CLASPs function redundantly to regulate astral microtubules in the C. elegans embryo

Developmental Biology

Volumn 368, Issue 2, 2012, Pages 242-254

  Espiritu, Eugenel B ^a   Krueger, Lori E ^a   Ye, Anna ^a   Rose, Lesilee S ^a  

^a UNIVERSITY OF CALIFORNIA   (United States)

Author keywords

Asymmetric division; Microtubules; Mitosis; Spindle positioning

Indexed keywords

MICROTUBULE ASSOCIATED PROTEIN; PROTEIN CLASP; PROTEIN CLS 1; PROTEIN CLS 2; PROTEIN CLS 3; UNCLASSIFIED DRUG; CAENORHABDITIS ELEGANS PROTEIN; CLS 1 PROTEIN, C ELEGANS; CLS 2 PROTEIN, C ELEGANS; CLS 3 PROTEIN, C ELEGANS; CLS-1 PROTEIN, C ELEGANS; CLS-2 PROTEIN, C ELEGANS; CLS-3 PROTEIN, C ELEGANS; PHOTOPROTEIN;

ARTICLE; CAENORHABDITIS ELEGANS; CELL POLARITY; CENTROMERE; CHROMOSOME SEGREGATION; CONTROLLED STUDY; EMBRYO; MEIOSIS; MICROTUBULE; MITOSIS; MITOSIS SPINDLE; NONHUMAN; POLYMERIZATION; PRIORITY JOURNAL; PROTEIN DEPLETION; PROTEIN FUNCTION; PROTEIN LOCALIZATION; REGULATORY MECHANISM; RNA INTERFERENCE; WILD TYPE; ANIMAL; ANIMAL EMBRYO; CONFOCAL MICROSCOPY; CYTOLOGY; CYTOPLASM; GENETICS; IMMUNOHISTOCHEMISTRY; METABOLISM; PHYSIOLOGY; PRENATAL DEVELOPMENT; TIME; TRANSGENIC ANIMAL; WESTERN BLOTTING;

CAENORHABDITIS ELEGANS;

ANIMALS; ANIMALS, GENETICALLY MODIFIED; BLOTTING, WESTERN; CAENORHABDITIS ELEGANS; CAENORHABDITIS ELEGANS PROTEINS; CYTOPLASM; EMBRYO, NONMAMMALIAN; IMMUNOHISTOCHEMISTRY; LUMINESCENT PROTEINS; MICROSCOPY, CONFOCAL; MICROTUBULE-ASSOCIATED PROTEINS; MICROTUBULES; MITOSIS; MITOTIC SPINDLE APPARATUS; RNA INTERFERENCE; TIME FACTORS;

EID: 84867911298     PISSN: 00121606     EISSN: 1095564X     Source Type: Journal    
DOI: 10.1016/j.ydbio.2012.05.016     Document Type: Article

References (49)

1. Akhmanova A., Hoogenraad C.C., Drabek K., Stepanova T., Dortland B., Verkerk T., Vermeulen W., Burgering B.M., De Zeeuw C.I., Grosveld F., Galjart N. Clasps are CLIP-115 and -170 associating proteins involved in the regional regulation of microtubule dynamics in motile fibroblasts. Cell 2001, 104:923-935.
2. Al-Bassam J., Chang F. Regulation of microtubule dynamics by TOG-domain proteins XMAP215/Dis1 and CLAS. Trends Cell Biol. 2011, 21:604-614.
3. Al-Bassam J., Kim H., Brouhard G., van Oijen A., Harrison S.C., Chang F. CLASP promotes microtubule rescue by recruiting tubulin dimers to the microtubule. Dev Cell. 2010, 19:245-258.
4. Bratman S.V., Chang F. Stabilization of overlapping microtubules by fission yeast CLASP. Dev. Cell 2007, 13:812-827.
5. Brenner S. The genetics of Caenorhabditis elegans. Genetics 1974, 77:71-94.
6. Cheeseman I.M., MacLeod I., Yates J.R., Oegema K., Desai A. The CENP-F-like proteins HCP-1 and HCP-2 target CLASP to kinetochores to mediate chromosome segregation. Curr. Biol. 2005, 15:771-777.
7. Cheeseman I.M., Niessen S., Anderson S., Hyndman F., Yates J.R., Oegema K., Desai A. A conserved protein network controls assembly of the outer kinetochore and its ability to sustain tension. Genes Dev. 2004, 18:2255-2268.
8. Church D.L., Guan K.L., Lambie E.J. Three genes of the MAP kinase cascade, mek-2, mpk-1/sur-1 and let-60 ras, are required for meiotic cell cycle progression in Caenorhabditis elegans. Development 1995, 121:2525-2535.
9. Dumont J., Oegema K., Desai A. A kinetochore-independent mechanism drives anaphase chromosome separation during acentrosomal meiosis. Nat. Cell Biol. 2010, 12:894-901.
10. Galli M., van den Heuvel S. Determination of the cleavage plane in early C. elegans embryos. Annu. Rev. Genet. 2008, 42:389-411.
11. Gonczy P. Mechanisms of asymmetric cell division: flies and worms pave the way. Nature reviews. Mol. Cell Biol. 2008, 9:355-366.
12. Gonczy P., Bellanger J.M., Kirkham M., Pozniakowski A., Baumer K., Phillips J.B., Hyman A.A. zyg-8, a gene required for spindle positioning in C. elegans, encodes a doublecortin-related kinase that promotes microtubule assembly. Dev. Cell 2001, 1:363-375.
13. Grill S.W., Gonczy 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. Hannak E., Heald R. Xorbit/CLASP links dynamic microtubules to chromosomes in the Xenopus meiotic spindle. J. Cell Biol. 2006, 172:19-25.
15. Hunt-Newbury R., Viveiros R., Johnsen R., Mah A., Anastas D., Fang L., Halfnight E., Lee D., Lin J., Lorch A., McKay S., Okada H.M., Pan J., Schulz A.K., Tu D., Wong K., Zhao Z., Alexeyenko A., Burglin T., Sonnhammer E., Schnabel R., Jones S.J., Marra M.A., Baillie D.L., Moerman D.G. High-throughput in vivo analysis of gene expression in Caenorhabditis elegans. PLoS Biol. 2007, 5:e237.
16. Kamath R.S., Fraser A.G., Dong Y., Poulin G., Durbin R., Gotta M., Kanapin A., Le Bot N., Moreno S., Sohrmann M., Welchman D.P., Zipperlen P., Ahringer J. Systematic functional analysis of the Caenorhabditis elegans genome using RNAi. Nature 2003, 421:231-237.
17. Knoblich J.A. Asymmetric cell division: recent developments and their implications for tumour biology. Nat. Rev. Mol. Cell Biol. 2010, 11:849-860.
18. Kozlowski C., Srayko M., Nedelec F. Cortical microtubule contacts position the spindle in C. elegans embryos. Cell 2007, 129:499-510.
19. Kumar P., Lyle K.S., Gierke S., Matov A., Danuser G., Wittmann T. GSK3beta phosphorylation modulates CLASP-microtubule association and lamella microtubule attachment. J. Cell Biol. 2009, 184:895-908.
20. Labbe J.C., Maddox P.S., Salmon E.D., Goldstein B. PAR proteins regulate microtubule dynamics at the cell cortex in C. elegans. Curr. Biol. 2003, 13:707-714.
21. Labbe J.C., McCarthy E.K., Goldstein B. The forces that position a mitotic spindle asymmetrically are tethered until after the time of spindle assembly. J Cell Biol. 2004, 167:245-256.
22. Lemos C.L., Sampaio P., Maiato H., Costa M., Omel'yanchuk L.V., Liberal V., Sunkel C.E Mast, a conserved microtubule-associated protein required for bipolar mitotic spindle organization. EMBO J. 2000, 19:3668-3682.
23. Lewis J.A., Fleming J.T. Basic culture methods. Methods Cell Biol. 1995, 48:3-29.
24. Lynch A.S., Briggs D., Hope I.A. Developmental expression pattern screen for genes predicted in the C. elegans genome sequencing project. Nat. Genet. 1995, 11:309-313.
25. Maiato H., Fairley E.A., Rieder C.L., Swedlow J.R., Sunkel C.E., Earnshaw W.C. Human CLASP1 is an outer kinetochore component that regulates spindle microtubule dynamics. Cell 2003, 113:891-904.
26. Maiato H., Khodjakov A., Rieder C.L. Drosophila CLASP is required for the incorporation of microtubule subunits into fluxing kinetochore fibres. Nat. Cell Biol. 2005, 7:42-47.
27. Maiato H., Sampaio P., Lemos C.L., Findlay J., Carmena M., Earnshaw W.C., Sunkel C.E. MAST/Orbit has a role in microtubule-kinetochore attachment and is essential for chromosome alignment and maintenance of spindle bipolarity. J. Cell Biol. 2002, 157:749-760.
28. Mathe E., Inoue Y.H., Palframan W., Brown G., Glover D.M. Orbit/Mast, the CLASP orthologue of Drosophila, is required for asymmetric stem cell and cystocyte divisions and development of the polarised microtubule network that interconnects oocyte and nurse cells during oogenesis. Development 2003, 130:901-915.
29. 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.
30. McNally K., Audhya A., Oegema K., McNally F.J. Katanin controls mitotic and meiotic spindle length. J. Cell Biol. 2006, 175:881-891.
31. 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.
32. Miller D.M., Shakes D.C. Immunofluorescence microscopy. Methods Cell Biol. 1995, 48:365-394.
33. Mimori-Kiyosue Y., Grigoriev I., Lansbergen G., Sasaki H., Matsui C., Severin F., Galjart N., Grosveld F., Vorobjev I., Tsukita S., Akhmanova A. CLASP1 and CLASP2 bind to EB1 and regulate microtubule plus-end dynamics at the cell cortex. J. Cell Biol. 2005, 168:141-153.
34. Oegema K., Desai A., Rybina S., Kirkham M., Hyman A.A. Functional analysis of kinetochore assembly in Caenorhabditis elegans. J Cell Biol. 2001, 153:1209-1226.
35. Ortiz J., Funk C., Schafer A., Lechner J. Stu1 inversely regulates kinetochore capture and spindle stability. Gene Develop. 2009, 23:2778-2791.
36. Park D.H., Rose L.S. Dynamic localization of LIN-5 and GPR-1/2 to cortical force generation domains during spindle positioning. Dev. Biol. 2008, 315:42-54.
37. Pereira A.L., Pereira A.J., Maia A.R., Drabek K., Sayas C.L., Hergert P.J., Lince-Faria M., Matos I., Duque C., Stepanova T., Rieder C.L., Earnshaw W.C., Galjart N., Maiato H. Mammalian CLASP1 and CLASP2 cooperate to ensure mitotic fidelity by regulating spindle and kinetochore function. Mol. Biol. Cell 2006, 17:4526-4542.
38. Slep K.C. The role of TOG domains in microtubule plus end dynamics. Biochem. Soc. Trans. 2009, 37:1002-1006.
39. Sonnichsen B., Koski L.B., Walsh A., Marschall P., Neumann B., Brehm M., Alleaume A.M., Artelt J., Bettencourt P., Cassin E., Hewitson M., Holz C., Khan M., Lazik S., Martin C., Nitzsche B., Ruer M., Stamford J., Winzi M., Heinkel R., Roder M., Finell J., Hantsch H., Jones S.J., Jones M., Piano F., Gunsalus K.C., Oegema K., Gonczy P., Coulson A., Hyman A.A., Echeverri C.J. Full-genome RNAi profiling of early embryogenesis in Caenorhabditis elegans. Nature 2005, 434:462-469.
40. Sousa A., Reis R., Sampaio P., Sunkel C.E. The Drosophila CLASP homologue, mast/orbit regulates the dynamic behaviour of interphase microtubules by promoting the pause state. Cell Motil. Cytoskeleton 2007, 64:605-620.
41. Srayko M., Kaya A., Stamford J., Hyman A.A. Identification and characterization of factors required for microtubule growth and nucleation in the early C. elegans embryo. Dev. Cell 2005, 9:223-236.
42. 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.
43. 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.
44. Toya M., Iida Y., Sugimoto A. Imaging of mitotic spindle dynamics in Caenorhabditis elegans embryos. Methods Cell Biol. 2010, 97:359-372.
45. Tsai M.C., Ahringer J. Microtubules are involved in anterior-posterior axis formation in C. elegans embryos. J. Cell Biol. 2007, 179:397-402.
46. Wallenfang M.R., Seydoux G. Polarization of the anterior-posterior axis of C. elegans is a microtubule-directed process. Nature 2000, 408:89-92.
47. Wittmann T., Waterman-Storer C.M. Spatial regulation of CLASP affinity for microtubules by Rac1 and GSK3beta in migrating epithelial cells. J. Cell Biol. 2005, 169:929-939.
48. 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.
49. Zonies S., Motegi F., Hao Y., Seydoux G. Symmetry breaking and polarization of the C. elegans zygote by the polarity protein PAR-2. Development 2010, 137:1669-1677.