Midzone microtubule bundles are continuously required for cytokinesis in cultured epithelial cells [published erratum appears in J Cell Biol 1996 Dec;135(6 Pt 1):1679]

The current model of cytokinesis proposes that spindle poles and associated microtubules determine the cleavage plane, and, once the signal has been delivered to the cortex, the entire mitotic apparatus can be removed without affecting cell division. While supported by compelling data from Echinoderm embryos, recent observations suggest that the model may not be universally applicable. In this study, we have examined the relationship(s) among microtubules, chromosomes, and cleavage activity in living normal rat kidney (NRK) cells with multipolar mitotic figures. We found that cleavage activity correlated with the distribution of midzone microtubule bundles and Telophase Disc 60 protein (TD60) rather than the position of spindle poles. In addition, reduction of midzone microtubules near the cortex, by either nocodazole treatment or spontaneous reorganization in tripolar cells, caused inhibition or regression of furrowing. These results demonstrate that continuous interaction between midzone microtubule bundles and the cortex is required for successful cleavage in tissue culture cells.

[1]  J. Silverman,et al.  Function of spindle microtubules in directing cortical movement and actin filament organization in dividing cultured cells. , 1996, Journal of cell science.

[2]  Dahong Zhang,et al.  'Anaphase' and cytokinesis in the absence of chromosomes , 1996, Nature.

[3]  Y. Wang,et al.  Signals from the spindle midzone are required for the stimulation of cytokinesis in cultured epithelial cells. , 1996, Molecular biology of the cell.

[4]  R. Margolis,et al.  Delay of HeLa cell cleavage into interphase using dihydrocytochalasin B: retention of a postmitotic spindle and telophase disc correlates with synchronous cleavage recovery , 1995, The Journal of cell biology.

[5]  M. Gatti,et al.  The Drosophila kinesin-like protein KLP3A is a midbody component required for central spindle assembly and initiation of cytokinesis , 1995, The Journal of cell biology.

[6]  W. Earnshaw,et al.  Role of nonhistone proteins in the chromosomal events of mitosis , 1994, FASEB journal : official publication of the Federation of American Societies for Experimental Biology.

[7]  D. Mastronarde,et al.  Interpolar spindle microtubules in PTK cells , 1993, The Journal of cell biology.

[8]  D. Fishkind,et al.  Orientation and three-dimensional organization of actin filaments in dividing cultured cells , 1993, The Journal of cell biology.

[9]  R. Rappaport,et al.  Duration of division-related events in cleaving sand dollar eggs. , 1993, Developmental biology.

[10]  R. Margolis,et al.  The telophase disc: its possible role in mammalian cell cleavage. , 1993, BioEssays : news and reviews in molecular, cellular and developmental biology.

[11]  S. Strome Determination of cleavage planes , 1993, Cell.

[12]  Corey Nislow,et al.  A plus-end-directed motor enzyme that moves antiparallel microtubules in vitro localizes to the interzone of mitotic spindles , 1992, Nature.

[13]  Abigail H. Conrad,et al.  The role of microtubules in contractile ring function. , 1992, The Journal of experimental zoology.

[14]  T. Pollard,et al.  Cytokinesis , 1992, Current Biology.

[15]  R. Margolis,et al.  Telophase disc: a new mammalian mitotic organelle that bisects telophase cells with a possible function in cytokinesis. , 1991, Journal of cell science.

[16]  R. Zinkowski,et al.  CENP‐E, a novel human centromere‐associated protein required for progression from metaphase to anaphase. , 1991, The EMBO journal.

[17]  A. Harris,et al.  Simulation testing of mechanisms for inducing the formation of the contractile ring in cytokinesis , 1989, The Journal of cell biology.

[18]  G. Conrad,et al.  A model for astral stimulation of cytokinesis in animal cells , 1989, The Journal of cell biology.

[19]  R. Rappaport,et al.  Reversing cytoplasmic flow in nucleated, constricted sand dollar eggs , 1988 .

[20]  C. Sellitto,et al.  Distribution of a matrix component of the midbody during the cell cycle in Chinese hamster ovary cells , 1988, The Journal of cell biology.

[21]  W. Earnshaw,et al.  The inner centromere protein (INCENP) antigens: movement from inner centromere to midbody during mitosis , 1987, The Journal of cell biology.

[22]  J. McIntosh,et al.  Interzone microtubule behavior in late anaphase and telophase spindles , 1987, The Journal of cell biology.

[23]  H. Sakai,et al.  Distribution of fluorescently labeled tubulin injected into sand dollar eggs from fertilization through cleavage , 1985, The Journal of cell biology.

[24]  R. Rappaport Repeated furrow formation from a single mitotic apparatus in cylindrical sand dollar eggs. , 1985, The Journal of experimental zoology.

[25]  H. Ris,et al.  Centriole distribution during tripolar mitosis in Chinese hamster ovary cells , 1984, The Journal of cell biology.

[26]  R. Sloboda,et al.  Microinjection of fluorescent tubulin into dividing sea urchin cells , 1983, The Journal of cell biology.

[27]  J. White,et al.  On the mechanisms of cytokinesis in animal cells. , 1983, Journal of theoretical biology.

[28]  J. Small Organization of actin in the leading edge of cultured cells: influence of osmium tetroxide and dehydration on the ultrastructure of actin meshworks , 1981, The Journal of cell biology.

[29]  T. E. Schroeder,et al.  The origin of cleavage forces in dividing eggs. A mechanism in two steps. , 1981, Experimental cell research.

[30]  T. E. Schroeder,et al.  Cell cleavage. Ultrastructural evidence against equatorial stimulation by aster microtubules. , 1979, Experimental cell research.

[31]  K. Kawamura Microdissection studies on the dividing neuroblast of the grasshopper, with special reference to the mechanism of unequal cytokinesis. , 1977, Experimental cell research.

[32]  R. Davidson,et al.  Improved techniques for the induction of mammalian cell hybridization by polyethylene glycol , 1976, Somatic cell genetics.

[33]  R. Rappaport,et al.  Establishment of cleavage furrows by the mitotic spindle. , 1974, The Journal of experimental zoology.

[34]  R. Ebstein,et al.  DURATION OF STIMULUS AND LATENT PERIODS PRECEDING FURROW FORMATION IN SAND DOLLAR EGGS. , 1965, The Journal of experimental zoology.

[35]  R. Rappaport Experiments concerning the cleavage stimulus in sand dollar eggs. , 1961, The Journal of experimental zoology.

[36]  Y. Hiramoto Cell division without mitotic apparatus in sea urchin eggs. , 1956, Experimental cell research.

[37]  J. Mitchison,et al.  Cleavage of Sea-Urchin Eggs in Colchicine , 1953 .

[38]  Y. Wang,et al.  New horizons for cytokinesis. , 1995, Current opinion in cell biology.

[39]  T. Arai,et al.  Different reactivity with monoclonal anti-tubulin antibodies between native and fixed mitotic microtubules in sea urchin eggs. , 1994, Cell motility and the cytoskeleton.

[40]  Y. Wang,et al.  Culturing cells on the microscope stage. , 1989, Methods in cell biology.

[41]  G. Borisy,et al.  Detection of single fluorescent microtubules and methods for determining their dynamics in living cells. , 1988, Cell motility and the cytoskeleton.

[42]  Yu-Li Wang,et al.  Chapter 12 Culturing Cells on the Microscope Stage , 1988 .

[43]  G. Albrecht-Buehler,et al.  Distribution of multiple centrospheres determines migration of BHK syncitia. , 1987, Cell motility and the cytoskeleton.

[44]  I. Mabuchi,et al.  Biochemical aspects of cytokinesis. , 1986, International review of cytology.

[45]  J. Small,et al.  Organization of actin meshworks in cultured cells: the leading edge. , 1982, Cold Spring Harbor symposia on quantitative biology.

[46]  J. Lee,et al.  Preparation of tubulin from brain. , 1982, Methods in enzymology.

[47]  James C. Lee,et al.  [36] Preparation of tubulin from brain , 1982 .

[48]  Y. Hamaguchi MICROINJECTION OF COLCHICINE INTO SEA URCHIN EGGS , 1975, Development, growth & differentiation.

[49]  T. E. Schroeder The contractile ring. I. Fine structure of dividing mammalian (HeLa) cells and the effects of cytochalasin B. , 1970, Zeitschrift fur Zellforschung und mikroskopische Anatomie.