Uncoupled embryonic and extra-embryonic tissues compromise blastocyst development after somatic cell nuclear transfer

PLoS ONE

Volumn 7, Issue 6, 2012, Pages

  Degrelle, Séverine A ^a,b,i   Jaffrezic, Florence ^c   Campion, Evelyne ^a,b   LêCao, Kim Anh ^d,j   Le Bourhis, Daniel ^a,b,e   Richard, Christophe ^f   Rodde, Nathalie ^a,b,d   Fleurot, Renaud ^a,b   Everts, Robin E ^g,k   Lecardonnel, Jérôme ^d   Heyman, Yvan ^a,b   Vignon, Xavier ^a,b   Yang, Xiangzhong ^h   Tian, Xiuchun C ^h   Lewin, Harris A ^g   Renard, Jean Paul ^a,b   Hue, Isabelle ^a,b  

^a INRA Institut National de la Recherche Agronomique   (France)

^b ECOLE NATIONALE VÉTÉRINAIRE D ALFORT   (France)

^c UMR1313 GÉNÉTIQUE ANIMALE ET BIOLOGIE INTÉGRATIVE   (France)

^d CEMAGREF   (France)

^e UNCEIA Union Nationale des Cooperatives d'Elevage et d'Insemination Animale   (France)

^f INRA   (France)

^g UNIVERSITY OF ILLINOIS AT URBANA CHAMPAIGN   (United States)

^h UNIVERSITY OF CONNECTICUT   (United States)

ⁱ INSTITUT COCHIN   (France)

^j UNIVERSITY OF QUEENSLAND   (Australia)

^k SEQUENOM INC   (United States)

more..

Author keywords

[No Author keywords available]

Indexed keywords

CASPASE; COLLAGEN; CYCLIC AMP RESPONSIVE ELEMENT BINDING PROTEIN; CYTOCHROME C; ENDOTHELIN RECEPTOR; EPIDERMAL GROWTH FACTOR RECEPTOR 2; ESTRADIOL; FOCAL ADHESION KINASE; GLYCINE TRANSPORTER 1; HISTONE H3; I KAPPA B KINASE BETA; INSULIN; INTERLEUKIN 2; INTERLEUKIN 6; JANUS KINASE; MITOGEN ACTIVATED PROTEIN KINASE; NICOTINAMIDE ADENINE DINUCLEOTIDE ADENOSINE DIPHOSPHATE RIBOSYLTRANSFERASE 2; PHOSPHATIDYLINOSITOL 4,5 BISPHOSPHATE; PHOSPHOINOSITIDE DEPENDENT PROTEIN KINASE 1; PROTEIN CDC42; PROTEIN MSH3; SODIUM GLUCOSE COTRANSPORTER 2; SYNAPTOTAGMIN II; TESTOSTERONE; TRANSCRIPTION FACTOR E2F; TRANSFORMING GROWTH FACTOR BETA; TRANSFORMING GROWTH FACTOR BETA1; TUMOR NECROSIS FACTOR RECEPTOR ASSOCIATED FACTOR 1; ZINC FINGER PROTEIN; PRIMER DNA;

ANIMAL CELL; ARTICLE; BLASTOCYST; CELL DIFFERENTIATION; CELL ELONGATION; CELL NUCLEUS TRANSPLANTATION; CELL STRUCTURE; CONTROLLED STUDY; COW; ECTODERM; EMBRYO; EMBRYO DEATH; EMBRYO PATTERN FORMATION; EMBRYO TRANSFER; EMBRYONAL TISSUE; FIBROBLAST; GASTRULATION; GENE EXPRESSION; GENE FUNCTION; IN SITU HYBRIDIZATION; NIDATION; NONHUMAN; NUCLEAR REPROGRAMMING; NUCLEOTIDE SEQUENCE; PLASTICITY; RNA EXTRACTION; SOMATIC CELL; ANIMAL; ANIMAL DISEASE; CASE CONTROL STUDY; CATTLE; CELL COMMUNICATION; COMPARATIVE STUDY; EMBRYO DEVELOPMENT; EMBRYO MEMBRANE; FEMALE; GENE EXPRESSION REGULATION; GENE REGULATORY NETWORK; GENETICS; PATHOPHYSIOLOGY; PHYSIOLOGY; PREGNANCY; REAL TIME POLYMERASE CHAIN REACTION; SCANNING ELECTRON MICROSCOPY; SEX DETERMINATION; ULTRASTRUCTURE;

ANIMALS; BLASTOCYST; CASE-CONTROL STUDIES; CATTLE; CELL COMMUNICATION; CELL DIFFERENTIATION; DNA PRIMERS; EMBRYO TRANSFER; EMBRYONIC DEVELOPMENT; EXTRAEMBRYONIC MEMBRANES; FEMALE; GENE EXPRESSION REGULATION, DEVELOPMENTAL; GENE REGULATORY NETWORKS; IN SITU HYBRIDIZATION; MICROSCOPY, ELECTRON, SCANNING; NUCLEAR TRANSFER TECHNIQUES; PREGNANCY; REAL-TIME POLYMERASE CHAIN REACTION; SEX DETERMINATION ANALYSIS;

EID: 84862001763     PISSN: None     EISSN: 19326203     Source Type: Journal    
DOI: 10.1371/journal.pone.0038309     Document Type: Article

References (84)

1. Jullien J, Pasque V, Halley-Stott RP, Miyamoto K, Gurdon JB, (2011) Mechanisms of nuclear reprogramming by eggs and oocytes: a deterministic process? Nat Rev Mol Cell Biol 12: 453-459.
2. Hanna JH, Saha K, Jaenisch R, (2010) Pluripotency and cellular reprogramming: facts, hypotheses, unresolved issues. Cell 143: 508-525.
3. Hochedlinger K, Plath K, (2009) Epigenetic reprogramming and induced pluripotency. Development 136: 509-523.
4. Maruotti J, Jouneau A, Renard JP, (2010) Faithful reprogramming to pluripotency in mammals- what does nuclear transfer teach us? Int J Dev Biol 54: 1609-1621.
5. Gaspar-Maia A, Alajem A, Meshorer E, Ramalho-Santos M, (2011) Open chromatin in pluripotency and reprogramming. Nat Rev Mol Cell Biol 12: 36-47.
6. Yang X, Smith SL, Tian XC, Lewin HA, Renard JP, et al. (2007) Nuclear reprogramming of cloned embryos and its implications for therapeutic cloning. Nat Genet 39: 295-302.
7. Greenstein JS, Murray RW, Foley RC, (1958) Observations on the morphogenesis and histochemistry of the bovine preattachment placenta between 16 and 33 days of gestation. Anat Rec 132: 321-341.
8. Heyman Y, (2005) Nuclear transfer: a new tool for reproductive biotechnology in cattle. Reprod Nutr Dev 45: 353-361.
9. King WA, Coppola G, Alexander B, Mastromonaco G, Perrault S, et al. (2006) The impact of chromosomal alteration on embryo development. Theriogenology 65: 166-177.
10. Loi P, Beaujean N, Khochbin S, Fulka J Jr, Ptak G, (2008) Asymmetric nuclear reprogramming in somatic cell nuclear transfer? Bioessays 30: 66-74.
11. Niemann H, Tian XC, King WA, Lee RS, (2008) Epigenetic reprogramming in embryonic and foetal development upon somatic cell nuclear transfer cloning. Reproduction 135: 151-163.
12. Tian XC, Kubota C, Enright B, Yang X, (2003) Cloning animals by somatic cell nuclear transfer-biological factors. Reprod Biol Endocrinol 1: 98.
13. Whitworth KM, Prather RS, (2010) Somatic cell nuclear transfer efficiency: how can it be improved through nuclear remodeling and reprogramming? Mol Reprod Dev 77: 1001-1015.
14. Wilmut I, (2006) Are there any normal clones? Methods Mol Biol 348: 307-318.
15. Zhao J, Whyte J, Prather RS, (2010) Effect of epigenetic regulation during swine embryogenesis and on cloning by nuclear transfer. Cell Tissue Res 341: 13-21.
16. Berg DK, van Leeuwen J, Beaumont S, Berg M, Pfeffer PL, (2010) Embryo loss in cattle between Days 7 and 16 of pregnancy. Theriogenology 73: 250-260.
17. Kato Y, Li X, Amarnath D, Ushizawa K, Hashizume K, et al. (2007) Comparative gene expression analysis of bovine nuclear-transferred embryos with different developmental potential by cDNA microarray and real-time PCR to determine genes that might reflect calf normality. Cloning Stem Cells 9: 495-511.
18. Lucifero D, Suzuki J, Bordignon V, Martel J, Vigneault C, et al. (2006) Bovine SNRPN methylation imprint in oocytes and day 17 in vitro-produced and somatic cell nuclear transfer embryos. Biol Reprod 75: 531-538.
19. Rodriguez-Alvarez L, Sharbati J, Sharbati S, Cox JF, Einspanier R, et al. (2010) Differential gene expression in bovine elongated (Day 17) embryos produced by somatic cell nucleus transfer and in vitro fertilization. Theriogenology 74: 45-59.
20. Suzuki J Jr, Therrien J, Filion F, Lefebvre R, Goff AK, et al. (2011) Loss of methylation at H19 DMD is associated with biallelic expression and reduced development in cattle derived by somatic cell nuclear transfer. Biol Reprod 84: 947-956.
21. Heyman Y, Camous S, Fevre J, Meziou W, Martal J, (1984) Maintenance of the corpus luteum after uterine transfer of trophoblastic vesicles to cyclic cows and ewes. J Reprod Fertil 70: 533-540.
22. Alexopoulos NI, Maddox-Hyttel P, Tveden-Nyborg P, D'Cruz NT, Tecirlioglu TR, et al. (2008) Developmental disparity between in vitro-produced and somatic cell nuclear transfer bovine days 14 and 21 embryos: implications for embryonic loss. Reproduction 136: 433-445.
23. Degrelle SA, Campion E, Cabau C, Piumi F, Reinaud P, et al. (2005) Molecular evidence for a critical period in mural trophoblast development in bovine blastocysts. Dev Biol 288: 448-460.
24. Degrelle SA, Le Cao KA, Heyman Y, Everts RE, Campion E, et al. (2011) A small set of extra-embryonic genes defines a new landmark for bovine embryo staging. Reproduction 141: 79-89.
25. Betteridge K, Flechon J, (1988) The anatomy and physiology of pre-attachment bovine embryos. Theriogenology 29: 155-187.
26. Hue I, Degrelle SA, Campion E, Renard JP, (2007) Gene expression in elongating and gastrulating embryos from ruminants. Soc Reprod Fertil (Suppl 64): 365-377.
27. Maddox-Hyttel P, Alexopoulos NI, Vajta G, Lewis I, Rogers P, et al. (2003) Immunohistochemical and ultrastructural characterization of the initial post-hatching development of bovine embryos. Reproduction 125: 607-623.
28. Flechon JE, Degrouard J, Flechon B, (2004) Gastrulation events in the prestreak pig embryo: ultrastructure and cell markers. Genesis 38: 13-25.
29. Guillomot M, (1995) Cellular interactions during implantation in domestic ruminants. J Reprod Fertil (Suppl 49): 39-51.
30. Flechon JE, Flechon B, Degrouard J, Guillomot M, (2007) Cellular features of the extra-embryonic endoderm during elongation in the ovine conceptus. Genesis 45: 709-715.
31. Guillomot M, Turbe A, Hue I, Renard JP, (2004) Staging of ovine embryos and expression of the T-box genes Brachyury and Eomesodermin around gastrulation. Reproduction 127: 491-501.
32. Bui LC, Evsikov AV, Khan DR, Archilla C, Peynot N, et al. (2009) Retrotransposon expression as a defining event of genome reprogramming in fertilized and cloned bovine embryos. Reproduction 138: 289-299.
33. Renard JP, Maruotti J, Jouneau A, Vignon X, (2007) Nuclear reprogramming and pluripotency of embryonic cells: Application to the isolation of embryonic stem cells in farm animals. Theriogenology 68 (Suppl 1): S196-205.
34. Ameen N, Apodaca G, (2007) Defective CFTR apical endocytosis and enterocyte brush border in myosin VI-deficient mice. Traffic 8: 998-1006.
35. Longo-Guess CM, Gagnon LH, Cook SA, Wu J, Zheng QY, et al. (2005) A missense mutation in the previously undescribed gene Tmhs underlies deafness in hurry-scurry (hscy) mice. Proc Natl Acad Sci U S A 102: 7894-7899.
36. Self T, Sobe T, Copeland NG, Jenkins NA, Avraham KB, et al. (1999) Role of myosin VI in the differentiation of cochlear hair cells. Dev Biol 214: 331-341.
37. Nadra K, Anghel SI, Joye E, Tan NS, Basu-Modak S, et al. (2006) Differentiation of trophoblast giant cells and their metabolic functions are dependent on peroxisome proliferator-activated receptor beta/delta. Mol Cell Biol 26: 3266-3281.
38. Hue I, Renard JP, Viebahn C, (2001) Brachyury is expressed in gastrulating bovine embryos well ahead of implantation. Dev Genes Evol 211: 157-159.
39. Martin L, Besch-Williford C, Lai L, Cheong HT, Im GS, et al. (2007) Morphologic and histologic comparisons between in vivo and nuclear transfer derived porcine embryos. Mol Reprod Dev 74: 952-960.
40. Rodriguez-Alvarez L, Cox J, Tovar H, Einspanier R, Castro FO, (2010) Changes in the expression of pluripotency-associated genes during preimplantation and peri-implantation stages in bovine cloned and in vitro produced embryos. Zygote 18: 269-279.
41. Tveden-Nyborg P, Peura TT, Hartwich KM, Walker SK, Maddox-Hyttel P, (2005) Morphological characterization of pre- and peri-implantation in vitro cultured, somatic cell nuclear transfer and in vivo derived ovine embryos. Reproduction 130: 681-694.
42. Hasler JF, Henderson WB, Hurtgen PJ, Jin ZQ, McCauley AD, et al. (1995) Production, freezing and transfer of bovine IVF embryos and subsequent calving results. Theriogenology 43: 141-152.
43. Reichenbach HD, Liebrich J, Berg U, Brem G, (1992) Pregnancy rates and births after unilateral or bilateral transfer of bovine embryos produced in vitro. J Reprod Fertil 95: 363-370.
44. Chesne P, Adenot PG, Viglietta C, Baratte M, Boulanger L, et al. (2002) Cloned rabbits produced by nuclear transfer from adult somatic cells. Nat Biotechnol 20: 366-369.
45. Bauersachs S, Ulbrich SE, Zakhartchenko V, Minten M, Reichenbach M, et al. (2009) The endometrium responds differently to cloned versus fertilized embryos. Proc Natl Acad Sci U S A 106: 5681-5686.
46. Mansouri-Attia N, Sandra O, Aubert J, Degrelle S, Everts RE, et al. (2009) Endometrium as an early sensor of in vitro embryo manipulation technologies. Proc Natl Acad Sci U S A 106: 5687-5692.
47. Bertocchini F, Stern CD, (2002) The hypoblast of the chick embryo positions the primitive streak by antagonizing nodal signaling. Dev Cell 3: 735-744.
48. Idkowiak J, Weisheit G, Plitzner J, Viebahn C, (2004) Hypoblast controls mesoderm generation and axial patterning in the gastrulating rabbit embryo. Dev Genes Evol 214: 591-605.
49. Perea-Gomez A, Vella FD, Shawlot W, Oulad-Abdelghani M, Chazaud C, et al. (2002) Nodal antagonists in the anterior visceral endoderm prevent the formation of multiple primitive streaks. Dev Cell 3: 745-756.
50. Jouneau A, Zhou Q, Camus A, Brochard V, Maulny L, et al. (2006) Developmental abnormalities of NT mouse embryos appear early after implantation. Development 133: 1597-1607.
51. Adams HA, Southey BR, Everts RE, Marjani SL, Tian CX, et al. (2011) Transferase activity function and system development process are critical in cattle embryo development. Funct Integr Genomics 11: 139-150.
52. Maruotti J, Muñoz M, Degrelle SA, Gómez E, Louet C, et al. (2012) Efficient derivation of bovine embryonic stem cells needs more than active core pluripotency factors. Mol Reprod Dev In press.
53. Alberio R, Croxall N, Allegrucci C, (2010) Pig epiblast stem cells depend on activin/nodal signaling for pluripotency and self-renewal. Stem Cells Dev 19: 1627-1636.
54. Maruotti J, Dai XP, Brochard V, Jouneau L, Liu J, et al. (2010) Nuclear transfer-derived epiblast stem cells are transcriptionally and epigenetically distinguishable from their fertilized-derived counterparts. Stem Cells 28: 743-752.
55. Sawai K, (2009) Studies on gene expression in bovine embryos derived from somatic cell nuclear transfer. J Reprod Dev 55: 11-16.
56. Sawai K, Kageyama S, Moriyasu S, Hirayama H, Minamihashi A, et al. (2007) Changes in the mRNA transcripts of insulin-like growth factor ligand, receptors and binding proteins in bovine blastocysts and elongated embryos derived from somatic cell nuclear transfer. J Reprod Dev 53: 77-86.
57. Fujii T, Moriyasu S, Hirayama H, Hashizume T, Sawai K, (2010) 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 12: 617-625.
58. Smith CS, Berg DK, Berg M, Pfeffer PL, (2010) Nuclear transfer-specific defects are not apparent during the second week of embryogenesis in cattle. Cell Reprogram 12: 699-707.
59. Kim JY, Burghardt RC, Wu G, Johnson GA, Spencer TE, et al. (2011) Select nutrients in the ovine uterine lumen. VII. Effects of arginine, leucine, glutamine, and glucose on trophectoderm cell signaling, proliferation, and migration. Biol Reprod 84: 62-69.
60. Rozario T, Dzamba B, Weber GF, Davidson LA, DeSimone DW, (2009) The physical state of fibronectin matrix differentially regulates morphogenetic movements in vivo. Dev Biol 327: 386-398.
61. Miki H, Wakisaka N, Inoue K, Ogonuki N, Mori M, et al. (2009) Embryonic rather than extraembryonic tissues have more impact on the development of placental hyperplasia in cloned mice. Placenta 30: 543-546.
62. Soares MJ, Asanoma K, (2009) Trophoblast stem cells derived from nuclear transfer embryos: phenotypically unique, bad neighbors, or poor communicators? Proc Natl Acad Sci U S A 106: 16014-16015.
63. Chavatte-Palmer P, Camous S, Jammes H, Le Cleac'h N, Guillomot M, et al. (2011) Review: Placental perturbations induce the developmental abnormalities often observed in bovine somatic cell nuclear transfer. Placenta 2011 13.
64. Schuettengruber B, Cavalli G, (2009) Recruitment of polycomb group complexes and their role in the dynamic regulation of cell fate choice. Development 136: 3531-3542.
65. Fitzpatrick E, Johnson MP, Dyer TD, Forrest S, Elliott K, et al. (2009) Genetic association of the activin A receptor gene (ACVR2A) and pre-eclampsia. Mol Hum Reprod 15: 195-204.
66. Roten LT, Johnson MP, Forsmo S, Fitzpatrick E, Dyer TD, et al. (2009) Association between the candidate susceptibility gene ACVR2A on chromosome 2q22 and pre-eclampsia in a large Norwegian population-based study (the HUNT study). Eur J Hum Genet 17: 250-257.
67. van Dijk M, Oudejans CB, (2011) STOX1: Key Player in Trophoblast Dysfunction Underlying Early Onset Preeclampsia with Growth Retardation. J Pregnancy 2011 521826.
68. Takahashi K, Yamanaka S, (2006) Induction of pluripotent stem cells from mouse embryonic and adult fibroblast cultures by defined factors. Cell 126: 663-676.
69. Wernig M, Meissner A, Foreman R, Brambrink T, Ku M, et al. (2007) In vitro reprogramming of fibroblasts into a pluripotent ES-cell-like state. Nature 448: 318-324.
70. Yu F, Li J, Chen H, Fu J, Ray S, et al. (2011) Kruppel-like factor 4 (KLF4) is required for maintenance of breast cancer stem cells and for cell migration and invasion. Oncogene 30: 2161-2172.
71. Akaogi K, Nakajima Y, Ito I, Kawasaki S, Oie SH, et al. (2009) KLF4 suppresses estrogen-dependent breast cancer growth by inhibiting the transcriptional activity of ERalpha. Oncogene 28: 2894-2902.
72. Kee HJ, Kook H, (2009) Kruppel-like factor 4 mediates histone deacetylase inhibitor-induced prevention of cardiac hypertrophy. J Mol Cell Cardiol 47: 770-780.
73. Khan DR, Dube D, Gall L, Peynot N, Ruffini S, et al. (2012) Expression of Pluripotency Master Regulators during Two Key Developmental Transitions: EGA and Early Lineage Specification in the Bovine Embryo. PLoS One 7: e34110.
74. Dai X, Hao J, Hou XJ, Hai T, Fan Y, et al. (2010) Somatic nucleus reprogramming is significantly improved by m-carboxycinnamic acid bishydroxamide, a histone deacetylase inhibitor. J Biol Chem 285: 31002-31010.
75. Hai T, Hao J, Wang L, Jouneau A, Zhou Q, (2011) Pluripotency maintenance in mouse somatic cell nuclear transfer embryos and its improvement by treatment with the histone deacetylase inhibitor TSA. Cell Reprogram 13: 47-56.
76. Matoba S, Inoue K, Kohda T, Sugimoto M, Mizutani E, et al. (2011) RNAi-mediated knockdown of Xist can rescue the impaired postimplantation development of cloned mouse embryos. Proc Natl Acad Sci U S A 108: 20621-20626.
77. Vignon X, Le Bourhis D, Adenot P, Marchal J, Lavergne Y, et al. (2000) Production of bovine embryos by nuclear transfer of adult skin fibroblasts: the effect of serum starvation. Theriogenology 53: 245.
78. Alves BC, Hossepian de Lima VF, Teixeira CM, Moreira-Filho CA, (2003) Use of primers derived from a new sequence of the bovine Y chromosome for sexing Bos taurus and Bos indicus embryos. Theriogenology 59: 1415-1419.
79. Degrelle SA, Hennequet-Antier C, Chiapello H, Piot-Kaminski K, Piumi F, et al. (2008) Amplification biases: possible differences among deviating gene expressions. BMC Genomics 9: 46.
80. Everts RE, Band MR, Liu ZL, Kumar CG, Liu L, et al. (2005) A 7872 cDNA microarray and its use in bovine functional genomics. Vet Immunol Immunopathol 105: 235-245.
81. Jaffrezic F, Marot G, Degrelle S, Hue I, Foulley JL, (2007) A structural mixed model for variances in differential gene expression studies. Genet Res 89: 19-25.
82. Degrelle SA, Murthi P, Evain-Brion D, Fournier T, Hue I, (2011) Expression and localization of DLX3, PPARG and SP1 in bovine trophoblast during binucleated cell differentiation. Placenta 32: 917-920.
83. 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.
84. Ushizawa K, Takahashi T, Hosoe M, Kizaki K, Hashizume K, (2010) Cloning and expression of SOLD1 in ovine and caprine placenta, and their expected roles during the development of placentomes. BMC Dev Biol 10: 9.