WASp is required for the correct temporal morphogenesis of rhabdomere microvilli

Journal of Cell Biology

Volumn 164, Issue 3, 2004, Pages 417-426

  Zelhof, Andrew C ^a   Hardy, Robert W ^a  

^a UNIVERSITY OF CALIFORNIA   (United States)

Author keywords

Amphiphysin; Chaoptin; Drosophila; Moesin; Photoreceptor

Indexed keywords

AMPHIPHYSIN; F ACTIN; MOESIN; WISKOTT ALDRICH SYNDROME PROTEIN;

ANIMAL CELL; APICAL MEMBRANE; ARTICLE; BRUSH BORDER; CELL ORGANELLE; CENTROMERE; CONTROLLED STUDY; CYTOSKELETON; DROSOPHILA MELANOGASTER; INTESTINE CELL; MICROVILLUS; MORPHOGENESIS; NONHUMAN; PHOTORECEPTOR; PRIORITY JOURNAL; PROTEIN INTERACTION; PROTEIN LOCALIZATION; RHABDOMERE;

ACTINS; ANIMALS; ARMADILLO DOMAIN PROTEINS; BIOLOGICAL MARKERS; CELL MEMBRANE; DROSOPHILA MELANOGASTER; DROSOPHILA PROTEINS; MEMBRANE GLYCOPROTEINS; MICROFILAMENT PROTEINS; MICROVILLI; MORPHOGENESIS; MUTATION; NERVE TISSUE PROTEINS; NEUROMUSCULAR JUNCTION; PHOTORECEPTORS, INVERTEBRATE; SIGNAL TRANSDUCTION; TIME FACTORS; TRANS-ACTIVATORS; TRANSCRIPTION FACTORS; WISKOTT-ALDRICH SYNDROME PROTEIN;

ANIMALIA; DROSOPHILA MELANOGASTER; MELANOGASTER; VESPIDAE;

EID: 0842266588     PISSN: 00219525     EISSN: None     Source Type: Journal    
DOI: 10.1083/jcb.200307048     Document Type: Article

References (51)

1. Arikawa, K., J.L. Hicks, and D.S. Williams. 1990. Identification of actin filaments in the rhabdomeral microvilli of Drosophila photoreceptors. J. Cell Biol. 110:1993-1998.
2. Bagrodia, S., and R.A. Cerione. 1999. Pak to the future. Trends Cell Biol. 9:350-355.
3. Bahri, S.M., X. Yang, and W. Chia. 1997. The Drosophila bifocal gene encodes a novel protein which colocalizes with actin and is necessary for photoreceptor morphogenesis. Mol. Cell. Biol. 17:5521-5529.
4. Baker, E.K., N.J. Colley, and C.S. Zuker. 1994. The cyclophilin homolog NinaA functions as a chaperone, forming a stable complex in vivo with its protein target rhodopsin. EMBO J. 13:4886-4895.
5. Ben-Yaacov, S., R. Le Borgne, I. Abramson, F. Schweisguth, and E.D. Schejter. 2001. Wasp, the Drosophila Wiskott-Aldrich syndrome gene homologue, is required for cell fate decisions mediated by Notch signaling. J. Cell Biol. 152:1-13.
6. Berryman, M., Z. Franck, and A. Bretscher. 1993. Ezrin is concentrated in the apical microvilli of a wide variety of epithelial cells whereas moesin is found primarily in endothelial cells. J. Cell Sci. 105:1025-1043.
7. Bonilha, V.L., S.C. Finnemann, and E. Rodriguez-Boulan. 1999. Ezrin promotes morphogenesis of apical microvilli and basal infoldings in retinal pigment epithelium. J. Cell Biol. 147:1533-1548.
8. Bretscher, A. 1989. Rapid phosphorylation and reorganization of ezrin and spectrin accompany morphological changes induced in A-431 cells by epidermal growth factor. J. Cell Biol. 108:921-930.
9. Bretscher, A., and K. Weber. 1979. Villin: the major microfilament-associated protein of the intestinal microvillus. Proc. Natl. Acad. Sci. USA. 76:2321-2325.
10. Bretscher, A., and K. Weber. 1980. Fimbrin, a new microfilament-associated protein present in microvilli and other cell surface structures. J. Cell Biol. 86:335-340.
11. Chang, H.Y., and D.F. Ready. 2000. Rescue of photoreceptor degeneration in rhodopsin-null Drosophila mutants by activated Rac1. Science. 290:1978-1980.
12. Coluccio, L.M., and A. Bretscher. 1989. Reassociation of microvillar core proteins: making a microvillar core in vitro. J. Cell Biol. 108:495-502.
13. Colwill, K., D. Field, L. Moore, J. Friesen, and B. Andrews. 1999. In vivo analysis of the domains of yeast Rvs167p suggests Rvs167p function is mediated through multiple protein interactions. Genetics. 152:881-893.
14. Daniels, R.H., and G.M. Bokoch. 1999. p21-activated protein kinase: a crucial component of morphological signaling? Trends Biochem. Sci. 24:350-355.
15. Derry, J.M., H.D. Ochs, and U. Francke. 1994. Isolation of a novel gene mutated in Wiskott-Aldrich syndrome. Cell. 78:635-644. (published erratum in Cell. 79:following 922)
16. Derry, J.M., H.D. Ochs, and U. Francke. 1994. Isolation of a novel gene mutated in Wiskott-Aldrich syndrome. Cell. 78:635-644. (published erratum in Cell. 79:following 922)
17. Fath, K.R., and D.R. Burgess. 1995. Microvillus assembly. Not actin alone. Curr. Biol. 5:591-593.
18. 2+-dependent F-actin disruption in intestinal brush borders. J. Cell Biol. 146:819-830.
19. Friederich, E., E. Pringault, M. Arpin, and D. Louvard. 1990. From the structure to the function of villin, an actin-binding protein of the brush border. Bioessays. 12:403-408.
20. Fukuoka, M., S. Suetsugu, H. Miki, K. Fukami, T. Endo, and T. Takenawa. 2001. A novel neural Wiskott-Aldrich syndrome protein (N-WASP) binding protein, WISH, induces Arp2/3 complex activation independent of Cdc42. J. Cell Biol. 152:471-482.
21. Genova, J.L., S. Jong, J.T. Camp, and R.G. Fehon. 2000. Functional analysis of Cdc42 in actin filament assembly, epithelial morphogenesis, and cell signaling during Drosophila development. Dev. Biol. 221:181-194.
22. Heintzelman, M.B., and M.S. Mooseker. 1992. Assembly of the intestinal brush border cytoskeleton. Curr. Top. Dev. Biol. 26:93-122.
23. Lee, T., and L. Luo. 1999. Mosaic analysis with a repressible cell marker for studies of gene function in neuronal morphogenesis. Neuron. 22:451-461.
24. Lemmon, M.A., K.M. Ferguson, R. O'Brien, P.B. Sigler, and J. Schlessinger. 1995. Specific and high-affinity binding of inositol phosphates to an isolated pleckstrin homology domain. Proc. Natl. Acad. Sci. USA. 92:10472-10476.
25. Lila, T., and D.G. Drubin. 1997. Evidence for physical and functional interactions among two Saccharomyces cerevisiae SH3 domain proteins, an adenylyl cyclase-associated protein and the actin cytoskeleton. Mol. Biol. Cell. 8:367-385.
26. Longley, R.L., Jr., and D.F. Ready. 1995. Integrins and the development of three-dimensional structure in the Drosophila compound eye. Dev. Biol. 171:415-433.
27. Louvard, D. 1989. The function of the major cytoskeletal components of the brush border. Curr. Opin. Cell Biol. 1:51-57.
28. Miki, H., K. Miura, and T. Takenawa. 1996. N-WASP, a novel actin-depolymerizing protein, regulates the cortical cytoskeletal rearrangement in a PIP2-dependent manner downstream of tyrosine kinases. EMBO J. 15:5326-5335.
29. Mooseker, M.S., and T.R. Coleman. 1989. The 110-kD protein-calmodulin complex of the intestinal microvillus (brush border myosin I) is a mechanoenzyme. J. Cell Biol. 108:2395-2400.
30. Mullins, R.D. 2000. How WASP-family proteins and the Arp2/3 complex convert intracellular signals into cytoskeletal structures. Curr. Opin. Cell Biol. 12:91-96.
31. Owen, D.J., P. Wigge, Y. Vallis, J.D. Moore, P.R. Evans, and H.T. McMahon. 1998. Crystal structure of the amphiphysin-2 SH3 domain and its role in the prevention of dynamin ring formation. EMBO J. 17:5273-5285.
32. Pinson, K.I., L. Dunbar, L. Samuelson, and D.L. Gumucio. 1998. Targeted disruption of the mouse villin gene does not impair the morphogenesis of microvilli. Dev. Dyn. 211:109-121.
33. Polesello, C., I. Delon, P. Valenti, P. Ferrer, and F. Payre. 2002. Dmoesin controls actin-based cell shape and polarity during Drosophila melanogaster oogenesis. Nat. Cell Biol. 4:782-789.
34. Prehoda, K.E., J.A. Scott, R.D. Mullins, and W.A. Lim. 2000. Integration of multiple signals through cooperative regulation of the N-WASP-Arp2/3 complex. Science. 290:801-806.
35. Raucher, D., T. Stauffer, W. Chen, K. Shen, S. Guo, J.D. York, M.P. Sheetz, and T. Meyer. 2000. Phosphatidylinositol 4,5-bisphosphate functions as a second messenger that regulates cytoskeleton-plasma membrane adhesion. Cell. 100:221-228.
36. Razzaq, A., I.M. Robinson, H.T. McMahon, J.N. Skepper, Y. Su, A.C. Zelhof, A.P. Jackson, N.J. Gay, and C.J. O'Kane. 2001. Amphiphysin is necessary for organization of the excitation-contraction coupling machinery of muscles, but not for synaptic vesicle endocytosis in Drosophila. Genes Dev. 15:2967-2979.
37. Sang, T.K., and D.F. Ready. 2002. Eyes closed, a Drosophila p47 homolog, is essential for photoreceptor morphogenesis. Development. 129:143-154.
38. Schneeberger, D., and T. Raabe. 2003. Mbt, a Drosophila PAK protein, combines with Cdc42 to regulate photoreceptor cell morphogenesis. Development. 130:427-437.
39. Speck, O., S.C. Hughes, N.K. Noren, R.M. Kulikauskas, and R.G. Fehon. 2003. Moesin functions antagonistically to the Rho pathway to maintain epithelial integrity. Nature. 421:83-87.
40. Symons, M., J.M. Derry, B. Karlak, S. Jiang, V. Lemahieu, F. McCormick, U. Francke, and A. Abo. 1996. Wiskott-Aldrich syndrome protein, a novel effector for the GTPase CDC42Hs, is implicated in actin polymerization. Cell. 84:723-734.
41. Takei, K., V.I. Slepnev, V. Haucke, and P. De Camilli. 1999. Functional partnership between amphiphysin and dynamin in clathrin-mediated endocytosis. Nat. Cell Biol. 1:33-39.
42. Takenawa, T., and H. Miki. 2001. WASP and WAVE family proteins: key molecules for rapid rearrangement of cortical actin filaments and cell movement. J. Cell Sci. 114:1801-1809.
43. Tal, T., D. Vaizel-Ohayon, and E.D. Schejter. 2002. Conserved interactions with cytoskeletal but not signaling elements are an essential aspect of Drosophila WASp function. Dev. Biol. 243:260-271.
44. Thrasher, A.J. 2002. WASp in immune-system organization and function. Nat. Rev. Immunol. 2:635-646.
45. Tilney, L.G., and M. Mooseker. 1971. Actin in the brush-border of epithelial cells of the chicken intestine. Proc. Natl. Acad. Sci. USA. 68:2611-2615.
46. Tong, A.H., B. Drees, G. Nardelli, G.D. Bader, B. Brannetti, L. Castagnoli, M. Evangelista, S. Ferracuti, B. Nelson, S. Paoluzi, et al. 2002. A combined experimental and computational strategy to define protein interaction networks for peptide recognition modules. Science. 295:321-324.
47. Van Vactor, D., Jr., D.E. Krantz, R. Reinke, and S.L. Zipursky. 1988. Analysis of mutants in chaoptin, a photoreceptor cell-specific glycoprotein in Drosophila, reveals its role in cellular morphogenesis. Cell 52:281-290.
48. Xu, T., and G.M. Rubin. 1993. Analysis of genetic mosaics in developing and adult Drosophila tissues. Development. 117:1223-1237.
49. Zallen, J.A., Y. Cohen, A.M. Hudson, L. Cooley, E. Wieschaus, and E.D. Schejter. 2002. SCAR is a primary regulator of Arp2/3-dependent morphological events in Drosophila. J. Cell Biol. 156:689-701.
50. Zelhof, A.C., H. Bao, R.W. Hardy, A. Razzaq, B. Zhang, and C.Q. Doe. 2001. Drosophila Amphiphysin is implicated in protein localization and membrane morphogenesis but not in synaptic vesicle endocytosis. Development. 128:5005-5015.
51. Zipursky, S.L., T.R. Venkatesh, D.B. Teplow, and S. Benzer. 1984. Neuronal development in the Drosophila retina: monoclonal antibodies as molecular probes. Cell. 36:15-26.