DOI: 10.1083/jcb.142.3.751. Spindle Self-organization and Cytokinesis During Male Meiosis in <i>asterless</i> Mutants of <i>Drosophila melanogaster </i>

Spindle Self-organization and Cytokinesis During Male Meiosis in asterless Mutants of Drosophila melanogaster

10.1083/jcb.142.3.751

Crossref journal-article

Rockefeller University Press

The Journal of Cell Biology (291)

Abstract

While Drosophila female meiosis is anastral, both meiotic divisions in Drosophila males exhibit prominent asters. We have identified a gene we call asterless (asl) that is required for aster formation during male meiosis. Ultrastructural analysis showed that asl mutants have morphologically normal centrioles. However, immunostaining with antibodies directed either to γ tubulin or centrosomin revealed that these proteins do not accumulate in the centrosomes, as occurs in wild-type. Thus, asl appears to specify a function required for the assembly of centrosomal material around the centrioles. Despite the absence of asters, meiotic cells of asl mutants manage to develop an anastral spindle. Microtubules grow from multiple sites around the chromosomes, and then focus into a peculiar bipolar spindle that mediates chromosome segregation, although in a highly irregular way. Surprisingly, asl spermatocytes eventually form a morphologically normal ana–telophase central spindle that has full ability to stimulate cytokinesis. These findings challenge the classical view on central spindle assembly, arguing for a self-organization of this structure from either preexisting or newly formed microtubules. In addition, these findings strongly suggest that the asters are not required for signaling cytokinesis.

Bibliography

Bonaccorsi, S., Giansanti, M. G., & Gatti, M. (1998). Spindle Self-organization and Cytokinesis During Male Meiosis in asterless Mutants of Drosophila melanogaster . The Journal of Cell Biology, 142(3), 751â761.

Authors 3

Silvia Bonaccorsi (first)
Maria Grazia Giansanti (additional)
Maurizio Gatti (additional)

References 59 Referenced 146

10.1007/BF00710603 / Chromosome Res / Segregation of holocentric chromosomes at meiosis in the nematode Caenorhabditis elegans. by Albertson (1993)
10.1016/0955-0674(94)90114-7 / Curr Opin Cell Biol / Centrosome and kinetochore movement during mitosis by Ault (1994)
10.1006/excr.1997.3618 / Exp Cell Res / Centriole and centrosome dynamics during the embryonic cell cycles that follow the formation of the cellular blastoderm in Drosophila. by Callaini (1997)
10.1091/mbc.7.2.225 / Mol Biol Cell / Signals from the spindle midzone are required for the stimulation of cytokinesis in cultured epithelial cells by Cao (1996)
10.1242/jcs.107.12.3521 / J Cell Sci / Chromatin and microtubule organization during premeiotic, meiotic, and early postmeiotic stages of Drosophila melanogasterspermatogenesis by Cenci (1994)
10.1083/jcb.103.6.2765 / J Cell Biol / Micromanipulated bivalents can trigger mini-spindle formation in Drosophila melanogasterspermatocyte cytoplasm by Church (1986)
10.1038/274255a0 / Nature / Aploid cell cultures of Drosophila melanogaster. by Debec (1978)
10.1242/jcs.108.7.2645 / J Cell Sci / Polar organization of γ tubulin in acentriolar mitotic spindles of Drosophila melanogastercells by Debec (1995)
{'key': '2023072823555888200_B9', 'first-page': '161', 'article-title': 'The dispensability of the centrioles in the spermatocyte divisions of Pales ferruginea (Nematocera).', 'volume': '19(Suppl.)', 'author': 'Dietz', 'year': '1966', 'journal-title': 'Heredity'} / Heredity / The dispensability of the centrioles in the spermatocyte divisions of Pales ferruginea (Nematocera). by Dietz (1966)
10.1101/SQB.1991.056.01.076 / Cold Spring Harbor Symp Quant Biol / Role of the centromere/kinetochore in cell cycle control by Earnshaw (1991)
10.1083/jcb.132.4.617 / J Cell Biol / Molecular characterization of the 50-kD subunit of dynactin reveals function for the complex in chromosome alignment and spindle organization during mitosis by Echeverri (1996)
10.1083/jcb.137.6.1321 / J Cell Biol / Spindle dynamics during meiosis in Drosophilaoocytes by Endow (1997)
10.1083/jcb.131.1.165 / J Cell Biol / Anillin, a contractile ring protein that cycles from the nucleus to the cell cortex by Field (1995)
10.1242/jcs.109.8.2041 / J Cell Sci / Function of spindle microtubules in directing cortical movements and actin filaments organization in dividing cultured cells by Fishkind (1996)
10.1016/0955-0674(95)80041-7 / Curr Opin Cell Biol / New horizons for cytokinesis by Fishkind (1995)
{'key': '2023072823555888200_B16'}
10.1083/jcb.138.5.1055 / J Cell Biol / Mitotic spindle poles are organized by structural and motor proteins in addition to centrosomes by Gaglio (1997)
10.1083/jcb.131.3.693 / J Cell Biol / NuMA is required for the organization of microtubules into aster-like mitotic arrays by Gaglio (1995)
10.1093/genetics/81.4.683 / Genetics / Isolation and characterization of sex-linked female sterile mutants in Drosophila melanogaster. by Gans (1975)
10.1016/0012-1606(92)90190-R / Dev Biol / Microtubule organization during maturation of Xenopusoocytes: assembly and rotation of the meiotic spindles by Gard (1992)
10.1101/gad.12.3.396 / Genes Dev / Cooperative interaction between the central spindle and the contractile ring during Drosophilacytokinesis by Giansanti (1998)
10.1016/S0955-0674(97)80082-8 / Curr Opin Cell Biol / The mechanism and control of cytokinesis by Glotzer (1997)
{'key': '2023072823555888200_B23'}
10.1016/0092-8674(81)90167-7 / Cell / Kinetochore structure and its role in chromosome orientation during the first meiotic division in male D. melanogaster. by Goldstein (1981)
10.1017/S0016672300028664 / Genet Res / Relationship between chromosome content and nuclear diameter in early spermatids of Drosophila melanogaster. by Gonzalez (1989)
10.1083/jcb.131.5.1243 / J Cell Biol / Mutations in twinstar, a Drosophilagene encoding a cofilin/ADF homologue, result in defects in centrosome migration and cytokinesis by Gunsalus (1995)
10.1242/jcs.101.3.547 / J Cell Sci / Mutants of the microtubule motor protein, nonclaret disjunctional, affect spindle structure and chromosome movement in meiosis and mitosis by Hatsumi (1992)
10.1038/382420a0 / Nature / Self-organization of microtubules into bipolar spindles around artificial chromosomes in Xenopusegg extracts by Heald (1996)
10.1083/jcb.138.3.615 / J Cell Biol / Spindle assembly in Xenopusegg extracts: respective roles of centrosomes and microtubule self-organization by Heald (1997)
10.1242/jcs.109.12.2779 / J Cell Sci / Assembly of ring canals in the male germ line from structural components of the contractile ring by Hime (1996)
10.1016/0014-4827(71)90153-4 / Exp Cell Res / Analysis of cleavage stimulus by means of micromanipulation of sea urchin eggs by Hiramoto (1971)
10.1016/0955-0674(94)90117-1 / Curr Opin Cell Biol / Cellular roles of kinesin and related proteins by Hoyt (1994)
10.1016/0092-8674(86)90318-1 / Cell / Beyond self-assembly: from microtubule to morphogenesis by Kirschner (1986)
{'key': '2023072823555888200_B34', 'first-page': '193', 'article-title': 'Method for feeding ethyl methane sulphonate (E.M.S.) to Drosophilamales', 'volume': '43', 'author': 'Lewis', 'year': '1968', 'journal-title': 'Drosophila Inform Serv'} / Drosophila Inform Serv / Method for feeding ethyl methane sulphonate (E.M.S.) to Drosophilamales by Lewis (1968)
10.1016/S0092-8674(00)81258-1 / Cell / The homeotic target gene centrosomin encodes an essential centrosomal component by Li (1996)
{'key': '2023072823555888200_B36'}
10.1083/jcb.123.6.1475 / J Cell Biol / Interpolar spindle microtubules in PtK cells by Mastronarde (1993)
10.1016/0092-8674(87)90560-5 / Cell / The role of tubulin polymerization during spindle elongation in vitro by Masuda (1987)
10.1083/jcb.134.2.455 / J Cell Biol / Anastral meiotic spindle morphogenesis: role of the non-claret disjunctional kinesin-like protein by Matthies (1996)
10.1126/science.270.5242.1595 / Science / Chromosomal control of meiotic cell division by McKim (1995)
10.1083/jcb.138.5.953 / J Cell Biol / Pathways of spindle pole formation: different mechanisms; conserved components by Merdes (1997)
10.1016/S0092-8674(00)81365-3 / Cell / A complex of NuMA and cytoplasmic dynein is essential for mitotic spindle assembly by Merdes (1996)
10.1002/jez.1401480107 / J Exp Zool / Experiments concerning the cleavage stimulus in sand dollar eggs by Rappaport (1961)
10.1016/S0074-7696(08)61065-7 / Int Rev Cytol / Establishment of the mechanism of cytokinesis in animal cells by Rappaport (1986)
10.1002/jez.1401890206 / J Exp Zool / Establishment of cleavage furrows by the mitotic spindle by Rappaport (1974)
10.1083/jcb.110.1.81 / J Cell Biol / Kinetochores are transported poleward along a single astral microtubule during chromosome attachment to the spindle in newt lung cells by Rieder (1990)
{'key': '2023072823555888200_B47'}
10.1002/bies.950150606 / BioEssays / Meiosis, mitosis and microtubule motors by Sawin (1993)
10.1083/jcb.103.5.1873 / J Cell Biol / The reproduction of centrosomes: nuclear versus cytoplasmic controls by Sluder (1986)
10.1083/jcb.100.3.897 / J Cell Biol / Experimental separation of pronuclei in fertilized sea urchin eggs: chromosomes do not organize a spindle in the absence of centrosomes by Sluder (1985)
10.1002/cm.970230102 / Cell Motil Cytoskelet / Spindle poles in higher plant mitosis by Smirnova (1992)
10.1083/jcb.102.5.1679 / J Cell Biol / Aster-free spindle poles in insect spermatocytes: evidence for chromosome-induced spindle formation by Steffen (1986)
10.1083/jcb.116.5.1167 / J Cell Biol / Meiotic spindle assembly in Drosophilafemales: behavior of nonexchange chromosomes and the effects of mutations in the nod kinesin-like protein by Theurkauf (1992)
10.1091/mbc.7.10.1547 / Mol Biol Cell / The kinetochore microtubule minus-ends disassembly associated with poleward flux produces a force that can do work by Waters (1996)
10.1016/S0955-0674(97)80149-4 / Curr Opin Cell Biol / Pathways of spindle assembly by Waters (1997)
10.1083/jcb.129.3.709 / J Cell Biol / The Drosophilakinesin-like protein KLP3A is a midbody component required for central spindle assembly and initiation of cytokinesis by Williams (1995)
10.1083/jcb.129.5.1287 / J Cell Biol / The impact of chromosomes and centrosomes on spindle assembly as observed in living cells by Zhang (1995)
10.1038/382466a0 / Nature / Anaphase and cytokinesis in the absence of chromosomes by Zhang (1996)
10.1016/0092-8674(91)90389-G / Cell / γ-tubulin is present in Drosophila melanogaster and homo sapiensand is associated with the centrosome by Zheng (1991)

Dates

Type	When
Created	23 years, 1 month ago (July 26, 2002, 12:47 p.m.)
Deposited	2 years, 1 month ago (July 28, 2023, 7:57 p.m.)
Indexed	2 months, 3 weeks ago (June 14, 2025, 1:42 a.m.)
Issued	27 years ago (Aug. 10, 1998)
Published	27 years ago (Aug. 10, 1998)
Published Online	27 years ago (Aug. 10, 1998)
Published Print	27 years ago (Aug. 10, 1998)

Funders 0

None

BibTeX

@article{Bonaccorsi_1998, title={Spindle Self-organization and Cytokinesis During Male Meiosis in asterless Mutants of Drosophila melanogaster }, volume={142}, ISSN={1540-8140}, url={http://dx.doi.org/10.1083/jcb.142.3.751}, DOI={10.1083/jcb.142.3.751}, number={3}, journal={The Journal of Cell Biology}, publisher={Rockefeller University Press}, author={Bonaccorsi, Silvia and Giansanti, Maria Grazia and Gatti, Maurizio}, year={1998}, month=aug, pages={751–761} }

JSON

{
  "indexed": {
    "date-parts": [
      [
        2025,
        6,
        14
      ]
    ],
    "date-time": "2025-06-14T05:42:49Z",
    "timestamp": 1749879769912
  },
  "reference-count": 59,
  "publisher": "Rockefeller University Press",
  "issue": "3",
  "content-domain": {
    "domain": [
      "rupress.org"
    ],
    "crossmark-restriction": true
  },
  "published-print": {
    "date-parts": [
      [
        1998,
        8,
        10
      ]
    ]
  },
  "abstract": "<jats:p>While Drosophila female meiosis is anastral, both meiotic divisions in Drosophila males exhibit prominent asters. We have identified a gene we call asterless (asl) that is required for aster formation during male meiosis. Ultrastructural analysis showed that asl mutants have morphologically normal centrioles. However, immunostaining with antibodies directed either to \u03b3 tubulin or centrosomin revealed that these proteins do not accumulate in the centrosomes, as occurs in wild-type. Thus, asl appears to specify a function required for the assembly of centrosomal material around the centrioles.</jats:p>\n               <jats:p>Despite the absence of asters, meiotic cells of asl mutants manage to develop an anastral spindle. Microtubules grow from multiple sites around the chromosomes, and then focus into a peculiar bipolar spindle that mediates chromosome segregation, although in a highly irregular way.</jats:p>\n               <jats:p>Surprisingly, asl spermatocytes eventually form a morphologically normal ana\u2013telophase central spindle that has full ability to stimulate cytokinesis. These findings challenge the classical view on central spindle assembly, arguing for a self-organization of this structure from either preexisting or newly formed microtubules. In addition, these findings strongly suggest that the asters are not required for signaling cytokinesis.</jats:p>",
  "DOI": "10.1083/jcb.142.3.751",
  "type": "journal-article",
  "created": {
    "date-parts": [
      [
        2002,
        7,
        26
      ]
    ],
    "date-time": "2002-07-26T16:47:50Z",
    "timestamp": 1027702070000
  },
  "page": "751-761",
  "update-policy": "http://dx.doi.org/10.1083/jcb.crossmarkpolicy",
  "source": "Crossref",
  "is-referenced-by-count": 146,
  "title": "Spindle Self-organization and Cytokinesis During Male Meiosis in <i>asterless</i> Mutants of <i>Drosophila melanogaster </i>",
  "prefix": "10.1083",
  "volume": "142",
  "author": [
    {
      "given": "Silvia",
      "family": "Bonaccorsi",
      "sequence": "first",
      "affiliation": [
        {
          "name": "Istituto Pasteur-Fondazione Cenci Bolognetti, Dipartimento di Genetica e Biologia Molecolare, Universita' di Roma La Sapienza, 00185 Rome, Italy"
        }
      ]
    },
    {
      "given": "Maria Grazia",
      "family": "Giansanti",
      "sequence": "additional",
      "affiliation": [
        {
          "name": "Istituto Pasteur-Fondazione Cenci Bolognetti, Dipartimento di Genetica e Biologia Molecolare, Universita' di Roma La Sapienza, 00185 Rome, Italy"
        }
      ]
    },
    {
      "given": "Maurizio",
      "family": "Gatti",
      "sequence": "additional",
      "affiliation": [
        {
          "name": "Istituto Pasteur-Fondazione Cenci Bolognetti, Dipartimento di Genetica e Biologia Molecolare, Universita' di Roma La Sapienza, 00185 Rome, Italy"
        }
      ]
    }
  ],
  "member": "291",
  "published-online": {
    "date-parts": [
      [
        1998,
        8,
        10
      ]
    ]
  },
  "reference": [
    {
      "key": "2023072823555888200_B1",
      "doi-asserted-by": "crossref",
      "first-page": "15",
      "DOI": "10.1007/BF00710603",
      "article-title": "Segregation of holocentric chromosomes at meiosis in the nematode Caenorhabditis elegans.",
      "volume": "1",
      "author": "Albertson",
      "year": "1993",
      "journal-title": "Chromosome Res"
    },
    {
      "key": "2023072823555888200_B2",
      "doi-asserted-by": "crossref",
      "first-page": "41",
      "DOI": "10.1016/0955-0674(94)90114-7",
      "article-title": "Centrosome and kinetochore movement during mitosis",
      "volume": "6",
      "author": "Ault",
      "year": "1994",
      "journal-title": "Curr Opin Cell Biol"
    },
    {
      "key": "2023072823555888200_B3",
      "doi-asserted-by": "crossref",
      "first-page": "183",
      "DOI": "10.1006/excr.1997.3618",
      "article-title": "Centriole and centrosome dynamics during the embryonic cell cycles that follow the formation of the cellular blastoderm in Drosophila.",
      "volume": "234",
      "author": "Callaini",
      "year": "1997",
      "journal-title": "Exp Cell Res"
    },
    {
      "key": "2023072823555888200_B4",
      "doi-asserted-by": "crossref",
      "first-page": "225",
      "DOI": "10.1091/mbc.7.2.225",
      "article-title": "Signals from the spindle midzone are required for the stimulation of cytokinesis in cultured epithelial cells",
      "volume": "7",
      "author": "Cao",
      "year": "1996",
      "journal-title": "Mol Biol Cell"
    },
    {
      "key": "2023072823555888200_B5",
      "doi-asserted-by": "crossref",
      "first-page": "3521",
      "DOI": "10.1242/jcs.107.12.3521",
      "article-title": "Chromatin and microtubule organization during premeiotic, meiotic, and early postmeiotic stages of Drosophila melanogasterspermatogenesis",
      "volume": "107",
      "author": "Cenci",
      "year": "1994",
      "journal-title": "J Cell Sci"
    },
    {
      "key": "2023072823555888200_B6",
      "doi-asserted-by": "crossref",
      "first-page": "2765",
      "DOI": "10.1083/jcb.103.6.2765",
      "article-title": "Micromanipulated bivalents can trigger mini-spindle formation in Drosophila melanogasterspermatocyte cytoplasm",
      "volume": "103",
      "author": "Church",
      "year": "1986",
      "journal-title": "J Cell Biol"
    },
    {
      "key": "2023072823555888200_B7",
      "doi-asserted-by": "crossref",
      "first-page": "255",
      "DOI": "10.1038/274255a0",
      "article-title": "Aploid cell cultures of Drosophila melanogaster.",
      "volume": "374",
      "author": "Debec",
      "year": "1978",
      "journal-title": "Nature"
    },
    {
      "key": "2023072823555888200_B8",
      "doi-asserted-by": "crossref",
      "first-page": "2645",
      "DOI": "10.1242/jcs.108.7.2645",
      "article-title": "Polar organization of \u03b3 tubulin in acentriolar mitotic spindles of Drosophila melanogastercells",
      "volume": "108",
      "author": "Debec",
      "year": "1995",
      "journal-title": "J Cell Sci"
    },
    {
      "key": "2023072823555888200_B9",
      "first-page": "161",
      "article-title": "The dispensability of the centrioles in the spermatocyte divisions of Pales ferruginea (Nematocera).",
      "volume": "19(Suppl.)",
      "author": "Dietz",
      "year": "1966",
      "journal-title": "Heredity"
    },
    {
      "key": "2023072823555888200_B10",
      "doi-asserted-by": "crossref",
      "first-page": "675",
      "DOI": "10.1101/SQB.1991.056.01.076",
      "article-title": "Role of the centromere/kinetochore in cell cycle control",
      "volume": "56",
      "author": "Earnshaw",
      "year": "1991",
      "journal-title": "Cold Spring Harbor Symp Quant Biol"
    },
    {
      "key": "2023072823555888200_B11",
      "doi-asserted-by": "crossref",
      "first-page": "617",
      "DOI": "10.1083/jcb.132.4.617",
      "article-title": "Molecular characterization of the 50-kD subunit of dynactin reveals function for the complex in chromosome alignment and spindle organization during mitosis",
      "volume": "132",
      "author": "Echeverri",
      "year": "1996",
      "journal-title": "J Cell Biol"
    },
    {
      "key": "2023072823555888200_B12",
      "doi-asserted-by": "crossref",
      "first-page": "1321",
      "DOI": "10.1083/jcb.137.6.1321",
      "article-title": "Spindle dynamics during meiosis in Drosophilaoocytes",
      "volume": "137",
      "author": "Endow",
      "year": "1997",
      "journal-title": "J Cell Biol"
    },
    {
      "key": "2023072823555888200_B13",
      "doi-asserted-by": "crossref",
      "first-page": "165",
      "DOI": "10.1083/jcb.131.1.165",
      "article-title": "Anillin, a contractile ring protein that cycles from the nucleus to the cell cortex",
      "volume": "131",
      "author": "Field",
      "year": "1995",
      "journal-title": "J Cell Biol"
    },
    {
      "key": "2023072823555888200_B14",
      "doi-asserted-by": "crossref",
      "first-page": "2041",
      "DOI": "10.1242/jcs.109.8.2041",
      "article-title": "Function of spindle microtubules in directing cortical movements and actin filaments organization in dividing cultured cells",
      "volume": "109",
      "author": "Fishkind",
      "year": "1996",
      "journal-title": "J Cell Sci"
    },
    {
      "key": "2023072823555888200_B15",
      "doi-asserted-by": "crossref",
      "first-page": "23",
      "DOI": "10.1016/0955-0674(95)80041-7",
      "article-title": "New horizons for cytokinesis",
      "volume": "7",
      "author": "Fishkind",
      "year": "1995",
      "journal-title": "Curr Opin Cell Biol"
    },
    {
      "key": "2023072823555888200_B16"
    },
    {
      "key": "2023072823555888200_B17",
      "doi-asserted-by": "crossref",
      "first-page": "1055",
      "DOI": "10.1083/jcb.138.5.1055",
      "article-title": "Mitotic spindle poles are organized by structural and motor proteins in addition to centrosomes",
      "volume": "138",
      "author": "Gaglio",
      "year": "1997",
      "journal-title": "J Cell Biol"
    },
    {
      "key": "2023072823555888200_B18",
      "doi-asserted-by": "crossref",
      "first-page": "693",
      "DOI": "10.1083/jcb.131.3.693",
      "article-title": "NuMA is required for the organization of microtubules into aster-like mitotic arrays",
      "volume": "131",
      "author": "Gaglio",
      "year": "1995",
      "journal-title": "J Cell Biol"
    },
    {
      "key": "2023072823555888200_B19",
      "doi-asserted-by": "crossref",
      "first-page": "683",
      "DOI": "10.1093/genetics/81.4.683",
      "article-title": "Isolation and characterization of sex-linked female sterile mutants in Drosophila melanogaster.",
      "volume": "81",
      "author": "Gans",
      "year": "1975",
      "journal-title": "Genetics"
    },
    {
      "key": "2023072823555888200_B20",
      "doi-asserted-by": "crossref",
      "first-page": "516",
      "DOI": "10.1016/0012-1606(92)90190-R",
      "article-title": "Microtubule organization during maturation of Xenopusoocytes: assembly and rotation of the meiotic spindles",
      "volume": "151",
      "author": "Gard",
      "year": "1992",
      "journal-title": "Dev Biol"
    },
    {
      "key": "2023072823555888200_B21",
      "doi-asserted-by": "crossref",
      "first-page": "396",
      "DOI": "10.1101/gad.12.3.396",
      "article-title": "Cooperative interaction between the central spindle and the contractile ring during Drosophilacytokinesis",
      "volume": "12",
      "author": "Giansanti",
      "year": "1998",
      "journal-title": "Genes Dev"
    },
    {
      "key": "2023072823555888200_B22",
      "doi-asserted-by": "crossref",
      "first-page": "815",
      "DOI": "10.1016/S0955-0674(97)80082-8",
      "article-title": "The mechanism and control of cytokinesis",
      "volume": "9",
      "author": "Glotzer",
      "year": "1997",
      "journal-title": "Curr Opin Cell Biol"
    },
    {
      "key": "2023072823555888200_B23"
    },
    {
      "key": "2023072823555888200_B24",
      "doi-asserted-by": "crossref",
      "first-page": "591",
      "DOI": "10.1016/0092-8674(81)90167-7",
      "article-title": "Kinetochore structure and its role in chromosome orientation during the first meiotic division in male D. melanogaster.",
      "volume": "25",
      "author": "Goldstein",
      "year": "1981",
      "journal-title": "Cell"
    },
    {
      "key": "2023072823555888200_B25",
      "doi-asserted-by": "crossref",
      "first-page": "205",
      "DOI": "10.1017/S0016672300028664",
      "article-title": "Relationship between chromosome content and nuclear diameter in early spermatids of Drosophila melanogaster.",
      "volume": "54",
      "author": "Gonzalez",
      "year": "1989",
      "journal-title": "Genet Res"
    },
    {
      "key": "2023072823555888200_B26",
      "doi-asserted-by": "crossref",
      "first-page": "1",
      "DOI": "10.1083/jcb.131.5.1243",
      "article-title": "Mutations in twinstar, a Drosophilagene encoding a cofilin/ADF homologue, result in defects in centrosome migration and cytokinesis",
      "volume": "131",
      "author": "Gunsalus",
      "year": "1995",
      "journal-title": "J Cell Biol"
    },
    {
      "key": "2023072823555888200_B27",
      "doi-asserted-by": "crossref",
      "first-page": "547",
      "DOI": "10.1242/jcs.101.3.547",
      "article-title": "Mutants of the microtubule motor protein, nonclaret disjunctional, affect spindle structure and chromosome movement in meiosis and mitosis",
      "volume": "101",
      "author": "Hatsumi",
      "year": "1992",
      "journal-title": "J Cell Sci"
    },
    {
      "key": "2023072823555888200_B28",
      "doi-asserted-by": "crossref",
      "first-page": "420",
      "DOI": "10.1038/382420a0",
      "article-title": "Self-organization of microtubules into bipolar spindles around artificial chromosomes in Xenopusegg extracts",
      "volume": "382",
      "author": "Heald",
      "year": "1996",
      "journal-title": "Nature"
    },
    {
      "key": "2023072823555888200_B29",
      "doi-asserted-by": "crossref",
      "first-page": "615",
      "DOI": "10.1083/jcb.138.3.615",
      "article-title": "Spindle assembly in Xenopusegg extracts: respective roles of centrosomes and microtubule self-organization",
      "volume": "138",
      "author": "Heald",
      "year": "1997",
      "journal-title": "J Cell Biol"
    },
    {
      "key": "2023072823555888200_B30",
      "doi-asserted-by": "crossref",
      "first-page": "2779",
      "DOI": "10.1242/jcs.109.12.2779",
      "article-title": "Assembly of ring canals in the male germ line from structural components of the contractile ring",
      "volume": "109",
      "author": "Hime",
      "year": "1996",
      "journal-title": "J Cell Sci"
    },
    {
      "key": "2023072823555888200_B31",
      "doi-asserted-by": "crossref",
      "first-page": "291",
      "DOI": "10.1016/0014-4827(71)90153-4",
      "article-title": "Analysis of cleavage stimulus by means of micromanipulation of sea urchin eggs",
      "volume": "8",
      "author": "Hiramoto",
      "year": "1971",
      "journal-title": "Exp Cell Res"
    },
    {
      "key": "2023072823555888200_B32",
      "doi-asserted-by": "crossref",
      "first-page": "63",
      "DOI": "10.1016/0955-0674(94)90117-1",
      "article-title": "Cellular roles of kinesin and related proteins",
      "volume": "6",
      "author": "Hoyt",
      "year": "1994",
      "journal-title": "Curr Opin Cell Biol"
    },
    {
      "key": "2023072823555888200_B33",
      "doi-asserted-by": "crossref",
      "first-page": "329",
      "DOI": "10.1016/0092-8674(86)90318-1",
      "article-title": "Beyond self-assembly: from microtubule to morphogenesis",
      "volume": "45",
      "author": "Kirschner",
      "year": "1986",
      "journal-title": "Cell"
    },
    {
      "key": "2023072823555888200_B34",
      "first-page": "193",
      "article-title": "Method for feeding ethyl methane sulphonate (E.M.S.) to Drosophilamales",
      "volume": "43",
      "author": "Lewis",
      "year": "1968",
      "journal-title": "Drosophila Inform Serv"
    },
    {
      "key": "2023072823555888200_B35",
      "doi-asserted-by": "crossref",
      "first-page": "585",
      "DOI": "10.1016/S0092-8674(00)81258-1",
      "article-title": "The homeotic target gene centrosomin encodes an essential centrosomal component",
      "volume": "85",
      "author": "Li",
      "year": "1996",
      "journal-title": "Cell"
    },
    {
      "key": "2023072823555888200_B36"
    },
    {
      "key": "2023072823555888200_B37",
      "doi-asserted-by": "crossref",
      "first-page": "1475",
      "DOI": "10.1083/jcb.123.6.1475",
      "article-title": "Interpolar spindle microtubules in PtK cells",
      "volume": "123",
      "author": "Mastronarde",
      "year": "1993",
      "journal-title": "J Cell Biol"
    },
    {
      "key": "2023072823555888200_B38",
      "doi-asserted-by": "crossref",
      "first-page": "193",
      "DOI": "10.1016/0092-8674(87)90560-5",
      "article-title": "The role of tubulin polymerization during spindle elongation in vitro",
      "volume": "49",
      "author": "Masuda",
      "year": "1987",
      "journal-title": "Cell"
    },
    {
      "key": "2023072823555888200_B39",
      "doi-asserted-by": "crossref",
      "first-page": "455",
      "DOI": "10.1083/jcb.134.2.455",
      "article-title": "Anastral meiotic spindle morphogenesis: role of the non-claret disjunctional kinesin-like protein",
      "volume": "134",
      "author": "Matthies",
      "year": "1996",
      "journal-title": "J Cell Biol"
    },
    {
      "key": "2023072823555888200_B40",
      "doi-asserted-by": "crossref",
      "first-page": "1595",
      "DOI": "10.1126/science.270.5242.1595",
      "article-title": "Chromosomal control of meiotic cell division",
      "volume": "270",
      "author": "McKim",
      "year": "1995",
      "journal-title": "Science"
    },
    {
      "key": "2023072823555888200_B41",
      "doi-asserted-by": "crossref",
      "first-page": "953",
      "DOI": "10.1083/jcb.138.5.953",
      "article-title": "Pathways of spindle pole formation: different mechanisms; conserved components",
      "volume": "138",
      "author": "Merdes",
      "year": "1997",
      "journal-title": "J Cell Biol"
    },
    {
      "key": "2023072823555888200_B42",
      "doi-asserted-by": "crossref",
      "first-page": "447",
      "DOI": "10.1016/S0092-8674(00)81365-3",
      "article-title": "A complex of NuMA and cytoplasmic dynein is essential for mitotic spindle assembly",
      "volume": "87",
      "author": "Merdes",
      "year": "1996",
      "journal-title": "Cell"
    },
    {
      "key": "2023072823555888200_B43",
      "doi-asserted-by": "crossref",
      "first-page": "81",
      "DOI": "10.1002/jez.1401480107",
      "article-title": "Experiments concerning the cleavage stimulus in sand dollar eggs",
      "volume": "148",
      "author": "Rappaport",
      "year": "1961",
      "journal-title": "J Exp Zool"
    },
    {
      "key": "2023072823555888200_B44",
      "doi-asserted-by": "crossref",
      "first-page": "245",
      "DOI": "10.1016/S0074-7696(08)61065-7",
      "article-title": "Establishment of the mechanism of cytokinesis in animal cells",
      "volume": "105",
      "author": "Rappaport",
      "year": "1986",
      "journal-title": "Int Rev Cytol"
    },
    {
      "key": "2023072823555888200_B45",
      "doi-asserted-by": "crossref",
      "first-page": "189",
      "DOI": "10.1002/jez.1401890206",
      "article-title": "Establishment of cleavage furrows by the mitotic spindle",
      "volume": "189",
      "author": "Rappaport",
      "year": "1974",
      "journal-title": "J Exp Zool"
    },
    {
      "key": "2023072823555888200_B46",
      "doi-asserted-by": "crossref",
      "first-page": "81",
      "DOI": "10.1083/jcb.110.1.81",
      "article-title": "Kinetochores are transported poleward along a single astral microtubule during chromosome attachment to the spindle in newt lung cells",
      "volume": "110",
      "author": "Rieder",
      "year": "1990",
      "journal-title": "J Cell Biol"
    },
    {
      "key": "2023072823555888200_B47"
    },
    {
      "key": "2023072823555888200_B48",
      "doi-asserted-by": "crossref",
      "first-page": "399",
      "DOI": "10.1002/bies.950150606",
      "article-title": "Meiosis, mitosis and microtubule motors",
      "volume": "15",
      "author": "Sawin",
      "year": "1993",
      "journal-title": "BioEssays"
    },
    {
      "key": "2023072823555888200_B49",
      "doi-asserted-by": "crossref",
      "first-page": "1873",
      "DOI": "10.1083/jcb.103.5.1873",
      "article-title": "The reproduction of centrosomes: nuclear versus cytoplasmic controls",
      "volume": "103",
      "author": "Sluder",
      "year": "1986",
      "journal-title": "J Cell Biol"
    },
    {
      "key": "2023072823555888200_B50",
      "doi-asserted-by": "crossref",
      "first-page": "897",
      "DOI": "10.1083/jcb.100.3.897",
      "article-title": "Experimental separation of pronuclei in fertilized sea urchin eggs: chromosomes do not organize a spindle in the absence of centrosomes",
      "volume": "100",
      "author": "Sluder",
      "year": "1985",
      "journal-title": "J Cell Biol"
    },
    {
      "key": "2023072823555888200_B51",
      "doi-asserted-by": "crossref",
      "first-page": "1",
      "DOI": "10.1002/cm.970230102",
      "article-title": "Spindle poles in higher plant mitosis",
      "volume": "23",
      "author": "Smirnova",
      "year": "1992",
      "journal-title": "Cell Motil Cytoskelet"
    },
    {
      "key": "2023072823555888200_B52",
      "doi-asserted-by": "crossref",
      "first-page": "1679",
      "DOI": "10.1083/jcb.102.5.1679",
      "article-title": "Aster-free spindle poles in insect spermatocytes: evidence for chromosome-induced spindle formation",
      "volume": "102",
      "author": "Steffen",
      "year": "1986",
      "journal-title": "J Cell Biol"
    },
    {
      "key": "2023072823555888200_B53",
      "doi-asserted-by": "crossref",
      "first-page": "1167",
      "DOI": "10.1083/jcb.116.5.1167",
      "article-title": "Meiotic spindle assembly in Drosophilafemales: behavior of nonexchange chromosomes and the effects of mutations in the nod kinesin-like protein",
      "volume": "116",
      "author": "Theurkauf",
      "year": "1992",
      "journal-title": "J Cell Biol"
    },
    {
      "key": "2023072823555888200_B54",
      "doi-asserted-by": "crossref",
      "first-page": "1547",
      "DOI": "10.1091/mbc.7.10.1547",
      "article-title": "The kinetochore microtubule minus-ends disassembly associated with poleward flux produces a force that can do work",
      "volume": "7",
      "author": "Waters",
      "year": "1996",
      "journal-title": "Mol Biol Cell"
    },
    {
      "key": "2023072823555888200_B55",
      "doi-asserted-by": "crossref",
      "first-page": "37",
      "DOI": "10.1016/S0955-0674(97)80149-4",
      "article-title": "Pathways of spindle assembly",
      "volume": "9",
      "author": "Waters",
      "year": "1997",
      "journal-title": "Curr Opin Cell Biol"
    },
    {
      "key": "2023072823555888200_B56",
      "doi-asserted-by": "crossref",
      "first-page": "709",
      "DOI": "10.1083/jcb.129.3.709",
      "article-title": "The Drosophilakinesin-like protein KLP3A is a midbody component required for central spindle assembly and initiation of cytokinesis",
      "volume": "129",
      "author": "Williams",
      "year": "1995",
      "journal-title": "J Cell Biol"
    },
    {
      "key": "2023072823555888200_B57",
      "doi-asserted-by": "crossref",
      "first-page": "1287",
      "DOI": "10.1083/jcb.129.5.1287",
      "article-title": "The impact of chromosomes and centrosomes on spindle assembly as observed in living cells",
      "volume": "129",
      "author": "Zhang",
      "year": "1995",
      "journal-title": "J Cell Biol"
    },
    {
      "key": "2023072823555888200_B58",
      "doi-asserted-by": "crossref",
      "first-page": "466",
      "DOI": "10.1038/382466a0",
      "article-title": "Anaphase and cytokinesis in the absence of chromosomes",
      "volume": "382",
      "author": "Zhang",
      "year": "1996",
      "journal-title": "Nature"
    },
    {
      "key": "2023072823555888200_B59",
      "doi-asserted-by": "crossref",
      "first-page": "817",
      "DOI": "10.1016/0092-8674(91)90389-G",
      "article-title": "\u03b3-tubulin is present in Drosophila melanogaster and homo sapiensand is associated with the centrosome",
      "volume": "65",
      "author": "Zheng",
      "year": "1991",
      "journal-title": "Cell"
    }
  ],
  "container-title": "The Journal of Cell Biology",
  "original-title": [],
  "language": "en",
  "link": [
    {
      "URL": "https://rupress.org/jcb/article-pdf/142/3/751/1845448/9803040.pdf",
      "content-type": "application/pdf",
      "content-version": "vor",
      "intended-application": "syndication"
    },
    {
      "URL": "https://rupress.org/jcb/article-pdf/142/3/751/1845448/9803040.pdf",
      "content-type": "unspecified",
      "content-version": "vor",
      "intended-application": "similarity-checking"
    }
  ],
  "deposited": {
    "date-parts": [
      [
        2023,
        7,
        28
      ]
    ],
    "date-time": "2023-07-28T23:57:05Z",
    "timestamp": 1690588625000
  },
  "score": 1,
  "resource": {
    "primary": {
      "URL": "https://rupress.org/jcb/article/142/3/751/15852/Spindle-Self-organization-and-Cytokinesis-During"
    }
  },
  "subtitle": [],
  "short-title": [],
  "issued": {
    "date-parts": [
      [
        1998,
        8,
        10
      ]
    ]
  },
  "references-count": 59,
  "journal-issue": {
    "issue": "3",
    "published-print": {
      "date-parts": [
        [
          1998,
          8,
          10
        ]
      ]
    }
  },
  "URL": "http://dx.doi.org/10.1083/jcb.142.3.751",
  "relation": {},
  "ISSN": [
    "0021-9525",
    "1540-8140"
  ],
  "subject": [],
  "published": {
    "date-parts": [
      [
        1998,
        8,
        10
      ]
    ]
  }
}