Advertisement
Journal Articles
Myosin II-independent processes in mitotic cells of Dictyostelium discoideum: redistribution of the nuclei, re-arrangement of the actin system and formation of the cleavage furrow
R. Neujahr, C. Heizer, G. Gerisch
Journal of Cell Science 1997 110: 123-137;

Summary

Mitosis was studied in multinucleated and mononucleated mutant cells of Dictyostelium discoideum that lack myosin II (Manstein et al. (1989) EMBO J. 8, 923–932). Multinucleated cells were produced by culture in suspension, mononucleated cells were enriched by growth on a solid surface (DeLozanne and Spudich (1987) Science 236, 1086–1091). The multinucleated cells disclosed interactions of mitotic complexes with the cell cortex that were not apparent in normal, mononucleated cells. During the anaphase stage, entire mitotic complexes consisting of spindle, microtubule asters, and separated sets of chromosomes were translocated to the periphery of the cells. These complexes were appended at a distance of about 3 microns from the cell surface, in a way that the spindle became orientated in parallel to the surface. Subsequently, lobes of the cell surface were formed around the asters of microtubules. These lobes were covered with tapered protrusions rich in coronin, an actin associated protein that typically accumulates in dynamic cell-surface projections (DeHostos et al. (1991) EMBO J. 10, 4097–4104). During their growth on a solid surface, mononucleated myosin II-null cells passed through the mitotic cleavage stages with a speed comparable to wild-type cells. Cytokinesis as linked to mitosis is distinguishable by several parameters from traction mediated cytofission, which results in the pinching off of pieces of a multinucleated cell in the interphase. The possibility is discussed that cells can cleave during mitosis without forming a contractile ring at the site of the cleavage furrow.

REFERENCES

    1. Baker J.,
    2. Theurkauf W. E. and
    3. Schubiger G.
    (1993). Dynamic changes in microtubule configuration correlate with nuclear migration in the preblastoderm Drosophila embryo. J. Cell Biol 122, 113–121
    OpenUrlAbstract/FREE Full Text
    1. Breckler J. and
    2. Burnside B.
    (1994). Myosin I localizes to the midbody region during mammalian cytokinesis. Cell Motil. Cytoskel 29, 312–320
    OpenUrlCrossRefPubMed
    1. Claviez M.,
    2. Pagh K.,
    3. Maruta H.,
    4. Baltes W.,
    5. Fisher P. and
    6. Gerisch G.
    (1982). Electron microscopic mapping of monoclonal antibodies on the tail region of Dictyostelium myosin. EMBO J 1, 1017–1022
    OpenUrlPubMedWeb of Science
    1. DeBiasio R. L.,
    2. LaRocca G. M.,
    3. Post P. L. and
    4. Taylor D. L.
    (1996). Myosin II transport, organization, and phosphorylation: evidence for cortical flow/solation-concentration coupling during cytokinesis and cell locomotion. Mol. Biol. Cell 7, 1259–1282
    OpenUrlAbstract/FREE Full Text
    1. DeHostos E. L.,
    2. Bradtke B.,
    3. Lottspeich F.,
    4. Guggenheim R. and
    5. Gerisch G.
    (1991). Coronin, an actin binding protein of Dictyostelium discoideum localized to cell surface projections, has sequence similarities to G proteinsubunits. EMBO J 10, 4097–4104
    OpenUrlPubMedWeb of Science
    1. DeHostos E. L.,
    2. Rehfueβ C.,
    3. Bradtke B.,
    4. Waddell D. R.,
    5. Albrecht R.,
    6. Murphy J. and
    7. Gerisch G.
    (1993). Dictyostelium mutants lacking the cytoskeletal protein coronin are defective in cytokinesis and cell motility. J. Cell Biol 120, 163–173
    OpenUrlAbstract/FREE Full Text
    1. DeLozanne 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. Fishkind D. J. and
    2. Wang Y.-I.
    (1995). New horizons for cytokinesis. Curr. Opin. Cell Biol 7, 23–31
    OpenUrlCrossRefPubMedWeb of Science
    1. Fujiwara K. and
    2. Pollard T. D.
    (1976). Fluorescent antibody localization of myosin in the cytoplasm, cleavage furrow, and mitotic spindle of human cells. J. Cell Biol 71, 848–875
    OpenUrlAbstract/FREE Full Text
    1. Fukui Y.,
    2. Lynch T. J.,
    3. Brzeska H. and
    4. Korn E. D.
    (1989). Myosin I is located at the leading edges of locomoting Dictyostelium amoebae. Nature 341, 328–331
    OpenUrlCrossRefPubMed
    1. Fukui Y.,
    2. DeLozanne A. and
    3. Spudich J. A.
    (1990). Structure and function of the cytoskeleton of a Dictyostelium myosin-defective mutant. J. Cell Biol 110, 367–378
    OpenUrlAbstract/FREE Full Text
    1. Fukui Y. and
    2. Inoue S.
    (1991). Cell division in Dictyostelium with special emphasis on actomyosin organization in cytokinesis. Cell Motil. Cytoskel 18, 41–54
    OpenUrlCrossRefPubMed
    1. Gerisch G.,
    2. Albrecht R.,
    3. Heizer C.,
    4. Hodgkinson S. and
    5. Maniak M.
    (1995). Chemoattractant-controlled accumulation of coronin at the leading edge of Dictyostelium cells monitored using a green fluorescent protein-coronin fusion protein. Curr. Biol 5, 1280–1285
    OpenUrlCrossRefPubMedWeb of Science
    1. Hellewell S. B. and
    2. Taylor D. L.
    (1979). The contractile basis of ameboid movement. VI. The solation-contraction coupling hypothesis. J. Cell Biol 83, 633–648
    OpenUrlAbstract/FREE Full Text
    1. Humbel P. K. and
    2. Biegelmann E.
    (1992). A preparation protocol for postembedding immunoelectron microscopy of Dictyostelium discoideum cells with monoclonal antibodies. Scan. Microsc 68, 817–825
    OpenUrl
    1. Jungbluth A.,
    2. von Arnim V.,
    3. Biegelmann E.,
    4. Humbel B.,
    5. Schweiger A. and
    6. Gerisch G.
    (1994). Strong increase in tyrosine phosphorylation of actin upon inhibition of oxidative phosphorylation: correlation with reversible rearrangements in the actin skeleton of Dictyostelium cells. J. Cell Sci 107, 117–125
    OpenUrlAbstract/FREE Full Text
    1. Karess R. E.,
    2. Chang X.,
    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 chromosome movement. J. Cell Biol 94, 165–178
    OpenUrlAbstract/FREE Full Text
    1. Kilmartin J. V.,
    2. Wright B. and
    3. Milstein C.
    (1982). Rat monoclonal antitubulin antibodies derived by using a new nonsecreting rat cell line. J. Cell Biol 93, 576–582
    OpenUrlAbstract/FREE Full Text
    1. Kitanishi-Yumura T. and
    2. Fukui Y.
    (1989). Actomyosin organization during cytokinesis: reversible translocation and differential redistribution in Dictyostelium. Cell Motil. Cytoskel 12, 78–89
    OpenUrlCrossRefPubMed
    1. Knecht D. A. and
    2. Loomis W. F.
    (1987). Antisense RNA inactivation of myosin heavy chain gene expression in Dictyostelium discoideum. Science 236, 1081–1085
    OpenUrlAbstract/FREE Full Text
    1. Kuspa A. and
    2. Loomis W. F.
    (1992). Tagging developmental genes in Dictyostelium by restriction enzyme-mediated integration of plasmid DNA. Proc. Nat. Acad. Sci. USA 89, 8803–8807
    OpenUrlAbstract/FREE Full Text
    1. Mabuchi I. and
    2. Okuno M.
    (1977). The effect of myosin antibody on the division of starfish blastomeres. J. Cell Biol 74, 251–263
    OpenUrlAbstract/FREE Full Text
    1. Manstein D. J.,
    2. Titus M. A.,
    3. DeLozanne A. and
    4. Spudich J. A.
    (1989). Gene replacement in Dictyostelium: generation of myosin null mutants. EMBO J 8, 923–932
    OpenUrlPubMedWeb of Science
    1. Pagh K. and
    2. Gerisch G.
    (1986). Monoclonal antibodies binding to the tail of Dictyostelium discoideum myosin: their effects on antiparallel and parallel assembly and actin-activated ATPase activity. J. Cell Biol 103, 1527–1538
    OpenUrlAbstract/FREE Full Text
    1. Rodriguez J. R. and
    2. Paterson B. M.
    (1990). Yeast myosin heavy chain mutant: Maintenance of the cell type specific budding pattern and the normaldeposition of chitin and cell wall components requires an intact myosin heavy chain gene. Cell Motil. Cytoskel 17, 301–308
    OpenUrlCrossRefPubMedWeb of Science
    1. Sanders S. L. and
    2. Field C. M.
    (1994). Septins in common?. Curr. Biol 4, 907–910
    OpenUrlCrossRefPubMed
    1. Schindl M.,
    2. Wallraff E.,
    3. Deubzer B.,
    4. Witke W.,
    5. Gerisch G. and
    6. Sackmann E.
    (1995). Cell-substrate interactions and locomotion of Dictyostelium wild-type and mutants defective in three cytoskeletal proteins: A study using quantitative reflection interference contrast microscopy. Biophys. J 68, 1177–1190
    OpenUrlCrossRefPubMedWeb of Science
    1. Spudich J. A.
    (1989). In pursuit of myosin function. Cell Regul 1, 1–11
    OpenUrlPubMedWeb of Science
    1. Sullivan W. and
    2. Theurkauf W. E.
    (1995). The cytoskeleton and morphogenesis of the early Drosophila embryo. Curr. Opin. Cell Biol 7, 18–22
    OpenUrlCrossRefPubMedWeb of Science
    1. Titus M. A.,
    2. Kuspa A. and
    3. Loomis W. F.
    (1994). Discovery of myosin genes by physical mapping in Dictyostelium. Proc. Nat. Acad. Sci. USA 91, 9446–9450
    OpenUrlAbstract/FREE Full Text
    1. Watts F. Z.,
    2. Shiels G. and
    3. Orr E.
    (1987). The yeast MY01 gene encoding a myosin-like protein required for cell division. EMBO J 6, 3499–3505
    OpenUrlPubMedWeb of Science
    1. Weber I.,
    2. Wallraff E.,
    3. Albrecht R. and
    4. Gerisch G.
    (1995). Motility and substratum adhesion of Dictyostelium wild-type and cytoskeletal mutant cells: a study by RICM/bright-field double-view image analysis. J. Cell Sci 108, 1519–1530
    OpenUrlAbstract/FREE Full Text
    1. Weeks G. and
    2. Weijer C. J.
    (1994). The Dictyostelium cell cycle and its relationship to differentiation. FEMS Microbiol. Lett 124, 123–130
    OpenUrlAbstract/FREE Full Text
    1. Wessels D.,
    2. Soll D. R.,
    3. Knecht D.,
    4. Loomis W. F.,
    5. DeLozanne A. and
    6. Spudich J.
    (1988). Cell motility and chemotaxis in Dictyostelium amebae lacking myosin heavy chain. Dev. Biol 128, 164–177
    OpenUrlCrossRefPubMedWeb of Science
    1. Yumura S.,
    2. Mori H. and
    3. Fukui Y.
    (1984). Localization of actin and myosin for the study of ameboid movement in Dictyostelium using improved immunofluorescence. J. Cell Biol 99, 894–899
    OpenUrlAbstract/FREE Full Text
    1. Yumura S. and
    2. Fukui Y.
    (1985). Reversible cyclic AMP-dependent change in distribution of myosin thick filaments in Dictyostelium. Nature 314, 194–196
    OpenUrlCrossRefPubMed
    1. Zurek B.,
    2. Sanger J. M.,
    3. Sanger J. W. and
    4. Jockusch B. M.
    (1990). Differential effects of myosin-antibody complexes on contractile rings and circumferential belts in epitheloid cells. J. Cell Sci 97, 297–306
    OpenUrlAbstract/FREE Full Text
Back to top

 Download PDF

Email
Journal Articles
Myosin II-independent processes in mitotic cells of Dictyostelium discoideum: redistribution of the nuclei, re-arrangement of the actin system and formation of the cleavage furrow
R. Neujahr, C. Heizer, G. Gerisch
Journal of Cell Science 1997 110: 123-137;
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

ASCBǀEMBO 2019 Special Collection

We're at ASCB - visit booth 1000 to meet the JCS team!
Enjoy a collection of articles published in Journal of Cell Science by a range of speakers at the ASCBǀEMBO 2019 Meeting. Featuring articles from the labs of JCS Editorial Advisory Board members, all articles in the collection are free to access.

Early-bird meeting deadline - 20 December

Wotton House

Don’t miss the early-bird application deadline for the 2020 JCS meeting on Host-Pathogen interface! Taking place 17-20 May 2020 at Wotton House, Surrey, UK, the meeting will bring together experts working at the interface between cell biology and pathogens. Places are limited, so apply to attend now.

Cell Scientist to Watch – Elizabeth Hinde

Elizabeth with her daughter and father.

From physics and chemistry to art and back again, Elizabeth Hinde is currently based at the University of Melbourne. Her research focuses on fluorescence microscopy methods to quantify live-cell nuclear organisation and the role chromatin dynamics play in maintaining genome function. Read the full interview to find out more. 

Have you heard about our Travelling Fellowships?

Huw and colleagues from the lab in Beijing

Early-career researchers can apply for up to £2,500 to offset the cost of travel and expenses to make collaborative visits to other labs around the world. Read about Huw’s experience in Beijing, where he spent time with the world leaders in the development of super-resolution microscopy, the Li lab at the Chinese Academy of Sciences.