Distinct roles for the actin and microtubule cytoskeletons in the morphogenesis of epidermal hairs during wing development in Drosophila

Mechanisms of Development

Volumn 70, Issue 1-2, 1998, Pages 181-192

  Turner, Christopher M ^a   Adler, Paul N ^a  

^a UNIVERSITY OF VIRGINIA   (United States)

Author keywords

Actin; Drosophila; Microtubules; Wing hair

Indexed keywords

ACTIN; CYTOCHALASIN D; VINBLASTINE;

ARTICLE; DROSOPHILA; FORELIMB; GENE MUTATION; HAIR GROWTH; LIMB DEVELOPMENT; MICROTUBULE; MORPHOGENESIS; NONHUMAN; PRIORITY JOURNAL;

ACTINS; ANIMALS; BODY PATTERNING; CYTOCHALASIN D; CYTOSKELETON; DROSOPHILA; GENES, INSECT; HAIR; MICROFILAMENTS; MICROSCOPY, ELECTRON; MICROTUBULES; MUTATION; PUPA; TUBULIN; WING;

EID: 0031882069     PISSN: 09254773     EISSN: None     Source Type: Journal    
DOI: 10.1016/S0925-4773(97)00194-9     Document Type: Article

References (49)

1. Achler C., Filmer D., Merte C., Drenckhahn D. Role of microtubules in polarized delivery of apical membrane proteins to the brush border of the intestinal epithelium. J. Cell Biol. 109:1989;179-189.
2. Adler, P.N., Charlton, J., Jones, K., Liu, J., 1994a. The cold-sensitive period for frizzled in the development of wing hair polarity ends prior to the start of hair morphogenesis. Mech. Dev. 46, 101-107.
3. Adler, P.N., Charlton, J., Park, W.J., 1994b. The Drosophila tissue polarity gene inturned functions prior to wing hair morphogenesis in the regulation of hair polarity and number. Genetics 137, 829-836.
4. Adler, P.N., Krasnow, R.E., Liu, J., 1997. Tissue palauty paints from cells that have higher frizzled levels toward cells that have lower frizzled levels. Current Biol. 7, 940-949.
5. Appel L., Prout M., Abu-Shumays R., Hammonds A., Garbe J., Fristrom D., Fristrom J. The Drosophila Stubble gene encodes an apparent transmembrane serine protease required for epithelial morphogenesis. Proc. Natl. Acad. Sci. USA. 90:1993;4937-4941.
6. Barnes G., Drubin D.G., Stearns T. The cytoskeleton of Saccharomyces cerevisiae. Curr. Opin. Cell Biol. 2:1990;109-115.
7. Burgess D.R., Grey R.D. Alterations in morphology of developing microvilli ellicited by cytochalasin. J. Cell Biol. 62:1974;566-574.
8. Cant K., Knowles B.A., Mooseker M.S., Cooley L. Drosophila Singed, a fascin homolog, is required for actin bundle formation during oogenesis and bristle extension. J. Cell Biol. 125:1994;369-380.
9. Clark I., Giniger H., Ruohola-Baker H., Jan L.Y., Jan Y.N. Transient posterior localization of a kinesin fusion protein reflects anteriorposterior polarity of the Drosophila oocyte. Curr. Biol. 4:1994;289-300.
10. Cooper J.A. Effects of cytochalasin and phalloidin on actin. J. Cell Biol. 105:1987;1473-1478.
11. Costa de Beauregard M., Pringault E.S.R., Louvard D. Suppression of villin expression by antisense RNA impairs brush border assembly in polarized intestinal epithelial cells. EMBO J. 14:1995;409-421.
12. Drubin D.G., Nelson W.J. Origins of cell polarity. Cell. 84:1996;335-344.
13. Dustin, P., 1984. Microtubules. Springer-Verlag, Berlin.
14. Eaton S., Auvinen P., Luo L., Jan Y.N., Simons K. CDC42 and RAC1 control different actin dependent processes in the Drosophila wing disc epithelium. J. Cell Biol. 131:1995;151-162.
15. Eaton S., Wepf R., Simons K. Roles for Rac1 and Cdc42 in planar polarization and hair outgrowth in the wing of Drosophila. J. Cell Biol. 135:1996;1277-1289.
16. Fristrom D., Fristrom J. The mechanism of evagination of imaginal discs of Drosophila. Dev. Biol. 43:1975;1-23.
17. Fristrom D., Wilcox M., Fristrom J. The distribution of PS integrins, laminin A and F-actin during key stages in Drosophila wing development. Development. 117:1993;509-523.
18. Gilbert T., Le Bivic A., Quaroni A., Rodriguez-Boulan E. Microtubular organization and its involvement in the biogenetic pathways of plasma membrane proteins in Caco-2 intestinal epithelial cells. J. Cell Biol. 113:1991;275-288.
19. Gubb D., Garcia-Bellido A. A genetic analysis of the determination of cuticular polarity during development in Drosophila melanogaster. J. Embryol. Exp. Morphol. 68:1982;37-57.
20. Hopmann R., Cooper J.A., Miller K.G. Actin organization, bristle morphology, and viability are affected by actin capping protein mutations in Drosophila. J. Cell Biol. 133:1996;1293-1305.
21. Karr T.L., Alberts B.M. Organization of the cytoskeleton in early Drosophila embryos. J. Cell Biol. 102:1986;1494-1509.
22. Krasnow R., Adler P.N. A single frizzled protein has a dual function in tissue polarity. Development. 120:1994;1883-1893.
23. Lew D.J., Reed S.I. Cell cycle control of morphogenesis in budding yeast. Curr. Opin. Gen. Dev. Biol. 5:1995;17-23.
24. Machesky L.M., Hall A. Rho: a connection between membrane receptor signaling and the cytoskeleton. Trends Cell Biol. 6:1996;304-310.
25. Mays R.W., Beck K.A., Nelson W.J. Organization of the cytoskeleton in polarized epithelial cells: a component of the protein sorting machinery. Curr. Topics Cell Biol. 6:1994;16-23.
26. Mitchell H.K., Edens J., Petersen N.S. Stages of cell hair construction in Drosophila. Dev. Gen. 11:1990;133-140.
27. Mitchell H.K., Roach J., Petersen N.S. The morphogenesis of cell hairs on Drosophila wings. Dev. Biol. 95:1983;387-398.
28. Mitchison T.J., Cramer L.P. Actin-based cell motility and cell locomotion. Cell. 84:1996;371-379.
29. Milner M.J., Muir J. The cell biology of Drosphila wing metamorphosis. Roux's Arch. Dev. Biol. 196:1987;191-201.
30. Nübler-Jung K. Insect epidermis: disturbance of supracellular tissue polarity does not prevent the expression of cell polarity. Roux's Arch. Dev. Biol. 196:1987;286-289.
31. Novick P., Botstein D. Phenotypic analysis of temperature-sensitive yeast actin mutants. Cell. 40:1985;405-416.
32. Overton J. The fine structure of developing bristles in wild type and mutant Drosophila melanogaster. J. Morphol. 122:1967;367-380.
33. Park W.J., Liu J., Adler P.N. The Drosophila tissue polarity gene inturned acts cell autonomously and encodes a novel protein. Development. 122:1996;961-969.
34. Pokrywka N.J., Stevenson E.C. Microtubules mediate the localization of bicoid RNA during Drosophila oogenesis. Development. 113:1991;55-66.
35. Ridley A.J., Peterson H.F., Johnston C.L., Diekman D., Hall A. The small GTP-binding protein rac regulates growth factor-induced membrane ruffling. Cell. 70:1992;401-410.
36. Simon M.N., DeVirgilio B., Souza B., Pringle J.R., Abo R., Reed S.I. Role for the Rho-family GTPase Cdc42 in yeast mating phermone signal pathway. Nature. 376:1995;702-705.
37. St.Johnston R.D., Nüsslein-Volhard C. The origin of pattern and polarity in the Drosophila embryo. Cell. 68:1992;201-219.
38. Strutt D.I., Weber U., Mlodzik M. The role of RhoA in tissue polarity and Frizzled signalling. Nature. 387:1997;292-295.
39. Tilney L.G., Connelly P., Smith S., Guild G.M. F-actin bundles in Drosophila bristles are assembled from modules composed of short filaments. J. Cell biol. 135:1996;1291-1308.
40. Tilney L.G., Inouye S. Acrosomal reaction of Thyone sperm. II Kinetics and possible reaction mechanism of acrosomal process elongation. J. Cell Biol. 93:1982;820-827.
41. Tilney L.G., Tilney M.S., Guild G.M. Actin bundles in Drosophila bristles. I. Two filament Cross-linked are involved in bundling. J. Cell Biol. 130:1995;629-638.
42. Theurkauf W.E., Smiley S., Wong M.L., Alberts B.M. Reorganization of the cytoskeleton during Drosophila oogenesis: implications for axis specification and intercellular transport. Development. 115:1992;923-936.
43. Trout L.L., Burnside B. The unusual microtubule polarity in teleost retinal pigment epithelial cells. J. Cell Biol. 107:1988;1461-1464.
44. Tucker J.B. Cytoskleletal coordination and intercellular signaling during metazoan embryogenesis. J. Embryol. Exp. Morph. 65:1981;1-25.
45. Turner C.M., Adler P.N. Morphogenesis of Drosophila pupal wings in vitro. Mech. Dev. 52:1995;247-255.
46. Verheyen E.M., Cooley L. Profilin mutations disrupt multiple actin-dependent processes during Drosophila development. Development. 120:1994;717-728.
47. Welch M.C., Holtzman D.A., Drubin D.G. The yeast actin cytoskeleton. Curr. Opin. Cell Biol. 6:1994;110-119.
48. Wong L.L., Adler P.N. Tissue polarity genes of Drosophila regulate the subcellular location for prehair initiation in pupal wing cells. J. Cell Biol. 123:1993;209-221.
49. Zhang Y., Cerione R., Bender A. Control of the yeast bud site assembly GTPase Cdc42. J. Biol. Chem. 269:1994;2369-2372.