The starfish egg mRNA responsible for meiosis reinitiation encodes cyclin

Tachibana, Kazunori; Ishiura, Masahiro; Uchida, Tsuyoshi; Kishimoto, Takeo

doi:10.1016/0012-1606(90)90074-s

Cited by 28 publications

(17 citation statements)

References 58 publications

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“…These are representative images of at least three mice for each age and probe examined. to the second meiotic divisions (37)(38)(39). Here, we report that cyclin B3 accumulates during leptotene and zygotene and is reduced in abundance before pachytene (Fig.…”

Section: Discussionmentioning

confidence: 87%

Characterization and Expression of Mammalian Cyclin B3, a Prepachytene Meiotic Cyclin

Nguyen¹,

Manova²,

Capodieci³

et al. 2002

Journal of Biological Chemistry

134

135

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We report the identification and expression pattern of a full-length human cDNA and a partial mouse cDNA encoding cyclin B3. Cyclin B3 (CCNB3) is conserved from Caenorhabditis elegans to Homo sapiens and has an undefined meiotic function in female, but not male Drosophila melanogaster. We show that H. sapiens cyclin B3 interacts with cdk2, is localized to the nucleus, and is degraded during anaphase entry after the degradation of cyclin B1. Degradation is dependent on sequences conserved in a destruction box motif. Overexpression of nondegradable cyclin B3 blocks the mitotic cell cycle in late anaphase, and at higher doses it can interfere with progression through G 1 and entry into S phase. H. sapiens cyclin B3 mRNA and protein are detected readily in developing germ cells in the human testis and not in any other tissue. The mouse cDNA has allowed us to further localize cyclin B3 mRNA to leptotene and zygotene spermatocytes. The expression pattern of mammalian cyclin B3 suggests that it may be important for events occurring in early meiotic prophase I.Cyclins are positive regulatory subunits of the cyclin-dependent kinases (cdks).1 Cyclins increase kinase activity by inducing structural changes in the cdk (1). Cyclins also provide substrate binding motifs (2, 3), signals that localize cdks (4, 5), and motifs that allow the incorporation of the cdk into higher order molecular complexes (6, 7). Although first identified as regulators of mitotic cell cycle transitions, cyclin-cdk complexes have other roles: cyclin C-cdk8 and cyclin H-cdk7 regulate transcription as part of the polymerase II holoenzyme (8 -10), pho80-pho85 regulates the localization of the pho4 transcription factor (11), p35-cdk5 regulates neuronal function (12, 13), and cyclin A1, with an unidentified cdk, regulates the pachytene to diplotene transition during male gametogenesis (14).Originally cloned from a chicken cDNA library, cyclin B3 is expressed at very low levels in virally transformed hematopoietic cell lines and early embryonic stages of chicken. When Gallus gallus cyclin B3 is expressed in HeLa cells, it is nuclear, interacts with cdk2 and cdc2, and is associated with a modest histone H1 kinase activity (15). In Drosophila, cyclin B3 is expressed in both mitotic and meiotic cells. In mitotic cells, it is only required when either cyclin A or cyclin B1 is absent. Its abundance is down-regulated during the metaphase to anaphase transition, following degradation of cyclin B1 (16). Overexpression of a nondegradable cyclin B3 is associated with chromatin decondensation defects at the end of mitosis (17). Cyclin B3 is essential for fertility; but unlike cyclin B1 deficiency, infertility of cyclin B3-deficient flies is restricted to the female germ line and does not appear to involve defects in ovary structure or in meiosis I entry (16).We report the cloning of a full-length human cyclin B3 cDNA and a partial mouse cyclin B3 cDNA. Like the previously described chicken and Drosophila homologs, when mammalian cyclin B3 expression is enforced in m...

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Section: Discussionmentioning

confidence: 87%

Characterization and Expression of Mammalian Cyclin B3, a Prepachytene Meiotic Cyclin

Nguyen¹,

Manova²,

Capodieci³

et al. 2002

Journal of Biological Chemistry

134

135

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“…The cyclin B sequence was from A. pectinifera (Tachibana et al, 1990). The linker sequence was AGAQFLE and the S65T variant of GFP without the start methionine was used (Heim et al, 1995).…”

Section: Cyclin B-gfp and Microinjectionmentioning

confidence: 99%

“…We made a similar construct using the previously cloned cyclin B from the starfish A. pectinifera (Tachibana et al, 1990). mRNA coding for this construct was injected into immature starfish oocytes (A. miniata).…”

Section: Cyclin B Gfp Localizes To Aggregatesmentioning

confidence: 99%

Localization and Dynamics of Cdc2-Cyclin B during Meiotic Reinitiation in Starfish Oocytes

Terasaki

Okumura

Hinkle

et al. 2003

MBoC

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The Cdc2-cyclin B kinase has a central role in regulating the onset of M phase. In starfish oocytes, Cdc2-cyclin B begins to be activated ϳ10 min after application of maturation hormone, followed by accumulation in the nucleus then nuclear envelope breakdown. By immunofluorescence and by expressing a green fluorescent (GFP) chimera of cyclin B, we find that cyclin B is present in aggregates in the cytoplasm of immature oocytes. The aggregates disperse at ϳ10 min, suggesting that the dispersal is closely related to the activation of the kinase. Using cyclin B-GFP, the dispersion begins from the region containing the centrosomes. Extractability of Cdc2-cyclin B changes with similar kinetics during maturation. Active Cdc25 phosphatase released Cdc2-cyclin B from the detergent-insoluble fraction independently of its phosphatase activity. Live cell imaging also showed that Cdc2-cyclin B begins to accumulate in the nucleus before changes in nuclear pore permeability, consistent with Cdc2-cyclin B-induced disassembly of the pores. INTRODUCTIONThe Cdc2/cdk1 kinase triggers the onset of M phase (Nurse, 1990). Activation of Cdc2 requires association with cyclin B and dephosphorylation of Thr 14 and Tyr 15 on Cdc2; the phosphorylation state is governed by the relative activities of Wee1 family kinases and Cdc25 phosphatase (reviewed in Lew and Kornbluth, 1996). Inactive Cdc2-cyclin B is present in the cytoplasm during interphase and after it is activated, accumulates in the nucleus where it phosphorylates multiple targets to cause nuclear envelope breakdown (Pines and Hunter, 1991;Ookata et al., 1992).There are still many aspects of this system that are not well understood. The pathway leading to activation is different in different organisms and has not been established except in starfish (Okumura et al., 2002). Phosphorylation of cyclin is probably involved in the regulation of nuclear entry (Li et al., 1997;Hagting et al., 1998;Toyoshima et al., 1998;Yang et al., 1998) but may have other roles as well (Peter et al., 2002).Another subject of uncertainty regards Cdc2-cyclin B localization in the cytoplasm and its possible associations with other molecules in the cytoplasm. There are several indications that inactive Cdc2-cyclin B is not free to diffuse in the cytosol but instead, is associated with other molecules or intracellular structures and undergoes changes in associations when it becomes activated. Among various reports, Picard and Peaucellier (1998) observed cyclin B in vesiclelike structures in starfish oocytes, Westendorf et al. (1989) found evidence for cyclin B aggregates in immature clam oocytes, and Lee and Kirschner (1996) found evidence for a binding inhibitor of Cdc2-cyclin B that is associated with membranes. More recently, inactive Cdc2-cyclin B was found to be associated with annulate lamellae in immature Xenopus oocytes (Beckhelling et al., 2003).Current techniques for localization are subject to limitations of various kinds. The use of green fluorescent protein (GFP) chimeras is promising because loc...

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“…However, when the tree is rooted differently, or when different residues are used, cdc13+ sometimes moves to the Clbl/2 branch. The cyclins used are as follows: Arp, Arbacia punctulata (sea urchin) (Pines and Hunter, 1987); Asp, Asterina pectinifera (starfish) (Tachibana et al, 1990); Gg, Gallus gallus (chicken) (Gallant and Nigg, 1992); Dm, Drosophila melanogaster (Lehner and O'Farrell, 1990b); Gm, Glycine max (soybean) (Hata et al, 1991); Hs, Homo sapien (human Bi, Pines and Hunter, 1989;B2, Xiong, Connolly, Caligiuri, Futcher, and Beach, personal communication); Pv, Patella vulgata (gastropod) (van Loon et al, 1991); Sc, S. cerevisiae (Ghiara et al, 1991;Surana et al, 1991; this report); Sp, S. pombe ; Ss, Spisula solidissima (clam) (Swenson et al, 1986); and XI, Xenopus laevis (frog) (Minshull et al, 1989). all genes tested, suggesting that the results accurately reflected the events occurring in an unperturbed cell cycle.…”

Section: Electron Microscopymentioning

confidence: 99%

Characterization of four B-type cyclin genes of the budding yeast Saccharomyces cerevisiae.

Fitch

Dahmann

Surana

et al. 1992

MBoC

289

330

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The previously described CLB1 and CLB2 genes encode a closely related pair of B-type cyclins. Here we present the sequences of another related pair of B-type cyclin genes, which we term CLB3 and CLB4. Although CLB1 and CLB2 mRNAs rise in abundance at the time of nuclear division, CLB3 and CLB4 are turned on earlier, rising early in S phase and declining near the end of nuclear division. When all possible single and multiple deletion mutants were constructed, some multiple mutations were lethal, whereas all single mutants were viable. All lethal combinations included the clb2 deletion, whereas the clbl clb3 clb4 triple mutant was viable, suggesting a key role for CLB2.

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The starfish egg mRNA responsible for meiosis reinitiation encodes cyclin

Cited by 28 publications

References 58 publications

Characterization and Expression of Mammalian Cyclin B3, a Prepachytene Meiotic Cyclin

Characterization and Expression of Mammalian Cyclin B3, a Prepachytene Meiotic Cyclin

Localization and Dynamics of Cdc2-Cyclin B during Meiotic Reinitiation in Starfish Oocytes

Characterization of four B-type cyclin genes of the budding yeast Saccharomyces cerevisiae.

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