Midbodies and phragmoplasts: analogous structures involved in cytokinesis.

Cytokinesis is an event common to all organisms that involves the precise coordination of independent pathways involved in cell-cycle regulation and microtubule, membrane, actin and organelle dynamics. In animal cells, the spindle midzone/midbody with associated endo-membrane system are required for late cytokinesis events, including furrow ingression and scission. In plants, cytokinesis is mediated by the phragmoplast, an array of microtubules, actin filaments and associated molecules that act as a framework for the future cell wall. In this article (which is part of the Cytokinesis series), we discuss recent studies that highlight the increasing number of similarities in the components and function of the spindle midzone/midbody in animals and the phragmoplast in plants, suggesting that they might be analogous structures.

[1]  T. O'Halloran,et al.  Cytokinesis failure in clathrin-minus cells is caused by cleavage furrow instability. , 2001, Cell motility and the cytoskeleton.

[2]  P. Hussey,et al.  A new class of microtubule-associated proteins in plants , 2000, Nature Cell Biology.

[3]  M. Glotzer,et al.  Central spindle assembly and cytokinesis require a kinesin-like protein/RhoGAP complex with microtubule bundling activity. , 2002, Developmental cell.

[4]  J. Scholey,et al.  Antagonistic microtubule-sliding motors position mitotic centrosomes in Drosophila early embryos , 1999, Nature Cell Biology.

[5]  M. Yanagida,et al.  Kinesin-related cut 7 protein associates with mitotic and meiotic spindles in fission yeast , 1992, Nature.

[6]  P. Hussey,et al.  The Arabidopsis Microtubule-Associated Protein AtMAP65-1: Molecular Analysis of Its Microtubule Bundling Activity , 2004, The Plant Cell Online.

[7]  J. Doonan,et al.  EB1 reveals mobile microtubule nucleation sites in Arabidopsis , 2003, Nature Cell Biology.

[8]  O. Rossanese,et al.  Deconstructing Golgi Inheritance , 2001, Traffic.

[9]  M. Glotzer,et al.  Animal cell cytokinesis. , 2001, Annual review of cell and developmental biology.

[10]  箕嶋 幸範 Phosphorylation by Aurora B converts MgcRacGAP to a RhoGAP during cytokinesis , 2005 .

[11]  J. Squirrell,et al.  Involvement of the actin cytoskeleton and homotypic membrane fusion in ER dynamics in Caenorhabditis elegans. , 2005, Molecular biology of the cell.

[12]  David Pellman,et al.  The molecular function of Ase1p , 2003, The Journal of cell biology.

[13]  T. O'Halloran,et al.  A novel role for clathrin in cytokinesis. , 1997, Proceedings of the National Academy of Sciences of the United States of America.

[14]  P. Hussey,et al.  The Plant Microtubule-Associated Protein AtMAP65-3/PLE Is Essential for Cytokinetic Phragmoplast Function , 2004, Current Biology.

[15]  J. M. Seguí-Simarro,et al.  Electron Tomographic Analysis of Somatic Cell Plate Formation in Meristematic Cells of Arabidopsis Preserved by High-Pressure Freezing , 2004, The Plant Cell Online.

[16]  M. Eliasa,et al.  The exocyst complex in plants , 2003 .

[17]  R. Gräf,et al.  Regulated expression of the centrosomal protein DdCP224 affects microtubule dynamics and reveals mechanisms for the control of supernumerary centrosome number. , 2003, Molecular biology of the cell.

[18]  R. Erikson,et al.  Peripheral Golgi protein GRASP65 is a target of mitotic polo-like kinase (Plk) and Cdc2. , 2000, Proceedings of the National Academy of Sciences of the United States of America.

[19]  David Pellman,et al.  Surfing on microtubule ends. , 2003, Trends in cell biology.

[20]  P. O’Farrell,et al.  Terminal Cytokinesis Events Uncovered after an RNAi Screen , 2004, Current Biology.

[21]  T. Mitchison,et al.  Mutations in the kinesin-like protein Eg5 disrupting localization to the mitotic spindle. , 1995, Proceedings of the National Academy of Sciences of the United States of America.

[22]  G. Fink,et al.  Two microtubule-associated proteins required for anaphase spindle movement in Saccharomyces cerevisiae [published erratum appears in J Cell Biol 1995 Oct;131(2):561] , 1995, The Journal of cell biology.

[23]  M. Fuller,et al.  Assembly of ring canals in the male germ line from structural components of the contractile ring. , 1996, Journal of cell science.

[24]  L. Blanchoin,et al.  Interactions of tobacco microtubule-associated protein MAP65-1b with microtubules. , 2004, The Plant journal : for cell and molecular biology.

[25]  H. Schwarz,et al.  Furrow-specific endocytosis during cytokinesis of zebrafish blastomeres. , 2002, Experimental cell research.

[26]  D. McCollum Cytokinesis: The Central Spindle Takes Center Stage , 2004, Current Biology.

[27]  P. Hussey,et al.  MOR1/GEM1 has an essential role in the plant-specific cytokinetic phragmoplast , 2002, Nature Cell Biology.

[28]  Anne Müsch,et al.  Microtubule Organization and Function in Epithelial Cells , 2004, Traffic.

[29]  J. Thyberg,et al.  Functions of the Golgi complex in cell division: formation of cell-matrix contacts and cell-cell communication channels in the terminal phase of cytokinesis. , 1994, Journal of submicroscopic cytology and pathology.

[30]  A. Valster,et al.  Caffeine inhibition of cytokinesis: effect on the phragmoplast cytoskeleton in livingTradescantia stamen hair cells , 1997, Protoplasma.

[31]  L. Peris,et al.  Evidence for the Involvement of Kif4 in the Anterograde Transport of L1-Containing Vesicles , 2000, The Journal of cell biology.

[32]  D. Geelen,et al.  Identification and Dynamics of Two Classes of Aurora-Like Kinases in Arabidopsis and Other Plantsw⃞ , 2005, The Plant Cell Online.

[33]  T. Weimbs,et al.  Syntaxin 2 and endobrevin are required for the terminal step of cytokinesis in mammalian cells. , 2003, Developmental cell.

[34]  J. Chan,et al.  The 65-kDa carrot microtubule-associated protein forms regularly arranged filamentous cross-bridges between microtubules. , 1999, Proceedings of the National Academy of Sciences of the United States of America.

[35]  John R. Pringle,et al.  Bni1p, a Yeast Formin Linking Cdc42p and the Actin Cytoskeleton During Polarized Morphogenesis , 1997, Science.

[36]  J. Garin,et al.  The mammalian passenger protein TD-60 is an RCC1 family member with an essential role in prometaphase to metaphase progression. , 2003, Developmental cell.

[37]  Norbert Perrimon,et al.  Parallel Chemical Genetic and Genome-Wide RNAi Screens Identify Cytokinesis Inhibitors and Targets , 2004, PLoS biology.

[38]  Barbara E. Bierer,et al.  The APC-associated protein EB1 associates with components of the dynactin complex and cytoplasmic dynein intermediate chain , 1999, Current Biology.

[39]  H. Schnabel,et al.  cyk-1: a C. elegans FH gene required for a late step in embryonic cytokinesis. , 1998, Journal of cell science.

[40]  W. Earnshaw,et al.  Chromosomal passengers and the (aurora) ABCs of mitosis. , 2001, Trends in cell biology.

[41]  W. Earnshaw,et al.  The cellular geography of Aurora kinases , 2003, Nature Reviews Molecular Cell Biology.

[42]  Hirofumi Tanaka,et al.  Human Mitotic Spindle-associated Protein PRC1 Inhibits MgcRacGAP Activity toward Cdc42 during the Metaphase* , 2004, Journal of Biological Chemistry.

[43]  P. Hussey,et al.  Two kinesin-related proteins associated with the cold-stable cytoskeleton of carrot cells: characterization of a novel kinesin, DcKRP120-2. , 2000, The Plant journal : for cell and molecular biology.

[44]  V. Litvak,et al.  Mitotic phosphorylation of the peripheral Golgi protein Nir2 by Cdk1 provides a docking mechanism for Plk1 and affects cytokinesis completion. , 2004, Molecular cell.

[45]  J. McIntosh,et al.  Isolation and initial characterization of the mammalian midbody , 1982, The Journal of cell biology.

[46]  D. Beach,et al.  Distinct nuclear and spindle pole body populations of cyclin–cdc2 in fission yeast , 1990, Nature.

[47]  G. Jürgens,et al.  Functional characterization of the KNOLLE-interacting t-SNARE AtSNAP33 and its role in plant cytokinesis , 2001, The Journal of cell biology.

[48]  F. Gergely,et al.  D‐TACC: a novel centrosomal protein required for normal spindle function in the early Drosophila embryo , 2000, The EMBO journal.

[49]  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.

[50]  Thomas Girke,et al.  The Vegetative Vacuole Proteome of Arabidopsis thaliana Reveals Predicted and Unexpected Proteinsw⃞ , 2004, The Plant Cell Online.

[51]  J. Yates,et al.  Dissection of the Mammalian Midbody Proteome Reveals Conserved Cytokinesis Mechanisms , 2004, Science.

[52]  J. Thyberg,et al.  Role of microtubules in the organization of the Golgi complex. , 1999, Experimental cell research.

[53]  F. Berger,et al.  Plant formin AtFH5 is an evolutionarily conserved actin nucleator involved in cytokinesis , 2005, Nature Cell Biology.

[54]  M. Glotzer,et al.  The Molecular Requirements for Cytokinesis , 2005, Science.

[55]  C. Mollinari,et al.  Ablation of PRC1 by small interfering RNA demonstrates that cytokinetic abscission requires a central spindle bundle in mammalian cells, whereas completion of furrowing does not. , 2005, Molecular biology of the cell.

[56]  T. G. Setty,et al.  Ase1p organizes antiparallel microtubule arrays during interphase and mitosis in fission yeast. , 2005, Molecular biology of the cell.

[57]  T. Lecuit,et al.  Trafficking through Rab11 Endosomes Is Required for Cellularization during Drosophila Embryogenesis , 2003, Current Biology.

[58]  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.

[59]  E. Nigg,et al.  Relocation of Aurora B from centromeres to the central spindle at the metaphase to anaphase transition requires MKlp2 , 2004, The Journal of cell biology.

[60]  R. Cyr,et al.  A kinesin-like protein, KatAp, in the cells of arabidopsis and other plants. , 1996, The Plant cell.

[61]  M. Glotzer,et al.  Depletion of syntaxins in the early Caenorhabditis elegans embryo reveals a role for membrane fusion events in cytokinesis , 1999, Current Biology.

[62]  Erich A. Nigg,et al.  Cell division: Mitotic kinases as regulators of cell division and its checkpoints , 2001, Nature Reviews Molecular Cell Biology.

[63]  J. David,et al.  Dynamic Recruitment of Cdc2 to Specific Microtubule Structures during Mitosis , 2001, The Plant Cell Online.

[64]  Wei Jiang,et al.  Cell cycle-dependent translocation of PRC1 on the spindle by Kif4 is essential for midzone formation and cytokinesis. , 2005, Proceedings of the National Academy of Sciences of the United States of America.

[65]  D. Birnbaum,et al.  Aurora B -TACC1 protein complex in cytokinesis , 2004, Oncogene.

[66]  A. Valster,et al.  Actomyosin promotes cell plate alignment and late lateral expansion in Tradescantia stamen hair cells , 2002, Planta.

[67]  Frank Küttner,et al.  Syntaxin specificity of cytokinesis in Arabidopsis , 2003, Nature Cell Biology.

[68]  D. Inzé,et al.  In Vivo Dynamics and Differential Microtubule-Binding Activities of MAP65 Proteins1 , 2004, Plant Physiology.

[69]  J. Ahringer,et al.  TAC-1, a Regulator of Microtubule Length in the C. elegans Embryo , 2003, Current Biology.

[70]  L. Staehelin,et al.  Electron tomographic analysis of post-meiotic cytokinesis during pollen development in Arabidopsis thaliana , 2004, Planta.

[71]  Sookhee Park,et al.  Characterization of AtCDC48. Evidence for Multiple Membrane Fusion Mechanisms at the Plane of Cell Division in Plants1 , 2002, Plant Physiology.

[72]  D. Pappin,et al.  Cdc2 Kinase Directly Phosphorylates the cis-Golgi Matrix Protein GM130 and Is Required for Golgi Fragmentation in Mitosis , 1998, Cell.

[73]  T. Pollard,et al.  Profilin-mediated competition between capping protein and formin Cdc12p during cytokinesis in fission yeast. , 2005, Molecular biology of the cell.

[74]  A. Nebenführ Vesicle traffic in the endomembrane system: a tale of COPs, Rabs and SNAREs. , 2002, Current opinion in plant biology.

[75]  C. Ritzenthaler,et al.  Brefeldin A: Deciphering an Enigmatic Inhibitor of Secretion , 2002, Plant Physiology.

[76]  X. Morin,et al.  Dynamics of the endoplasmic reticulum during early development of Drosophila melanogaster. , 2003, Cell motility and the cytoskeleton.

[77]  R. Zhong,et al.  A Kinesin-Like Protein Is Essential for Oriented Deposition of Cellulose Microfibrils and Cell Wall Strength Article, publication date, and citation information can be found at www.plantcell.org/cgi/doi/10.1105/tpc.005801. , 2002, The Plant Cell Online.

[78]  D. Roof,et al.  The Kinesin-related Protein Kip1p of Saccharomyces cerevisiae Is Bipolar* , 1999, The Journal of Biological Chemistry.

[79]  J. Ecker,et al.  NPSN11 Is a Cell Plate-Associated SNARE Protein That Interacts with the Syntaxin KNOLLE1 , 2002, Plant Physiology.

[80]  A. Hyman,et al.  Control of microtubule dynamics by the antagonistic activities of XMAP215 and XKCM1 in Xenopus egg extracts , 1999, Nature Cell Biology.

[81]  V. Malhotra,et al.  Fragmentation and Dispersal of the Pericentriolar Golgi Complex Is Required for Entry into Mitosis in Mammalian Cells , 2002, Cell.

[82]  A. Marcus,et al.  A minus-end-directed kinesin with plus-end tracking protein activity is involved in spindle morphogenesis. , 2005, Molecular biology of the cell.

[83]  John White,et al.  Completion of cytokinesis in C. elegans requires a brefeldin A-sensitive membrane accumulation at the cleavage furrow apex , 2001, Current Biology.

[84]  T. Asada,et al.  TKRP125, a kinesin-related protein involved in the centrosome-independent organization of the cytokinetic apparatus in tobacco BY-2 cells. , 1997, Journal of cell science.

[85]  Timothy J Mitchison,et al.  Dissecting Temporal and Spatial Control of Cytokinesis with a Myosin II Inhibitor , 2003, Science.

[86]  Peter K Hepler,et al.  Cytokinesis in Higher Plants , 1996, Cell.

[87]  L. Staehelin,et al.  Cytokinesis in flowering plants: more than one way to divide a cell. , 2000, Current opinion in plant biology.

[88]  V. Litvak,et al.  Targeting of Nir2 to Lipid Droplets Is Regulated by a Specific Threonine Residue within Its PI-Transfer Domain , 2002, Current Biology.

[89]  K. Gunsalus,et al.  Feo, the Drosophila Homolog of PRC1, Is Required for Central-Spindle Formation and Cytokinesis , 2004, Current Biology.

[90]  D. McCollum,et al.  The S. pombe Cdc14-like phosphatase Clp1p regulates chromosome biorientation and interacts with Aurora kinase. , 2004, Developmental cell.

[91]  M. McNiven,et al.  The Large GTPase Dynamin Associates with the Spindle Midzone and Is Required for Cytokinesis , 2002, Current Biology.

[92]  Bo Liu,et al.  Cytoskeletal Motors in Arabidopsis. Sixty-One Kinesins and Seventeen Myosins1 , 2004, Plant Physiology.

[93]  Dannel McCollum,et al.  The multiprotein exocyst complex is essential for cell separation in Schizosaccharomyces pombe. , 2002, Molecular biology of the cell.

[94]  T. Hunter,et al.  PRC1 is a microtubule binding and bundling protein essential to maintain the mitotic spindle midzone , 2002, The Journal of cell biology.

[95]  Bo Liu,et al.  Localization of two homologous Arabidopsis kinesin-related proteins in the phragmoplast , 2004, Planta.

[96]  Yu-Li Wang,et al.  Both midzone and astral microtubules are involved in the delivery of cytokinesis signals , 2002, The Journal of cell biology.

[97]  J. H. Wang,et al.  p34cdc2 kinase is localized to distinct domains within the mitotic apparatus. , 1990, Cell motility and the cytoskeleton.

[98]  S. Wasserman,et al.  Diaphanous is required for cytokinesis in Drosophila and shares domains of similarity with the products of the limb deformity gene. , 1994, Development.

[99]  J. Schumacher,et al.  The Caenorhabditis elegans Aurora B kinase AIR-2 phosphorylates and is required for the localization of a BimC kinesin to meiotic and mitotic spindles. , 2004, Molecular biology of the cell.

[100]  Wankee Kim,et al.  Kinesin superfamily protein member 4 (KIF4) is localized to midzone and midbody in dividing cells , 2004, Experimental & Molecular Medicine.

[101]  Bo Liu,et al.  A Novel Plant Kinesin-Related Protein Specifically Associates with the Phragmoplast Organelles Article, publication date, and citation information can be found at www.aspb.org/cgi/doi/10.1105/tpc.010225. , 2001, The Plant Cell Online.

[102]  J. Demeter,et al.  The Ran GTPase System in Fission Yeast Affects Microtubules and Cytokinesis in Cells That Are Competent for Nucleocytoplasmic Protein Transport , 2002, Molecular and Cellular Biology.

[103]  R. Pepperkok,et al.  Partitioning of the Golgi Apparatus during Mitosis in Living HeLa Cells , 1997, The Journal of cell biology.

[104]  W. Earnshaw,et al.  Essential roles of KIF4 and its binding partner PRC1 in organized central spindle midzone formation , 2004, The EMBO journal.

[105]  G. Wasteneys,et al.  MOR1 is essential for organizing cortical microtubules in plants , 2001, Nature.

[106]  V. Malhotra,et al.  Cell-cycle-specific Golgi fragmentation: how and why? , 2003, Current opinion in cell biology.

[107]  T. Shimmen,et al.  Characterization of a 200 kDa microtubule-associated protein of tobacco BY-2 cells, a member of the XMAP215/MOR1 family. , 2004, Plant & cell physiology.

[108]  T. Toda,et al.  The roles of fission yeast ase1 in mitotic cell division, meiotic nuclear oscillation, and cytokinesis checkpoint signaling. , 2005, Molecular biology of the cell.

[109]  K. Gould,et al.  Requirements of fission yeast septins for complex formation, localization, and function. , 2004, Molecular biology of the cell.

[110]  S. Reed,et al.  Differential contribution of Bud6p and Kar9p to microtubule capture and spindle orientation in S. cerevisiae , 2004, The Journal of cell biology.

[111]  R. Nishihama,et al.  NQK1/NtMEK1 is a MAPKK that acts in the NPK1 MAPKKK-mediated MAPK cascade and is required for plant cytokinesis. , 2003, Genes & development.

[112]  B. Kang,et al.  Members of the Arabidopsis Dynamin-Like Gene Family, ADL1, Are Essential for Plant Cytokinesis and Polarized Cell Growth Online version contains Web-only data. Article, publication date, and citation information can be found at www.plantcell.org/cgi/doi/10.1105/tpc.009670. , 2003, The Plant Cell Online.

[113]  S. Moreno,et al.  Flp1, a fission yeast orthologue of the s. cerevisiae CDC14 gene, is not required for cyclin degradation or rum1p stabilisation at the end of mitosis. , 2001, Journal of cell science.

[114]  W. Trimble,et al.  Syntaxin 5 is required for cytokinesis and spermatid differentiation in Drosophila. , 2002, Developmental biology.

[115]  Erich A. Nigg,et al.  Polo-like kinases and the orchestration of cell division , 2004, Nature Reviews Molecular Cell Biology.

[116]  A. Schmit,et al.  The growing cell plate of higher plants is a site of both actin assembly and vinculin-like antigen recruitment. , 1998, European journal of cell biology.

[117]  W. Sullivan,et al.  Membrane traffic: a driving force in cytokinesis. , 2005, Trends in cell biology.

[118]  J. Lippincott-Schwartz,et al.  Golgi Membranes Are Absorbed into and Reemerge from the ER during Mitosis , 1999, Cell.

[119]  D. Pellman,et al.  Search, capture and signal: games microtubules and centrosomes play. , 2001, Journal of cell science.

[120]  T. Gadella,et al.  Alteration of Microtubule Dynamic Instability during Preprophase Band Formation Revealed by Yellow Fluorescent Protein–CLIP170 Microtubule Plus-End Labeling Online version contains Web-only data. Article, publication date, and citation information can be found at www.plantcell.org/cgi/doi/10.1105/tp , 2003, The Plant Cell Online.

[121]  D. Gard,et al.  MAPping the eukaryotic tree of life: structure, function, and evolution of the MAP215/Dis1 family of microtubule-associated proteins. , 2004, International review of cytology.

[122]  S. Munro,et al.  Vesicle tethering complexes in membrane traffic. , 2002, Journal of cell science.

[123]  T. Mitchison,et al.  The Bipolar Kinesin, KLP61F, Cross-links Microtubules within Interpolar Microtubule Bundles of Drosophila Embryonic Mitotic Spindles , 1999, The Journal of cell biology.

[124]  D. Mastronarde,et al.  Three-Dimensional Analysis of Syncytial-Type Cell Plates during Endosperm Cellularization Visualized by High Resolution Electron Tomography , 2001, The Plant Cell Online.

[125]  W. Sullivan,et al.  Lava Lamp, a Novel Peripheral Golgi Protein, Is Required for Drosophila melanogaster Cellularization , 2000, The Journal of cell biology.