DOI: 10.1091/mbc.10.10.3279. Two Distinct Mechanisms Control the Accumulation of Cyclin B1 and Mos in<i>Xenopus</i>Oocytes in Response to Progesterone

Two Distinct Mechanisms Control the Accumulation of Cyclin B1 and Mos inXenopusOocytes in Response to Progesterone

10.1091/mbc.10.10.3279

Crossref journal-article

American Society for Cell Biology (ASCB)

Molecular Biology of the Cell (1076)

Abstract

Progesterone-induced meiotic maturation of Xenopusoocytes requires the synthesis of new proteins, such as Mos and cyclin B. Synthesis of Mos is thought to be necessary and sufficient for meiotic maturation; however, it has recently been proposed that newly synthesized proteins binding to p34cdc2could be involved in a signaling pathway that triggers the activation of maturation-promoting factor. We focused our attention on cyclin B proteins because they are synthesized in response to progesterone, they bind to p34cdc2, and their microinjection into resting oocytes induces meiotic maturation. We investigated cyclin B accumulation in response to progesterone in the absence of maturation-promoting factor–induced feedback. We report here that the cdk inhibitor p21cip1, when microinjected into immatureXenopus oocytes, blocks germinal vesicle breakdown induced by progesterone, by maturation-promoting factor transfer, or by injection of okadaic acid. After microinjection of p21cip1, progesterone fails to induce the activation of MAPK or p34cdc2, and Mos does not accumulate. In contrast, the level of cyclin B1 increases normally in a manner dependent on down-regulation of cAMP-dependent protein kinase but independent of cap-ribose methylation of mRNA.

Authors 5

Marie Frank-Vaillant (first)
Catherine Jessus (additional)
René Ozon (additional)
James L. Maller (additional)
Olivier Haccard (additional)

References 52 Referenced 82

10.1128/JVI.12.2.241-252.1973 / J. Virol. by Anderson C.W. (1973)
10.1091/mbc.8.8.1633
10.1093/emboj/17.11.3168 / EMBO J. by Barkoff A. (1998)
10.1042/bj2560283 / Biochem. J. by Bialojan C. (1988)
10.1073/pnas.94.17.9136 / Proc. Natl. Acad. Sci. USA by Chen M.Z. (1997)
10.1083/jcb.120.5.1197 / J. Cell Biol. by Daar I. (1993)
10.1093/emboj/18.8.2294 / EMBO J. by de Moor C.H. (1999)
10.1016/0092-8674(89)90687-9 / Cell by Draetta G. (1989)
10.1016/0092-8674(88)90205-X / Cell by Dunphy W.G. (1988)
10.1038/sj.onc.1202056 / Oncogene by Faure S. (1998)
10.1074/jbc.272.30.19008 / J. Biol. Chem. by Ferrell J.E. (1997)
10.1002/j.1460-2075.1994.tb06524.x / EMBO J. by Furuno N. (1994)
10.1093/emboj/16.13.3860 / EMBO J. by Furuno N. (1997)
10.1002/j.1460-2075.1991.tb07934.x / EMBO J. by Gautier J. (1991)
10.1016/0092-8674(90)90599-A / Cell by Gautier J. (1990)
10.1016/0092-8674(88)90206-1 / Cell by Gautier J. (1988)
10.1083/jcb.98.4.1247 / J. Cell Biol. by Gerhart J. (1984)
10.1016/0014-5793(89)80198-X / FEBS Lett. by Goris J. (1989)
10.1002/j.1460-2075.1991.tb07809.x / EMBO J. by Gotoh Y. (1991)
10.1038/366707a0 / Nature by Gu Y. (1993)
10.1016/0303-7207(81)90092-7 / Mol. Cell. Endocrinol. by Huchon D. (1981)
10.1091/mbc.4.12.1337
10.1242/dev.111.3.813 / Development by Jessus C. (1991)
10.1242/jcs.87.5.705 / J. Cell Sci. by Jessus C. (1987)
10.1006/excr.1998.4220 / Exp. Cell Res. by Karaiskou A. (1998)
10.1083/jcb.114.4.755 / J. Cell Biol. by Kobayashi H. (1991)
10.1093/nar/26.13.3208 / Nucleic Acids Res. by Kuge H. (1998)
10.1038/227680a0 / Nature by Laemmli U.K. (1970)
10.1093/emboj/18.7.1869 / EMBO J. by Lenormand J.L. (1999)
10.1016/S0021-9258(17)37841-9 / J. Biol. Chem. by Maller J.L. (1979)
10.1016/S0021-9258(17)40606-5 / J. Biol. Chem. by Maller J.L. (1977)
10.1016/S0074-7696(08)61464-3 / Int. Rev. Cytol. by Masui Y. (1979)
10.1002/jez.1401770202 / J. Exp. Zool. by Masui Y. (1971)
10.1002/j.1460-2075.1992.tb05136.x / EMBO J. by Matsuda S. (1992)
10.1002/j.1460-2075.1989.tb08353.x / EMBO J. by Meijer L. (1989)
10.1002/j.1460-2075.1995.tb00247.x / EMBO J. by Nebreda A. (1995)
10.1016/0014-5793(93)80401-F / FEBS Lett. by Nebreda A.R. (1993)
10.1002/j.1460-2075.1993.tb06080.x / EMBO J. by Nishizawa M. (1993)
10.1016/S0021-9258(18)43211-5 / J. Biol. Chem. by Olmsted J.B. (1981)
10.1128/MCB.13.4.2546 / Mol. Cell. Biol. by Posada J. (1993)
10.1074/jbc.270.12.6843 / J. Biol. Chem. by Rempel R.E. (1995)
10.1016/0922-3371(90)90023-P / Cell Differ. Dev. by Rime H. (1990)
{'key': 'B43', 'first-page': '2203', 'volume': '12', 'author': 'Roy L.M.', 'year': '1996', 'journal-title': 'Oncogene'} / Oncogene by Roy L.M. (1996)
10.1083/jcb.113.3.507 / J. Cell Biol. by Roy L.M. (1991)
10.1126/science.2474853 / Science by Sagata N. (1989)
10.1038/335519a0 / Nature by Sagata N. (1988)
10.1091/mbc.4.8.781
10.1038/267848a0 / Nature by Speaker M.G. (1977)
10.1073/pnas.92.22.10187 / Proc. Natl. Acad. Sci. USA by Su J. (1995)
10.1006/dbio.1997.8543 / Dev. Biol. by Thibier C. (1997)
10.1016/0014-4827(75)90118-4 / Exp. Cell Res. by Wasserman W.J. (1975)
10.1038/366701a0 / Nature by Xiong Y. (1993)

Dates

Type	When
Created	12 years, 1 month ago (July 2, 2013, 7:19 p.m.)
Deposited	3 years, 5 months ago (Feb. 26, 2022, 9:37 p.m.)
Indexed	4 days, 23 hours ago (Aug. 21, 2025, 12:34 p.m.)
Issued	25 years, 10 months ago (Oct. 1, 1999)
Published	25 years, 10 months ago (Oct. 1, 1999)
Published Print	25 years, 10 months ago (Oct. 1, 1999)

Funders 0

None

BibTeX

@article{Frank_Vaillant_1999, title={Two Distinct Mechanisms Control the Accumulation of Cyclin B1 and Mos inXenopusOocytes in Response to Progesterone}, volume={10}, ISSN={1939-4586}, url={http://dx.doi.org/10.1091/mbc.10.10.3279}, DOI={10.1091/mbc.10.10.3279}, number={10}, journal={Molecular Biology of the Cell}, publisher={American Society for Cell Biology (ASCB)}, author={Frank-Vaillant, Marie and Jessus, Catherine and Ozon, René and Maller, James L. and Haccard, Olivier}, editor={Yanagida, Mitsuhiro}, year={1999}, month=oct, pages={3279–3288} }

JSON

{
  "indexed": {
    "date-parts": [
      [
        2025,
        8,
        21
      ]
    ],
    "date-time": "2025-08-21T16:34:22Z",
    "timestamp": 1755794062998
  },
  "reference-count": 52,
  "publisher": "American Society for Cell Biology (ASCB)",
  "issue": "10",
  "content-domain": {
    "domain": [],
    "crossmark-restriction": false
  },
  "published-print": {
    "date-parts": [
      [
        1999,
        10
      ]
    ]
  },
  "abstract": "<jats:p>Progesterone-induced meiotic maturation of Xenopusoocytes requires the synthesis of new proteins, such as Mos and cyclin B. Synthesis of Mos is thought to be necessary and sufficient for meiotic maturation; however, it has recently been proposed that newly synthesized proteins binding to p34<jats:sup>cdc2</jats:sup>could be involved in a signaling pathway that triggers the activation of maturation-promoting factor. We focused our attention on cyclin B proteins because they are synthesized in response to progesterone, they bind to p34<jats:sup>cdc2</jats:sup>, and their microinjection into resting oocytes induces meiotic maturation. We investigated cyclin B accumulation in response to progesterone in the absence of maturation-promoting factor\u2013induced feedback. We report here that the cdk inhibitor p21<jats:sup>cip1</jats:sup>, when microinjected into immatureXenopus oocytes, blocks germinal vesicle breakdown induced by progesterone, by maturation-promoting factor transfer, or by injection of okadaic acid. After microinjection of p21<jats:sup>cip1</jats:sup>, progesterone fails to induce the activation of MAPK or p34<jats:sup>cdc2</jats:sup>, and Mos does not accumulate. In contrast, the level of cyclin B1 increases normally in a manner dependent on down-regulation of cAMP-dependent protein kinase but independent of cap-ribose methylation of mRNA.</jats:p>",
  "DOI": "10.1091/mbc.10.10.3279",
  "type": "journal-article",
  "created": {
    "date-parts": [
      [
        2013,
        7,
        2
      ]
    ],
    "date-time": "2013-07-02T23:19:39Z",
    "timestamp": 1372807179000
  },
  "page": "3279-3288",
  "source": "Crossref",
  "is-referenced-by-count": 82,
  "title": "Two Distinct Mechanisms Control the Accumulation of Cyclin B1 and Mos in<i>Xenopus</i>Oocytes in Response to Progesterone",
  "prefix": "10.1091",
  "volume": "10",
  "author": [
    {
      "given": "Marie",
      "family": "Frank-Vaillant",
      "sequence": "first",
      "affiliation": [
        {
          "name": "Laboratoire de Physiologie de la Reproduction, Centre National de la Recherche Scientifique, Universit\u00e9 Pierre et Marie Curie, Paris 05, France; and"
        }
      ]
    },
    {
      "given": "Catherine",
      "family": "Jessus",
      "sequence": "additional",
      "affiliation": [
        {
          "name": "Laboratoire de Physiologie de la Reproduction, Centre National de la Recherche Scientifique, Universit\u00e9 Pierre et Marie Curie, Paris 05, France; and"
        }
      ]
    },
    {
      "given": "Ren\u00e9",
      "family": "Ozon",
      "sequence": "additional",
      "affiliation": [
        {
          "name": "Laboratoire de Physiologie de la Reproduction, Centre National de la Recherche Scientifique, Universit\u00e9 Pierre et Marie Curie, Paris 05, France; and"
        }
      ]
    },
    {
      "given": "James L.",
      "family": "Maller",
      "sequence": "additional",
      "affiliation": [
        {
          "name": "Howard Hughes Medical Institute and Department of Pharmacology, University of Colorado School of Medicine, Denver, Colorado 80262"
        }
      ]
    },
    {
      "given": "Olivier",
      "family": "Haccard",
      "sequence": "additional",
      "affiliation": [
        {
          "name": "Laboratoire de Physiologie de la Reproduction, Centre National de la Recherche Scientifique, Universit\u00e9 Pierre et Marie Curie, Paris 05, France; and"
        }
      ]
    }
  ],
  "member": "1076",
  "reference": [
    {
      "key": "B1",
      "doi-asserted-by": "crossref",
      "first-page": "241",
      "DOI": "10.1128/JVI.12.2.241-252.1973",
      "volume": "12",
      "author": "Anderson C.W.",
      "year": "1973",
      "journal-title": "J. Virol."
    },
    {
      "key": "B2",
      "doi-asserted-by": "publisher",
      "DOI": "10.1091/mbc.8.8.1633"
    },
    {
      "key": "B3",
      "doi-asserted-by": "crossref",
      "first-page": "3168",
      "DOI": "10.1093/emboj/17.11.3168",
      "volume": "17",
      "author": "Barkoff A.",
      "year": "1998",
      "journal-title": "EMBO J."
    },
    {
      "key": "B4",
      "doi-asserted-by": "crossref",
      "first-page": "283",
      "DOI": "10.1042/bj2560283",
      "volume": "256",
      "author": "Bialojan C.",
      "year": "1988",
      "journal-title": "Biochem. J."
    },
    {
      "key": "B5",
      "doi-asserted-by": "crossref",
      "first-page": "9136",
      "DOI": "10.1073/pnas.94.17.9136",
      "volume": "94",
      "author": "Chen M.Z.",
      "year": "1997",
      "journal-title": "Proc. Natl. Acad. Sci. USA"
    },
    {
      "key": "B6",
      "doi-asserted-by": "crossref",
      "first-page": "1197",
      "DOI": "10.1083/jcb.120.5.1197",
      "volume": "120",
      "author": "Daar I.",
      "year": "1993",
      "journal-title": "J. Cell Biol."
    },
    {
      "key": "B7",
      "doi-asserted-by": "crossref",
      "first-page": "2294",
      "DOI": "10.1093/emboj/18.8.2294",
      "volume": "18",
      "author": "de Moor C.H.",
      "year": "1999",
      "journal-title": "EMBO J."
    },
    {
      "key": "B8",
      "doi-asserted-by": "crossref",
      "first-page": "829",
      "DOI": "10.1016/0092-8674(89)90687-9",
      "volume": "56",
      "author": "Draetta G.",
      "year": "1989",
      "journal-title": "Cell"
    },
    {
      "key": "B9",
      "doi-asserted-by": "crossref",
      "first-page": "423",
      "DOI": "10.1016/0092-8674(88)90205-X",
      "volume": "54",
      "author": "Dunphy W.G.",
      "year": "1988",
      "journal-title": "Cell"
    },
    {
      "key": "B10",
      "doi-asserted-by": "crossref",
      "first-page": "1215",
      "DOI": "10.1038/sj.onc.1202056",
      "volume": "17",
      "author": "Faure S.",
      "year": "1998",
      "journal-title": "Oncogene"
    },
    {
      "key": "B11",
      "doi-asserted-by": "crossref",
      "first-page": "19008",
      "DOI": "10.1074/jbc.272.30.19008",
      "volume": "272",
      "author": "Ferrell J.E.",
      "year": "1997",
      "journal-title": "J. Biol. Chem."
    },
    {
      "key": "B12",
      "doi-asserted-by": "crossref",
      "first-page": "2399",
      "DOI": "10.1002/j.1460-2075.1994.tb06524.x",
      "volume": "13",
      "author": "Furuno N.",
      "year": "1994",
      "journal-title": "EMBO J."
    },
    {
      "key": "B13",
      "doi-asserted-by": "crossref",
      "first-page": "3860",
      "DOI": "10.1093/emboj/16.13.3860",
      "volume": "16",
      "author": "Furuno N.",
      "year": "1997",
      "journal-title": "EMBO J."
    },
    {
      "key": "B14",
      "doi-asserted-by": "crossref",
      "first-page": "177",
      "DOI": "10.1002/j.1460-2075.1991.tb07934.x",
      "volume": "10",
      "author": "Gautier J.",
      "year": "1991",
      "journal-title": "EMBO J."
    },
    {
      "key": "B15",
      "doi-asserted-by": "crossref",
      "first-page": "487",
      "DOI": "10.1016/0092-8674(90)90599-A",
      "volume": "60",
      "author": "Gautier J.",
      "year": "1990",
      "journal-title": "Cell"
    },
    {
      "key": "B16",
      "doi-asserted-by": "crossref",
      "first-page": "433",
      "DOI": "10.1016/0092-8674(88)90206-1",
      "volume": "54",
      "author": "Gautier J.",
      "year": "1988",
      "journal-title": "Cell"
    },
    {
      "key": "B17",
      "doi-asserted-by": "crossref",
      "first-page": "1247",
      "DOI": "10.1083/jcb.98.4.1247",
      "volume": "98",
      "author": "Gerhart J.",
      "year": "1984",
      "journal-title": "J. Cell Biol."
    },
    {
      "key": "B18",
      "doi-asserted-by": "crossref",
      "first-page": "91",
      "DOI": "10.1016/0014-5793(89)80198-X",
      "volume": "245",
      "author": "Goris J.",
      "year": "1989",
      "journal-title": "FEBS Lett."
    },
    {
      "key": "B19",
      "doi-asserted-by": "crossref",
      "first-page": "2661",
      "DOI": "10.1002/j.1460-2075.1991.tb07809.x",
      "volume": "10",
      "author": "Gotoh Y.",
      "year": "1991",
      "journal-title": "EMBO J."
    },
    {
      "key": "B20",
      "doi-asserted-by": "crossref",
      "first-page": "707",
      "DOI": "10.1038/366707a0",
      "volume": "366",
      "author": "Gu Y.",
      "year": "1993",
      "journal-title": "Nature"
    },
    {
      "key": "B21",
      "doi-asserted-by": "crossref",
      "first-page": "211",
      "DOI": "10.1016/0303-7207(81)90092-7",
      "volume": "22",
      "author": "Huchon D.",
      "year": "1981",
      "journal-title": "Mol. Cell. Endocrinol."
    },
    {
      "key": "B22",
      "doi-asserted-by": "publisher",
      "DOI": "10.1091/mbc.4.12.1337"
    },
    {
      "key": "B23",
      "doi-asserted-by": "crossref",
      "first-page": "813",
      "DOI": "10.1242/dev.111.3.813",
      "volume": "111",
      "author": "Jessus C.",
      "year": "1991",
      "journal-title": "Development"
    },
    {
      "key": "B24",
      "doi-asserted-by": "crossref",
      "first-page": "705",
      "DOI": "10.1242/jcs.87.5.705",
      "volume": "87",
      "author": "Jessus C.",
      "year": "1987",
      "journal-title": "J. Cell Sci."
    },
    {
      "key": "B25",
      "doi-asserted-by": "crossref",
      "first-page": "491",
      "DOI": "10.1006/excr.1998.4220",
      "volume": "244",
      "author": "Karaiskou A.",
      "year": "1998",
      "journal-title": "Exp. Cell Res."
    },
    {
      "key": "B26",
      "doi-asserted-by": "crossref",
      "first-page": "755",
      "DOI": "10.1083/jcb.114.4.755",
      "volume": "114",
      "author": "Kobayashi H.",
      "year": "1991",
      "journal-title": "J. Cell Biol."
    },
    {
      "key": "B27",
      "doi-asserted-by": "crossref",
      "first-page": "3208",
      "DOI": "10.1093/nar/26.13.3208",
      "volume": "26",
      "author": "Kuge H.",
      "year": "1998",
      "journal-title": "Nucleic Acids Res."
    },
    {
      "key": "B28",
      "doi-asserted-by": "crossref",
      "first-page": "680",
      "DOI": "10.1038/227680a0",
      "volume": "227",
      "author": "Laemmli U.K.",
      "year": "1970",
      "journal-title": "Nature"
    },
    {
      "key": "B29",
      "doi-asserted-by": "crossref",
      "first-page": "1869",
      "DOI": "10.1093/emboj/18.7.1869",
      "volume": "18",
      "author": "Lenormand J.L.",
      "year": "1999",
      "journal-title": "EMBO J."
    },
    {
      "key": "B30",
      "doi-asserted-by": "crossref",
      "first-page": "579",
      "DOI": "10.1016/S0021-9258(17)37841-9",
      "volume": "254",
      "author": "Maller J.L.",
      "year": "1979",
      "journal-title": "J. Biol. Chem."
    },
    {
      "key": "B31",
      "doi-asserted-by": "crossref",
      "first-page": "1712",
      "DOI": "10.1016/S0021-9258(17)40606-5",
      "volume": "252",
      "author": "Maller J.L.",
      "year": "1977",
      "journal-title": "J. Biol. Chem."
    },
    {
      "key": "B32",
      "doi-asserted-by": "crossref",
      "first-page": "185",
      "DOI": "10.1016/S0074-7696(08)61464-3",
      "volume": "57",
      "author": "Masui Y.",
      "year": "1979",
      "journal-title": "Int. Rev. Cytol."
    },
    {
      "key": "B33",
      "doi-asserted-by": "crossref",
      "first-page": "129",
      "DOI": "10.1002/jez.1401770202",
      "volume": "177",
      "author": "Masui Y.",
      "year": "1971",
      "journal-title": "J. Exp. Zool."
    },
    {
      "key": "B34",
      "doi-asserted-by": "crossref",
      "first-page": "973",
      "DOI": "10.1002/j.1460-2075.1992.tb05136.x",
      "volume": "11",
      "author": "Matsuda S.",
      "year": "1992",
      "journal-title": "EMBO J."
    },
    {
      "key": "B35",
      "doi-asserted-by": "crossref",
      "first-page": "2275",
      "DOI": "10.1002/j.1460-2075.1989.tb08353.x",
      "volume": "8",
      "author": "Meijer L.",
      "year": "1989",
      "journal-title": "EMBO J."
    },
    {
      "key": "B36",
      "doi-asserted-by": "crossref",
      "first-page": "5597",
      "DOI": "10.1002/j.1460-2075.1995.tb00247.x",
      "volume": "14",
      "author": "Nebreda A.",
      "year": "1995",
      "journal-title": "EMBO J."
    },
    {
      "key": "B37",
      "doi-asserted-by": "crossref",
      "first-page": "183",
      "DOI": "10.1016/0014-5793(93)80401-F",
      "volume": "333",
      "author": "Nebreda A.R.",
      "year": "1993",
      "journal-title": "FEBS Lett."
    },
    {
      "key": "B38",
      "doi-asserted-by": "crossref",
      "first-page": "4021",
      "DOI": "10.1002/j.1460-2075.1993.tb06080.x",
      "volume": "12",
      "author": "Nishizawa M.",
      "year": "1993",
      "journal-title": "EMBO J."
    },
    {
      "key": "B39",
      "doi-asserted-by": "crossref",
      "first-page": "11955",
      "DOI": "10.1016/S0021-9258(18)43211-5",
      "volume": "256",
      "author": "Olmsted J.B.",
      "year": "1981",
      "journal-title": "J. Biol. Chem."
    },
    {
      "key": "B40",
      "doi-asserted-by": "crossref",
      "first-page": "2546",
      "DOI": "10.1128/MCB.13.4.2546",
      "volume": "13",
      "author": "Posada J.",
      "year": "1993",
      "journal-title": "Mol. Cell. Biol."
    },
    {
      "key": "B41",
      "doi-asserted-by": "crossref",
      "first-page": "6843",
      "DOI": "10.1074/jbc.270.12.6843",
      "volume": "270",
      "author": "Rempel R.E.",
      "year": "1995",
      "journal-title": "J. Biol. Chem."
    },
    {
      "key": "B42",
      "doi-asserted-by": "crossref",
      "first-page": "47",
      "DOI": "10.1016/0922-3371(90)90023-P",
      "volume": "29",
      "author": "Rime H.",
      "year": "1990",
      "journal-title": "Cell Differ. Dev."
    },
    {
      "key": "B43",
      "first-page": "2203",
      "volume": "12",
      "author": "Roy L.M.",
      "year": "1996",
      "journal-title": "Oncogene"
    },
    {
      "key": "B44",
      "doi-asserted-by": "crossref",
      "first-page": "507",
      "DOI": "10.1083/jcb.113.3.507",
      "volume": "113",
      "author": "Roy L.M.",
      "year": "1991",
      "journal-title": "J. Cell Biol."
    },
    {
      "key": "B45",
      "doi-asserted-by": "crossref",
      "first-page": "643",
      "DOI": "10.1126/science.2474853",
      "volume": "245",
      "author": "Sagata N.",
      "year": "1989",
      "journal-title": "Science"
    },
    {
      "key": "B46",
      "doi-asserted-by": "crossref",
      "first-page": "519",
      "DOI": "10.1038/335519a0",
      "volume": "335",
      "author": "Sagata N.",
      "year": "1988",
      "journal-title": "Nature"
    },
    {
      "key": "B47",
      "doi-asserted-by": "publisher",
      "DOI": "10.1091/mbc.4.8.781"
    },
    {
      "key": "B48",
      "doi-asserted-by": "crossref",
      "first-page": "848",
      "DOI": "10.1038/267848a0",
      "volume": "267",
      "author": "Speaker M.G.",
      "year": "1977",
      "journal-title": "Nature"
    },
    {
      "key": "B49",
      "doi-asserted-by": "crossref",
      "first-page": "10187",
      "DOI": "10.1073/pnas.92.22.10187",
      "volume": "92",
      "author": "Su J.",
      "year": "1995",
      "journal-title": "Proc. Natl. Acad. Sci. USA"
    },
    {
      "key": "B50",
      "doi-asserted-by": "crossref",
      "first-page": "55",
      "DOI": "10.1006/dbio.1997.8543",
      "volume": "185",
      "author": "Thibier C.",
      "year": "1997",
      "journal-title": "Dev. Biol."
    },
    {
      "key": "B51",
      "doi-asserted-by": "crossref",
      "first-page": "381",
      "DOI": "10.1016/0014-4827(75)90118-4",
      "volume": "91",
      "author": "Wasserman W.J.",
      "year": "1975",
      "journal-title": "Exp. Cell Res."
    },
    {
      "key": "B52",
      "doi-asserted-by": "crossref",
      "first-page": "701",
      "DOI": "10.1038/366701a0",
      "volume": "366",
      "author": "Xiong Y.",
      "year": "1993",
      "journal-title": "Nature"
    }
  ],
  "container-title": "Molecular Biology of the Cell",
  "original-title": [],
  "language": "en",
  "deposited": {
    "date-parts": [
      [
        2022,
        2,
        27
      ]
    ],
    "date-time": "2022-02-27T02:37:33Z",
    "timestamp": 1645929453000
  },
  "score": 1,
  "resource": {
    "primary": {
      "URL": "https://www.molbiolcell.org/doi/10.1091/mbc.10.10.3279"
    }
  },
  "subtitle": [],
  "editor": [
    {
      "given": "Mitsuhiro",
      "family": "Yanagida",
      "sequence": "additional",
      "affiliation": []
    }
  ],
  "short-title": [],
  "issued": {
    "date-parts": [
      [
        1999,
        10
      ]
    ]
  },
  "references-count": 52,
  "journal-issue": {
    "issue": "10",
    "published-print": {
      "date-parts": [
        [
          1999,
          10
        ]
      ]
    }
  },
  "alternative-id": [
    "10.1091/mbc.10.10.3279"
  ],
  "URL": "http://dx.doi.org/10.1091/mbc.10.10.3279",
  "relation": {},
  "ISSN": [
    "1059-1524",
    "1939-4586"
  ],
  "subject": [],
  "container-title-short": "MBoC",
  "published": {
    "date-parts": [
      [
        1999,
        10
      ]
    ]
  }
}