Increased MAP kinase inhibition enhances epiblast-specific gene expression in Bovine Blastocysts

Biology of Reproduction

Volumn 91, Issue 2, 2014, Pages

  McLean, Zachariah ^b   Meng, Fanli ^b   Henderson, Harold ^a   Turner, Pavla ^a   Oback, Björn ^a  

^a RUAKURA RESEARCH CENTRE   (New Zealand)

^b NONE

Author keywords

Blastocyst; Embryo culture; Gene expression; Inner cell mass; Trophoblast

Indexed keywords

1 TERT BUTYL 3 [6 (3,5 DIMETHOXYPHENYL) 2 (4 DIETHYLAMINOBUTYLAMINO)PYRIDO[2,3 D]PYRIMIDIN 7 YL]UREA; 4 (4 FLUOROPHENYL) 2 (4 HYDROXYPHENYL) 5 (4 PYRIDYL)IMIDAZOLE; 6 [[2 [[4 (2,4 DICHLOROPHENYL) 5 (4 METHYL 1H IMIDAZOL 2 YL) 2 PYRIMIDINYL]AMINO]ETHYL]AMINO]NICOTINONITRILE; ANTHRA[1,9 CD]PYRAZOL 6(2H) ONE; BIX 02189; FIBROBLAST GROWTH FACTOR 4; MESSENGER RNA; MITOGEN ACTIVATED PROTEIN KINASE; MITOGEN ACTIVATED PROTEIN KINASE 7; MITOGEN ACTIVATED PROTEIN KINASE INHIBITOR; MITOGEN ACTIVATED PROTEIN KINASE KINASE; MITOGEN ACTIVATED PROTEIN KINASE P38; N (2,3 DIHYDROXYPROPOXY) 3,4 DIFLUORO 2 (2 FLUORO 4 IODOANILINO)BENZAMIDE; PLATELET DERIVED GROWTH FACTOR ALPHA RECEPTOR; STRESS ACTIVATED PROTEIN KINASE; TRANSCRIPTION FACTOR NANOG; TRANSCRIPTION FACTOR SOX17; UNCLASSIFIED DRUG; BENZAMIDE DERIVATIVE; DIPHENYLAMINE; PYRIMIDINE DERIVATIVE;

ANIMAL CELL; ARTICLE; BLASTOCYST; CELL LINEAGE; CELL STRUCTURE; CONTROLLED STUDY; DNA METHYLATION; ECTODERM; ENZYME INHIBITION; FEMALE; FERTILIZATION IN VITRO; GENE EXPRESSION PROFILING; GERM LAYER; HYPOBLAST; IN VITRO STUDY; NONHUMAN; POLYMERASE CHAIN REACTION; PRIORITY JOURNAL; QUANTITATIVE ANALYSIS; SIGNAL TRANSDUCTION; ANALOGS AND DERIVATIVES; ANIMAL; ANTAGONISTS AND INHIBITORS; BOVINE; DRUG EFFECTS; EMBRYO CULTURE; EMBRYOLOGY; GENE EXPRESSION REGULATION; GENETICS; METABOLISM;

BOVINAE; MAMMALIA; RATTUS;

ANIMALS; BENZAMIDES; BLASTOCYST; CATTLE; DIPHENYLAMINE; EMBRYO CULTURE TECHNIQUES; GENE EXPRESSION REGULATION, DEVELOPMENTAL; GENE EXPRESSION REGULATION, ENZYMOLOGIC; GERM LAYERS; MITOGEN-ACTIVATED PROTEIN KINASE KINASES; PYRIMIDINES;

EID: 84938929858     PISSN: 00063363     EISSN: 15297268     Source Type: Journal    
DOI: 10.1095/biolreprod.114.120832     Document Type: Article

References (66)

1. Brook FA, Gardner RL. The origin and efficient derivation of embryonic stem cells in the mouse. Proc Natl Acad Sci U S A 1997; 94:5709-5712.
2. 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.
3. 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.
4. 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.
5. Plusa B, Piliszek A, Frankenberg S, Artus J, Hadjantonakis AK. Distinct sequential cell behaviours direct primitive endoderm formation in the mouse blastocyst. Development 2008; 135:3081-3091.
6. 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.
7. Lanner F, Rossant J. The role of FGF/Erk signaling in pluripotent cells. Development 2010; 137:3351-3360.
8. Kunath T, Saba-El-Leil MK, Almousailleakh M, Wray J, Meloche S, Smith A. FGF stimulation of the Erk1/2 signalling cascade triggers transition of pluripotent embryonic stem cells from self-renewal to lineage commitment. Development 2007; 134:2895-2902.
9. Nichols J, Silva J, Roode M, Smith A. Suppression of Erk signalling promotes ground state pluripotency in the mouse embryo. Development 2009; 136:3215-3222.
10. Nichols J, Davidson D, Taga T, Yoshida K, Chambers I, Smith A. Complementary tissue-specific expression of LIF and LIF-receptor mRNAs in early mouse embryogenesis. Mech Dev 1996; 57:123-131.
11. ten Berge D, Kurek D, Blauwkamp T, Koole W, Maas A, Eroglu E, Siu RK, Nusse R. Embryonic stem cells require Wnt proteins to prevent differentiation to epiblast stem cells. Nat Cell Biol 2011; 13:1070-1075.
12. Ying QL, Wray J, Nichols J, Batlle-Morera L, Doble B, Woodgett J, Cohen P, Smith A. The ground state of embryonic stem cell self-renewal. Nature 2008; 453:519-523.
13. Leitch HG, Blair K, Mansfield W, Ayetey H, Humphreys P, Nichols J, Surani MA, Smith A. Embryonic germ cells from mice and rats exhibit properties consistent with a generic pluripotent ground state. Development 2010; 137:2279-2287.
14. Silva J, Barrandon O, Nichols J, Kawaguchi J, Theunissen TW, Smith A. Promotion of reprogramming to ground state pluripotency by signal inhibition. PLoS Biol2008; 6:e253.
15. Buehr M, Meek S, Blair K, Yang J, Ure J, Silva J, McLay R, Hall J, Ying QL, Smith A. Capture of authentic embryonic stem cells from rat blastocysts. Cell 2008; 135:1287-1298.
16. Li P, Tong C, Mehrian-Shai R, Jia L, Wu N, Yan Y, Maxson RE, Schulze EN, Song H, Hsieh CL, Pera MF, Ying QL. Germline competent embryonic stem cells derived from rat blastocysts. Cell 2008; 135:1299-1310.
17. Eakin GS, Behringer RR. Diversity of germ layer and axis formation among mammals. Semin Cell Dev Biol 2004; 15:619-629.
18. Flechon JE, Degrouard J, Flechon B. Gastrulation events in the prestreak pig embryo: ultrastructure and cell markers. Genesis 2004; 38:13-25.
19. Guillomot M, Turbe A, Hue I, Renard JP. Staging of ovine embryos and expression of the T-box genes Brachyury and Eomesodermin around gastrulation. Reproduction 2004; 127:491-501.
20. Hue I, Renard JP, Viebahn C. Brachyury is expressed in gastrulating bovine embryos well ahead of implantation. Dev Genes Evol 2001; 211:157-159.
21. 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.
22. 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.
23. 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.
24. 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.
25. 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.
26. 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.
27. Harris D, Huang B, Oback B. Inhibition of MAP2K and GSK3 signaling promotes bovine blastocyst development and epiblast-associated expression of pluripotency factors. Biol Reprod 2013; 88:74.
28. Verma V, Huang B, Kallingappa PK, Oback B. Dual kinase inhibition promotes pluripotency in finite bovine embryonic cell lines. Stem Cells Dev 2013; 22:1728-1742.
29. Geiss GK, Bumgarner RE, Birditt B, Dahl T, Dowidar N, Dunaway DL, Fell HP, Ferree S, George RD, Grogan T, James JJ, Maysuria M, et al. Direct multiplexed measurement of gene expression with color-coded probe pairs. Nat Biotechnol 2008; 26:317-325.
30. Schurmann A, Wells DN, Oback B. Early zygotes are suitable recipients for bovine somatic nuclear transfer and result in cloned offspring. Reproduction 2006; 132:839-848.
31. Thompson JG, McNaughton C, Gasparrini B, McGowan LT, Tervit HR. Effect of inhibitors and uncouplers of oxidative phosphorylation during compaction and blastulation of bovine embryos cultured in vitro. J Reprod Fertil 2000; 118:47-55.
32. Robertson I, R. Nelson Certification and identification of embryos In:Stringfellow DA, Givens MD (eds.), Manual of the International Embryo Transfer Society: A Procedural Guide and General Information for the Use of Embryo Transfer Technology, Emphasizing Sanitary Precautions, 4th ed. Champaign, IL: International Embryo Transfer Society; 2011:86-105.
33. Oback B, Wiersema AT, Gaynor P, Laible G, Tucker FC, Oliver JE, Miller AL, Troskie HE, Wilson KL, Forsyth JT, Berg MC, Cockrem K, et al. Cloned cattle derived from a novel zona-free embryo reconstruction system. Cloning Stem Cells 2003; 5:3-12.
34. Handyside AH, Hunter S. A rapid procedure for visualising the inner cell mass and trophectoderm nuclei of mouse blastocysts in situ using polynucleotide-specific fluorochromes. J Exp Zool 1984; 231:429-434.
35. Kulkarni MM. Digital multiplexed gene expression analysis using the NanoString nCounter system. Curr Protoc Mol Biol 2011; 94:25B.10.1-25B.10.17.
36. Misica-Turner PM, Oback FC, Eichenlaub M, Wells DN, Oback B. Aggregating embryonic but not somatic nuclear transfer embryos increases cloning efficiency in cattle. Biol Reprod 2007; 76:268-278.
37. Leitch HG, McEwen KR, Turp A, Encheva V, Carroll T, Grabole N, Mansfield W, Nashun B, Knezovich JG, Smith A, Surani MA, Hajkova P. Naive pluripotency is associated with global DNA hypomethylation. Nat Struct Mol Biol 2013; 20:311-316.
38. Yamaji M, Ueda J, Hayashi K, Ohta H, Yabuta Y, Kurimoto K, Nakato R, Yamada Y, Shirahige K, Saitou M. PRDM14 ensures naive pluripotency through dual regulation of signaling and epigenetic pathways in mouse embryonic stem cells. Cell Stem Cell 2013; 12:368-382.
39. Huang B, Li T, Alonso-Gonzalez L, Gorre R, Keatley S, Green A, Turner P, Kallingappa PK, Verma V, Oback BA. Virus-free poly-promoter vector induces pluripotency in quiescent bovine cells under chemically defined conditions of dual kinase inhibition. PLoS ONE 2011; 6:e24501.
40. Kinase Inhibitor Database. Dundee, Scotland: University of Dundee. http://www.kinase-screen.mrc.ac.uk/kinase-inhibitors. Accessed July 2, 2014.
41. Bain J, Plater L, Elliott M, Shpiro N, Hastie CJ, McLauchlan H, Klevernic I, Arthur JS, Alessi DR, Cohen P. The selectivity of protein kinase inhibitors: a further update. Biochem J 2007; 408:297-315.
42. Claveria C, Giovinazzo G, Sierra R, Torres M. Myc-driven endogenous cell competition in the early mammalian embryo. Nature 2013; 500:39-44.
43. Kim J, Chu J, Shen X, Wang J, Orkin SH. An extended transcriptional network for pluripotency of embryonic stem cells. Cell 2008; 132:1049-1061.
44. Nagatomo H, Kagawa S, Kishi Y, Takuma T, Sada A, Yamanaka K, Abe Y, Wada Y, Takahashi M, Kono T, Kawahara M. Transcriptional wiring for establishing cell lineage specification at the blastocyst stage in cattle. Biol Reprod2013; 88:158.
45. 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.
46. Marks H, Kalkan T, Menafra R, Denissov S, Jones K, Hofemeister H, Nichols J, Kranz A, Stewart AF, Smith A, Stunnenberg HG. The transcriptional and epigenomic foundations of ground state pluripotency. Cell 2012; 149:590-604.
47. Betschinger J, Nichols J, Dietmann S, Corrin PD, Paddison PJ, Smith A. Exit from pluripotency is gated by intracellular redistribution of the bHLH transcription factor Tfe3. Cell 2013; 153:335-347.
48. Ullal AV, Peterson V, Agasti SS, Tuang S, Juric D, Castro CM, Weissleder R. Cancer cell profiling by barcoding allows multiplexed protein analysis in fine-needle aspirates. Sci Transl Med 2014; 6:219ra9.
49. Roode M, Blair K, Snell P, Elder K, Marchant S, Smith A, Nichols J. Human hypoblast formation is not dependent on FGF signalling. Dev Biol 2012; 361:358-363.
50. Yuan H, Corbi N, Basilico C, Dailey L. Developmental-specific activity of the FGF-4 enhancer requires the synergistic action of Sox2 and Oct-3. Genes Dev 1995; 9:2635-2645.
51. Chen X, Xu H, Yuan P, Fang F, Huss M, Vega VB, Wong E, Orlov YL, Zhang W, Jiang J, Loh YH, Yeo HC, et al. Integration of external signaling pathways with the core transcriptional network in embryonic stem cells. Cell 2008; 133:1106-1117.
52. 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.
53. Gafni O, Weinberger L, Mansour AA, Manor YS, Chomsky E, Ben-Yosef D, Kalma Y, Viukov S, Maza I, Zviran A, Rais Y, Shipony Z, et al. Derivation of novel human ground state naive pluripotent stem cells. Nature 2013; 504:282-286.
54. Frankenberg S, Gerbe F, Bessonnard S, Belville C, Pouchin P, Bardot O, Chazaud C. Primitive endoderm differentiates via a three-step mechanism involving Nanog and RTK signaling. Dev Cell 2011; 21:1005-1013.
55. Santostefano KE, Hamazaki T, Pardo CE, Kladde MP, Terada N. Fibroblast growth factor receptor 2 homodimerization rapidly reduces transcription of the pluripotency gene Nanog without dissociation of activating transcription factors. J Biol Chem 2012; 287:30507-30517.
56. Hamazaki T, Kehoe SM, Nakano T, Terada N. The Grb2/Mek pathway represses Nanog in murine embryonic stem cells. Mol Cell Biol 2006; 26:7539-7549.
57. Niwa H, Ogawa K, Shimosato D, Adachi K. A parallel circuit of LIF signalling pathways maintains pluripotency of mouse ES cells. Nature 2009; 460:118-122.
58. Festuccia N, Osorno R, Halbritter F, Karwacki-Neisius V, Navarro P, Colby D, Wong F, Yates A, Tomlinson SR, Chambers I. Esrrb is a direct Nanog target gene that can substitute for Nanog function in pluripotent cells. Cell Stem Cell 2012; 11:477-490.
59. Frum T, Halbisen MA, Wang C, Amiri H, Robson P, Ralston A. Oct4 cellautonomously promotes primitive endoderm development in the mouse blastocyst. Dev Cell 2013; 25:610-622.
60. Artus J, Piliszek A, Hadjantonakis AK. The primitive endoderm lineage of the mouse blastocyst: sequential transcription factor activation and regulation of differentiation by Sox17. Dev Biol 2011; 350:393-404.
61. 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.
62. Ramakrishna S, Suresh B, Lim KH, Cha BH, Lee SH, Kim KS, Baek KH. PEST motif sequence regulating human NANOG for proteasomal degradation. Stem Cells Dev 2011; 20:1511-1519.
63. Moretto-Zita M, Jin H, Shen Z, Zhao T, Briggs SP, Xu Y. Phosphorylation stabilizes Nanog by promoting its interaction with Pin1. Proc Natl Acad Sci U S A 2010; 107:13312-13317.
64. Brumbaugh J, Russell JD, Yu P, Westphall MS, Coon JJ, Thomson JA. NANOG is multiply phosphorylated and directly modified by ERK2 and CDK1 in vitro. Stem Cell Reports 2014; 2:18-25.
65. Shimada A, Nakano H, Takahashi T, Imai K, Hashizume K. Isolation and characterization of a bovine blastocyst-derived trophoblastic cell line, BT-1: development of a culture system in the absence of feeder cell. Placenta 2001; 22:652-662.
66. Talbot NC, Caperna TJ, Edwards JL, Garrett W, Wells KD, Ealy AD. Bovine blastocyst-derived trophectoderm and endoderm cell cultures:interferon tau and transferrin expression as respective in vitro markers. Biol Reprod 2000; 62:235-247.