edenhofer F, Ward CM, Kimber SJ. Sox2 is essential for formation of trophectoderm in the preimplantation embryo. PLoS One 2010; 5:e13952.
38. Guo G, Huss M, Tong GQ, Wang C, Li Sun L, Clarke ND, Robson P. Resolution of cell fate decisions revealed by single-cell gene expression analysis from zygote to blastocyst. Dev Cell 2010; 18:675-685.
39. Richardson RT, Alekseev OM, Grossman G, Widgren EE, Thresher R, Wagner EJ, Sullivan KD, Marzluff WF, O'Rand MG. Nuclear autoantigenic sperm protein (NASP), a linker histone chaperone that is required for cell proliferation. J Biol Chem 2006; 281:21526-21534.
40. Niswander L, Martin GR. Fgf-4 expression during gastrulation, myogenesis, limb and tooth development in the mouse. Development 1992; 114: 755-768.
41. Thomas T, Voss AK, Petrou P, Gruss P. The murine gene, Traube, is essential for the growth of preimplantation embryos. Dev Biol 2000; 227: 324-342.
42. 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.
43. Feldman B, Poueymirou W, Papaioannou VE, DeChiara TM, Goldfarb M. Requirement of FGF-4 for postimplantation mouse development. Science 1995; 267:246-249.
44. Tanaka S, Kunath T, Hadjantonakis AK, Nagy A, Rossant J. Promotion of trophoblast stem cell proliferation by FGF4. Science 1998; 282: 2072-2075.
45. Haffner-Krausz R, Gorivodsky M, Chen Y, Lonai P. Expression of Fgfr2 in the early mouse embryo indicates its involvement in preimplantation development. Mech Dev 1999; 85:167-172.
46. Arman E, Haffner-Krausz R, Chen Y, Heath JK, Lonai P. Targeted disruption of fibroblast growth factor (FGF) receptor 2 suggests a role for FGF signaling in pregastrulation mammalian development. Proc Natl Acad Sci U S A 1998; 95:5082-5087.
47. Grigor'eva EV, Shevchenko AI, Mazurok NA, Elisaphenko EA, Zhelezova AI, Shilov AG, Dyban PA, Dyban AP, Noniashvili EM, Slobodyanyuk SY, Nesterova TB, Brockdorff N, et al. FGF4 independent derivation of trophoblast stem cells from the common vole. PLoS One 2009; 4: e7161
48. Kim MS, Kim CJ, Jung HS, Seo MR, Juhnn YS, Shin HY, Ahn HS, Thiele CJ, Chi JG. Fibroblast growth factor 2 induces differentiation and apoptosis of Askin tumour cells. J Pathol 2004; 202:103-112.
49. Shimizu T, Ishikawa T, Iwai S, Ueki A, Sugihara E, Onishi N, Kuninaka S, Miyamoto T, Toyama Y, Ijiri H, Mori H, Matsuzaki Y, et al. Fibroblast growth factor-2 is an important factor that maintains cellular immaturity and contributes to aggressiveness of osteosarcoma. Mol Cancer Res 2012; 10:454-468.
50. Taniguchi F, Harada T, Yoshida S, Iwabe T, Onohara Y, Tanikawa M, Terakawa N. Paracrine effects of bFGF and KGF on the process of mouse blastocyst implantation. Mol Reprod Dev 1998; 50:54-62.
51. Bai H, Sakurai T, Kim MS, Muroi Y, Ideta A, Aoyagi Y, Nakajima H, Takahashi M, Nagaoka K, Imakawa K. Involvement of GATA transcription factors in the regulation of endogenous bovine interferontau gene transcription. Mol Reprod Dev 2009; 76:1143-1152.
52. Lifsey BJ Jr, Baumbach GA, Godkin JD. Isolation, characterization and immunocytochemical localization of bovine trophoblast protein-1. Biol Reprod 1989; 40:343-352.
53. Quinn LM, Latham SE, Kalionis B. A distal-less class homeobox gene, DLX4, is a candidate for regulating epithelial-mesenchymal cell interactions in the human placenta. Placenta 1998; 19:87-93.
54. Coubrough ML, Bendall AJ. Impaired nuclear import of mammalian Dlx4 proteins as a consequence of rapid sequence divergence. Exp Cell Res 2006; 312:3880-3891.
55. Kim JH, Wilder PJ, Hou J, Nowling T, Rizzino A. Activation of the murine type II transforming growth factor-beta receptor gene: upregulation and function of the transcription factor Elf-3/Ert/Esx/Ese-1. J Biol Chem 2002; 277:17520-17530.
56. Koinuma D, Tsutsumi S, Kamimura N, Taniguchi H, Miyazawa K, Sunamura M, Imamura T, Miyazono K, Aburatani H. Chromatin immunoprecipitation on microarray analysis of Smad2/3 binding sites reveals roles of ETS1 and TFAP2A in transforming growth factor beta signaling. Mol Cell Biol 2009; 29:172-186.
57. Miyazaki K, Inoue S, Yamada K, Watanabe M, Liu Q, Watanabe T, Adachi MT, Tanaka Y, Kitajima S. Differential usage of alternate promoters of the human stress response gene ATF3 in stress response and cancer cells. Nucleic Acids Res 2009; 37:1438-1451.
58. Fujii M, Nakanishi H, Toyoda T, Tanaka I, Kondo Y, Osada H, Sekido Y. Convergent signaling in the regulation of connective tissue growth factor in malignant mesothelioma: TGFbeta signaling and defects in the Hippo signaling cascade. Cell Cycle 2012; 11:3373-3379.
59. Moussad EE, Rageh MA, Wilson AK, Geisert RD, Brigstock DR. Temporal and spatial expression of connective tissue growth factor (CCN2; CTGF) and transforming growth factor beta type 1 (TGF-beta1) at the utero-placental interface during early pregnancy in the pig. Mol Pathol 2002; 55:186-192.
60. Nishioka N, Inoue K, Adachi K, Kiyonari H, Ota M, Ralston A, Yabuta N, Hirahara S, Stephenson RO, Ogonuki N, Makita R, Kurihara H, et al. The Hippo signaling pathway components Lats and Yap pattern Tead4 activity to distinguish mouse trophectoderm from inner cell mass. Dev Cell 2009; 16:398-410.