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JOURNAL ARTICLES
Spindlin, a major maternal transcript expressed in the mouse during the transition from oocyte to embryo
B. Oh, S.Y. Hwang, D. Solter, B.B. Knowles
Development 1997 124: 493-503;

Summary

Timely translation of maternal transcripts and post-translational modification of their gene products control the initial development of preimplantation-stage embryos. We have isolated and characterized a gene encoding a stage-specific embryonic protein. This novel gene, spindlin (Spin), is an abundant maternal transcript present in the unfertilized egg and 2-cell, but not 8-cell, stage embryo. Spin exhibits high homology to a multicopy gene, Y-linked spermiogenesis-specific transcript (Ssty), and together they form a new gene family expressed during gametogenesis. We find that spindlin associates with the meiotic spindle and is modified by phosphorylation in a cell-cycle-dependent fashion. Furthermore, it comigrates with the previously described 30x10(3) Mr metaphase complex which is posttranslationally modified during the first mitotic cell cycle. Our data suggest that spindlin plays a role in cell-cycle regulation during the transition from gamete to embryo.

REFERENCES

    1. Al Ubaidi M. R.,
    2. Pittler S. J.,
    3. Champagnes M. S.,
    4. Triantafyllos J. T.,
    5. McGinnis J. F.,
    6. Baehr W.
    (1990) Mouse opsin: gene structure and molecular basis of multiple transcripts. J. Biol. Chem 267, 20563–20569
    OpenUrl
    1. Bachvarova R. F.
    (1992) A maternal tail of poly(A): the long and the short of it. Cell 69, 895–897
    OpenUrlCrossRefPubMedWeb of Science
    1. Bailly E.,
    2. Pines J.,
    3. Hunter T.,
    4. Bornens M.
    (1992) Cytoplasmic accumulation of cyclin B1 in human cells: association with a detergent-resistant compartment and with the centrosome. J. Cell Sci 101, 529–545
    OpenUrlAbstract/FREE Full Text
    1. Bishop C. E.,
    2. Hatat D.
    (1987) Molecular cloning and sequence analysis of a mouse Y chromosome RNA transcript expressed in the testis. Nucleic Acids Res 15, 2959–2969
    OpenUrlAbstract/FREE Full Text
    1. Bishop C. E.
    (1992) Mouse Y chromosome. Mammalian Genome 3, 289–.
    OpenUrlCrossRef
    1. Bolton V. N.,
    2. Oades P. J.,
    3. Johnson M. H.
    (1984) The relationship between cleavage, DNA replication and activation of transcription in the mouse 2-cell embryo. J. Embryol. Exp. Morph 79, 139–163
    OpenUrlPubMedWeb of Science
    1. Burd C. G.,
    2. Dreyfuss G.
    (1994) Conserved structures and diversity of functions of RNA-binding proteins. Science 265, 615–620
    OpenUrlAbstract/FREE Full Text
    1. Burgoyne P. S.,
    2. Mahadevaiah S. K.,
    3. Sutcliffe M. J.,
    4. Palmer S. J.
    (1992) Fertility in mice requires X-Y pairing and a Y-chromosomal ‘Spermiogenesis’ gene mapping to the long arm. Cell 71, 391–398
    OpenUrlCrossRefPubMedWeb of Science
    1. Cascio S. M.,
    2. Wassarman P. M.
    (1982) Program of early development in the mammal: posttranscriptional control of a class of proteins synthesized by mouse oocytes and early embryos. Dev. Biol 89, 397–408
    OpenUrlCrossRefPubMedWeb of Science
    1. Chapman D. L.,
    2. Wolgemuth D. J.
    (1992) Identification of a mouse B-type cyclin which exhibits developmentally regulated expression in the germ cell. Mol. Rep. Dev 33, 259–269
    OpenUrlCrossRefPubMedWeb of Science
    1. Chesnel F.,
    2. Wigglesworth K.,
    3. Eppig J. J.
    (1994) Acquisition of meiotic competence by denuded mouse oocytes: participation of somatic-cell product(s) and cAMP. Dev. Biol 161, 285–295
    OpenUrlCrossRefPubMedWeb of Science
    1. Code R. J.,
    2. Olmstead J. B.
    (1992) Mouse microtubule-associated protein 4 (MAP4) transcript diversity generated by alternative polyadenylation. Gene 122, 367–370
    OpenUrlCrossRefPubMed
    1. Conway S. J.,
    2. Mahadevaiah S. K.,
    3. Darling S. M.,
    4. Capel B.,
    5. Rattigan A. M.,
    6. Burgoyne P. S.
    (1994) Y353/B: a candidate multiple-copy spermiogenesis gene on the mouse Y chromosome. Mammalian Genome 5, 203–210
    OpenUrlCrossRefPubMedWeb of Science
    1. Cullen B. R.,
    2. Emigholz K.,
    3. Monahan J. J.
    (1980) Protein patterns of early mouse embryos during development. Differentiation 17, 151–160
    OpenUrlCrossRefPubMed
    1. De Pennart H.,
    2. Verlhac M.-H.,
    3. Cibert C.,
    4. Santa Maria A.,
    5. Maro B.
    (1993) Okadaic acid induces spindle lengthening and disrupts the interactionof microtubules with the kinetochores in metaphase II-arrested mouse oocytes. Dev. Biol 157, 170–181
    OpenUrlCrossRefPubMed
    1. Della N. G.,
    2. Bowtell D. D.,
    3. Beck F.
    (1995) Expression of Siah −2, a vertebrate homologue of Drosophila sina, in germ cells of the mouse ovary and testis. Cell Tissue Res 279, 411–9
    OpenUrlPubMedWeb of Science
    1. Fox C. A.,
    2. Sheets M. D.,
    3. Wickens M. P.
    (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
    OpenUrlAbstract/FREE Full Text
    1. Gebauer F.,
    2. Xu W.,
    3. Cooper G. M.,
    4. Richter J. D.
    (1994) Translational control by cytoplasmic polyadenylation of c-mos mRNA is necessary for oocyte maturation in the mouse. EMBO J 13, 5712–5720
    OpenUrlPubMedWeb of Science
    1. Globus M. S.,
    2. Stein M. P.
    (1976) Qualitative patterns of protein synthesis in the mouse oocyte. J. Exp. Zool 198, 337–342
    OpenUrlCrossRefPubMed
    1. Haccard O.,
    2. Sarcevic B.,
    3. Lewellyn A.,
    4. Hartley R.,
    5. Roy L.,
    6. Izumi T.,
    7. Erikson E.,
    8. Maller J. M.
    (1993) Induction of metaphase arrest in cleaving Xenopus embryos by MAP kinase. Science 262, 1262–5
    OpenUrlAbstract/FREE Full Text
    1. Hake L. E.,
    2. Richter J. D.
    (1994) CPEB is a specificity factor that mediates cytoplasmic polyadenylation during Xenopus oocyte maturation. Cell 79, 617–627
    OpenUrlCrossRefPubMedWeb of Science
    1. Hampl A.,
    2. Eppig J. J.
    (1995) Analysis of the mechanism(s) of metaphase I arrest in maturing mouse oocytes. Development 121, 925–933
    OpenUrlAbstract
    1. Howe C. C.,
    2. Solter D.
    (1979) Cytoplasmic and nuclear protein synthesis in preimplantation mouse embryo. J. Embryol. Exp. Morph 52, 209–225
    OpenUrlPubMedWeb of Science
    1. Howlett S. K.,
    2. Bolton V. N.
    (1985) Sequence and regulation of morphological and molecular events during the first cell cycle of mouse embryogenesis. J. Embryol. Exp. Morph 87, 175–206
    OpenUrlPubMedWeb of Science
    1. Howlett S. K.
    (1986) A set of proteins showing cell cycle dependent modification in the early mouse embryo. Cell 45, 387–396
    OpenUrlCrossRefPubMedWeb of Science
    1. Huarte J.,
    2. Belin D.,
    3. Vassalli A.,
    4. Strickland S.,
    5. Vassalli J.-D.
    (1987) Meiotic maturation of mouse oocytes triggers the translation and polyadenylation of dormant tissue-type plasminogen activator mRNA. Genes Dev 1, 1201–1211
    OpenUrlAbstract/FREE Full Text
    1. Huarte J. Stutz A.,
    2. O'Connell M. L.,
    3. Gubler P.,
    4. Belin D.,
    5. Darrow A. L.,
    6. Strickland S.,
    7. Vassalli J.-D.
    (1992) Transient translational silencing by reversible mRNA deadenylation. Cell 69, 1021–1030
    OpenUrlCrossRefPubMedWeb of Science
    1. Hwang S.-Y.,
    2. Benjamin L. E.,
    3. Oh B.,
    4. Rothstein J. L.,
    5. Ackerman S. L.,
    6. Beddington R. S. P.,
    7. Solter D.,
    8. Knowles B. B.
    (1996) Genetic mapping and embryonic expression of a novel, maternally transcribed gene Mem3. Mammalian Genome 7, 586–590
    OpenUrlCrossRefPubMedWeb of Science
    1. Kessel M.,
    2. Gruss P.
    (1991) Homeotic transformations of murine vertebrae and concomitant alteration of Hox codes induced by retinoic acid. Cell 67, 89–104
    OpenUrlCrossRefPubMedWeb of Science
    1. Knowland J.,
    2. Graham C.
    (1972) RNA synthesis at the two-cell stage of mouse development. J. Embryol. Exp. Morph 27, 167–176
    OpenUrlPubMedWeb of Science
    1. Langan T. A.,
    2. Gautier J.,
    3. Lohka M.,
    4. Hollingsworth R.,
    5. Moreno S.,
    6. Nurse P.,
    7. Maller J.,
    8. Sclafani R. A.
    (1989) Mammalian growth-associated H1 histone kinase: a homolog of cdc2+/CDC28 protein kinases controlling mitotic entry in yeast and frog cells. Mol. Cell. Biol 9, 3860–3868
    OpenUrlAbstract/FREE Full Text
    1. Lantz V.,
    2. Chang J. S.,
    3. Horabin J. I.,
    4. Bopp D.,
    5. Schedl P.
    (1994) The Drosophila orb RNA-binding protein is required for the formation of the egg chamber and establishment of polarity. Genes Dev 8, 598–613
    OpenUrlAbstract/FREE Full Text
    1. Latham K. E.,
    2. Garrels J. I.,
    3. Chang C.,
    4. Solter D.
    (1991) Quantitative analysis of protein synthesis in mouse embryos. I. Extensive reprogramming at the one-and two-cell stages. Development 112, 921–932
    OpenUrlAbstract
    1. Leff S. E.,
    2. Rosenfeld M. G.
    (1986) Complex transcriptional units: diversity in gene expression by alternative RNA processing. Ann. Rev. Biochem 55, 1091–1117
    OpenUrlCrossRefPubMedWeb of Science
    1. Levinson J.,
    2. Goodfellow P.,
    3. Vadeboncoeur M.,
    4. McDevitt H.
    (1978) Identification of stage-specific polypeptides synthesized during murine preimplantation development. Proc. Natl. Acad. Sci. USA 75, 3332–3336
    OpenUrlAbstract/FREE Full Text
    1. Magnuson T.,
    2. Epstein C. J.
    (1981) Characterization of concanavalin A precipitated proteins from early mouse embryos: a 2-dimensional gel electrophoresis study. Dev. Biol 81, 193–199
    OpenUrlCrossRefPubMed
    1. McGrew L. L.,
    2. Dworkin-Rastl E.,
    3. Dworkin M. B.,
    4. Richter J. D.
    (1989) Poly(A) elongation during Xenopus oocyte maturation is required for translation recruitment and is mediated by a short sequence element. Genes Dev 3, 803–815
    OpenUrlAbstract/FREE Full Text
    1. McGrew L. L.,
    2. Richter J. D.
    (1990) Translational control bycytoplasmic polyadenylation during Xenopus oocyte maturation: characterization of cis and trans elements and regulation by cyclin/MPF. EMBO J 9, 3743–3751
    OpenUrlPubMedWeb of Science
    1. Moore G. P. M.
    (1975) The RNA polymerase activity of the preimplantation mouse embryo. J. Embryol. Exp. Morph 34, 291–298
    OpenUrlPubMedWeb of Science
    1. Nishioka Y.
    (1988) Evolutionary characterization of a Y chromosomal sequence conserved in the genus Mus. Genet. Res 52, 145–150
    OpenUrlPubMed
    1. Ohsugi M.,
    2. Hwang S.-H.,
    3. Butz S.,
    4. Knowles B. B.,
    5. Solter D.,
    6. Kemler R.
    (1996) Expression and cell membrane localization of catenins during mouse preimplantation development. Dev. Dynamics 206, 391–402
    OpenUrlCrossRefPubMed
    1. Ookata K.,
    2. Hisanaga S.,
    3. Okumura E.,
    4. Kishimoto T.
    (1993) Association of p34cdc2/cyclin B complex with microtubules in starfish oocytes. J. Cell Sci 105, 873–881
    OpenUrlAbstract/FREE Full Text
    1. Paynton B. S.,
    2. Rempel R.,
    3. Bachvarova R. F.
    (1988) Changes in the state of adenylation and time course of degradation of maternal RNAs during oocyte maturation and early embryonic development in the mouse. Dev. Biol 129, 304–314
    OpenUrlCrossRefPubMedWeb of Science
    1. Peter M.,
    2. Nakagawa J.,
    3. Doree M.,
    4. Labbe J. C.,
    5. Nigg E. A.
    (1990) In vitro disassembly of the nuclear lamina and M phase-specific phosphorylation of lamins by cdc2 Kinase. Cell 61, 591–602
    OpenUrlCrossRefPubMedWeb of Science
    1. Pines J.,
    2. Hunter T.
    (1991) Human cyclins A and B1 are differentially located in the cell and undergo cell cycle dependent nuclear transport. J. Cell Biol 115, 1–17
    OpenUrlAbstract/FREE Full Text
    1. Poueymirou W. T.,
    2. Schultz R. M.
    (1987) Differential effects of activators of cAMP-dependent protein kinase and protein kinase C on cleavage of one-cell mouse embryos and protein synthesis and phosphorylation in one-and two-cell embryos. Dev. Biol 121, 489–498
    OpenUrlCrossRefPubMed
    1. Rime H.,
    2. Neant I.,
    3. Guerrier P.,
    4. Ozon R.
    (1989) 6-dimethylaminopurine (6-DMAP), a reversible inhibitor of the transition to metaphase during the first meiotic cell division of the mouse oocyte. Dev. Biol 133, 169–179
    OpenUrlCrossRefPubMedWeb of Science
    1. Rothstein J. L.,
    2. Johnson D.,
    3. DeLoia J. A.,
    4. Skowronski J.,
    5. Solter D.,
    6. Knowles B. B.
    (1992) Gene expression during preimplantation mouse development. Genes Dev 6, 1190–1201
    OpenUrlAbstract/FREE Full Text
    1. Rothstein J. L.,
    2. Johnson D.,
    3. Jesse J.,
    4. Skowronski J.,
    5. DeLoia J.,
    6. Solter D.,
    7. Knowles B. B.
    (1993) Construction of primary and subtracted cDNA libraries from early embryos. Methods Enzymol 225, 587–610
    OpenUrlPubMedWeb of Science
    1. Roy L. M.,
    2. Singh B.,
    3. Gautier J.,
    4. Arlinghous R. B.,
    5. Nordeen S. K.,
    6. Maller J. M.
    (1990) The cyclin B2 component of MPF is a substrate for the c-mosXE proto-oncogene product. Cell 61, 825–831
    OpenUrlCrossRefPubMedWeb of Science
    1. Saez C. G.,
    2. Myers J. C.,
    3. Shows T. B.,
    4. Leinwand L. A.
    (1990) Human non-muscle myosin heavy chain mRNA: generation of diversity through alternative polyadenylation. Proc. Natl. Acad. Sci. USA 87, 1164–1168
    OpenUrlAbstract/FREE Full Text
    1. Salles F. J.,
    2. Darrow A. L.,
    3. O'Connell M. L.,
    4. Strickland S.
    (1992) Isolation of novel murine maternal mRNAs regulated by cytoplasmic polyadenylation. Genes Dev 6, 1202–1212
    OpenUrlAbstract/FREE Full Text
    1. Schultz R. M.
    (1993) Regulation of zygotic gene activation in the mouse. BioEssays 15, 531–538
    OpenUrlCrossRefPubMedWeb of Science
    1. Schultz R. M.,
    2. Wassarman P. M.
    (1977) Biochemical studies of mammalian oogenesis: protein synthesis during oocyte growth and meiotic maturation in the mouse. J. Cell Sci 24, 167–194
    OpenUrlFREE Full Text
    1. Simon R.,
    2. Tassan J.-P.,
    3. Richter J. D.
    (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
    OpenUrlAbstract/FREE Full Text
    1. Simon R.,
    2. Richter J. D.
    (1994) Further analysis of cytoplasmic polyadenylation in Xenopus embryos and identification of embryonic cytoplasmic polyadenylation element-binding proteins. Mol. Cell. Biol 14, 7867–7875
    OpenUrlAbstract/FREE Full Text
    1. Van Blerkom J.
    (1981) Structural relationship and posttranslational modification of stage-specific proteins synthesized during early preimplantation development of the mouse. Proc. Natl. Acad. Sci. USA 78, 7629–7633
    OpenUrlAbstract/FREE Full Text
    1. Verde F.,
    2. Labbe J.-C.,
    3. Doree M.,
    4. Karsenti E.
    (1990) Regulation of microtubule dynamics by cdc2 protein kinase in cell-free extracts of Xenopus eggs. Nature 343, 233–238
    OpenUrlCrossRefPubMed
    1. Verlhac M.-H.,
    2. Pennart H.,
    3. Maro B.,
    4. Cobb M. H.,
    5. Clarke H. J.
    (1993) MAP kinase become stably activated at metaphase and is associated with microtubule-organizing centers during meiotic maturation of mouse oocytes. Dev. Biol 158, 330–340
    OpenUrlCrossRefPubMedWeb of Science
    1. Verlhac M.-H.,
    2. Kubiak J. Z.,
    3. Weber M.,
    4. Geraud G.,
    5. Colledge W. H.,
    6. Evans M. J.,
    7. Maro B.
    (1996) Mos is required for MAP kinase activation and is involved in microtubule organization during meiotic maturation in the mouse. Development 122, 815–822
    OpenUrlAbstract
    1. Yew N.,
    2. Mellini M. L.,
    3. Vande Woude G. F.
    (1992) Meiotic initiation by the mos protein in Xenopus. Nature 355, 649–652
    OpenUrlCrossRefPubMed
    1. Zhou R.,
    2. Oskarsson M.,
    3. Paules R. S.,
    4. Schultz N.,
    5. Cleveland D.,
    6. Vande Woude G. F.
    (1991) Ability of the c- mos product to associate with and phosphorylate tubulin. Science 251, 671–675
    OpenUrlAbstract/FREE Full Text
    1. Zhou R.,
    2. Daar I.,
    3. Ferris D. K.,
    4. White G.,
    5. Paules R. S.,
    6. Vande Woude G.
    (1992) pp39mos is associated with p34cdc2kinase in c- mosxe -transformed NIH 3T3 cells. Mol. Cell. Biol 12, 3583–3589
    OpenUrlAbstract/FREE Full Text
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JOURNAL ARTICLES
Spindlin, a major maternal transcript expressed in the mouse during the transition from oocyte to embryo
B. Oh, S.Y. Hwang, D. Solter, B.B. Knowles
Development 1997 124: 493-503;
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