Kinesin-1 Prevents Capture of the Oocyte Meiotic Spindle by the Sperm Aster

Developmental Cell

Volumn 22, Issue 4, 2012, Pages 788-798

  McNally, Karen L P ^a   Fabritius, Amy S ^a   Ellefson, Marina L ^a   Flynn, Jonathan R ^a   Milan, Jennifer A ^a   McNally, Francis J ^a  

^a UNIVERSITY OF CALIFORNIA   (United States)

Author keywords

[No Author keywords available]

Indexed keywords

CELL PROTEIN; DNA; KINESIN; KINESIN 1; PERICENTRIOLAR PROTEIN; UNCLASSIFIED DRUG;

ANIMAL CELL; ARTICLE; CAENORHABDITIS ELEGANS; CELL GROWTH; CELL MATURATION; CENTRIOLE; CENTROSOME; CONTROLLED STUDY; MEIOSIS; MEIOSIS SPINDLE; NONHUMAN; OOCYTE; PRIORITY JOURNAL; PROTEIN BINDING; PROTEIN DEPLETION; PROTEIN FUNCTION; SPERM; SPERM ASTER; SPINDLE CELL; WILD TYPE; ZYGOTE;

ANIMALS; CAENORHABDITIS ELEGANS; CAENORHABDITIS ELEGANS PROTEINS; CELL CYCLE PROTEINS; CELLS, CULTURED; CENTRIOLES; CENTROSOME; EMBRYO, NONMAMMALIAN; FEMALE; FERTILIZATION; FLUORESCENT ANTIBODY TECHNIQUE; KINESIN; MALE; MEIOSIS; MITOTIC SPINDLE APPARATUS; OOCYTES; OOGENESIS; SPERMATOZOA;

CAENORHABDITIS ELEGANS;

EID: 84859872385     PISSN: 15345807     EISSN: 18781551     Source Type: Journal    
DOI: 10.1016/j.devcel.2012.01.010     Document Type: Article

References (49)

1. Albertson D.G., Thomson J.N. Segregation of holocentric chromosomes at meiosis in the nematode, Caenorhabditis elegans. Chromosome Res. 1993, 1:15-26.
2. Batchelder E.L., Thomas-Virnig C.L., Hardin J.D., White J.G. Cytokinesis is not controlled by calmodulin or myosin light chain kinase in the Caenorhabditis elegans early embryo. FEBS Lett. 2007, 581:4337-4341.
3. Cooke S., Tyler J.P., Driscoll G.L. Meiotic spindle location and identification and its effect on embryonic cleavage plane and early development. Hum. Reprod. 2003, 18:2397-2405.
4. Cowan C.R., Hyman A.A. Cyclin E-Cdk2 temporally regulates centrosome assembly and establishment of polarity in Caenorhabditis elegans embryos. Nat. Cell Biol. 2006, 8:1441-1447.
5. Ellefson M.L., McNally F.J. Kinesin-1 and cytoplasmic dynein act sequentially to move the meiotic spindle to the oocyte cortex in Caenorhabditis elegans. Mol. Biol. Cell 2009, 20:2722-2730.
6. Ellefson M.L., McNally F.J. CDK-1 inhibits meiotic spindle shortening and dynein-dependent spindle rotation in C. elegans. J. Cell Biol. 2011, 193:1229-1244.
7. Gönczy, P., and Rose, L.S. (2005). Asymmetric cell division and axis formation in the embryo. In WormBook, The C. elegans Research Community, ed., 10.1895/wormbook.1.30.1, . http://www.wormbook.org.
8. Gould M.C., Stephano J.L. MAP kinase, meiosis, and sperm centrosome suppression in Urechis caupo. Dev. Biol. 1999, 216:348-358.
9. 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.
10. Harris P., Osborn M., Weber K. Distribution of tubulin-containing structures in the egg of the sea urchin Strongylocentrotus purpuratus from fertilization through first cleavage. J. Cell Biol. 1980, 84:668-679.
11. Johnston W.L., Krizus A., Dennis J.W. Eggshell chitin and chitin-interacting proteins prevent polyspermy in C. elegans. Curr. Biol. 2010, 20:1932-1937.
12. Kemp C.A., Kopish K.R., Zipperlen P., Ahringer J., O'Connell K.F. Centrosome maturation and duplication in C. elegans require the coiled-coil protein SPD-2. Dev. Cell 2004, 6:511-523.
13. Kilani S., Cooke S., Tilia L., Chapman M. Does meiotic spindle normality predict improved blastocyst development, implantation and live birth rates?. Fertil. Steril. 2011, 96:389-393.
14. Kim D.Y., Roy R. Cell cycle regulators control centrosome elimination during oogenesis in Caenorhabditis elegans. J. Cell Biol. 2006, 174:751-757.
15. 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. TAC-1.
16. Lee M.H., Ohmachi M., Arur S., Nayak S., Francis R., Church D., Lambie E., Schedl T. Multiple functions and dynamic activation of MPK-1 extracellular signal-regulated kinase signaling in Caenorhabditis elegans germline development. Genetics 2007, 177:2039-2062.
17. Leidel S., Gönczy P. Centrosome duplication and nematodes: recent insights from an old relationship. Dev. Cell 2005, 9:317-325.
18. Li S., Armstrong C.M., Bertin N., Ge H., Milstein S., Boxem M., Vidalain P.O., Han J.D., Chesneau A., Hao T., et al. A map of the interactome network of the metazoan C. elegans. Science 2004, 303:540-543.
19. McCarter J., Bartlett B., Dang T., Schedl T. On the control of oocyte meiotic maturation and ovulation in Caenorhabditis elegans. Dev. Biol. 1999, 205:111-128.
20. McNally K.L., McNally F.J. Fertilization initiates the transition from anaphase I to metaphase II during female meiosis in C. elegans. Dev. Biol. 2005, 282:218-230.
21. McNally K.L., Martin J.L., Ellefson M., McNally F.J. Kinesin-dependent transport results in polarized migration of the nucleus in oocytes and inward movement of yolk granules in meiotic embryos. Dev. Biol. 2010, 339:126-140.
22. Mio Y. Morphological analysis of human embryonic development using time-lapse cinematography. J. Mamm. Ova Res. 2006, 23:27-36.
23. Nakamura S., Terada Y., Horiuchi T., Emuta C., Murakami T., Yaegashi N., Okamura K. Human sperm aster formation and pronuclear decondensation in bovine eggs following intracytoplasmic sperm injection using a Piezo-driven pipette: a novel assay for human sperm centrosomal function. Biol. Reprod. 2001, 65:1359-1363.
24. Navara C.S., First N.L., Schatten G. Microtubule organization in the cow during fertilization, polyspermy, parthenogenesis, and nuclear transfer: the role of the sperm aster. Dev. Biol. 1994, 162:29-40.
25. Nishi Y., Lin R. DYRK2 and GSK-3 phosphorylate and promote the timely degradation of OMA-1, a key regulator of the oocyte-to-embryo transition in C. elegans. Dev. Biol. 2005, 288:139-149.
26. Oegema, K., and Hyman, A.A. (2006). Cell division. In WormBook, The C. elegans Research Community, ed. WormBook, . http://10.1895/wormbook.1.72.1.
27. O'Rourke S.M., Carter C., Carter L., Christensen S.N., Jones M.P., Nash B., Price M.H., Turnbull D.W., Garner A.R., Hamill D.R., et al. A survey of new temperature-sensitive, embryonic-lethal mutations in C. elegans: 24 alleles of thirteen genes. PLoS ONE 2011, 6:e16644.
28. Parvin J.D. The BRCA1-dependent ubiquitin ligase, γ-tubulin, and centrosomes. Environ. Mol. Mutagen. 2009, 50:649-653.
29. Payne D., Flaherty S.P., Barry M.F., Matthews C.D. Preliminary observations on polar body extrusion and pronuclear formation in human oocytes using time-lapse video cinematography. Hum. Reprod. 1997, 12:532-541.
30. Pelletier L., Ozlü N., Hannak E., Cowan C., Habermann B., Ruer M., Müller-Reichert T., Hyman A.A. The Caenorhabditis elegans centrosomal protein SPD-2 is required for both pericentriolar material recruitment and centriole duplication. Curr. Biol. 2004, 14:863-873.
31. Pelletier L., O'Toole E., Schwager A., Hyman A.A., Müller-Reichert T. Centriole assembly in Caenorhabditis elegans. Nature 2006, 444:619-623.
32. Pellettieri J., Reinke V., Kim S.K., Seydoux G. Coordinate activation of maternal protein degradation during the egg-to-embryo transition in C. elegans. Dev. Cell 2003, 5:451-462.
33. Pintard L., Willis J.H., Willems A., Johnson J.L., Srayko M., Kurz T., Glaser S., Mains P.E., Tyers M., Bowerman B., Peter M. The BTB protein MEL-26 is a substrate-specific adaptor of the CUL-3 ubiquitin-ligase. Nature 2003, 425:311-316.
34. Rappleye C.A., Tagawa A., Lyczak R., Bowerman B., Aroian R.V. The anaphase-promoting complex and separin are required for embryonic anterior-posterior axis formation. Dev. Cell 2002, 2:195-206.
35. Sakamoto R., Byrd D.T., Brown H.M., Hisamoto N., Matsumoto K., Jin Y. The Caenorhabditis elegans UNC-14 RUN domain protein binds to the kinesin-1 and UNC-16 complex and regulates synaptic vesicle localization. Mol. Biol. Cell 2005, 16:483-496.
36. Samuel A.D., Murthy V.N., Hengartner M.O. Calcium dynamics during fertilization in C. elegans. BMC Dev. Biol. 2001, 1:8.
37. Sato K., Sato M., Audhya A., Oegema K., Schweinsberg P., Grant B.D. Dynamic regulation of caveolin-1 trafficking in the germ line and embryo of Caenorhabditis elegans. Mol. Biol. Cell 2006, 17:3085-3094.
38. Schott S., Coustham V., Simonet T., Bedet C., Palladino F. Unique and redundant functions of C. elegans HP1 proteins in post-embryonic development. Dev. Biol. 2006, 298:176-187.
39. Song M.H., Aravind L., Müller-Reichert T., O'Connell K.F. The conserved protein SZY-20 opposes the Plk4-related kinase ZYG-1 to limit centrosome size. Dev. Cell 2008, 15:901-912.
40. Stearns T., Kirschner M. In vitro reconstitution of centrosome assembly and function: the central role of γ-tubulin. Cell 1994, 76:623-637.
41. Stephano J.L., Gould M.C. MAP kinase, a universal suppressor of sperm centrosomes during meiosis?. Dev. Biol. 2000, 222:420-428.
42. Timmons L., Court D.L., Fire A. Ingestion of bacterially expressed dsRNAs can produce specific and potent genetic interference in Caenorhabditis elegans. Gene 2001, 263:103-112.
43. Toda H., Mochizuki H., Flores R., Josowitz R., Krasieva T.B., Lamorte V.J., Suzuki E., Gindhart J.G., Furukubo-Tokunaga K., Tomoda T. UNC-51/ATG1 kinase regulates axonal transport by mediating motor-cargo assembly. Genes Dev. 2008, 22:3292-3307.
44. Ward S., Argon Y., Nelson G.A. Sperm morphogenesis in wild-type and fertilization-defective mutants of Caenorhabditis elegans. J. Cell Biol. 1981, 91:26-44.
45. Tsuboi D., Hikita T., Qadota H., Amano M., Kaibuchi K. Regulatory machinery of UNC-33 Ce-CRMP localization in neurites during neuronal development in Caenorhabditis elegans. J. Neurochem. 2005, 95:1629-1641.
46. Wu X., Palazzo R.E. Differential regulation of maternal vs. paternal centrosomes. Proc. Natl. Acad. Sci. USA 1999, 96:1397-1402.
47. Yang H.Y., McNally K., McNally F.J. MEI-1/katanin is required for translocation of the meiosis I spindle to the oocyte cortex in C elegans. Dev. Biol. 2003, 260:245-259.
48. Yang H.Y., Mains P.E., McNally F.J. Kinesin-1 mediates translocation of the meiotic spindle to the oocyte cortex through KCA-1, a novel cargo adapter. J. Cell Biol. 2005, 169:447-457.
49. Zhou K., Rolls M.M., Hall D.H., Malone C.J., Hanna-Rose W. A ZYG-12-dynein interaction at the nuclear envelope defines cytoskeletal architecture in the C. elegans gonad. J. Cell Biol. 2009, 186:229-241.