Coupling of cortical dynein and Gα proteins mediates spindle positioning in Caenorhabditis elegans

Nature Cell Biology

Volumn 9, Issue 11, 2007, Pages 1294-1302

  Nguyen Ngoc, Tu ^a   Afshar, Katayoun ^a   Gönczy, Pierre ^a  

^a EPFL   (Switzerland)

Author keywords

[No Author keywords available]

Indexed keywords

BINDING PROTEIN; DYNEIN ADENOSINE TRIPHOSPHATASE; G PROTEIN COUPLED RECEPTOR; GUANINE NUCLEOTIDE BINDING PROTEIN ALPHA SUBUNIT; HETEROTRIMERIC GUANINE NUCLEOTIDE BINDING PROTEIN; PROTEIN LIN 5; UNCLASSIFIED DRUG;

ANAPHASE; ANIMAL CELL; ARTICLE; CAENORHABDITIS ELEGANS; CELL DIVISION; CONTROLLED STUDY; DEVELOPMENTAL STAGE; EMBRYO; EMBRYO DEVELOPMENT; GENE INACTIVATION; IN VIVO STUDY; MICROTUBULE; MITOSIS SPINDLE; NONHUMAN; PRIORITY JOURNAL; PROTEIN INTERACTION; PROTEIN TRANSPORT;

ANIMALS; CAENORHABDITIS ELEGANS; CAENORHABDITIS ELEGANS PROTEINS; CELL CYCLE PROTEINS; CELL POLARITY; DYNEIN ATPASE; GTP-BINDING PROTEIN ALPHA SUBUNITS; MICROTUBULES; MITOTIC SPINDLE APPARATUS;

CAENORHABDITIS ELEGANS;

EID: 35548975477     PISSN: 14657392     EISSN: None     Source Type: Journal    
DOI: 10.1038/ncb1649     Document Type: Article

References (35)

1. Colombo, K. et al. Translation of polarity cues into asymmetric spindle positioning in Caenorhabditis elegans embryos. Science 300, 1957-1961 (2003).
2. Grill, S. W., Howard, J., Schaffer, E., Stelzer, E. H. & Hyman, A. A. The distribution of active force generators controls mitotic spindle position. Science 301, 518-521 (2003).
3. Grill, S. W., Gönczy, P., Stelzer, E. H. & Hyman, A. A. Polarity controls forces governing asymmetric spindle positioning in the Caenorhabditis elegans embryo. Nature 409, 630-633 (2001).
4. Gotta, M. & Ahringer, J. Distinct roles for Galpha and Gbetagamma in regulating spindle position and orientation in Caenorhabditis elegans embryos. Nature Cell Biol. 3, 297-300 (2001).
5. Gotta. M., Dong, Y., Paterson, Y. K., Lanier, S. M. & Ahringer, J. Asymmetrically distributed C. elegans homologs of AGS3/PINS control spindle position in the early embryo. Curr. Biol. 13 1029-1037 (2003).
6. 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. 17, 1225-1239 (2003).
7. 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. 148, 73-86 (2000).
8. Afshar, K., Willard, F. S., Colombo, K., Siderovski, D. P. & Gönczy, P. Cortical localization of the Galpha protein GPA-16 requires RIC-8 function during C. elegans asymmetric cell division. Development 132, 4449-B4459 (2005).
9. Bellaiche, Y. & Gotta, M. Heterotrimeric G proteins and regulation of size asymmetry during cell division. Curr. Opin. Cell Biol. 17 658-663 (2005).
10. Du, Q. & Macara, I. G. Mammalian Pins is a conformational switch that links NuMA to heterotrimeric G proteins. Cell 119, 503-516 (2004).
11. Izumi, Y., Ohta, N., Hisata, K., Raabe, T. & Matsuzaki, F. Drosophila Pins-binding protein Mud regulates spindle-polarity coupling and centrosome organization. Nature Cell Biol. 8, 586-593 (2006).
12. Siller, K. H., Cabernard, C. & Doe, C. Q. The NuMA-related Mud protein binds Pins and regulates spindle orientation in Drusophila neuroblasts. Nature Cell Biol. 8, 594-600 (2006).
13. Bowman, S. K., Neumuller, R. A., Novatchkova, M., Du, Q. & Knoblich, J. A. The Drosophila NuMA Homolog Mud regulates spindle orientation in asymmetric cell division. Dev. Cell 10, 731-742 (2006).
14. Kozlowski, C., Srayko, M. & Nedelec, F. Cortical microtubule contacts position the spindle in C. elegans embryos. Cell 129, 499-510 (2007).
15. Wright, A. J. & Hunter, C. P. Mutations in a beta-tubulin disrupt spindle orientation and microtubule dynamics in the early Caenorhabditis elegans embryo. Mol. Biol. Cell 14, 4512-4525. (2003).
16. Hyman, A. A. & White, J. G. Determination of cell division axes in the early embryogenesis of Caenorhabditis elegans. J. Cell Biol. 105, 2123-2135 (1987).
17. Severson, A. F. & Bowerman, B. Myosin and the PAR proteins polarize microfilament-dependent forces that shape and position mitotic spindles in Caenorhabditis elegans. J Cell Biol. 161, 21-26 (2003).
18. Schmidt, D. J., Rose, D. J., Saxton, W. M. & Strome, S. Functional analysis of cytoplasmic dynein heavy chain in Caenorhabditis elegans with fast-acting temperature-sensitive mutations. Mol. Biol. Cell 16, 1200-1212 (2005).
19. 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. 147, 135-150 (1999).
20. 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 3 673-684 (2002).
21. Encalada, S. E., Willis, J., Lyczak, R. & Bowerman, B. A spindle checkpoint functions during mitosis in the early Caenorhabditis elegans embryo. Mol. Biol. Cell 16, 1056-1070 (2005).
22. Merdes, A., Ramyar, K., Vechio, J. D. & Cleveland, D. W. A complex of NuMA and cytoplasmic dynein is essential for mitotic spindle assembly. Cell 87, 447-468 (1996).
23. Cockell, M. M., Baumer, K. & Gönczy, P. lis-1 is required for dynein-dependent cell division processed in C. elegans embryos. J. Cell Sci. 117, 4571-4582 (2004).
24. Vallee, R. B., Tai, C. & Faulkner, N. E. LIS1: Cellular function of a disease-causing gene. Trends Cell Biol. 11, 155-160 (2001).
25. Carminati, J. L. & Stearns, T. Microtubules orient the mitotic spindle in yeast through dynein-dependent interactions with the cell cortex. J. Cell Biol. 138, 629-641. (1997).
26. Gupta, M. L. Jr., Carvalho, P., Roof, D. M. & Pellman, D. Plus end-specific depolymerase activity of Kip3, a kinesin-8 protein, explains its role in positioning the yeast mitotic spindle. Nature Cell Biol. 8, 913-923 (2006).
27. Cottingham, F. R. & Hoyt, M. A. Mitotic spindle positioning in Saccharomyces cerevisiae is accomplished by antagonistically acting microtubule motor proteins. J. Cell Biol. 138, 1041-1053 (1997).
28. Fink, G., Schuchardt, I., Colombelli, J., Stelzer, E. & Steinberg, G. Dynein-mediated pulling forces-drive rapid mitotic spindle elongation in, Ustilago maydis. EMBO J, 25, 4897-4908 (2006).
29. Pecreaux, J. et al. Spindle oscillations during asymmetric cell division require a threshold number of active cortical force generators. Curr. Biol. 16, 2111-2122 (2006).
30. Mallik, R., Carter, B. C., Lex, S. A., King, S. J. & Gross, S. P. Cytoplasmic dynein functions as a gear in response to load. Nature 427, 649-652 (2004).
31. Daniels, B. R., Masi, B. C. & Wirtz, D. Probing single-cell micromechanics in vivo: The microrheology of C. elegans developing embryos. Biophys. J. 90, 4712-4719 (2006).
32. Strome, S. et al. Spindle dynamics and the role of gamma-tubulin in early Caenorhabditis elegans embryos. Mol. Biol. Cell 12 1751-1764 (2001).
33. Schlaitz, A L. et al. The C. elegans RSA complex localizes protein phosphatase 2A to centrosomes and regulates mitotic spindle assembly. Cell 128, 115-127 (2007).
34. Afshar, K. et al. RIC-8 is required for GPR-1/2-dependent Galpha function during asymmetric division of C. elegans embryos. Cell 119, 219-230 (2004).
35. Gönczy, P. et al. Dissection of cell division processes in the one cell stage Caenorhabditis elegans embryo by mutational analysis. J. Cell Biol. 144, 927-946 (1999).