Timing of first embryonic cleavage is a positive indicator of the in vitro developmental potential of porcine embryos derived from in vitro fertilization, somatic cell nuclear transfer and parthenogenesis

Molecular Reproduction and Development

Volumn 79, Issue 3, 2012, Pages 197-207

  Isom, S Clay ^a   Li, Rong Feng ^a,b   Whitworth, Kristin M ^a   Prather, Randall S ^a  

^a UNIVERSITY OF MISSOURI   (United States)

^b NANJING MEDICAL UNIVERSITY   (China)

Author keywords

[No Author keywords available]

Indexed keywords

ANIMAL CELL; ANIMAL EXPERIMENT; ARTICLE; BLASTOCYST; CELL DIVISION; CELL NUCLEUS TRANSPLANTATION; DEVELOPMENTAL STAGE; EMBRYO; EMBRYO DEVELOPMENT; FERTILIZATION IN VITRO; NONHUMAN; OOCYTE; PARTHENOGENESIS; PRIORITY JOURNAL; QUANTITATIVE ANALYSIS; REAL TIME POLYMERASE CHAIN REACTION; RNA DEGRADATION; SWINE;

AGNOSIA; ANIMALS; BLASTOCYST; CLEAVAGE STAGE, OVUM; EMBRYO CULTURE TECHNIQUES; EMBRYONIC DEVELOPMENT; FEMALE; FERTILIZATION IN VITRO; NUCLEAR TRANSFER TECHNIQUES; PARTHENOGENESIS; SWINE;

SUIDAE; SUS;

EID: 84857193139     PISSN: 1040452X     EISSN: 10982795     Source Type: Journal    
DOI: 10.1002/mrd.22013     Document Type: Article

References (72)

1. Abeydeera LR, Day BN. 1997. Fertilization and subsequent development in vitro of pig oocytes inseminated in a modified tris-buffered medium with frozen-thawed ejaculated spermatozoa. Biol Reprod 57: 729-734.
2. Abeydeera LR, Wang WH, Prather RS, Day BN. 1998. Maturation in vitro of pig oocytes in protein-free culture media: Fertilization and subsequent embryo development in vitro. Biol Reprod 58: 1316-1320.
3. Alomar M, Tasiaux H, Remacle S, George F, Paul D, Donnay I. 2008. Kinetics of fertilization and development, and sex ratio of bovine embryos produced using the semen of different bulls. Anim Reprod Sci 107: 48-4861.
4. Bashirullah A, Cooperstock RL, Lipshitz HD. 2001. Spatial and temporal control of RNA stability. Proc Natl Acad Sci USA 98: 7025-7028.
5. Biase FH, Fonseca Merighe GK, Santos Biase WK, Martelli L, Meirelles FV. 2008. Global poly(A) mRNA expression profile measured in individual bovine oocytes and cleavage embryos. Zygote 16: 29-38.
6. Booth PJ, Holm P, Callesen H. 2005. The effect of oxygen tension on porcine embryonic development is dependent on embryo type. Theriogenology 63: 2040-2052.
7. Booth PJ, Watson TJ, Leese HJ. 2007. Prediction of porcine blastocyst formation using morphological, kinetic, and amino acid depletion and appearance criteria determined during the early cleavage of in vitro-produced embryos. Biol Reprod 77: 765-779.
8. Combelles CM, Racowsky C. 2005. Assessment and optimization of oocyte quality during assisted reproductive technology treatment. Semin Reprod Med 23: 277-284.
9. Comiskey M, Goldstein CY, De Fazio SR, Mammolenti M, Newmark JA, Warner CM. 2003. Evidence that HLA-G is the functional homolog of mouse Qa-2, the Ped gene product. Hum Immunol 64: 999-1004.
10. Comizzoli P, Marquant-Le Guienne B, Heyman Y, Renard JP. 2000. Onset of the first S-phase is determined by a paternal effect during the G1-phase in bovine zygotes. Biol Reprod 62: 1677-1684.
11. Conley AJ, Jung YC, Schwartz NK, Warner CM, Rothschild MF, Ford SP. 1988. Influence of SLA haplotype on ovulation rate and litter size in miniature pigs. J Reprod Fertil 82: 595-601.
12. Coutinho ARS, Assumpção MEO, Bordignon V. 2011. Presence of cleaved caspase 3 in swine embryos of different developmental capacities produced by parthenogenetic activation. Mol Reprod Dev 78: 673-683.
13. Dang-Nguyen TQ, Kikuchi K, Somfai T, Ozawa M, Nakai M, Maedomari N, Viet-Linh N, Kanai Y, Nguyen BX, Nagai T. 2010. Evaluation of developmental competence of in vitro-produced porcine embryos based on the timing, pattern and evenness of the first cleavage and onset of the second cleavage. J Reprod Dev 56: 593-600.
14. Dobbs KB, Spollen WG, Springer G, Prather RS. 2010. The role of cytoplasmic polyadenylation element sequence on mRNA abundance during porcine embryogenesis and parthenogenetic development. Mol Reprod Dev 77: 699-709.
15. Dunne LD, Diskin MG, Sreenan JM. 2000. Embryo and foetal loss in beef heifers between day 14 of gestation and full term. Anim Reprod Sci 58: 39-44.
16. Edwards JL, King WA, Kawarsky SJ, Ealy AD. 2001. Responsiveness of early embryos to environmental insults: Potential protective roles of HSP70 and glutathione. Theriogenology 55: 209-223.
17. Eid LN, Lorton SP, Parrish JJ. 1994. Paternal influence on S-phase in the first cell cycle of the bovine embryo. Biol Reprod 51: 1232-1237.
18. Fair T, Gutierrez-Adan A, Murphy M, Rizos D, Martin F, Boland MP, Lonergan P. 2004. Search for the bovine homolog of the murine ped gene and characterization of its messenger RNA expression during bovine preimplantation development. Biol Reprod 70: 488-494.
19. Fenwick J, Platteau P, Murdoch AP, Herbert M. 2002. Time from insemination to first cleavage predicts developmental competence of human preimplantation embryos in vitro. Hum Reprod 17: 407-412.
20. Ford SP, Schwartz NK, Rothschild MF, Conley AJ, Warner CM. 1988. Influence of SLA haplotype on preimplantation embryonic cell number in miniature pigs. J Reprod Fertil 84: 99-104.
21. Garneau NL, Wilusz J, Wilusz CJ. 2007. The highways and byways of mRNA decay. Nat Rev Mol Cell Biol 8: 113-126.
22. Gates AH. 2008. Rate of Ovular Development as a Factor in Embryonic Survival, in Ciba Foundation Symposium-Preimplantation Stages of Pregnancy. In: G. E. W. Wolstenholme and M. O'Connor, editors. Chichester, UK: John Wiley & Sons, Ltd. doi: 0.1002/9780470719435.ch13.
23. Giraldez AJ, Mishima Y, Rihel J, Grocock RJ, Van Dongen S, Inoue K, Enright AJ, Schier AF. 2006. Zebrafish MiR-430 promotes deadenylation and clearance of maternal mRNAs. Science 312: 75-79.
24. Goldbard SB, Warner CM. 1982. Genes affect the timing of early mouse embryo development. Biol Reprod 27: 419-424.
25. Hamatani T, Carter MG, Sharov AA, Ko MSH. 2004. Dynamics of global gene expression changes during mouse preimplantation development. Dev cell 6: 117-131.
26. Hao Y, Lai L, Mao J, Im GS, Bonk A, Prather RS. 2003. Apoptosis and in vitro development of preimplantation porcine embryos derived in vitro or by nuclear transfer. Biol Reprod 69: 501-507.
27. Hao Y, Lai L, Mao J, Im GS, Bonk A, Prather RS. 2004. Apoptosis in parthenogenetic preimplantation porcine embryos. Biol Reprod 70: 1644-1649.
28. Holm P, Booth PJ, Callesen H. 2002. Kinetics of early in vitro development of bovine in vivo- and in vitro-derived zygotes produced and/or cultured in chemically defined or serum-containing media. Reproduction 123: 553-565.
29. Isom SC, Lai L, Prather RS, Rucker EB IIIrd. 2009. Heat shock of porcine zygotes immediately after oocyte activation increases viability. Mol Reprod Dev 76: 548-554.
30. Jeon Y, Jeong SH, Biswas D, Jung EM, Jeung EB, Lee ES, Hyun SH. 2011. Cleavage pattern and survivin expression in porcine embryos by somatic cell nuclear transfer. Theriogenology 76: 1187-1196.
31. Jurisicova A, Casper RF, MacLusky NJ, Mills GB, Librach CL. 1996. HLA-G expression during preimplantation human embryo development. Proc Natl Acad Sci USA 93: 161-165.
32. Lai L, Prather RS. 2003. Production of cloned pigs by using somatic cells as donors. Cloning Stem Cells 5: 233-241.
33. Larionov A, Krause A, Miller W. 2005. A standard curve based method for relative real time PCR data processing. BMC Bioinform 6: 62.
34. Lechniak D, Pers-Kamczyc E, Pawlak P. 2008. Timing of the first zygotic cleavage as a marker of developmental potential of mammalian embryos. Reprod Biol 8: 23-42.
35. Lonergan P, Gutierrez-Adan A, Pintado B, Fair T, Ward F, Fuente JD, Boland M. 2000. Relationship between time of first cleavage and the expression of IGF-I growth factor, its receptor, and two housekeeping genes in bovine two-cell embryos and blastocysts produced in vitro. Mol Reprod Dev 57: 146-152.
36. Lonergan P, Khatir H, Piumi F, Rieger D, Humblot P, Boland MP. 1999. Effect of time interval from insemination to first cleavage on the developmental characteristics, sex ratio and pregnancy rate after transfer of bovine embryos. J Reprod Fertil 117: 159-167.
37. Lundin K, Bergh C, Hardarson T. 2001. Early embryo cleavage is a strong indicator of embryo quality in human IVF. Hum Reprod 16: 2652-2657.
38. Mallard BA, Wilkie BN, Croy BA, Kennedy BW, Friendship R. 1987. Influence of the swine major histocompatibility complex on reproductive traits in miniature swine. J Reprod Immunol 12: 201-214.
39. McElhinny AS, Exley GE, Warner CM. 2000. Painting Qa-2 onto Ped slow preimplantation embryos increases the rate of cleavage. Am J Reprod Immunol 44: 52-58.
40. McElhinny AS, Kadow N, Warner CM. 1998. The expression pattern of the Qa-2 antigen in mouse preimplantation embryos and its correlation with the Ped gene phenotype. Mol Hum Reprod 4: 966-971.
41. McElhinny AS, Warner CM. 2000. Cross-linking of Qa-2 protein, the Ped gene product, increases the cleavage rate of C57BL/6 preimplantation mouse embryos. Mol Hum Reprod 6: 517-522.
42. Medvedev S, Yang J, Hecht NB, Schultz RM. 2008. CDC2A (CDK1)-mediated phosphorylation of MSY2 triggers maternal mRNA degradation during mouse oocyte maturation. Dev Biol 321: 205-215.
43. Nemcova L, Machatkova M, Hanzalova K, Horakova J, Kanka J. 2006. Gene expression in bovine embryos derived from oocytes with different developmental competence collected at the defined follicular developmental stage. Theriogenology 65: 1254-1264.
44. Nothias JY, Majumder S, Kaneko KJ, DePamphilis ML. 1995. Regulation of gene expression at the beginning of mammalian development. J Biol Chem 270: 22077-22080.
45. Patel OV, Bettegowda A, Ireland JJ, Coussens PM, Lonergan P, Smith GW. 2007. Functional genomics studies of oocyte competence: Evidence that reduced transcript abundance for follistatin is associated with poor developmental competence of bovine oocytes. Reproduction 133: 95-106.
46. Patten BM. 1931. The embryology of the pig. Philadelphia: P. Blakiston's Son & Co. pp ix, 327 p.
47. Paynton BV, Bachvarova R. 1994. Polyadenylation and deadenylation of maternal mRNAs during oocyte growth and maturation in the mouse. Mol Reprod Dev 37: 172-180.
48. Plante L, Plante C, Shepherd DL, King WA. 1994. Cleavage and 3H-uridine incorporation in bovine embryos of high in vitro developmental potential. Mol Reprod Dev 39: 375-383.
49. Pope WF. 1994. Embryonic mortality in swine. In: Zavy MT, Geisert RD, editors. Embryonic mortality in domestic species. Boca Raton, FL: CRC Press. pp 53-77.
50. Roberts RM. 2005. Embryo culture conditions: What embryos like best. Endocrinology 146: 2140-2141.
51. Romar R, De Santis T, Papillier P, Perreau C, Thelie A, Dell'Aquila ME, Mermillod P, Dalbies-Tran R. 2011. Expression of maternal transcripts during bovine oocyte in vitro maturation is affected by donor age. Reprod Domest Anim 46: e23-e30.
52. Rouget C, Papin C, Boureux A, Meunier AC, Franco B, Robine N, Lai EC, Pelisson A, Simonelig M. 2010. Maternal mRNA deadenylation and decay by the piRNA pathway in the early Drosophila embryo. Nature 467: 1128-1132.
53. Rutledge RG, Cote C. 2003. Mathematics of quantitative kinetic PCR and the application of standard curves. Nucleic Acids Res 31: e93.
54. Salumets A, Hyden-Granskog C, Makinen S, Suikkari AM, Tiitinen A, Tuuri T. 2003. Early cleavage predicts the viability of human embryos in elective single embryo transfer procedures. Hum Reprod 18: 821-825.
55. Schier AF. 2007. The maternal-zygotic transition: Death and birth of RNAs. Science 316: 406-407.
56. Schultz RM. 2002. The molecular foundations of the maternal to zygotic transition in the preimplantation embryo. Hum Reprod Update 8: 323-331.
57. Senger PL. 2005. Pathways to pregnancy and parturition. Pullman, WA: Current Conceptions. pp xii, 373 p.
58. Sirard MA, Richard F, Blondin P, Robert C. 2006. Contribution of the oocyte to embryo quality. Theriogenology 65: 126-136.
59. Steuerwald N, Cohen J, Herrera RJ, Brenner CA. 2000. Quantification of mRNA in single oocytes and embryos by real-time rapid cycle fluorescence monitored RT-PCR. Mol Hum Reprod 6: 448-453.
60. Tadros W, Lipshitz HD. 2009. The maternal-to-zygotic transition: A play in two acts. Development 136: 3033-3042.
61. Thelie A, Papillier P, Pennetier S, Perreau C, Traverso JM, Uzbekova S, Mermillod P, Joly C, Humblot P, Dalbies-Tran R. 2007. Differential regulation of abundance and deadenylation of maternal transcripts during bovine oocyte maturation in vitro and in vivo. BMC Dev Biol 7: 125.
62. Thelie A, Papillier P, Perreau C, Uzbekova S, Hennequet-Antier C, Dalbies-Tran R. 2009. Regulation of bovine oocyte-specific transcripts during in vitro oocyte maturation and after maternal-embryonic transition analyzed using a transcriptomic approach. Mol Reprod Dev 76: 773-782.
63. Totey SM, Daliri M, Appa Rao KB, Pawshe CH, Taneja M, Chillar RS. 1996. Differential cleavage and developmental rates and their correlation with cell numbers and sex ratios in buffalo embryos generated in vitro. Theriogenology 45: 521-533.
64. van Soom A, Ysebaert MT, de Kruif A. 1997. Relationship between timing of development, morula morphology, and cell allocation to inner cell mass and trophectoderm in in vitro-produced bovine embryos. Mol Reprod Dev 47: 47-56.
65. Wang Q, Sun QY. 2007. Evaluation of oocyte quality: Morphological, cellular and molecular predictors. Reprod Fertil Dev 19: 1-12.
66. Ward F, Rizos D, Corridan D, Quinn K, Boland M, Lonergan P. 2001. Paternal influence on the time of first embryonic cleavage post insemination and the implications for subsequent bovine embryo development in vitro and fertility in vivo. Mol Reprod Dev 60: 47-55.
67. Warner CM, Exley GE, McElhinny AS, Tang C. 1998a. Genetic regulation of preimplantation mouse embryo survival. J Exp Zool 282: 272-279.
68. Warner CM, McElhinny AS, Wu L, Cieluch C, Ke X, Cao W, Tang C, Exley GE. 1998b. Role of the Ped gene and apoptosis genes in control of preimplantation development. J Assist Reprod Genet 15: 331-337.
69. Whitworth KM, Agca C, Kim JG, Patel RV, Springer GK, Bivens NJ, Forrester LJ, Mathialagan N, Green JA, Prather RS. 2005. Transcriptional profiling of pig embryogenesis by using a 15-K member unigene set specific for pig reproductive tissues and embryos. Biol Reprod 72: 1437-1451.
70. Yadav BR, King WA, Betteridge KJ. 1993. Relationships between the completion of first cleavage and the chromosomal complement, sex, and developmental rates of bovine embryos generated in vitro. Mol Reprod Dev 36: 434-439.
71. Yoshioka K, Suzuki C, Tanaka A, Anas IM, Iwamura S. 2002. Birth of piglets derived from porcine zygotes cultured in a chemically defined medium. Biol Reprod 66: 112-119.
72. Zhao J, Hao Y, Ross JW, Spate LD, Walters EM, Samuel MS, Rieke A, Murphy CN, Prather RS. 2010. Histone deacetylase inhibitors improve in vitro and in vivo developmental competence of somatic cell nuclear transfer porcine embryos. Cell Reprogram 12: 75-83.