Asymmetric microtubule function is an essential requirement for polarized organization of the drosophila bristle

Molecular and Cellular Biology

Volumn 30, Issue 2, 2010, Pages 496-507

  Bitan, Amir ^a   Guild, Gregory M ^b   Bar Dubin, Dikla ^a   Abdu, Uri ^a  

^a BEN GURION UNIVERSITY OF THE NEGEV   (Israel)

^b UNIVERSITY OF PENNSYLVANIA   (United States)

Author keywords

[No Author keywords available]

Indexed keywords

CHIMERIC PROTEIN; DROSOPHILA PROTEIN; HOOK PROTEIN; KINESIN 1; MUTANT PROTEIN; PROTEIN IK2; PROTEIN SPINDLE F; UNCLASSIFIED DRUG;

ACTIN POLYMERIZATION; ARTICLE; BRISTLE CELL; CELLULAR DISTRIBUTION; CONTROLLED STUDY; DROSOPHILA; ENDOCYTOSIS; INSECT CELL; INSECT DEVELOPMENT; MICROTUBULE ASSEMBLY; NONHUMAN; PRIORITY JOURNAL; PROTEIN LOCALIZATION;

ACTINS; ANIMALS; DROSOPHILA MELANOGASTER; DROSOPHILA PROTEINS; GENE EXPRESSION REGULATION, DEVELOPMENTAL; I-KAPPA B KINASE; MICROSCOPY, ELECTRON, SCANNING; MICROTUBULE-ASSOCIATED PROTEINS; MICROTUBULES; MUTATION;

EID: 73549108721     PISSN: 02707306     EISSN: None     Source Type: Journal    
DOI: 10.1128/MCB.00861-09     Document Type: Article

References (52)

1. Abdu, U., D. Bar, and T. Schupbach. 2006. Spn-F encodes a novel protein that affects oocyte patterning and bristle morphology in Drosophila. Development 133:1477-1484.
2. Andersen, R., Y. Li, M. Resseguie, and J. E. Brenman. 2005. Calcium/ calmodulin-dependent protein kinase II alters structural plasticity and cytoskeletal dynamics in Drosophila. J. Neurosci. 25:8878-8888.
3. Apodaca, G. 2001. Endocytic traffic in polarized epithelial cells: role of the actin and microtubule cytoskeleton. Traffic 2:149-159.
4. Baas, P. W., C. Vidya Nadar, and K. A. Myers. 2006. Axonal transport of microtubules: the long and short of it. Traffic 7:490-498.
5. Bainbridge, S. P., and M. Bownes. 1981. Staging the metamorphosis of Drosophila melanogaster. J. Embryol. Exp. Morphol. 66:57-80.
6. Bartolini, F., and G. G. Gundersen. 2006. Generation of noncentrosomal microtubule arrays. J. Cell Sci. 119:4155-4163.
7. Clark, I. E., L. Y. Jan, and Y. N. Jan. 1997. Reciprocal localization of Nod and Kinesin fusion proteins indicates microtubule polarity in the Drosophila oocyte, epithelium, neuron and muscle. Development 124:461-470.
8. Cui, W., L. R. Sproul, S. M. Gustafson, H. J. Matthies, S. P. Gilbert, and R. S. Hawley. 2005. Drosophila Nod protein binds preferentially to the plus ends of microtubules and promotes microtubule polymerization in vitro. Mol. Biol. Cell 16:5400-5409.
9. DeRosier, D. J., and L. G. Tilney. 2000. F-actin bundles are derivatives of microvilli: what does this tell us about how bundles might form? J. Cell Biol. 148:1-6.
10. Drubin, D. G., and W. J. Nelson. 1996. Origins of cell polarity. Cell 84:335-344.
11. Dubin-Bar, D., A. Bitan, A. Bakhrat, R. Kaiden-Hasson, S. Etzion, B. Shaanan, and U. Abdu. 2008. The Drosophila IKK-related kinase (Ik2) and Spindle-F proteins are part of a complex that regulates cytoskeleton organization during oogenesis. BMC Cell Biol. 9:51.
12. Duffy, J. B. 2002. GAL4 system in Drosophila: a fly geneticist's Swiss army knife. Genesis 34:1-15.
13. Fei, X., B. He, and P. N. Adler. 2002. The growth of Drosophila bristles and laterals is not restricted to the tip or base. J. Cell Sci. 115:3797-3806.
14. Frank, D. J., R. Hopmann, M. Lenartowska, and K. G. Miller. 2006. Capping protein and the arp2/3 complex regulate nonbundle actin filament assembly to indirectly control actin bundle positioning during Drosophila melanogaster bristle development. Mol. Biol. Cell 17:3930-3939.
15. Guild, G. M., P. S. Connelly, L. Ruggiero, K. A. Vranich, and L. G. Tilney. 2003. Long continuous actin bundles in Drosophila bristles are constructed by overlapping short filaments. J. Cell Biol. 162:1069-1077.
16. Guild, G. M., P. S. Connelly, L. Ruggiero, K. A. Vranich, and L. G. Tilney. 2005. Actin filament bundles in Drosophila wing hairs: hairs and bristles use different strategies for assembly. Mol. Biol. Cell 16:3620-3631.
17. Guild, G. M., P. S. Connelly, K. A. Vranich, M. K. Shaw, and L. G. Tilney. 2002. Actin filament turnover removes bundles from Drosophila bristle cells. J. Cell Sci. 115:641-653.
18. Heuer, J. G., K. Li, and T. C. Kaufman. 1995. The Drosophila homeotic target gene Centrosomin (Cnn) encodes a novel centrosomal protein with leucine zippers and maps to a genomic region required for midgut morphogenesis. Development 121:3861-3876.
19. Khodosh, R., A. Augsburger, T. L. Schwarz, and P. A. Garrity. 2006. Bchs, a BEACH domain protein, antagonizes Rab11 in synapse morphogenesis and other developmental events. Development 133:4655-4665.
20. Krämer, H., and M. Phistry. 1996. Mutations in the Drosophila hook gene inhibit endocytosis of the boss transmembrane ligand into multivesicular bodies. J. Cell Biol. 133:1205-1215.
21. Krämer, H., and M. Phistry. 1999. Genetic analysis of hook, a gene required for endocytic trafficking in Drosophila. Genetics 151:675-684.
22. Kuranaga, E., H. Kanuka, A. Tonoki, K. Takemoto, T. Tomioka, M. Kobayashi, S. Hayashi, and M. Miura. 2006. Drosophila IKK-related kinase regulates nonapoptotic function of caspases via degradation of IAPs. Cell 126:583-596.
23. Lee, H. H., L. Y. Jan, and Y. N. Jan. 2009. Drosophila IKK-related kinase Ik2 and Katanin p60-like 1 regulate dendrite pruning of sensory neuron during metamorphosis. Proc. Natl. Acad. Sci. U. S. A. 106:6363-6368.
24. Lee, T., C. Winter, S. S. Marticke, A. Lee, and L. Luo. 2000. Essential roles of Drosophila RhoA in the regulation of neuroblast proliferation and dendritic but not axonal morphogenesis. Neuron 25:307-316.
25. Li, K., and T. C. Kaufman. 1996. The homeotic target gene Centrosomin encodes an essential centrosomal component. Cell 85:585-596.
26. Manders, E. M. M., F. J. Verbeek, and J. A. Aten. 1993. Measurement of co-localization of objects in dual-colour confocal images. J. Microsc. 169: 375-382.
27. Müsch, A. 2004. Microtubule organization and function in epithelial cells. Traffic 5:1-9.
28. Narayanan, R., H. Krämer, and M. Ramaswami. 2000. Drosophila endosomal proteins hook and deep orange regulate synapse size but not synaptic vesicle recycling. J. Neurobiol. 45:105-119.
29. Oshima, K., M. Takeda, E. Kuranaga, R. Ueda, T. Aigaki, M. Miura, and S. Hayashi. 2006. IKK Epsilon regulates F actin assembly and interacts with drosophila IAP1 in cellular morphogenesis. Curr. Biol. 16:1531-1537.
30. Overton, J. 1967. The fine structure of developing bristles in wild-type and mutant Drosophila melanogaster. J. Morphol. 122:367-380.
31. Purcell, K., and S. Artavanis Tsakonas. 1999. The developmental role of warthog, the notch modifier encoding Drab6. J. Cell Biol. 146:731-740.
32. Rodriguez-Boulan, E., G. Kreitzer, and A. Müsch. 2005. Organization of vesicular trafficking in epithelia. Nat. Rev. Mol. Cell Biol. 6:233-247.
33. Rogers, G. C., N. M. Rusan, M. Peifer, and S. L. Rogers. 2008. A multicomponent assembly pathway contributes to the formation of acentrosomal microtubule arrays in interphase Drosophila cells. Mol. Biol. Cell 19:3163-3178.
34. Rolls, M. M., D. Satoh, P. J. Clyne, A. L. Henner, T. Uemura, and C. Q. Doe. 2007. Polarity and intracellular compartmentalization of Drosophila neurons. Neural Dev. 2:7.
35. Sánchez-Soriano, N., W. Bottenberg, A. Fiala, U. Haessler, A. Kerassoviti, E. Knust, R. Löhr, and A. Prokop. 2005. Are dendrites in Drosophila homologous to vertebrate dendrites? Dev. Biol. 288:126-138.
36. Sevrioukov, E. A., J. P. He, N. Moghrabi, A. Sunio, and H. Krämer. 1999. A role for the deep orange and carnation eye color genes in lysosomal delivery in Drosophila. Mol. Cell 4:479-486.
37. Shapiro, R. S., and K. V. Anderson. 2006. Drosophila Ik2, a member of the I Kappa B Kinase family, is required for mRNA localization during oogenesis. Development 133:1467-1475.
38. Stone, M. C., F. Roegiers, and M. M. Rolls. 2008. Microtubules have opposite orientation in axons and dendrites of Drosophila neurons. Mol. Biol. Cell 19:4122-4129.
39. Sunio, A., A. B. Metcalf, and H. Krämer. 1999. Genetic dissection of endocytic trafficking in Drosophila using a horseradish peroxidase-bride of sevenless chimera: hook is required for normal maturation of multivesicular endosomes. Mol. Biol. Cell 4:847-859.
40. Tilney, L. G., P. Connelly, S. Smith, and G. M. Guild. 1996. F-actin bundles in Drosophila bristles are assembled from modules composed of short filaments. J. Cell Biol. 135:1291-1308.
41. Tilney, L. G., P. S. Connelly, and G. M. Guild. 2004. Microvilli appear to represent the first step in actin bundle formation in Drosophila bristles. J. Cell Sci. 117:3531-3538.
42. Tilney, L. G., P. S. Connelly, L. Ruggiero, K. A. Vranich, and G. M. Guild. 2003. Actin filament turnover regulated by cross-linking accounts for the size, shape, location, and number of actin bundles in Drosophila bristles. Mol. Biol. Cell 14:3953-3966.
43. Tilney, L. G., P. S. Connelly, K. A. Vranich, M. K. Shaw, and G. M. Guild. 1998. Why are two different cross-linkers necessary for actin bundle formation in vivo and what does each cross-link contribute? J. Cell Biol. 143:121-133.
44. Tilney, L. G., P. S. Connelly, K. A. Vranich, M. K. Shaw, and G. M. Guild. 2000. Actin filaments and microtubules play different roles during bristle elongation in Drosophila. J. Cell Sci. 113:1255-1265.
45. Tilney, L. G., P. S. Connelly, K. A. Vranich, M. K. Shaw, and G. M. Guild. 2000. Regulation of actin filament cross-linking and bundle shape in Drosophila bristles. J. Cell Biol. 148:87-100.
46. Tilney, L. G., M. S. Tilney, and G. M. Guild. 1995. F actin bundles in Drosophila bristles. I. Two filament cross-links are involved in bundling. J. Cell Biol. 130:629-638.
47. Wiese, C., and Y. Zheng. 2006. Microtubule nucleation: gamma-tubulin and beyond. J. Cell Sci. 119:4143-4153.
48. Yamamoto, M., R. Ueda, K. Takahashi, K. Saigo, and T. Uemura. 2006. Control of axonal sprouting and dendrite branching by the Nrg-Ank complex at the neuron-glia interface. Curr. Biol. 22:1678-1683.
49. Ye, B., Y. Zhang, W. Song, S. H. Younger, L. Y. Jan, and Y. N. Jan. 2007. Growing dendrites and axons differ in their reliance on the secretory pathway. Cell 130:717-729.
50. Zhang, J., K. L. Schulze, P. R. Hiesinger, K. Suyama, S. Wang, M. Fish, M. Acar, R. A. Hoskins, H. J. Bellen, and M. P. Scott. 2007. Thirty-one flavors of Drosophila rab proteins. Genetics 176:1307-1322.
51. Zhang, J., M. Fonovic, K. Suyama, M. Bogyo, and M. P. Scott. 2009. Rab35 controls actin bundling by recruiting fascin as an effector protein. Science 325:1250-1254.
52. Zimyanin, V. L., K. Belaya, J. Pecreaux, M. J. Gilchrist, A. Clark, I. Davis, and D. St Johnston. 2008. In vivo imaging of oskar mRNA transport reveals the mechanism of posterior localization. Cell 134:843-853.