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PMID: 16464828 Published · epublish English Journal Article Research Support, Non-U.S. Gov't

Identification of post-transcriptionally regulated Xenopus tropicalis maternal mRNAs by microarray.

Nucleic acids research ·Vol. 34 ·No. 3 ·2006-00-00 ·Pages 986-95

Graindorge A, Thuret R, Pollet N, Osborne HB, Audic Y

Abstract

Cytoplasmic control of the adenylation state of mRNAs is a critical post-transcriptional process involved in the regulation of mRNAs stability and translational efficiency. The early development of Xenopus laevis has been a major model for the study of such regulations. We describe here a microarray analysis to identify mRNAs that are regulated by changes in their adenylation state during oogenesis and early development of the diploid frog Xenopus tropicalis. The microarray data were validated using qRT-PCR and direct analysis of the adenylation state of endogenous maternal mRNAs during the period studied. We identified more than 500 mRNAs regulated at the post-transcriptional level among the 3000 mRNAs potentially detected by the microarray. The mRNAs were classified into nine different adenylation behavior categories. The various adenylation profiles observed during oocyte maturation and early development and the analyses of 3'-untranslated region sequences suggest that previously uncharacterized sequence elements control the adenylation behavior of the newly identified mRNAs. These data should prove useful in identifying mRNAs with important functions during oocyte maturation and early development.

MeSH Terms
3' Untranslated Regions/chemistry Animals Cells, Cultured Embryo, Nonmammalian/metabolism Female Gene Expression Regulation, Developmental Meiosis Oligonucleotide Array Sequence Analysis Oocytes/cytology,metabolism Oogenesis Polyadenylation RNA 3' Polyadenylation Signals RNA, Messenger/metabolism Reproducibility of Results Reverse Transcriptase Polymerase Chain Reaction Xenopus
Chemicals
3' Untranslated Regions RNA, Messenger
Authors & Affiliations
5 authors, click to expand affiliations / ORCID
Graindorge Antoine
CNRS UMR 6061, IFR 140, Functional Genetics, Agricultural and Health Sciences, Faculté de Médecine, Université de Rennes, 1 Rennes, France.
Thuret Raphaël
Pollet Nicolas
Osborne H Beverley
Audic Yann
References (62)
62 references, click to expand
  1. Identification of a C-rich element as a novel cytoplasmic polyadenylation element in Xenopus embryos.
    Mech Dev. 2000 May;93(1-2):117-25 PMID: 10781945
  2. The Xenopus protein kinase pEg2 associates with the centrosome in a cell cycle-dependent manner, binds to the spindle microtubules and is involved in bipolar mitotic spindle assembly.
    J Cell Sci. 1998 Mar;111 ( Pt 5):557-72 PMID: 9454730
  3. Spacing constraints on reinitiation of paramyxovirus transcription: the gene end U tract acts as a spacer to separate gene end from gene start sites.
    Virology. 2000 Sep 1;274(2):438-49 PMID: 10964786
  4. Zygotic regulation of maternal cyclin A1 and B2 mRNAs.
    Mol Cell Biol. 2001 Mar;21(5):1662-71 PMID: 11238903
  5. Significance analysis of microarrays applied to the ionizing radiation response.
    Proc Natl Acad Sci U S A. 2001 Apr 24;98(9):5116-21 PMID: 11309499
  6. Translational control by CPEB: a means to the end.
    Nat Rev Mol Cell Biol. 2001 Jul;2(7):521-9 PMID: 11433366
  7. Regulation of the mRNAs encoding proteins of the BMP signaling pathway during the maternal stages of Xenopus development.
    Dev Biol. 2001 Aug 1;236(1):230-43 PMID: 11456457
  8. A role for the cytoplasmic polyadenylation element in NMDA receptor-regulated mRNA translation in neurons.
    J Neurosci. 2001 Dec 15;21(24):9541-8 PMID: 11739565
  9. Emi1 regulates the anaphase-promoting complex by a different mechanism than Mad2 proteins.
    Genes Dev. 2001 Dec 15;15(24):3278-85 PMID: 11751633
  10. Cell cycle regulation of pEg3, a new Xenopus protein kinase of the KIN1/PAR-1/MARK family.
    Dev Biol. 2002 Jan 15;241(2):327-38 PMID: 11784115
  11. Emi1 is required for cytostatic factor arrest in vertebrate eggs.
    Nature. 2002 Apr 25;416(6883):850-4 PMID: 11976684
  12. Characterization of MPF and MAPK activities during meiotic maturation of Xenopus tropicalis oocytes.
    Dev Biol. 2002 May 15;245(2):348-61 PMID: 11977986
  13. A novel regulatory element determines the timing of Mos mRNA translation during Xenopus oocyte maturation.
    EMBO J. 2002 Jun 3;21(11):2798-806 PMID: 12032092
  14. Zygotic control of maternal cyclin A1 translation and mRNA stability.
    Dev Dyn. 2002 Dec;225(4):511-21 PMID: 12454927
  15. Survivin mRNA is down-regulated during early Xenopus laevis embryogenesis.
    Dev Dyn. 2002 Dec;225(4):597-601 PMID: 12454937
  16. TM4: a free, open-source system for microarray data management and analysis.
    Biotechniques. 2003 Feb;34(2):374-8 PMID: 12613259
  17. Expression and functional dynamics of the XCAP-D2 condensin subunit in Xenopus laevis oocytes.
    J Biol Chem. 2003 Jul 11;278(28):25708-15 PMID: 12730203
  18. East of EDEN was a poly(A) tail.
    Biol Cell. 2003 May-Jun;95(3-4):211-9 PMID: 12867084
  19. Regulation of the G2/M transition in oocytes of xenopus tropicalis.
    Dev Biol. 2003 Aug 15;260(2):438-48 PMID: 12921744
  20. Cytoplasmic polyadenylation element (CPE)- and CPE-binding protein (CPEB)-independent mechanisms regulate early class maternal mRNA translational activation in Xenopus oocytes.
    J Biol Chem. 2004 Apr 23;279(17):17650-9 PMID: 14752101
  21. Post-transcriptional regulation in cancer.
    Biol Cell. 2004 Sep;96(7):479-98 PMID: 15380615
  22. The dynamics of maternal poly(A)-containing mRNA in fertilized sea urchin eggs.
    Cell. 1977 Jul;11(3):673-81 PMID: 560258
  23. Cell-free cytoplasmic polyadenylation of oogenic RNA.
    Differentiation. 1979;13(2):109-15 PMID: 467871
  24. Cellular titers and subcellular distributions of abundant polyadenylate-containing ribonucleic acid species during early development in the frog Xenopus laevis.
    Mol Cell Biol. 1981 Nov;1(11):983-93 PMID: 6180297
  25. A major developmental transition in early Xenopus embryos: I. characterization and timing of cellular changes at the midblastula stage.
    Cell. 1982 Oct;30(3):675-86 PMID: 6183003
  26. Stimulation of p53-mediated transcriptional activation by the p53-binding proteins, 53BP1 and 53BP2.
    J Biol Chem. 1998 Oct 2;273(40):26061-8 PMID: 9748285
  27. Embryo deadenylation element-dependent deadenylation is enhanced by a cis element containing AUU repeats.
    Mol Cell Biol. 1998 Dec;18(12):6879-84 PMID: 9819376
  28. AUUUA sequences direct mRNA deadenylation uncoupled from decay during Xenopus early development.
    Mol Cell Biol. 1998 Dec;18(12):7537-45 PMID: 9819439
  29. pEg7, a new Xenopus protein required for mitotic chromosome condensation in egg extracts.
    J Cell Biol. 1998 Dec 14;143(6):1437-46 PMID: 9852142
  30. EDEN-BP-dependent post-transcriptional regulation of gene expression in Xenopus somitic segmentation.
    Development. 2004 Dec;131(24):6107-17 PMID: 15548579
  31. A large-scale analysis of mRNA polyadenylation of human and mouse genes.
    Nucleic Acids Res. 2005;33(1):201-12 PMID: 15647503
  32. Mechanisms of translational control by the 3' UTR in development and differentiation.
    Semin Cell Dev Biol. 2005 Feb;16(1):49-58 PMID: 15659339
  33. Gene expression levels assessed by oligonucleotide microarray analysis and quantitative real-time RT-PCR -- how well do they correlate?
    BMC Genomics. 2005;6:59 PMID: 15854232
  34. In vivo analysis of mRNA stability using the Tet-Off system in the chicken embryo.
    Dev Biol. 2005 Aug 15;284(2):292-300 PMID: 15993405
  35. Activity-dependent polyadenylation in neurons.
    RNA. 2005 Sep;11(9):1340-7 PMID: 16043499
  36. A major developmental transition in early Xenopus embryos: II. Control of the onset of transcription.
    Cell. 1982 Oct;30(3):687-96 PMID: 7139712
  37. The poly(A)(+)RNA sequence complexity is also represented in poly(A)(-)RNA in sea-urchin embryos.
    Differentiation. 1984;28(1):24-9 PMID: 6083890
  38. Mobilization of specific maternal RNA species into polysomes after fertilization in Xenopus laevis.
    Proc Natl Acad Sci U S A. 1985 Nov;82(22):7636-40 PMID: 2415967
  39. Changes in RNA titers and polyadenylation during oogenesis and oocyte maturation in Xenopus laevis.
    Dev Biol. 1985 Dec;112(2):451-7 PMID: 2416617
  40. Metabolic regulation during early frog development. Identification of proteins labeled by 32P-glycolytic intermediates.
    J Biol Chem. 1987 Dec 15;262(35):17038-45 PMID: 2824510
  41. Changes in the polyadenylation of specific stable RNA during the early development of Xenopus laevis.
    Gene. 1988 Dec 10;72(1-2):169-76 PMID: 2468559
  42. Poly(A) elongation during Xenopus oocyte maturation is required for translational recruitment and is mediated by a short sequence element.
    Genes Dev. 1989 Jun;3(6):803-15 PMID: 2568313
  43. Poly(A) addition during maturation of frog oocytes: distinct nuclear and cytoplasmic activities and regulation by the sequence UUUUUAU.
    Genes Dev. 1989 Dec;3(12B):2151-62 PMID: 2628165
  44. Poly(A) metabolism and polysomal recruitment of maternal mRNAs during early Xenopus development.
    Dev Biol. 1990 Jul;140(1):221-4 PMID: 2358121
  45. Endonucleolytic cleavage of a maternal homeo box mRNA in Xenopus oocytes.
    Genes Dev. 1990 Nov;4(11):1925-35 PMID: 1980477
  46. Deadenylation of maternal mRNAs during Xenopus oocyte maturation does not require specific cis-sequences: a default mechanism for translational control.
    Genes Dev. 1990 Dec;4(12B):2278-86 PMID: 1980656
  47. Poly(A) removal during oocyte maturation: a default reaction selectively prevented by specific sequences in the 3' UTR of certain maternal mRNAs.
    Genes Dev. 1990 Dec;4(12B):2287-98 PMID: 1980657
  48. Post-transcriptional regulation of ornithine decarboxylase in Xenopus laevis oocytes.
    Development. 1990 Nov;110(3):955-62 PMID: 2088731
  49. Cloning by differential screening of a Xenopus cDNA that encodes a kinesin-related protein.
    Mol Cell Biol. 1991 Jun;11(6):3395-8 PMID: 1710028
  50. Expression and post-transcriptional regulation of ornithine decarboxylase during early Xenopus development.
    Eur J Biochem. 1991 Dec 5;202(2):575-81 PMID: 1761057
  51. Sequence-specific endonucleolytic cleavage and protection of mRNA in Xenopus and Drosophila.
    Genes Dev. 1993 Aug;7(8):1620-31 PMID: 8339937
  52. Translational control by poly(A) elongation during Xenopus development: differential repression and enhancement by a novel cytoplasmic polyadenylation element.
    Genes Dev. 1992 Dec;6(12B):2580-91 PMID: 1285126
  53. The deadenylation conferred by the 3' untranslated region of a developmentally controlled mRNA in Xenopus embryos is switched to polyadenylation by deletion of a short sequence element.
    Mol Cell Biol. 1994 Mar;14(3):1893-900 PMID: 8114721
  54. Two cellular proteins that bind to wild-type but not mutant p53.
    Proc Natl Acad Sci U S A. 1994 Jun 21;91(13):6098-102 PMID: 8016121
  55. The kinesin-related protein Eg5 associates with both interphase and spindle microtubules during Xenopus early development.
    Dev Biol. 1994 Jul;164(1):147-59 PMID: 8026619
  56. Further analysis of cytoplasmic polyadenylation in Xenopus embryos and identification of embryonic cytoplasmic polyadenylation element-binding proteins.
    Mol Cell Biol. 1994 Dec;14(12):7867-75 PMID: 7969126
  57. The nonamer UUAUUUAUU is the key AU-rich sequence motif that mediates mRNA degradation.
    Mol Cell Biol. 1995 Apr;15(4):2219-30 PMID: 7891716
  58. Translational control. Awakening dormant mRNAs.
    Curr Biol. 1995 May 1;5(5):476-9 PMID: 7583092
  59. The p53-binding protein 53BP2 also interacts with Bc12 and impedes cell cycle progression at G2/M.
    Mol Cell Biol. 1996 Jul;16(7):3884-92 PMID: 8668206
  60. Evolutionary conservation of sequence elements controlling cytoplasmic polyadenylylation.
    Proc Natl Acad Sci U S A. 1996 Aug 20;93(17):9027-32 PMID: 8799148
  61. Postfertilization deadenylation of mRNAs in Xenopus laevis embryos is sufficient to cause their degradation at the blastula stage.
    Mol Cell Biol. 1997 Jan;17(1):209-18 PMID: 8972201
  62. Patterns of variant polyadenylation signal usage in human genes.
    Genome Res. 2000 Jul;10(7):1001-10 PMID: 10899149
Article Info
Journal
Nucleic acids research
Abbr.
Nucleic Acids Res
ISSN
1362-4962
Published
2006-00-00
Epub
2006-00-07
Pages
986-95
Language
English
Region
England
NLM ID
0411011
PMCID
PMC1361620
Subset
IM
Analysis Services
Analysis Services

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