Mechanisms of spindle positioning

Accurate positioning of spindles is essential for asymmetric mitotic and meiotic cell divisions that are crucial for animal development and oocyte maturation, respectively. The predominant model for spindle positioning, termed “cortical pulling,” involves attachment of the microtubule-based motor cytoplasmic dynein to the cortex, where it exerts a pulling force on microtubules that extend from the spindle poles to the cell cortex, thereby displacing the spindle. Recent studies have addressed important details of the cortical pulling mechanism and have revealed alternative mechanisms that may be used when microtubules do not extend from the spindle to the cortex.

[1]  M. Rose,et al.  Bim1p/Yeb1p mediates the Kar9p-dependent cortical attachment of cytoplasmic microtubules. , 2000, Molecular biology of the cell.

[2]  G. Schatten,et al.  Differential behavior of centrosomes in unequally dividing blastomeres during fourth cleavage of sea urchin embryos. , 1991, Journal of cell science.

[3]  Brian D. Slaughter,et al.  Dynamic maintenance of asymmetric meiotic spindle position through Arp2/3-complex-driven cytoplasmic streaming in mouse oocytes , 2011, Nature Cell Biology.

[4]  J. Ahringer,et al.  A Casein Kinase 1 and PAR Proteins Regulate Asymmetry of a PIP2 Synthesis Enzyme for Asymmetric Spindle Positioning , 2008, Developmental cell.

[5]  R. Pielak,et al.  Formation and function of the polar body contractile ring in Spisula. , 2004, Developmental biology.

[6]  J. McIntosh,et al.  Force production by disassembling microtubules , 2005, Nature.

[7]  T. Huffaker,et al.  Constitutive dynein activity in she1 mutants reveals differences in microtubule attachment at the yeast spindle pole body , 2012, Molecular biology of the cell.

[8]  R. Vallee,et al.  MAP 1C is a microtubule-activated ATPase which translocates microtubules in vitro and has dynein-like properties , 1987, The Journal of cell biology.

[9]  D. Pellman,et al.  Positioning of the mitotic spindle by a cortical-microtubule capture mechanism. , 2000, Science.

[10]  Y. Hiramoto,et al.  Analysis of the Role of Astral Rays in Pronuclear Migration in Sand Dollar Eggs by the Colcemid‐UV Method , 1986, Development, growth & differentiation.

[11]  M. Srayko,et al.  Visualization of dynein-dependent microtubule gliding at the cell cortex: implications for spindle positioning , 2011, The Journal of cell biology.

[12]  P. Gönczy,et al.  Coupling of cortical dynein and Gα proteins mediates spindle positioning in Caenorhabditis elegans , 2007, Nature Cell Biology.

[13]  X. Cui,et al.  Arp2/3 Complex Regulates Asymmetric Division and Cytokinesis in Mouse Oocytes , 2011, PloS one.

[14]  Wei-Lih Lee,et al.  She1-Mediated Inhibition of Dynein Motility along Astral Microtubules Promotes Polarized Spindle Movements , 2012, Current Biology.

[15]  C. Racowsky,et al.  Mechanism of the chromosome-induced polar body extrusion in mouse eggs , 2011, Cell Division.

[16]  J. Cooper,et al.  The Cortical Protein Num1p Is Essential for Dynein-Dependent Interactions of Microtubules with the Cortex , 2000, The Journal of cell biology.

[17]  Anthony A. Hyman,et al.  Polarity controls forces governing asymmetric spindle positioning in the Caenorhabditis elegans embryo , 2001, Nature.

[18]  M. Schuh,et al.  Spire-Type Actin Nucleators Cooperate with Formin-2 to Drive Asymmetric Oocyte Division , 2011, Current Biology.

[19]  B. Yurke,et al.  Measurement of the force-velocity relation for growing microtubules. , 1997, Science.

[20]  J. Cooper,et al.  Microtubule Interactions with the Cell Cortex Causing Nuclear Movements in Saccharomyces cerevisiae , 2000, The Journal of cell biology.

[21]  R. T. Hoopen,et al.  Mechanism for Astral Microtubule Capture by Cortical Bud6p Priming Spindle Polarity in S. cerevisiae , 2012, Current Biology.

[22]  S. O’Rourke,et al.  Caenorhabditis elegans EFA-6 limits microtubule growth at the cell cortex , 2010, Nature Cell Biology.

[23]  I. Cheeseman,et al.  Chromosome and spindle pole-derived signals generate an intrinsic code for spindle position and orientation , 2012, Nature Cell Biology.

[24]  D. Drubin,et al.  Dynein-driven mitotic spindle positioning restricted to anaphase by She1p inhibition of dynactin recruitment. , 2009, Molecular biology of the cell.

[25]  Alisa Zhiteneva,et al.  Actin-mediated Delivery of Astral Microtubules Instructs Kar9p Asymmetric Loading to the Bud-Ward Spindle Pole , 2010, Molecular biology of the cell.

[26]  J. McIntosh,et al.  Kinesin-8 from fission yeast: a heterodimeric, plus-end-directed motor that can couple microtubule depolymerization to cargo movement. , 2008, Molecular biology of the cell.

[27]  B. Westermann,et al.  Mdm36 Is a Mitochondrial Fission-promoting Protein in Saccharomyces cerevisiae , 2010, Molecular biology of the cell.

[28]  Anthony Bretscher,et al.  Myosin V orientates the mitotic spindle in yeast , 2000, Nature.

[29]  Y. Barral,et al.  Spindle orientation in Saccharomyces cerevisiae depends on the transport of microtubule ends along polarized actin cables , 2003, The Journal of cell biology.

[30]  P. Wadsworth,et al.  Cell cycle–regulated cortical dynein/dynactin promotes symmetric cell division by differential pole motion in anaphase , 2012, Molecular biology of the cell.

[31]  A. Hyman,et al.  Spindle positioning by cortical pulling forces. , 2005, Developmental cell.

[32]  Y. Bellaïche,et al.  Mitotic spindle orientation in asymmetric and symmetric cell divisions during animal development. , 2011, Developmental cell.

[33]  P. Gönczy,et al.  Cortical dynein is critical for proper spindle positioning in human cells , 2012, The Journal of cell biology.

[34]  J. McIntosh,et al.  Minus-end-directed motion of kinesin–coated microspheres driven by microtubule depolymerization , 1995, Nature.

[35]  R. Vale,et al.  Crystal Structure of the Dynein Motor Domain , 2011, Science.

[36]  J. Cooper,et al.  The role of the lissencephaly protein Pac1 during nuclear migration in budding yeast , 2003, The Journal of cell biology.

[37]  A. Chaudhuri,et al.  Molecular linkage underlying microtubule orientation toward cortical sites in yeast. , 2000, Science.

[38]  Jonathon Howard,et al.  Kinesin-8 Motors Act Cooperatively to Mediate Length-Dependent Microtubule Depolymerization , 2009, Cell.

[39]  B. Ibrahim,et al.  Monitoring spindle orientation: Spindle position checkpoint in charge , 2010, Cell Division.

[40]  Wei-Lih Lee,et al.  Regulated offloading of cytoplasmic dynein from microtubule plus ends to the cortex. , 2011, Developmental cell.

[41]  R. Vallee,et al.  Microtubule-associated protein 1C from brain is a two-headed cytosolic dynein , 1988, Nature.

[42]  T. Mitchison,et al.  Growth, interaction, and positioning of microtubule asters in extremely large vertebrate embryo cells , 2012, Cytoskeleton.

[43]  F. McNally,et al.  MEI-1/katanin is required for translocation of the meiosis I spindle to the oocyte cortex in C elegans. , 2003, Developmental biology.

[44]  P. Philippsen,et al.  Asymmetric recruitment of dynein to spindle poles and microtubules promotes proper spindle orientation in yeast. , 2006, Developmental cell.

[45]  Brian D. Slaughter,et al.  Symmetry breaking in the life cycle of the budding yeast. , 2009, Cold Spring Harbor perspectives in biology.

[46]  K. Bloom,et al.  The Role of Actin in Spindle Orientation Changes during the Saccharomyces cerevisiae Cell Cycle , 1999, The Journal of cell biology.

[47]  S. Markoulaki,et al.  Antagonists of Myosin Light Chain Kinase and of Myosin II Inhibit Specific Events of Egg Activation in Fertilized Mouse Eggs1 , 2006, Biology of reproduction.

[48]  A. Hyman,et al.  Membrane Invaginations Reveal Cortical Sites that Pull on Mitotic Spindles in One-Cell C. elegans Embryos , 2010, PloS one.

[49]  P. Gönczy,et al.  ZYG-9, TAC-1 and ZYG-8 together ensure correct microtubule function throughout the cell cycle of C. elegans embryos , 2007, Journal of Cell Science.

[50]  Wei-Lih Lee,et al.  A novel patch assembly domain in Num1 mediates dynein anchoring at the cortex during spindle positioning , 2012, The Journal of cell biology.

[51]  J. Cooper,et al.  Dynein-dependent movements of the mitotic spindle in Saccharomyces cerevisiae Do not require filamentous actin. , 2000, Molecular biology of the cell.

[52]  F. McNally,et al.  Kinesin-dependent transport results in polarized migration of the nucleus in oocytes and inward movement of yolk granules in meiotic embryos. , 2010, Developmental biology.

[53]  Fengli Guo,et al.  Actin-driven chromosomal motility leads to symmetry breaking in mammalian meiotic oocytes , 2008, Nature Cell Biology.

[54]  L. Harispe,et al.  The eisosome core is composed of BAR domain proteins , 2011, Molecular biology of the cell.

[55]  Yves Barral,et al.  Asymmetric Loading of Kar9 onto Spindle Poles and Microtubules Ensures Proper Spindle Alignment , 2003, Cell.

[56]  S. Kandels-Lewis,et al.  CLIP-170 tracks growing microtubule ends by dynamically recognizing composite EB1/tubulin-binding sites , 2008, The Journal of cell biology.

[57]  Cleopatra Kozlowski,et al.  Cortical Microtubule Contacts Position the Spindle in C. elegans Embryos , 2007, Cell.

[58]  P. Guillaud,et al.  Asymmetric division in mouse oocytes: with or without Mos , 2000, Current Biology.

[59]  J. Ellenberg,et al.  A New Model for Asymmetric Spindle Positioning in Mouse Oocytes , 2008, Current Biology.

[60]  A. Andrieux,et al.  A new role for kinesin-directed transport of Bik1p (CLIP-170) in Saccharomyces cerevisiae , 2008, Journal of Cell Science.

[61]  Lesilee S. Rose,et al.  Dynamic localization of LIN-5 and GPR-1/2 to cortical force generation domains during spindle positioning. , 2008, Developmental biology.

[62]  Jonathon Howard,et al.  The Distribution of Active Force Generators Controls Mitotic Spindle Position , 2003, Science.

[63]  D. Robinson,et al.  Cortical Mechanics and Meiosis II Completion in Mammalian Oocytes Are Mediated by Myosin-II and Ezrin-Radixin-Moesin (ERM) Proteins , 2010, Molecular biology of the cell.

[64]  Melina Schuh,et al.  An actin-dependent mechanism for long-range vesicle transport , 2011, Nature Cell Biology.

[65]  Mohan L Gupta,et al.  Plus end-specific depolymerase activity of Kip3, a kinesin-8 protein, explains its role in positioning the yeast mitotic spindle , 2006, Nature Cell Biology.

[66]  A. Mccarthy Development , 1996, Current Opinion in Neurobiology.

[67]  Frank Jülicher,et al.  Cortical Dynein Controls Microtubule Dynamics to Generate Pulling Forces that Position Microtubule Asters , 2012, Cell.

[68]  J Richard McIntosh,et al.  Tubulin depolymerization may be an ancient biological motor , 2010, Journal of Cell Science.

[69]  J. Labbé,et al.  Heterotrimeric G protein signaling functions with dynein to promote spindle positioning in C. elegans , 2007, The Journal of cell biology.

[70]  P. Gönczy,et al.  NuMA-related LIN-5, ASPM-1, calmodulin and dynein promote meiotic spindle rotation independently of cortical LIN-5/GPR/Gα , 2009, Nature Cell Biology.

[71]  Pedro Carvalho,et al.  Determinants of S. cerevisiae Dynein Localization and Activation Implications for the Mechanism of Spindle Positioning , 2003, Current Biology.

[72]  Kenji Kimura,et al.  Intracellular organelles mediate cytoplasmic pulling force for centrosome centration in the Caenorhabditis elegans early embryo , 2010, Proceedings of the National Academy of Sciences.

[73]  L. Frisén,et al.  The kinesin-related proteins, Kip2p and Kip3p, function differently in nuclear migration in yeast. , 1998, Molecular biology of the cell.

[74]  V. Georget,et al.  Symmetry breaking in mouse oocytes requires transient F-actin meshwork destabilization , 2011, Development.

[75]  M. Petronczki,et al.  Cytokinesis in animal cells. , 2015, Cold Spring Harbor perspectives in biology.

[76]  F. McNally,et al.  CDK-1 inhibits meiotic spindle shortening and dynein-dependent spindle rotation in C. elegans , 2011, The Journal of cell biology.

[77]  S. Inoué,et al.  Micromanipulation studies of the asymmetric positioning of the maturation spindle in Chaetopterus sp. oocytes: I. Anchorage of the spindle to the cortex and migration of a displaced spindle. , 1988, Cell motility and the cytoskeleton.

[78]  J. Ahringer,et al.  Asymmetrically Distributed C. elegans Homologs of AGS3/PINS Control Spindle Position in the Early Embryo , 2003, Current Biology.

[79]  S. Pickering,et al.  Changes in actin distribution during fertilization of the mouse egg. , 1984, Journal of embryology and experimental morphology.

[80]  Carolyn G Rasmussen,et al.  Determination of symmetric and asymmetric division planes in plant cells. , 2011, Annual review of plant biology.

[81]  Kara L. Cerveny,et al.  Yeast mitochondrial division and distribution require the cortical num1 protein. , 2007, Developmental cell.

[82]  F. McNally,et al.  Kinesin-1 and cytoplasmic dynein act sequentially to move the meiotic spindle to the oocyte cortex in Caenorhabditis elegans. , 2009, Molecular biology of the cell.

[83]  K. Mechtler,et al.  Phosphoregulation of the budding yeast EB1 homologue Bim1p by Aurora/Ipl1p , 2009, The Journal of cell biology.

[84]  F. McNally,et al.  Kinesin-1 mediates translocation of the meiotic spindle to the oocyte cortex through KCA-1, a novel cargo adapter , 2005, The Journal of cell biology.

[85]  K. Sutoh,et al.  The 2.8 Å crystal structure of the dynein motor domain , 2012, Nature.

[86]  F. McNally,et al.  Nuclear and spindle positioning during oocyte meiosis. , 2011, Current opinion in cell biology.

[87]  L. Rose,et al.  LET-99 inhibits lateral posterior pulling forces during asymmetric spindle elongation in C. elegans embryos , 2010, The Journal of cell biology.

[88]  J. Labbé,et al.  PAR Proteins Regulate Microtubule Dynamics at the Cell Cortex in C. elegans , 2003, Current Biology.

[89]  Mohan L Gupta,et al.  Cell cycle control of kinesin-mediated transport of Bik1 (CLIP-170) regulates microtubule stability and dynein activation. , 2004, Developmental cell.

[90]  P. Walter,et al.  Eisosomes mark static sites of endocytosis , 2006, Nature.

[91]  L. Rose,et al.  CLASPs function redundantly to regulate astral microtubules in the C. elegans embryo. , 2012, Developmental biology.

[92]  D. C. Pfeiffer,et al.  Microtubules in Xenopus oocytes are oriented with their minus-ends towards the cortex. , 1999, Cell motility and the cytoskeleton.

[93]  P. Gönczy,et al.  zyg-8, a gene required for spindle positioning in C. elegans, encodes a doublecortin-related kinase that promotes microtubule assembly. , 2001, Developmental cell.

[94]  P. Cossart,et al.  Listeria comet tails: the actin-based motility machinery at work. , 2008, Trends in cell biology.

[95]  H. Lim,et al.  Formin-2 is required for spindle migration and for the late steps of cytokinesis in mouse oocytes. , 2007, Developmental biology.