Mos 3′ UTR regulatory differences underlie species-specific temporal patterns of Mos mRNA cytoplasmic polyadenylation and translational recruitment during oocyte maturation

Molecular Reproduction and Development

Volumn 75, Issue 8, 2008, Pages 1258-1268

  Prasad, C Krishna ^a,c   Mahadevan, Mahendran ^a   MacNicol, Melanie C ^a   MacNicol, Angus M ^a,b  

^a UNIVERSITY OF ARKANSAS FOR MEDICAL SCIENCES   (United States)

^b UNIVERSITY OF ARKANSAS FOR MEDICAL SCIENCES   (United States)

^c ITPL   (India)

Author keywords

CPE; Cytoplasmic polyadenylation; Human; Mos; mRNA; Oocyte; Translation

Indexed keywords

CYTOPLASMIC POLYADENYLATION ELEMENT BINDING PROTEIN; MESSENGER RNA; CLEAVAGE AND POLYADENYLATION SPECIFICITY FACTOR; CPEB1 PROTEIN, HUMAN; PRIMER DNA; TRANSCRIPTION FACTOR;

3' UNTRANSLATED REGION; ANIMAL CELL; ARTICLE; CYTOPLASM; CYTOPLASMIC POLYADENYLATION ELEMENT; HUMAN; HUMAN CELL; NONHUMAN; ONCOGENE; OOCYTE MATURATION; POLYADENYLATION; PRIORITY JOURNAL; PROTEIN FUNCTION; PROTEIN PROTEIN INTERACTION; SPECIES DIFFERENCE; TRANSLATION INITIATION; TRANSLATION REGULATION; XENOPUS LAEVIS; ANIMAL; COMPARATIVE STUDY; GEL MOBILITY SHIFT ASSAY; GENE EXPRESSION REGULATION; GENETICS; GROWTH, DEVELOPMENT AND AGING; METABOLISM; OOCYTE; SITE DIRECTED MUTAGENESIS; WESTERN BLOTTING; XENOPUS;

ANURA; MAMMALIA; VERTEBRATA; XENOPUS LAEVIS;

3' UNTRANSLATED REGIONS; ANIMALS; BLOTTING, WESTERN; DNA PRIMERS; ELECTROPHORETIC MOBILITY SHIFT ASSAY; GENE EXPRESSION REGULATION, DEVELOPMENTAL; GENES, MOS; HUMANS; MRNA CLEAVAGE AND POLYADENYLATION FACTORS; MUTAGENESIS, SITE-DIRECTED; OOCYTES; POLYADENYLATION; RNA, MESSENGER; SPECIES SPECIFICITY; TRANSCRIPTION FACTORS; XENOPUS;

EID: 46049099368     PISSN: 1040452X     EISSN: 10982795     Source Type: Journal    
DOI: 10.1002/mrd.20877     Document Type: Article

References (65)

1. Ali A, Benkhalifa M, Miron P. 2006. In-vitro maturation of oocytes: Biological aspects. Reprod Biomed Online 13:437-446.
2. Araki K, Naito K, Haraguchi S, Suzuki R, Yokoyama M, Inoue M, Aizawa S, Toyoda Y, Sato E. 1996. Meiotic abnormalities of c-mos knockout mouse oocytes: Activation after first meiosis or entrance into third meiotic metaphase. Biol Reprod 55:1315-1324.
3. Ballantyne S, Daniel DLJ, Wickens M. 1997. A dependent pathway of cytoplasmic polyadenylation reactions linked to cell cycle control by c-mos and CDK1 activation. Mol Biol Cell 8:1633-1648.
4. Barkoff AF, Dickson KS, Gray NK, Wickens M. 2000. Translational control of cyclin B1 mRNA during meiotic maturation: Coordinated repression and cytoplasmic polyadenylation. Dev Biol 220:97-109.
5. Charlesworth A, Welk J, MacNicol A. 2000. The temporal control of Wee1 mRNA translation during Xenopus oocyte maturation is regulated by cytoplasmic polyadenylation elements within the 3′ untranslated region. Dev Biol 227:706-719.
6. Charlesworth A, Ridge JA, King LA, MacNicol MC, MacNicol AM. 2002. A novel regulatory element determines the timing of Mos mRNA translation during Xenopus oocyte maturation. EMBO J 21:2798-2806.
7. Charlesworth A, Cox LL, MacNicol AM. 2004. Cytoplasmic polyadenylation element (CPE)- and CPE-binding protein (CPEB)-independent mechanisms regulate early class maternal mRNA translational activation in xenopus oocytes. J Biol Chem 279:17650-17659.
8. Charlesworth A, Wilczynska A, Thampi P, Cox LL, MacNicol AM. 2006. Musashi regulates the temporal order of mRNA translation during Xenopus oocyte maturation. EMBO J 25:2792-2801.
9. Chian RC, Buckett WM, Tan SL. 2004. In-vitro maturation of human oocytes. Reprod Biomed Online 8:148-166.
10. Colledge WH, Carlton MB, Udy GB, Evans MJ. 1994. Disruption of c-mos causes parthenogenetic development of unfertilized mouse eggs. Nature 370:65-68.
11. Daar I, Paules RS, Vande Woude GF. 1991. A characterization of cytostatic factor activity from Xenopus eggs and c-mos-transformed cells. J Cell Biol 114:329-335.
12. de Moor CH, Richter JD. 1997. The Mos pathway regulates cytoplasmic polyadenylation in Xenopus oocytes. Mol Cell Biol 17:6419-6426.
13. de Moor CH, Richter JD. 1999. Cytoplasmic polyadenylation elements mediate masking and unmasking of cyclin B1 mRNA. EMBO J 18:2294-2303.
14. Dupre A, Jessus C, Ozon R, Haccard O. 2002. Mos is not required for the initiation of meiotic maturation in Xenopus oocytes. EMBO J 21:4026-4036.
15. Ferby I, Blazquez M, Palmer A, Eritja R, Nebreda AR. 1999. A novel p34(cdc2)-binding and activating protein that is necessary and sufficient to trigger G(2)/M progression in Xenopus oocytes. Genes Dev 13:2177-2189.
16. Fox CA, Sheets MD, Wickens MP. 1989. Poly(A) addition during maturation of frog oocytes: Distinct nuclear and cytoplasmic activities and regulation by the sequence UUUUUAU. Genes Dev 3:2151-2162.
17. Gebauer F, Richter JD. 1996. Mouse cytoplasmic polyadenylylation element binding protein: An evolutionarily conserved protein that interacts with the cytoplasmic polyadenylylation elements of c-mos mRNA. Proc Natl Acad Sci USA 93:14602-14607.
18. Gebauer F, Xu W, Cooper GM, Richter JD. 1994. Translational control by cytoplasmic polyadenylation of c-mos mRNA is necessary for oocyte maturation in the mouse. EMBO J 13:5712.
19. Goldman DS, Kiessling AA, Cooper GM. 1988. Post-transcriptional processing suggests that c-mos functions as a maternal message in mouse eggs. Oncogene 3:159-1162.
20. Gross SD, Schwab MS, Taieb FE, Lewellyn AL, Qian YW, Maller JL. 2000. The critical role of the MAP kinase pathway in meiosis II in Xenopus oocytes is mediated by p90(Rsk). Curr Biol 10:430-438.
21. Hashiba Y, Asada Y, Heikinheimo O, Lanzendorf SE, Mizutani S. 2001. Microinjection of antisense c-mos oligonucleotides prevents the progression of meiosis in human and hamster oocytes. Fertil Steril 76:143-147.
22. Hashimoto N. 1996. Role of c-mos proto-oncogene product in the regulation of mouse oocyte maturation. Horm Res 46:11-14.
23. Hashimoto N, Watanabe N, Furuta Y, Tamemoto H, Sagata N, Yokoyama M, Okazaki K, Nagayoshi M, Takeda N, Ikawa Y., et al. 1994. Parthenogenetic activation of oocytes in c-mos-deficient mice. Nature 370:68-71.
24. Hochegger H, Klotzbucher A, Kirk J, Howell M, le Guellec K, Fletcher K, Duncan T, Sohail M, Hunt T. 2001. New B-type cyclin synthesis is required between meiosis I and II during Xenopus oocyte maturation. Development 128:3795-3807.
25. Howard EL, Charlesworth A, Welk J, MacNicol AM. 1999. The mitogen-activated protein kinase signaling pathway stimulates mos mRNA cytoplasmic polyadenylation during Xenopus oocyte maturation. Mol Cell Biol 19:1990-1999.
26. Hyman LE, Wormington WM. 1988. Translational inactivation of ribosomal protein mRNAs during Xenopus oocyte maturation. Genes Dev 2:598-605.
27. Imai T, Tokunaga A, Yoshida T, Hashimoto M, Mikoshiba K, Weinmaster G, Nakafuku M, Okano H. 2001. The neural RNA-binding protein Musashi1 translationally regulates mammalian numb gene expression by interacting with its mRNA. Mol Cell Biol 21:3888-3900.
28. Knaut H, Steinbeisser H, Schwarz H, Nusslein-Volhard C. 2002. An evolutionary conserved region in the vasa 3′UTR targets RNA translation to the germ cells in the zebrafish. Curr Biol 12:454-466.
29. Krey L, Liu H, Zhang J, Grifo J. 2001. Fertility and maternal age strategies to improve pregnancy outcome. Ann N Y Acad Sci 943:26-33.
30. Lazar S, Galiani D, Dekel N. 2002. cAMP-Dependent PKA negatively regulates polyadenylation of c-mos mRNA in rat oocytes. Mol Endocrinol 16:331-341.
31. Machaca K, Haun S. 2002. Induction of maturation-promoting factor during Xenopus oocyte maturation uncouples Ca(2+) store depletion from store-operated Ca(2+) entry. J Cell Biol 156:75-85.
32. Mahadevan MM, Miller MM, Maris MO, Moutos D, Finkbeiner A. 1998. Intracytoplasmic sperm injection into oocytes of severe male infertility patients: UAMS experience. University of Arkansas for Medical Sciences. J Ark Med Soc 94:487-489.
33. McGrew LL, Richter JD. 1990. Translational control by cytoplasmic polyadenylation during Xenopus oocyte maturation: Characterization of cis and trans elements and regulation by cyclin/MPF. EMBO J 9:3743-3751.
34. McGrew LL, Dworkin-Rastl E, Dworkin MB, Richter JD. 1989. Poly(A) elongation during Xenopus oocyte maturation is required for translational recruitment and is mediated by a short sequence element. Genes Dev 3:803-815.
35. Mendez R, Richter JD. 2001. Translational control by CPEB: A means to the end. Nat Rev Mol Cell Biol 2:521-529.
36. Mignone F, Grillo G, Licciulli F, Iacono M, Liuni S, Kersey PJ, Duarte J, Saccone C, Pesole G. 2005. UTRdb and UTRsite: A collection of sequences and regulatory motifs of the untranslated regions of eukaryotic mRNAs. Nucleic Acids Res 33:D141-D146.
37. Minshall N, Walker J, Dale M, Standart N. 1999. Dual roles of p82, the clam CPEB homolog, in cytoplasmic polyadenylation and translational masking. RNA 5:27-38.
38. Moor RM, Dai Y, Lee C, Fulka J Jr. 1998. Oocyte maturation and embryonic failure. Hum Reprod Update 4:223-236.
39. Nakajo N, Yoshitome S, Iwashita J, Iida M, Uto K, Ueno S, Okamoto K, Sagata N. 2000. Absence of weel ensures the meiotic cell cycle in xenopus oocytes. Genes Dev 14:328-338.
40. Newman B, Dai Y. 1996. Transcription of c-mos protooncogene in the pig involves both tissue-specific promoters and alternative polyadenylation sites. Mol Reprod Dev 44:275-288.
41. Okano H, Kawahara H, Toriya M, Nakao K, Shibata S, Imai T. 2005. Function of RNA-binding protein Musashi-1 in stem cells. Exp Cell Res 306:349-356.
42. Pal SK, Torry D, Serta R, Crowell RC, Seibel MM, Cooper GM, Kiessling AA. 1994. Expression and potential function of the c-mos proto-oncogene in human eggs. Fertil Steril 61:496-503.
43. Paris J, Richter JD. 1990. Maturation-specific polyadenylation and translational control: Diversity of cytoplasmic polyadenylation elements, influence of poly(A) tail size, and formation of stable polyadenylation complexes. Mol Cell Biol 10:5634-5645.
44. Posada J, Yew N, Ahn NG, Vande WG, Cooper JA. 1993. Mos stimulates MAP kinase in Xenopus oocytes and activates a MAP kinase kinase in vitro. Mol Cell Biol 13:2546-2553.
45. Rassa JC, Wilson GM, Brewer GA, Parks GD. 2000. 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 274:438-449.
46. Sagata N, Oskarsson M, Copeland T, Brumbaugh J, Vande Woude GF. 1988. Function of c-mos proto-oncogene product in meiotic maturation in Xenopus oocytes. Nature 335:519-525.
47. Sagata N, Watanabe N, Vande Woude GF, Ikawa Y. 1989. The c-mos proto-oncogene product is a cytostatic factor responsible for meiotic arrest in vertebrate eggs [see comments]. Nature 342:512-518.
48. Sakakibara S, Imai T, Hamaguchi K, Okabe M, Aruga J, Nakajima K, Yasutomi D, Nagata T, Kurihara Y, Uesugi S, Miyata T, Ogawa M, Mikoshiba K, Okano H. 1996. Mouse-Musashi-1, a neural RNA-binding protein highly enriched in the mammalian CNS stem cell. Dev Biol 176:230-242.
49. SallÈs FJ, Darrow AL, O'Connell ML, Strickland S. 1992. Isolation of novel murine maternal mRNAs regulated by cytoplasmic polyadenylation. Genes Dev 6:1202-1212.
50. Sheets MD, Fox CA, Hunt T, Vande Woude G, Wickens M. 1994. The 3′-untranslated regions of c-mos and cyclin mRNAs stimulate translation by regulating cytoplasmic polyadenylation. Genes Dev 8:926-938.
51. Sheets MD, Wu M, Wickens M. 1995. Polyadenylation of c-mos mRNA as a control point in Xenopus meiotic maturation. Nature 374:511-516.
52. Shibuya EK, Morris J, Rapp UR, Ruderman JV. 1996. Activation of the Xenopus oocyte mitogen-activated protein kinase pathway by Mos is independent of Raf. Cell Growth Differ 7:235-241.
53. Simon R, Tassan JP, Richter JD. 1992. Translational control by poly(A) elongation during Xenopus development: Differential repression and enhancement by a novel cytoplasmic polyadenylation element. Genes Dev 6:2580-2591.
54. Standart N, Dale M. 1993. Regulated polyadenylation of clam maternal mRNAs in vitro. Dev Genet 14:492-499.
55. Stebbins-Boaz B, Richter JD. 1994. Multiple sequence elements and a maternal mRNA product control cdk2 RNA polyadenylation and translation during early Xenopus development. Mol Cell Biol 14:5870-5880.
56. Stebbins-Boaz B, Hake LE, Richter JD. 1996. CPEB controls the cytoplasmic polyadenylation of cyclin, Cdk2 and c-mos mRNAs and is necessary for oocyte maturation in Xenopus. EMBO J 15:2582-2592.
57. Stutz A, Conne B, Huarte J, Gubler P, Volkel V, Flandin P, Vassalli JD. 1998. Masking, unmasking, and regulated polyadenylation cooperate in the translational control of a dormant mRNA in mouse oocytes. Genes Dev 12:2535-2548.
58. Tay J, Hodgman R, Richter JD. 2000. The control of cyclin B1 mRNA translation during mouse oocyte maturation. Dev Biol 221:1-9.
59. Thompson SR, Goodwin EB, Wickens M. 2000. Rapid deadenylation and poly(A)-dependent translational repression mediated by the Caenorhabditis elegans tra-2 3′ untranslated region in Xenopus embryos. Mol Cell Biol 20:2129-2137.
60. Trounson A, Anderiesz C, Jones G. 2001. Maturation of human oocytes in vitro and their developmental competence. Reproduction 121:51-75.
61. van der Hoorn FA, Firzlaff J. 1984. Complete c-mos (rat) nucleotide sequence: Presence of conserved domains in c-mos proteins. Nucleic Acids Res 12:2147-2156.
62. Verrotti AC, Thompson SR, Wreden C, Strickland S, Wickens M. 1996. Evolutionary conservation of sequence elements controlling cytoplasmic polyadenylation. Proc Natl Acad Sci USA 93:9027-9032.
63. Watson R, Oskarsson M, Vande WG. 1982. Human DNA sequence homologous to the transforming gene (mos) of Moloney murine sarcoma virus. Proc Natl Acad Sci USA 79:4078-4082.
64. Welk J, Charlesworth A, Smith GD, MacNicol AM. 2001. Identification of the gene encoding human cytoplasmic polyadenylation element binding protein. Gene 263:113-121.
65. Wickens M, Goodwin EB, Kimble J, Strictland S, Hentze MW. 2000. Translational control of developmental decisions. In: Sonenberg N, Hershey J, Mathews MB, editors. Translational control of gene expression. Woodbury, NY: Cold Spring Harbor Laboratory Press, p. 295-370.