Advertisement
Journal Articles
Cleavage furrow: timing of emergence of contractile ring actin filaments and establishment of the contractile ring by filament bundling in sea urchin eggs
I. Mabuchi
Journal of Cell Science 1994 107: 1853-1862;

Summary

Cleavage furrow formation at the first cell division of sea urchin and sand dollar eggs was investigated in detail by fluorescence staining of actin filaments with rhodamine-phalloidin of either whole eggs or isolated egg cortices. Cortical actin filaments were clustered at anaphase and then the clusters became fibrillar at the end of anaphase. The timing when the contractile ring actin filaments appear was precisely determined in the course of mitosis: accumulation of the contractile ring actin filaments at the equatorial cell cortex is first noticed at the beginning of telophase (shortly before furrow formation), when the chromosomal vesicles are fusing with each other. The accumulated actin filaments were not well organized at the early stage but were organized into parallel bundles as the furrowing progressed. The bundles were finally fused into a tightly packed filament belt. Wheat germ agglutinin (WGA)-binding sites were distributed on the surface of the egg in a manner similar to the actin filaments after anaphase. The WGA-binding sites became accumulated in the contractile ring together with the contractile ring actin filaments, indicating an intimate relationship between these sites and actin filament-anchoring sites on the plasma membrane. Myosin also appeared in the contractile ring together with the actin filaments. The ‘cleavage stimulus’, a signal hypothesized by Rappaport (reviewed by R. Rappaport (1986) Int. Rev. Cytol. 105, 245–281) was suggested to induce aggregation or bundling of the actin filaments in the cortical layer.

REFERENCES

    1. Berlin, R. D.,
    2. Oliver, J. M. and
    3. Walter, R. J.
    (1978). Surface functions during mitosis. I. Phagocytosis, pinocytosis and mobility of surface-bound Con A. Cell 15, 327–341
    OpenUrlCrossRefPubMedWeb of Science
    1. Burgess, D. R. and
    2. Schroeder, T. E.
    (1977). Polarized bundles of actin filaments within microvilli of fertilized sea urchin eggs. J. Cell Biol 74, 1032–1037
    OpenUrlAbstract/FREE Full Text
    1. Cande, W. Z.
    (1980). A permeabilized cell model for studying cytokinesis using mammalian tissue culture cells. J. Cell Biol 87, 326–335
    OpenUrlAbstract/FREE Full Text
    1. De Lozanne, A. and
    2. Spudich, J. A.
    (1987). Disruption of the Dictyostelium myosin heavy chain gene by homologous recombination. Science 236, 1086–1091
    OpenUrlAbstract/FREE Full Text
    1. Devore, J. J.,
    2. Conrad, G. W. and
    3. Rappaport, R.
    (1989). A model for astral stimulation of cytokinesis in animal cells. J. Cell Biol 109, 2225–2232
    OpenUrlAbstract/FREE Full Text
    1. Fishkind, D. J.,
    2. Bonder, E. M. and
    3. Begg, D. A.
    (1987). Isolation and characterization of sea urchin egg spectrin: calcium modulation of the spectrin-actin interaction. Cell Motil. Cytoskel 7, 304–314
    OpenUrlCrossRefPubMed
    1. Hayashi, T.,
    2. Silver, R. B.,
    3. Ip, W.,
    4. Cayer, M. L. and
    5. Smith, D. S.
    (1977). Actin-myosin interaction. Self assembly into a bipolar ‘contractile unit’. J. Mol. Biol 111, 159–171
    OpenUrlCrossRefPubMed
    1. Henson, J. H.,
    2. Begg, D. A.,
    3. Beaulieu, S. M.,
    4. Fishkind, D. J.,
    5. Bonder, E. M.,
    6. Terasaki, M.,
    7. Lebeche, D. and
    8. Kaminer, B.
    (1989). A calsequestrin-like protein in the endoplasmic reticulum of the sea urchin: localization and dynamics in the egg and first cell cycle embryo. J. Cell Biol 109, 149–161
    OpenUrlAbstract/FREE Full Text
    1. Hiramoto, Y.
    (1968). The mechanics and mechanism of cleavage in the sea-urchin egg. Symp. Soc. Exp. Biol 22, 311–327
    OpenUrlPubMed
    1. Hiramoto, Y.
    (1975). Force exerted by the cleavage furrow of sea urchin eggs. Dev. Growth Differ 17, 27–38
    OpenUrlCrossRef
    1. Kane, R. E.
    (1980). Induction of either contractile or structural actin-based gels in sea urchin egg cytoplasmic extract. J. Cell Biol 86, 803–809
    OpenUrlAbstract/FREE Full Text
    1. Karess, R. E.,
    2. Chang, X.-j,
    3. Edwards, K. A.,
    4. Kulkarni, S.,
    5. Aguilera, I. and
    6. Kiehart, D. P.
    (1991). The regulatory light chain of nonmuscle myosin is encoded by spaghetti-squash, a gene required for cytokinesis in Drosophila. Cell 65, 1177–1189
    OpenUrlCrossRefPubMedWeb of Science
    1. Kiehart, D. P.,
    2. Mabuchi, I. and
    3. Inoue, S.
    (1982). Evidence that myosin does not contribute to force production in chromosone movement. J. Cell Biol 103, 165–178
    OpenUrl
    1. Kishi, K.,
    2. Sakaki, T.,
    3. Kuroda, S.,
    4. Itoh, T. and
    5. Takai, Y.
    (1993). Regulation of cytoplasmic division of Xenopus embryo by rho p2l and its inhibitory GDP/GTP exchange protein (rho GDI). J. Cell Biol 120, 1187–1195
    OpenUrlAbstract/FREE Full Text
    1. Koppel, D. E.,
    2. Oliver, J. M. and
    3. Berlin, R. D.
    (1982). Surface functions during mitosis. III. Quantitative analysis of ligand-receptor movement into the cleavage furrow: diffusion vs flow. J. Cell Biol 93, 950–960
    OpenUrlAbstract/FREE Full Text
    1. Mabuchi, I. and
    2. Okuno, M.
    (1977). The effect of myosin antibody on the division of starfish balstomeres. J. Cell Biol 74, 251–263
    OpenUrlAbstract/FREE Full Text
    1. Mabuchi, I.,
    2. Hamaguchi, Y.,
    3. Kobayashi, T.,
    4. Hosoya, H.,
    5. Tsukita, S. and
    6. Tsukita, S.
    (1985). Alpha-actinin from sea urchin eggs: biochemical properties, interaction with actin, and distribution in the cell during fertilization and cleavage. J. Cell Biol 100, 375–383
    OpenUrlAbstract/FREE Full Text
    1. Mabuchi, I.
    (1986). Biochemical aspects of cytokinesis. Int. Rev. Cytol 101, 175–213
    OpenUrlCrossRefPubMedWeb of Science
    1. Mabuchi, I. and
    2. Kane, R. E.
    (1987). A 250K molecular weight actin-binding protein from actin-based gels formed in sea urchin egg cytoplasmic extract. J. Biochem 102, 947–956
    OpenUrlAbstract/FREE Full Text
    1. Mabuchi, I.,
    2. Tsukita, Sh.,
    3. Tsukita, Sa. and
    4. Sawai, T.
    (1988). Cleavage furrow isolated from newt eggs: contraction, organization of the actin filaments, and protein components of the furrow. Proc. Nat. Acad. Sci. USA 85, 5966–5970
    OpenUrlAbstract/FREE Full Text
    1. Mabuchi, I.
    (1990). Cleavage furrow formation and actin-modulating proteins. Ann. NY Acad. Sci 582, 131–146
    OpenUrlCrossRefPubMed
    1. Mabuchi, I. and
    2. Takano-Ohmuro, H.
    (1990). Effects of inhibitors of myosin light chain kinase and other protein kinases on the first cell division of sea urchin eggs. Dev. Growth Differ 32, 549–556
    OpenUrlCrossRefWeb of Science
    1. McCaig, C. D. and
    2. Robinson, K. R.
    (1982). The distribution of lectin receptors on the plasma membrane of the fertilized sea urchin egg during first and second cleavage. Dev. Biol 92, 197–202
    OpenUrlCrossRefPubMedWeb of Science
    1. Maekawa, S.,
    2. Endo, S. and
    3. Sakai, H.
    (1987). A high molecular weight actin binding protein: its localization in the cortex of the sea urchin egg. Exp. Cell Res 172, 340–353
    OpenUrlCrossRefPubMed
    1. Mittal, B.,
    2. Sanger, J. M. and
    3. Sanger, J. W.
    (1987). Visualization of myosin in living cells. J. Cell Biol 105, 1753–1760
    OpenUrlAbstract/FREE Full Text
    1. Norberg, R.,
    2. Lidman, K. and
    3. Fagraeus, A.
    (1975). Effects of cytochalasin B on fibroblasts, lymphoid cells, and platelets revealed by human anti-actin antibodies. Cell 6, 507–512
    OpenUrlCrossRef
    1. Otto, J. J.,
    2. Kane, R. E. and
    3. Bryan, J.
    (1980). Redistribution of actin and fascin in sea urchin eggs after fertilization. Cell Motil 1, 31–40
    OpenUrlCrossRefPubMed
    1. Rappaport, R.
    (1967). Cell division: Direct measurement of maximum tension exerted by furrow of echinoderm eggs. Science 156, 1241–1243
    OpenUrlAbstract/FREE Full Text
    1. Rappaport, R.
    (1986). Establishment of the mechanism of cytokinesis in animal cells. Int. Rev. Cytol 105, 245–281
    OpenUrlCrossRefPubMedWeb of Science
    1. Sanger, J. M. and
    2. Sanger, J. W.
    (1980). Banding and polarity of actin filaments in interphase and cleaving cells. J. Cell Biol 86, 568–575
    OpenUrlAbstract/FREE Full Text
    1. Satterwhite, L. L.,
    2. Lohka, M. J.,
    3. Wilson, K. L.,
    4. Scherson, T. Y.,
    5. Cisek, L. J.,
    6. Corden, J. L. and
    7. Pollard, T. D.
    (1992). Phosphorylation of myosin-II regulatory light chain by cyclin-p34cdc2: A mechanism for the timing of cytokinesis. J. Cell Biol 118, 595–605
    OpenUrlAbstract/FREE Full Text
    1. Schroeder, T. E.
    (1972). The contractile ring. II. Determining its brief existence, volumetric changes, and vital role in cleaving Arbacia eggs. J. Cell Biol 53, 419–434
    OpenUrlAbstract/FREE Full Text
    1. Schroeder, T. E.
    (1987). Fourth cleavage of sea urchin blastomeres: microtubule patterns and myosin localization in equal and unequal cell divisions. Dev. Biol 124, 9–22
    OpenUrlCrossRefPubMed
    1. Schroeder, T. E. and
    2. Otto, J. J.
    (1988). Immunofluorescent analysis of actin and myosin in isolated contractile rings of sea urchin eggs. Zool. Sci 5, 713–725
    OpenUrl
    1. Tosuji, H.,
    2. Mabuchi, I.,
    3. Fusetani, N. and
    4. Nakazawa, T.
    (1992). Calyculin A induces contractile ring-like apparatus formation and condensation of chromosomes in unfertilized sea urchin eggs. Proc. Nat. Acad. Sci. USA 89, 10613–10617
    OpenUrlAbstract/FREE Full Text
    1. Usui, N. and
    2. Yoneda, M.
    (1982). Ultrastructural basis of the tension increase in sea-urchin eggs prior to cytokinesis. Dev. Growth Differ 24, 453–465
    OpenUrlCrossRef
    1. Vacquier, V. D.
    (1975). The isolation of intact cortical granules from sea urchin eggs:. Calcium ions trigger granule discharge. Dev. Biol 43, 62–74
    OpenUrlCrossRefPubMed
    1. Weber, K.,
    2. Rathke, P. C.,
    3. Osborn, M. and
    4. Franke, W. W.
    (1976). Distribution of actin and tubulin in cells and in glycerinated cell models after treatment with cytochalasin B (CB). Exp. Cell Res 102, 285–297
    OpenUrlCrossRefPubMedWeb of Science
    1. Yamakita, Y.,
    2. Yamashiro, S. and
    3. Matsumura, F.
    (1994). In vivo phosphorylation of regulatory light chain of myosin II during mitosis of cultured cells. J. Cell Biol 124, 129–137
    OpenUrlAbstract/FREE Full Text
    1. Yoneda, M. and
    2. Dan, K.
    (1972). Tension at the surface of the dividing sea-urchin egg. J. Exp. Biol 57, 575–587
    OpenUrlAbstract/FREE Full Text
    1. Yonemura, S. and
    2. Kinoshita, S.
    (1986). Actin filament organization in the sand dollar egg cortex. Dev. Biol 115, 171–183
    OpenUrlCrossRefWeb of Science
    1. Yonemura, S. and
    2. Mabuchi, I.
    (1987). A wave of actin polymerization in the sea urchin egg cortex. Cell Motil. Cytoskel 7, 46–53
    OpenUrlCrossRefPubMedWeb of Science
    1. Yoshigaki, T.,
    2. Maekawa, S. and
    3. Sakai, H.
    (1989). Accumulation of WGA receptors in the cleavage furrow during cytokinesis in sea urchin eggs. Zool. Sci 6, 1153–.
    OpenUrl
Back to top

 Download PDF

Email
Journal Articles
Cleavage furrow: timing of emergence of contractile ring actin filaments and establishment of the contractile ring by filament bundling in sea urchin eggs
I. Mabuchi
Journal of Cell Science 1994 107: 1853-1862;
del.icio.us logo Digg logo Reddit logo Twitter logo CiteULike logo Facebook logo Google logo Mendeley logo
Citation Tools
Alerts

Article navigation

Other journals from The Company of Biologists

Advertisement

First Person interviews

Photo collage of Chen Yu, Sushmita Chatterjee, Ruiqi Wang and Lotte Vanheer.

Have you seen our First Person interviews with the early-career first authors of our papers? The authors talk about their work in and out of the lab, the journeys that led them to where they are now and the scientists who inspired them along the way. Recently, we caught up with first authors Maitreyi Rathod, Sushmita Chatterjee, Lotte Vanheer, Rachel Furlong, Pamela Adami, Ruiqi Wang and Chen Yu.

Travelling Fellowship – New imaging approach unveils a bigger picture

Highlights from Travelling Fellowship trips

Find out how Pamela Imperadore’s Travelling Fellowship grant from The Company of Biologists took her to Germany, where she used new imaging techniques to investigate the cellular machinery underlying octopus arm regeneration. Don’t miss the next application deadline for 2020 travel, coming up on 29 November. Where will your research take you?

preLights – Meet the preLighters: an interview with Maiko Kitaoka

Maiko Kitaoka

Maiko Kitaoka is a graduate student in the lab of Rebecca Heald at the University of California, Berkeley. Here she studies the cause of chromosome mis-segregation defects in Xenopus hybrids. We caught up with Maiko to discuss her research, science communication, ballet, preprints and more.

Journal Meeting – Cell Dynamics: Host-Pathogen Interface

Registration is now open for the third instalment of the highly successful Cellular Dynamics Meeting Series, and will focus on ‘Host-Pathogen Interface’. The meeting will take place 17-20 May 2020, and further information is available here.

Cell Science at a Glance – Adaptor protein complexes and disease at a glance

A new poster from the Robinson lab summarises what is known about the five adaptor protein complexes and discuss how this helps to explain the clinical features of different genetic disorders.

JCS joins the Review Commons initiative

Journal of Cell Science is pleased to be a part of the new and exciting Review Commons initiative, launched by EMBO and ASAPbio. Streamlining the publishing process, Review Commons enables high-quality peer review to take place before journal submission. Papers submitted to Review Commons will be assessed independently of any journal, focusing solely on the paper’s scientific rigor and merit.