Dynein Transmits Polarized Actomyosin Cortical Flows to Promote Centrosome Separation

Cell Reports

Volumn 14, Issue 9, 2016, Pages 2250-2262

  De Simone, Alessandro ^a   Nédélec, François ^b   Gönczy, Pierre ^a  

^a EPFL   (Switzerland)

^b EUROPEAN MOLECULAR BIOLOGY LABORATORY   (Germany)

Author keywords

[No Author keywords available]

Indexed keywords

DYNEIN ADENOSINE TRIPHOSPHATASE; MYOSIN ADENOSINE TRIPHOSPHATASE; CAENORHABDITIS ELEGANS PROTEIN;

ADULT; ANIMAL CELL; ANIMAL EXPERIMENT; ARTICLE; CAENORHABDITIS ELEGANS; CELL NUCLEUS MEMBRANE; CELL SEPARATION; CENTROSOME; COMPUTER SIMULATION; CONTROLLED STUDY; EMBRYO; FEMALE; MALE; MICROSCOPY; NONHUMAN; POLARIZATION; PRIORITY JOURNAL; PROTEIN DEPLETION; PROTEIN FUNCTION; ACTIN FILAMENT; ANIMAL; CELL CYCLE; CYTOLOGY; METABOLISM; MICROTUBULE; MITOSIS; NONMAMMALIAN EMBRYO; PHYSIOLOGY; SPINDLE APPARATUS;

ACTIN CYTOSKELETON; ACTOMYOSIN; ANIMALS; CAENORHABDITIS ELEGANS; CAENORHABDITIS ELEGANS PROTEINS; CELL CYCLE; CENTROSOME; DYNEINS; EMBRYO, NONMAMMALIAN; MICROTUBULES; MITOSIS; SPINDLE APPARATUS;

EID: 84960395276     PISSN: None     EISSN: 22111247     Source Type: Journal    
DOI: 10.1016/j.celrep.2016.01.077     Document Type: Article

References (52)

1. Bellanger J.M., Gönczy P. TAC-1 and ZYG-9 form a complex that promotes microtubule assembly in C. elegans embryos. Curr. Biol. 2003, 13:1488-1498.
2. Bienkowska D., Cowan C.R. Centrosomes can initiate a polarity axis from any position within one-cell C. elegans embryos. Curr. Biol. 2012, 22:583-589.
3. Cao J., Crest J., Fasulo B., Sullivan W. Cortical actin dynamics facilitate early-stage centrosome separation. Curr. Biol. 2010, 20:770-776.
4. Colombo K., Grill S.W., Kimple R.J., Willard F.S., Siderovski D.P., Gönczy P. Translation of polarity cues into asymmetric spindle positioning in Caenorhabditis elegans embryos. Science 2003, 300:1957-1961.
5. Cytrynbaum E.N., Sommi P., Brust-Mascher I., Scholey J.M., Mogilner A. Early spindle assembly in Drosophila embryos: role of a force balance involving cytoskeletal dynamics and nuclear mechanics. Mol. Biol. Cell 2005, 16:4967-4981.
6. Dujardin D.L., Vallee R.B. Dynein at the cortex. Curr. Opin. Cell Biol. 2002, 14:44-49.
7. Ferenz N.P., Gable A., Wadsworth P. Mitotic functions of kinesin-5. Semin. Cell Dev. Biol. 2010, 21:255-259.
8. Foethke D., Makushok T., Brunner D., Nédélec F. Force- and length-dependent catastrophe activities explain interphase microtubule organization in fission yeast. Mol. Syst. Biol. 2009, 5:241.
9. Goldstein B., Hird S.N. Specification of the anteroposterior axis in Caenorhabditis elegans. Development 1996, 122:1467-1474.
10. Gönczy P., Pichler S., Kirkham M., Hyman A.A. Cytoplasmic dynein is required for distinct aspects of MTOC positioning, including centrosome separation, in the one cell stage Caenorhabditis elegans embryo. J. Cell Biol. 1999, 147:135-150.
11. Gotta M., Ahringer J. Distinct roles for Galpha and Gbetagamma in regulating spindle position and orientation in Caenorhabditis elegans embryos. Nat. Cell Biol. 2001, 3:297-300.
12. Gotta M., Dong Y., Peterson Y.K., Lanier S.M., Ahringer J. Asymmetrically distributed C. elegans homologs of AGS3/PINS control spindle position in the early embryo. Curr. Biol. 2003, 13:1029-1037.
13. Grill S.W., Gönczy P., Stelzer E.H., Hyman A.A. Polarity controls forces governing asymmetric spindle positioning in the Caenorhabditis elegans embryo. Nature 2001, 409:630-633.
14. Hamahashi S., Onami S., Kitano H. Detection of nuclei in 4D Nomarski DIC microscope images of early Caenorhabditis elegans embryos using local image entropy and object tracking. BMC Bioinformatics 2005, 6:125.
15. Hamill D.R., Severson A.F., Carter J.C., Bowerman B. Centrosome maturation and mitotic spindle assembly in C. elegans require SPD-5, a protein with multiple coiled-coil domains. Dev. Cell 2002, 3:673-684.
16. Kemphues K.J., Wolf N., Wood W.B., Hirsh D. Two loci required for cytoplasmic organization in early embryos of Caenorhabditis elegans. Dev. Biol. 1986, 113:449-460.
17. Kimura A., Onami S. Computer simulations and image processing reveal length-dependent pulling force as the primary mechanism for C. elegans male pronuclear migration. Dev. Cell 2005, 8:765-775.
18. Kotak S., Gönczy P. Mechanisms of spindle positioning: cortical force generators in the limelight. Curr. Opin. Cell Biol. 2013, 25:741-748.
19. Kozlowski C., Srayko M., Nedelec F. Cortical microtubule contacts position the spindle in C. elegans embryos. Cell 2007, 129:499-510.
20. Le Bot N., Tsai M.C., Andrews R.K., Ahringer J. TAC-1, a regulator of microtubule length in the C. elegans embryo. Curr. Biol. 2003, 13:1499-1505.
21. Lorson M.A., Horvitz H.R., van den Heuvel S. LIN-5 is a novel component of the spindle apparatus required for chromosome segregation and cleavage plane specification in Caenorhabditis elegans. J. Cell Biol. 2000, 148:73-86.
22. Malone C.J., Misner L., Le Bot N., Tsai M.C., Campbell J.M., Ahringer J., White J.G. The C. elegans hook protein, ZYG-12, mediates the essential attachment between the centrosome and nucleus. Cell 2003, 115:825-836.
23. Matthews L.R., Carter P., Thierry-Mieg D., Kemphues K. ZYG-9, a Caenorhabditis elegans protein required for microtubule organization and function, is a component of meiotic and mitotic spindle poles. J. Cell Biol. 1998, 141:1159-1168.
24. Mayer M., Depken M., Bois J.S., Jülicher F., Grill S.W. Anisotropies in cortical tension reveal the physical basis of polarizing cortical flows. Nature 2010, 467:617-621.
25. Motegi F., Sugimoto A. Sequential functioning of the ECT-2 RhoGEF, RHO-1 and CDC-42 establishes cell polarity in Caenorhabditis elegans embryos. Nat. Cell Biol. 2006, 8:978-985.
26. Munro E., Nance J., Priess J.R. Cortical flows powered by asymmetrical contraction transport PAR proteins to establish and maintain anterior-posterior polarity in the early C. elegans embryo. Dev. Cell 2004, 7:413-424.
27. Naganathan S.R., Fürthauer S., Nishikawa M., Jülicher F., Grill S.W. Active torque generation by the actomyosin cell cortex drives left-right symmetry breaking. eLife 2014, 3:e04165.
28. Nance J., Munro E.M., Priess J.R. C. elegans PAR-3 and PAR-6 are required for apicobasal asymmetries associated with cell adhesion and gastrulation. Development 2003, 130:5339-5350.
29. Nedelec F., Foethke D. Collective Langevin dynamics of flexible cytoskeletal fibers. New J. Phys. 2007, 9:427.
30. Nguyen-Ngoc T., Afshar K., Gönczy P. Coupling of cortical dynein and G alpha proteins mediates spindle positioning in Caenorhabditis elegans. Nat. Cell Biol. 2007, 9:1294-1302.
31. Nobuhito, M., and Kuang-An, C. (2003). Introduction to MPIV, user reference manual. http://www.oceanwave.jp/softwares/mpiv.
32. Raaijmakers J.A., van Heesbeen R.G., Meaders J.L., Geers E.F., Fernandez-Garcia B., Medema R.H., Tanenbaum M.E. Nuclear envelope-associated dynein drives prophase centrosome separation and enables Eg5-independent bipolar spindle formation. EMBO J. 2012, 31:4179-4190.
33. Redemann S., Schloissnig S., Ernst S., Pozniakowsky A., Ayloo S., Hyman A.A., Bringmann H. Codon adaptation-based control of protein expression in C. elegans. Nat. Methods 2011, 8:250-252.
34. Reinsch S., Gönczy P. Mechanisms of nuclear positioning. J. Cell Sci. 1998, 111:2283-2295.
35. Robinson J.T., Wojcik E.J., Sanders M.A., McGrail M., Hays T.S. Cytoplasmic dynein is required for the nuclear attachment and migration of centrosomes during mitosis in Drosophila. J. Cell Biol. 1999, 146:597-608.
36. Rose L., Gönczy P. Polarity establishment, asymmetric division and segregation of fate determinants in early C. elegans embryos. WormBook 2014, 1-43.
37. Rosenblatt J., Cramer L.P., Baum B., McGee K.M. Myosin II-dependent cortical movement is required for centrosome separation and positioning during mitotic spindle assembly. Cell 2004, 117:361-372.
38. Rual J.F., Ceron J., Koreth J., Hao T., Nicot A.S., Hirozane-Kishikawa T., Vandenhaute J., Orkin S.H., Hill D.E., van den Heuvel S., Vidal M. Toward improving Caenorhabditis elegans phenome mapping with an ORFeome-based RNAi library. Genome Res. 2004, 14(10B):2162-2168.
39. Rupp B., Nédélec F. Patterns of molecular motors that guide and sort filaments. Lab Chip 2012, 12:4903-4910.
40. Saunders A.M., Powers J., Strome S., Saxton W.M. Kinesin-5 acts as a brake in anaphase spindle elongation. Curr. Biol. 2007, 17:R453-R454.
41. Sharp D.J., Brown H.M., Kwon M., Rogers G.C., Holland G., Scholey J.M. Functional coordination of three mitotic motors in Drosophila embryos. Mol. Biol. Cell 2000, 11:241-253.
42. Shelton C.A., Carter J.C., Ellis G.C., Bowerman B. The nonmuscle myosin regulatory light chain gene mlc-4 is required for cytokinesis, anterior-posterior polarity, and body morphology during Caenorhabditis elegans embryogenesis. J. Cell Biol. 1999, 146:439-451.
43. Silkworth W.T., Nardi I.K., Paul R., Mogilner A., Cimini D. Timing of centrosome separation is important for accurate chromosome segregation. Mol. Biol. Cell 2012, 23:401-411.
44. Splinter D., Tanenbaum M.E., Lindqvist A., Jaarsma D., Flotho A., Yu K.L., Grigoriev I., Engelsma D., Haasdijk E.D., Keijzer N., et al. Bicaudal D2, dynein, and kinesin-1 associate with nuclear pore complexes and regulate centrosome and nuclear positioning during mitotic entry. PLoS Biol. 2010, 8:e1000350.
45. Srayko M., Quintin S., Schwager A., Hyman A.A. Caenorhabditis elegans TAC-1 and ZYG-9 form a complex that is essential for long astral and spindle microtubules. Curr. Biol. 2003, 13:1506-1511.
46. Srinivasan D.G., Fisk R.M., Xu H., van den Heuvel S. A complex of LIN-5 and GPR proteins regulates G protein signaling and spindle function in C elegans. Genes Dev. 2003, 17:1225-1239.
47. Tanenbaum M.E., Medema R.H. Mechanisms of centrosome separation and bipolar spindle assembly. Dev. Cell 2010, 19:797-806.
48. Tikhonenko I., Nag D.K., Martin N., Koonce M.P. Kinesin-5 is not essential for mitotic spindle elongation in Dictyostelium. Cell Motil. Cytoskeleton 2008, 65:853-862.
49. Toya M., Terasawa M., Nagata K., Iida Y., Sugimoto A. A kinase-independent role for Aurora A in the assembly of mitotic spindle microtubules in Caenorhabditis elegans embryos. Nat. Cell Biol. 2011, 13:708-714.
50. Tsou M.-F.B., Hayashi A., DeBella L.R., McGrath G., Rose L.S. LET-99 determines spindle position and is asymmetrically enriched in response to PAR polarity cues in C. elegans embryos. Development 2002, 129:4469-4481.
51. Vogel S.K., Pavin N., Maghelli N., Jülicher F., Tolić-Nørrelykke I.M. Self-organization of dynein motors generates meiotic nuclear oscillations. PLoS Biol. 2009, 7:918-928.
52. Waters J.C., Cole R.W., Rieder C.L. The force-producing mechanism for centrosome separation during spindle formation in vertebrates is intrinsic to each aster. J. Cell Biol. 1993, 122:361-372.