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

Volumn 130, Issue 5, 2003, Pages 901-915

  Máthé, Endre ^a   Inoue, Yoshihiro H ^b   Palframan, William ^a   Brown, Gemma ^a   Glover, David M ^a  

^a UNIVERSITY OF CAMBRIDGE   (United Kingdom)

^b KYOTO INSTITUTE OF TECHNOLOGY   (Japan)

Author keywords

Anillin; Asymmetric division; CLASP; CLIP 190; Cytokinesis; Drosophila; Fusome; Mast; Oogenesis; Orbit; Pavarotti KLP

Indexed keywords

DROSOPHILA PROTEIN; MICROTUBULE ASSOCIATED PROTEIN;

ANIMAL CELL; CELL COMMUNICATION; CELL DIFFERENTIATION; CELL DIVISION; CELL FATE; CELL ORGANELLE; CELL POLARITY; COMPLEX FORMATION; CONTROLLED STUDY; CYTOKINESIS; DROSOPHILA; MICROTUBULE ASSEMBLY; MITOSIS; MITOSIS SPINDLE; NONHUMAN; OOCYTE; OOCYTE DEVELOPMENT; PRIORITY JOURNAL; PROTEIN LOCALIZATION; REVIEW; STEM CELL; WILD TYPE;

ANIMALS; CELL DIFFERENTIATION; CELL DIVISION; CELL POLARITY; CHIMERA; CONTRACTILE PROTEINS; DROSOPHILA MELANOGASTER; DROSOPHILA PROTEINS; FEMALE; MICROTUBULE-ASSOCIATED PROTEINS; MICROTUBULES; MITOTIC SPINDLE APPARATUS; MUTATION; OOCYTES; OOGENESIS; OVARY; PHENOTYPE; STEM CELLS; TUBULIN;

ANIMALIA;

EID: 0037344894     PISSN: 09501991     EISSN: None     Source Type: Journal    
DOI: 10.1242/dev.00315     Document Type: Review

References (52)

1. Adams, R. R., Tavares, A. A., Salzberg, A., Bellen, H. J. and Glover, D. M. (1998). Pavarotti encodes a kinesin-like protein required to organize the central spindle and contractile ring for cytokinesis. Genes Dev. 12, 1483-1494.
2. Akhmanova, A., Hoogenraad, C. C., Drabek, K., Stepanova, T., Dortland, B., Verkerk, T., Vermeulen, W., Burgering, B. M., de Zeeuw, C. I., Grosveld, F. and Galjart, N. (2001). CLASPs are CLIP-115 and -170 associating proteins involved in the regional regulation of microtubule dynamics in motile fibroblasts. Cell 104, 923-935.
3. Allan, V. and Näthke, I. S. (2001). Catch and pull a microtubule: getting a grasp on the cortex. Nat. Cell Biol. 3, E226-E228.
4. Büning, J. (1994). The insect ovary: ultrastructure, previtellogenic growth and evolution. New York: Chapman & Hall.
5. Carmena, M., Riparbelli, M. G., Minestrini, G., Tavares, A. M., Adams, R., Callaini, G. and Glover, D. M. (1999). Drosophila polo kinase is required for cytokinesis. J. Cell Biol. 143, 659-671.
6. de Cuevas, M. and Spradling, A. C. (1998). Morphogenesis of the Drosophila fusome and its implications for oocyte specification. Development 125, 2781-2789.
7. de Cuevas, M., Lee, J. K. and Spradling, A. C. (1996). α-spectrin is required for germline cell division and differentiation the Drosophila ovary. Development 122, 3959-3968.
8. de Cuevas, M., Lilly, M. A. and Spradling, A. C. (1997). Germline cyst formation in Drosophila. Annu. Rev. Genet. 31, 405-428.
9. Deák, P., Omar, M. M., Saunders, R. D. C., Pál, M., Komonyi, O., Szidonya, J., Maróy, P., Zhang, Y., Ashburner, M., Benos, P. et al. (1997). P-element insertion alleles of essential genes on the third chromosome of Drosophila melanogaster: correlation of physical and cytogenetic maps in chromosomal region 86E-87F. Genetics 147, 1697-1722.
10. Deng, W. and Lin, H. (1997). Spectrosomes and fusomes anchor mitotic spindles during asymmetric germ cell divisions and facilitate the formation of a polarised microtubule array for oocyte specification in Drosophila. Dev. Biol. 189, 79-94.
11. Field, C. D. and Alberts, B. M. (1995). Anillin, a contractile ring protein that cycles from the nucleus to the cell cortex. J. Cell Biol. 131, 165-178.
12. Grieder, N. C., de Cuevas, M. and Spradling, A. C. (2000). The fusome organizes the microtubule network during oocyte differentiation in Drosophila. Development 127, 4253-4264.
13. Huynh, J. R. and St Johnston, D. (2000). The role of BicD, Egl, Orb and the microtubules in the restriction of meiosis to the Drosophila oocyte. Development 127, 2785-2794.
14. Inoue, Y. H., Avides, M. C., Shiraki, M., Deák, P., Yamaguchi, M., Nishimoto, Y., Matsukage, A. and Glover, D. M, (2000). Orbit, a novel microtubule-associated protein essential for mitosis in Drosophila melanogaster. J. Cell Biol. 149, 153-165.
15. Johnstone, O. and Lasko, P. (2001). Translational regulation and RNA localization in Drosophila oocytes and embryos. Annu. Rev. Genet. 35, 365-406.
16. King, R. C., Bahns, M., Horowitz, R. and Larremendi, P. (1978). A mutation that affects female and male cells differentially in Drosophila melanogaster. Int. J. Insect Morphol. Embryol. 7, 359-375.
17. Knowles, B. A. and Cooley, L. (1994). The specialized cytoskeleton of Drosophila egg chamber. Trends Genet. 10, 235-241.
18. Komitopoulou, K., Gans, M., Margaritis, L., Kafatos, F. C. and Masson, M. (1983). Isolation and characterization of sex-linked female sterile mutations in Drosophila melanogaster with special attention to eggshell mutants. Genetics 105, 897-920.
19. Lantz, V. A. and Miller, K. G. (1998). A class VI unconventional Myosin is associated with a homologue of a microtubule-binding protein, Cytoplasmic Linker Protein-170, in neurons and at the posterior pole of Drosophila embryos. J. Cell Biol. 140, 897-910.
20. Lemos, C. L., Sampaio, P., Maiato, H., Costa, M., Omel'yanchuk, L. V., Liberal, V. and Sunkel, C. E. (2000). Mast, a conserved microtubule-associated protein required for bipolar mitotic spindle organization. EMBO. J. 19, 3668-3682.
21. León, A. and McKearin, D. (1999). Identification of TER94, an AAA ATPase protein, as a bam-dependent component of the Drosophila fusome. Mol. Biol. Cell 11, 3825-3834.
22. Li, M. G., Serr, M., Edwards, K., Ludmann, S., Yamamoto, D., Tilney, L. G. and Field, C. M. (1999). Filamin is required for ring canal assembly and actin organization during Drosophila oogenesis. J. Cell Biol. 146, 1061-1073.
23. Lin, H., Yue, L. and Spradling, A. C. (1994). The Drosophila fusome, a germline-specific organelle, contains membrane skeletal proteins and functions in cyst formation. Development 120, 947-956.
24. Lin, H. and Spradling, A. C. (1995). Fusome asymmetry and oocyte determination in Drosophila. Dev. Genet. 16, 6-12.
25. Liu, Z., Xie, T. and Steward, R. (1999). Lis1, the Drosophila homolog of a human lissencephaly disease gene, is required for germline cell division and oocyte differentiation. Development 126, 4477-4488.
26. Mahjan-Miklos, S. and Cooley, L. (1994). Intercellular cytoplasm transport during Drosophila oogenesis. Dev. Biol. 165, 336-351.
27. Maiato, H., Sampaio, P., Lemos, C. L., Findlay, J., Carmena, M., Earnshaw, W. C. and Sunkel, C. E. (2002). Mast/Orbit has a role in microtubule - kinetochore attachment and is essential for chromosome alignment and maintenance of spindle bipolarity. J. Cell Biol. 157, 749-760.
28. McKearin, D. and Ohlstein, B. (1995). A role for the Drosophila Bag-of-marbles protein in the differentiation of cystoblasts from germ line stem-cells. Development 121, 2937-2947.
29. McGrail, M. and Hays, T. S. (1997). The microtubule motor cytoplasmic Dynein is required for spindle orientation during germline cell divisions and oocyte differentiation in Drosophila. Development 124, 2409-2419.
30. McGrail, M., Gepner, J., Silvanovich, A., Ludmann, S., Serr, M. and Hays, T. S. (1995). Regulation of cytoplasmic dynein function in vivo by the Drosophila Glued complex. J. Cell Biol. 131, 411-425.
31. McKearin, D. (1997). The Drosophila fusome, organelle biogenesis and germ cell differentiation: if you bild it... BioEssays 19, 147-152.
32. McNally, F. J. (2001). Cytoskeleton: CLASPing the end to the edge. Curr. Biol. 11, R477-R480.
33. Minestrini, G., Máthé, E. and Glover, D. M. (2002). Domains of the Pavarotti kinesin-like protein that direct its subcellular distribution: effects of mislocalisation on the tubulin and actin cytoskeleton during Drosophila oogenesis. J. Cell Sci. 115, 725-736.
34. Navarro, C., Lehmann, R. and Morris, J. (2001). Oogenesis: setting one sister above the rest. Curr. Biol. 11, R162-R165.
35. Paddy, M. R., Belmont, A. S., Saumweber, H., Agard, D. A. and Sedat, J. W. (1990). Interphase nuclear envelope lamins form a discontinuous network that interacts with only a function of the heterochromatin in the nuclear periphery. Cell 62, 89-106.
36. Riechmann, V. and Ephrussi, A. (2001). Axis formation during Drosophila oogenesis. Curr. Opin. Genet. Dev. 11, 374-383.
37. Robinson, D. N., Cant, K. and Cooley, L. (1994). Morphogenesis of Drosophila ovarian ring canals. Development 120, 2015-2025.
38. Rosin-Arbesfeld, R., Ihrke, G. and Bienz, M. (2001). Actin-dependent membrane association of APC tumour suppressor in polarized mammalian epithelial cells. EMBO J. 20, 5929-5939.
39. Schuyler, S. C. and Pellman, D. (2001). Microtubule 'plus-end-tracking proteins': the end is just the beginning. Cell 105, 421-424.
40. Shulman, J. M., Benton, R. and St Johnstone, D. (2000). The Drosophila homolog of C. elegans Par-1 organizes the oocyte cytoskeleton and directs oskar mRNA localization to the posterior pole. Cell 101, 377-388.
41. Sisson, J. C., Field, C., Ventura, R., Royou, A. and Sullivan, W. (2000). Lava lamp, a novel peripheral Golgi protein, is required for Drosophila melanogaster cellularization. J. Cell Biol. 151, 905-917.
42. Sokol, N. S. and Cooley, L. (1999). Drosophila Filamin encoded by the cheerio locus is a component of ovarian ring canals. Curr. Biol. 9, 1221-1230.
43. Spradling, A., Drummond-Barbosa, D. and Kai, T. (2001). Stem cells find their niche. Nature 414, 98-104.
44. Storto, P. D. and King, R. C. (1989). The role of polyfusomes in generating branched chains of cystocytes during Drosophila oogenesis. Dev. Genetics 10, 70-86.
45. Swan, A., Nguyen, T. and Suter, B. (1999). Drosophila Lissencephaly-1 functions with Bic-D and dynein in oocyte determination and nuclear positioning. Nat. Cell Biol. 1, 444-449.
46. Telfer, W. H. (1975). Development and physiology of the oocyte-nurse cell syncitium. Adv. Insect Physiol. 11, 223-319.
47. Theurkauf, W. E. (1994). Microtubules and cytoplasm organization during Drosophila oogenesis. Dev. Biol. 165, 352-360.
48. Theurkauf, W. E., Alberts, B. M., Jan, Y. N. and Jogens, T. A. (1993). A central role for microtubules in the differentiation of Drosophila oocytes. Development 118, 1169-1180.
49. Tomancak, P., Piano, F., Reichmann, V., Gunsalus, K. C., Kemphues, K. J. and Ephrussi, A. (2000). A Drosophila melanogaster homologue of Caenorhabditis elegans par-1 acts at an early step in embryonic axix formation. Nat. Cell Biol. 2, 458-460.
50. Xue, F. and Cooley, L. (1993). kelch encodes a component of intercellular bridges in Drosophila egg chambers. Cell 72, 681-693.
51. Yue, L. and Spradling, A. (1992). Hu-li tai shao, a gene required for ring canal formation during Drosophila oogenesis, encodes a homolog of adducin. Genes Dev. 6, 2443-2454.
52. Zaccai, M. and Lipshitz, H. D. (1996). Differential distribution of two adducin-like protein isoforms in the Drosophila ovary and early embryo. Zygote 4, 159-166.