Differential regulation of abundance and deadenylation of maternal transcripts during bovine oocyte maturation in vitro and in vivo
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  • 作者:Aurore Thélie (1) (2) (3) (4)
    Pascal Papillier (1) (2) (3) (4)
    Sophie Pennetier (1) (2) (3) (4) (5)
    Christine Perreau (1) (2) (3) (4)
    Juan Martin Traverso (1) (2) (3) (4)
    Svetlana Uzbekova (1) (2) (3) (4)
    Pascal Mermillod (1) (2) (3) (4)
    Catherine Joly (6)
    Patrice Humblot (7)
    Rozenn Dalbiès-Tran (1) (2) (3) (4)
  • 刊名:BMC Developmental Biology
  • 出版年:2007
  • 出版时间:December 2007
  • 年:2007
  • 卷:7
  • 期:1
  • 全文大小:382KB
  • 参考文献:1. Sharov AA, Piao Y, Matoba R, Dudekula DB, Qian Y, VanBuren V, Falco G, Martin PR, Stagg CA, Bassey UC, Wang Y, Carter MG, Hamatani T, Aiba K, Akutsu H, Sharova L, Tanaka TS, Kimber WL, Yoshikawa T, Jaradat SA, Pantano S, Nagaraja R, Boheler KR, Taub D, Hodes RJ, Longo DL, Schlessinger D, Keller J, Klotz E, Kelsoe G, Umezawa A, Vescovi AL, Rossant J, Kunath T, Hogan BL, Curci A, D'Urso M, Kelso J, Hide W, Ko MS: Transcriptome analysis of mouse stem cells and early embryos. / PLoS Biol 2003, 1:E74. CrossRef
    2. Hamatani T, Carter MG, Sharov AA, Ko MS: Dynamics of global gene expression changes during mouse preimplantation development. / Dev Cell 2004, 6:117-31. CrossRef
    3. Kocabas AM, Crosby J, Ross PJ, Otu HH, Beyhan Z, Can H, Tam WL, Rosa GJ, Halgren RG, Lim B, Fernandez E, Cibelli JB: The transcriptome of human oocytes. / Proc Natl Acad Sci USA 2006, 103:14027-4032. CrossRef
    4. Misirlioglu M, Page GP, Sagirkaya H, Kaya A, Parrish JJ, First NL, Memili E: Dynamics of global transcriptome in bovine matured oocytes and preimplantation embryos. / Proc Natl Acad Sci USA 2006, 103:18905-8910. CrossRef
    5. Mendez R, Richter JD: Translational control by CPEB: a means to the end. / Nat Rev Mol Cell Biol 2001, 2:521-29. CrossRef
    6. Richter JD: Cytoplasmic polyadenylation in development and beyond. / Microbiol Mol Biol Rev 1999, 63:446-56.
    7. Racki WJ, Richter JD: CPEB controls oocyte growth and follicle development in the mouse. / Development 2006, 133:4527-537. CrossRef
    8. Varnum SM, Wormington WM: Deadenylation of maternal mRNAs during Xenopus oocyte maturation does not require specific cis-sequences: a default mechanism for translational control. / Genes Dev 1990, 4:2278-286. CrossRef
    9. Paynton BV, Bachvarova R: Polyadenylation and deadenylation of maternal mRNAs during oocyte growth and maturation in the mouse. / Mol Reprod Dev 1994, 37:172-80. CrossRef
    10. Evsikov AV, Graber JH, Brockman JM, Hampl A, Holbrook AE, Singh P, Eppig JJ, Solter D, Knowles BB: Cracking the egg: molecular dynamics and evolutionary aspects of the transition from the fully grown oocyte to embryo. / Genes Dev 2006, 20:2713-127. CrossRef
    11. Dean J: Oocyte-specific genes regulate follicle formation, fertility and early mouse development. / J Reprod Immunol 2002, 53:171-80. CrossRef
    12. Rajkovic A, Matzuk MM: Functional analysis of oocyte-expressed genes using transgenic models. / Mol Cell Endocrinol 2002, 187:5-. CrossRef
    13. Dade S, Callebaut I, Paillisson A, Bontoux M, Dalbies-Tran R, Monget P: In silico identification and structural features of six new genes similar to MATER specifically expressed in the oocyte. / Biochem Biophys Res Commun 2004, 324:547-53. CrossRef
    14. Tong ZB, Gold L, Pfeifer KE, Dorward H, Lee E, Bondy CA, Dean J, Nelson LM: Mater, a maternal effect gene required for early embryonic development in mice. / Nat Genet 2000, 26:267-68. CrossRef
    15. Wu X, Viveiros MM, Eppig JJ, Bai Y, Fitzpatrick SL, Matzuk MM: Zygote arrest 1 (Zar1) is a novel maternal-effect gene critical for the oocyte-to-embryo transition. / Nat Genet 2003, 33:187-91. CrossRef
    16. Bortvin A, Goodheart M, Liao M, Page DC: Dppa3/Pgc7/stella is a maternal factor and is not required for germ cell specification in mice. / BMC Dev Biol 2004, 4:2. CrossRef
    17. Payer B, Saitou M, Barton SC, Thresher R, Dixon JP, Zahn D, Colledge WH, Carlton MB, Nakano T, Surani MA: Stella is a maternal effect gene required for normal early development in mice. / Curr Biol 2003, 13:2110-117. CrossRef
    18. Yan C, Pendola FL, Jacob R, Lau AL, Eppig JJ, Matzuk MM: Oosp1 encodes a novel mouse oocyte-secreted protein. / Genesis 2001, 31:105-10. CrossRef
    19. Heyer BS, Warsowe J, Solter D, Knowles BB, Ackerman SL: New member of the Snf1/AMPK kinase family, Melk, is expressed in the mouse egg and preimplantation embryo. / Mol Reprod Dev 1997, 47:148-56. CrossRef
    20. Dade S, Callebaut I, Mermillod P, Monget P: Identification of a new expanding family of genes characterized by atypical LRR domains. Localization of a cluster preferentially expressed in oocyte. / FEBS Lett 2003, 555:533-38. CrossRef
    21. Minami N, Aizawa A, Ihara R, Miyamoto M, Ohashi A, Imai H: Oogenesin is a novel mouse protein expressed in oocytes and early cleavage-stage embryos. / Biol Reprod 2003, 69:1736-742. CrossRef
    22. Pennetier S, Uzbekova S, Perreau C, Papillier P, Mermillod P, Dalbies-Tran R: Spatio-temporal expression of the germ cell marker genes MATER, ZAR1, GDF9, BMP15, andVASA in adult bovine tissues, oocytes, and preimplantation embryos. / Biol Reprod 2004, 71:1359-366. CrossRef
    23. Pennetier S, Uzbekova S, Guyader-Joly C, Humblot P, Mermillod P, Dalbies-Tran R: Genes preferentially expressed in bovine oocytes revealed by subtractive and suppressive hybridization. / Biol Reprod 2005, 73:713-20. CrossRef
    24. Dalbies-Tran R, Papillier P, Pennetier S, Uzbekova S, Monget P: Bovine mater-like NALP9 is an oocyte marker gene. / Mol Reprod Dev 2005, 71:414-21. CrossRef
    25. Uzbekova S, Roy-Sabau M, Dalbies-Tran R, Perreau C, Papillier P, Mompart F, Thelie A, Pennetier S, Cognie J, Cadoret V, Royere D, Monget P, Mermillod P: Zygote arrest 1 gene in pig, cattle and human: evidence of different transcript variants in male and female germ cells. / Reprod Biol Endocrinol 2006, 4:12. CrossRef
    26. Vallee M, Robert C, Methot S, Palin MF, Sirard MA: Cross-species hybridizations on a multi-species cDNA microarray to identify evolutionarily conserved genes expressed in oocytes. / BMC Genomics 2006, 7:113. CrossRef
    27. Tremblay K, Vigneault C, McGraw S, Morin G, Sirard MA: Identification and characterization of a novel bovine oocyte-specific secreted protein gene. / Gene 2006, 375:44-3. CrossRef
    28. Sirard MA, Richard F, Blondin P, Robert C: Contribution of the oocyte to embryo quality. / Theriogenology 2006, 65:126-36. CrossRef
    29. Humblot P, Holm P, Lonergan P, Wrenzycki C, Lequarre AS, Joly CG, Herrmann D, Lopes A, Rizos D, Niemann H, Callesen H: Effect of stage of follicular growth during superovulation on developmental competence of bovine oocytes. / Theriogenology 2005, 63:1149-166. CrossRef
    30. Rizos D, Ward F, Duffy P, Boland MP, Lonergan P: Consequences of bovine oocyte maturation, fertilization or early embryo development in vitro versus in vivo: implications for blastocyst yield and blastocyst quality. / Mol Reprod Dev 2002, 61:234-48. CrossRef
    31. Dieleman SJ, Hendriksen PJ, Viuff D, Thomsen PD, Hyttel P, Knijn HM, Wrenzycki C, Kruip TA, Niemann H, Gadella BM, Bevers MM, Vos PL: Effects of in vivo prematuration and in vivo final maturation on developmental capacity and quality of pre-implantation embryos. / Theriogenology 2002, 57:5-0. CrossRef
    32. van de Leemput EE, Vos PL, Zeinstra EC, Bevers MM, van der Weijden GC, Dieleman SJ: Improved in vitro embryo development using in vivo matured oocytes from heifers superovulated with a controlled preovulatory LH surge. / Theriogenology 1999, 52:335-49. CrossRef
    33. Dalbies-Tran R, Mermillod P: Use of heterologous complementary DNA array screening to analyze bovine oocyte transcriptome and its evolution during in vitro maturation. / Biol Reprod 2003, 68:252-61. CrossRef
    34. Yoshikawa T, Seki N, Azuma T, Masuho Y, Muramatsu M, Miyajima N, Saito T: Isolation of a cDNA for a novel human RING finger protein gene, RNF18, by the virtual transcribed sequence (VTS) approach(1). / Biochim Biophys Acta 2000, 1493:349-55.
    35. Seydoux G: Mechanisms of translational control in early development. / Curr Opin Genet Dev 1996, 6:555-61. CrossRef
    36. Chen CY, Shyu AB: AU-rich elements: characterization and importance in mRNA degradation. / Trends Biochem Sci 1995, 20:465-70. CrossRef
    37. Barreau C, Paillard L, Osborne HB: AU-rich elements and associated factors: are there unifying principles? / Nucleic Acids Res 2005, 33:7138-150. CrossRef
    38. Marquis J, Paillard L, Audic Y, Cosson B, Danos O, Le Bec C, Osborne HB: CUG-BP1/CELF1 requires UGU-rich sequences for high-affinity binding. / Biochem J 2006, 400:291-01. CrossRef
    39. Lequarre AS, Traverso JM, Marchandise J, Donnay I: Poly(A) RNA is reduced by half during bovine oocyte maturation but increases when meiotic arrest is maintained with CDK inhibitors. / Biol Reprod 2004, 71:425-31. CrossRef
    40. Bettegowda A, Patel OV, Ireland JJ, Smith GW: Quantitative analysis of messenger RNA abundance for ribosomal protein L-15, cyclophilin-A, phosphoglycerokinase, beta-glucuronidase, glyceraldehyde 3-phosphate dehydrogenase, beta-actin, and histone H2A during bovine oocyte maturation and early embryogenesis in vitro. / Mol Reprod Dev 2006, 73:267-78. CrossRef
    41. Vigneault C, Gilbert I, Sirard MA, Robert C: Using the histone H2a transcript as an endogenous standard to study relative transcript abundance during bovine early development. / Mol Reprod Dev 2006, 74:703-15. CrossRef
    42. Fair T, Murphy M, Rizos D, Moss C, Martin F, Boland MP, Lonergan P: Analysis of differential maternal mRNA expression in developmentally competent and incompetent bovine two-cell embryos. / Mol Reprod Dev 2004, 67:136-44. CrossRef
    43. Gutierrez-Adan A, Rizos D, Fair T, Moreira PN, Pintado B, de la Fuente J, Boland MP, Lonergan P: Effect of speed of development on mRNA expression pattern in early bovine embryos cultured in vivo or in vitro. / Mol Reprod Dev 2004, 68:441-48. CrossRef
    44. Li XY, Cui XS, Kim NH: Transcription profile during maternal to zygotic transition in the mouse embryo. / Reprod Fertil Dev 2006, 18:635-45. CrossRef
    45. Mamo S, Bodo S, Kobolak J, Polgar Z, Tolgyesi G, Dinnyes A: Gene expression profiles of vitrified in vivo derived 8-cell stage mouse embryos detected by high density oligonucleotide microarrays. / Mol Reprod Dev 2006, 73:1380-392. CrossRef
    46. Fair T, Carter F, Park S, Evans AC, Lonergan P: Global gene expression analysis during bovine oocyte in vitro maturation. / Theriogenology 2007,68(Suppl 1):S91-. CrossRef
    47. Corcoran D, Fair T, Park S, Rizos D, Patel OV, Smith GW, Coussens PM, Ireland JJ, Boland MP, Evans AC, Lonergan P: Suppressed expression of genes involved in transcription and translation in in vitro compared with in vivo cultured bovine embryos. / Reproduction 2006, 131:651-60. CrossRef
    48. Sagirkaya H, Misirlioglu M, Kaya A, First NL, Parrish JJ, Memili E: Developmental and molecular correlates of bovine preimplantation embryos. / Reproduction 2006, 131:895-04. CrossRef
    49. Su YQ, Sugiura K, Woo Y, Wigglesworth K, Kamdar S, Affourtit J, Eppig JJ: Selective degradation of transcripts during meiotic maturation of mouse oocytes. / Dev Biol 2007, 302:104-17. CrossRef
    50. Sakurai T, Sato M, Kimura M: Diverse patterns of poly(A) tail elongation and shortening of murine maternal mRNAs from fully grown oocyte to 2-cell embryo stages. / Biochem Biophys Res Commun 2005, 336:1181-189. CrossRef
    51. Bachvarova R, De Leon V, Johnson A, Kaplan G, Paynton BV: Changes in total RNA, polyadenylated RNA, and actin mRNA during meiotic maturation of mouse oocytes. / Dev Biol 1985, 108:325-31. CrossRef
    52. Paynton BV, Rempel R, Bachvarova R: Changes in state of adenylation and time course of degradation of maternal mRNAs during oocyte maturation and early embryonic development in the mouse. / Dev Biol 1988, 129:304-14. CrossRef
    53. Olszanska B, Borgul A: Maternal RNA content in oocytes of several mammalian and avian species. / J Exp Zool 1993, 265:317-20. CrossRef
    54. Bachvarova R, Paynton BV: Gene expression during growth and meiotic maturation of mouse oocytes. / Prog Clin Biol Res 1988, 267:67-5.
    55. Vigneron C, Perreau C, Dalbies-Tran R, Joly C, Humblot P, Uzbekova S, Mermillod P: Protein synthesis and mRNA storage in cattle oocytes maintained under meiotic block by roscovitine inhibition of MPF activity. / Mol Reprod Dev 2004, 69:457-65. CrossRef
    56. Pennetier S, Perreau C, Uzbekova S, Thelie A, Delaleu B, Mermillod P, Dalbies-Tran R: MATER protein expression and intracellular localization throughout folliculogenesis and preimplantation embryo development in the bovine. / BMC Dev Biol 2006, 6:26. CrossRef
    57. Bhojwani M, Rudolph E, Kanitz W, Zuehlke H, Schneider F, Tomek W: Molecular analysis of maturation processes by protein and phosphoprotein profiling during in vitro maturation of bovine oocytes: a proteomic approach. / Cloning Stem Cells 2006, 8:259-74. CrossRef
    58. Mourot M, Dufort I, Gravel C, Algriany O, Dieleman S, Sirard MA: The influence of follicle size, FSH-enriched maturation medium, and early cleavage on bovine oocyte maternal mRNA levels. / Mol Reprod Dev 2006, 73:1367-379. CrossRef
    59. Brevini-Gandolfi TA, Favetta LA, Mauri L, Luciano AM, Cillo F, Gandolfi F: Changes in poly(A) tail length of maternal transcripts during in vitro maturation of bovine oocytes and their relation with developmental competence. / Mol Reprod Dev 1999, 52:427-33. CrossRef
    60. Gandolfi F, Luciano AM, Modina S, Ponzini A, Pocar P, Armstrong DT, Lauria A: The in vitro developmental competence of bovine oocytes can be related to the morphology of the ovary. / Theriogenology 1997, 48:1153-160. CrossRef
    61. Graindorge A, Thuret R, Pollet N, Osborne HB, Audic Y: Identification of post-transcriptionally regulated Xenopus tropicalis maternal mRNAs by microarray. / Nucleic Acids Res 2006, 34:986-95. CrossRef
    62. Krischek C, Meinecke B: In vitro maturation of bovine oocytes requires polyadenylation of mRNAs coding proteins for chromatin condensation, spindle assembly, MPF and MAP kinase activation. / Anim Reprod Sci 2002, 73:129-40. CrossRef
    63. Traverso JM, Donnay I, Lequarre AS: Effects of polyadenylation inhibition on meiosis progression in relation to the polyadenylation status of cyclins A2 and B1 during in vitro maturation of bovine oocytes. / Mol Reprod Dev 2005, 71:107-14. CrossRef
    64. Tremblay K, Vigneault C, McGraw S, Sirard MA: Expression of cyclin B1 messenger RNA isoforms and initiation of cytoplasmic polyadenylation in the bovine oocyte. / Biol Reprod 2005, 72:1037-044. CrossRef
    65. Mermillod P, Tomanek M, Marchal R, Meijer L: High developmental competence of cattle oocytes maintained at the germinal vesicle stage for 24 hours in culture by specific inhibition of MPF kinase activity. / Mol Reprod Dev 2000, 55:89-5. CrossRef
    66. Ovogenae database[http://wcentre.tours.inra.fr/ovogenae]
  • 作者单位:Aurore Thélie (1) (2) (3) (4)
    Pascal Papillier (1) (2) (3) (4)
    Sophie Pennetier (1) (2) (3) (4) (5)
    Christine Perreau (1) (2) (3) (4)
    Juan Martin Traverso (1) (2) (3) (4)
    Svetlana Uzbekova (1) (2) (3) (4)
    Pascal Mermillod (1) (2) (3) (4)
    Catherine Joly (6)
    Patrice Humblot (7)
    Rozenn Dalbiès-Tran (1) (2) (3) (4)

    1. INRA, UMR85 Physiologie de la Reproduction et des Comportements, F-37380, Nouzilly, France
    2. CNRS, UMR6175, F-37380, Nouzilly, France
    3. Université de Tours, F-37041, Tours, France
    4. Haras Nationaux, F-37380, Nouzilly, France
    5. Centre de Recherche en Biologie de la Reproduction, Département des Sciences Animales, Université Laval, G1K 7P4, Québec, Canada
    6. Union Nationale des Coopératives d'Elevage et d'Insémination Animale, station UNCEIA/UCEAR, F-38300, Chateauvillain, France
    7. Département R&D, Union Nationale des Coopératives d'Elevage et d'Insémination Animale, F-94703, Maisons-Alfort, France
文摘
Background In bovine maturing oocytes and cleavage stage embryos, gene expression is mostly controlled at the post-transcriptional level, through degradation and deadenylation/polyadenylation. We have investigated how post transcriptional control of maternal transcripts was affected during in vitro and in vivo maturation, as a model of differential developmental competence. Results Using real time PCR, we have analyzed variation of maternal transcripts, in terms of abundance and polyadenylation, during in vitro or in vivo oocyte maturation and in vitro embryo development. Four genes are characterized here for the first time in bovine: ring finger protein 18 (RNF18) and breast cancer anti-estrogen resistance 4 (BCAR4), whose oocyte preferential expression was not previously reported in any species, as well as Maternal embryonic leucine zipper kinase (MELK) and STELLA. We included three known oocyte marker genes (Maternal antigen that embryos require (MATER), Zygote arrest 1 (ZAR1), NACHT, leucine rich repeat and PYD containing 9 (NALP9)). In addition, we selected transcripts previously identified as differentially regulated during maturation, peroxiredoxin 1 and 2 (PRDX1, PRDX2), inhibitor of DNA binding 2 and 3 (ID2, ID3), cyclin B1 (CCNB1), cell division cycle 2 (CDC2), as well as Aurora A (AURKA). Most transcripts underwent a moderate degradation during maturation. But they displayed sharply contrasted deadenylation patterns that account for variations observed previously by DNA array and correlated with the presence of a putative cytoplasmic polyadenylation element in their 3' untranslated region. Similar variations in abundance and polyadenylation status were observed during in vitro maturation or in vivo maturation, except for PRDX1, that appears as a marker of in vivo maturation. Throughout in vitro development, oocyte restricted transcripts were progressively degraded until the morula stage, except for MELK ; and the corresponding genes remained silent after major embryonic genome activation. Conclusion Altogether, our data emphasize the extent of post-transcriptional regulation during oocyte maturation. They do not evidence a general alteration of this phenomenon after in vitro maturation as compared to in vivo maturation, but indicate that some individual messenger RNA can be affected.

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