Zygotically controlled F-actin establishes cortical compartments to stabilize furrows during Drosophila cellularization

Journal of Cell Science

Volumn 121, Issue 11, 2008, Pages 1815-1824

  Sokac, Anna Marie ^a   Wieschaus, Eric ^a  

^a PRINCETON UNIVERSITY   (United States)

Author keywords

Cellularization; Cortical compartments; F actin

Indexed keywords

ANILINE; CHLOROPHYLL; F ACTIN; GENE PRODUCT; MUTANT PROTEIN; MYOSIN II;

ANIMAL CELL; ARTICLE; CELL COMPARTMENTALIZATION; CELL DISRUPTION; CELL JUNCTION; CELL MEMBRANE; CELL SURFACE; CONTROLLED STUDY; DROSOPHILA; EMBRYO; INSECT DEVELOPMENT; NONHUMAN; PHENOTYPE; PRECIPITATION; PRIORITY JOURNAL; PROTEIN DEPLETION; PROTEIN FUNCTION; PROTEIN STABILITY; REGULATORY MECHANISM; ZYGOTE;

ACTINS; ANIMALS; CELL COMPARTMENTATION; CELL MEMBRANE STRUCTURES; CONTRACTILE PROTEINS; CYTOSKELETAL PROTEINS; DOWN-REGULATION; DROSOPHILA; DROSOPHILA PROTEINS; EMBRYO, NONMAMMALIAN; EMBRYONIC DEVELOPMENT; FEMALE; IMAGE CYTOMETRY; MALE; MICROSCOPY, CONFOCAL; MICROSCOPY, ELECTRON, TRANSMISSION; MYOSIN TYPE II; ZYGOTE;

EID: 46749127414     PISSN: 00219533     EISSN: None     Source Type: Journal    
DOI: 10.1242/jcs.025171     Document Type: Article

References (56)

1. Albertson, R., Riggs, B. and Sullivan, W. (2005). Membrane traffic: a driving force in cytokinesis. Trends Cell Biol. 15, 92-101.
2. Byers, T. J. and Armstrong, P. B. (1986). Membrane protein redistribution during Xenopus first cleavage. J Cell Biol. 102, 2176-2184.
3. Chou, T. B. and Perrimon, N. (1992). Use of ay east site-specific recombinase to produce female germline chimeras in Drosophila. Genetics 131, 643-653.
4. Cox, R. T., Kirkpatrick, C. and Peifer, M. (1996). Armadillo is required for adherens junction assembly, cell polarity, and morphogenesis during Drosophila embryogenesis. J. Cell Biol. 134, 133-148.
5. Dawes-Hoang, R. E., Parmar, K. M., Christiansen, A. E., Phelps, C. B., Brand, A. H. and Wleschaus, E. F. (2005). Folded gastrulation, cell shape change and the control of myosin localization. Development 132, 4165-4178.
6. De Renzis, S., Elemento, O., Tavazoie, S. and Wieschaus, E. F. (2007). Unmasking activation of the zygotic genome using chromosomal deletions in the Drosophila embryo. PLoS Biol. 5, e117.
7. Dobbelaere, J. and Barral, Y. (2004). Spatial coordination of cytokinetic events by compartmentalization of the cell cortex. Science 305, 393-396.
8. Dzhashiashvili, Y., Zhang, Y., Galinska, J., Lam, I., Grumet, M. and Salzer, J. L. (2007). Nodes of Ranvier and axon initial segments are ankyrin G-dependent domains that assemble by distinct mechanisms. J Cell Biol. 177, 857-870.
9. Ehre, C., Rossi, A. H., Abdullah, L. H., De Pestel, K., Hill, S., Olsen, J. C. and Davis, C. W. (2005). Barrier role of actin filaments in regulated mucin secretion from airway goblet cells. Am. J. Physiol. Cell Physiol. 288, C46-C56.
10. Field, C. M. 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.
11. Field, C. M., Coughlin, M., Doberstein, S., Marty, T. and Sullivan, W. (2005). Characterization of anillin mutants reveals essential roles in septin localization and plasma membrane integrity. Development 132, 2849-2860.
12. Field, S. J., Madson, N., Kerr, M. L., Galbraith, K. A., Kennedy, C. E., Tahiliani, M., Wilkins, A. and Cantley, L. C. (2005). PtdIns(4,5)P2 functions at the cleavage furrow during cytokinesis. Curr. Biol. 15, 1407-1412.
13. Gheber, L. A. and Edidin, M. (1999). A model for membrane patchiness: lateral diffusion in the presence of barriers and vesicle traffic. Biophys. J. 77, 3163-3175.
14. Grevengoed, E. E., Fox, D. T., Gates, J. and Peifer, M. (2003). Balancing different types of actin polymerization at distinct sites: roles for Abelson kinase and Enabled. J. Cell Biol. 163, 1267-1279.
15. Grosshans, J., Wenzl, C., Herz, H. M., Bartoszewski, S., Schnorrer, F., Vogt, N., Schwarz, H. and Muller, H. A. (2005), RhoGEF2 and the formin Dia control the formation of the furrow canal by directed actin assembly during Drosophila cellularisation. Development 132, 1009-1020.
16. Harris, T. J. and Peifer, M. (2004). Adherens junction-dependent and -independent steps in the establishment of epithelial cell polarity in Drosophila. J. Cell Biol. 167, 135-147.
17. Harris, T. J. and Peifer, M. (2005). The positioning and segregation of apical cues during epithelial polarity establishment in Drosophila. J. Cell Biol. 170, 813-823.
18. Holowka, D., Sheets, E. D. and Baird, B. (2000). Interactions between Fc(cpsilon)RI and lipid raft components are regulated by the actin cytoskeleton. J. Cell Sci. 113, 1009-1019.
19. Hunter, C. and Wieschaus, E. (2000). Regulated expression of nullo is required for the formation of distinct apical and basal adherens junctions in the Drosophila blastoderm. J. Cell Biol. 150, 391-401.
20. Hunter, C., Sung, P., Schejter, E. D. and Wieschaus, E. (2002). Conserved domains of the Nullo protein required for cell-surface localization and formation of adherens junctions. Mol. Biol. Cell 13, 146-157.
21. Kaksonen, M., Toret, C. P. and Drubin, D. G. (2006). Harnessing actin dynamics for clathrin-mediated endocytosis. Nat. Rev. Mol. Cell Biol. 7, 404-414.
22. Lecuit, T. and Wieschaus, E. (2000). Polarized insertion of new membrane from a cytoplasmic reservoir during cleavage of the Drosophila embryo. J Cell Biol. 150, 849-860.
23. Lee, O. K., Frese, K. K., James, J. S., Chadda, D., Chen, Z. H., Javier, R. T. and Cho, K. O. (2003). Discs-Large and Strabismus are functionally linked to plasma membrane formation. Nat. Cell Biol. 5, 987-993.
24. Marco, E., Wedlich-Soldner, R., Li, R., Altschuler, S. J. and Wu, L. F. (2007). Endocytosis optimizes the dynamic localization of membrane proteins that regulate cortical polarity. Cell 129, 411-422.
25. Maxfield, F. R. and Tabas, J. (2005). Role of cholesterol and lipid organization in disease. Nature 438, 612-621.
26. Mazumdar, A. and Mazuradar, M. (2002). How one becomes many: blastoderm cellularization in Drosophila melanogaster. BioEssays 24, 1012-1022.
27. Muller, H. A. and Wieschaus, E. (1996). armadillo, bazooka, and stardust are critical for early stages in formation of the zonula adherens and maintenance of the polarized blastoderm epithelium in Drosophila. J. Cell Biol. 134, 149-163.
28. Nakada, C., Ritchie, K., Oba, Y., Nakamura, M., Hotta, Y., Iion, R., Kasai, R. S., Yamaguchi, K., Fujiwara, T. and Kusumi, A. (2003). Accumulation of anchored proteins forms membrane diffusion barriers during neuronal polarization. Nat. Cell Biol. 5, 626-632.
29. Oliferenko, S., Paiha, K., Harder, T., Gerke, V., Schwarzler, C., Schwarz, H., Beug, H., Gunthert, U. and Huber, L. A. (1999). Analysis of CD44-containing lipid rafts: Recruitment of annexin II and stabilization by the actin cytoskeleton. J. Cell Biol. 146, 843-854.
30. Padash Barmchi, M., Rogers, S. and Hacker, U. (2005). DRhoGEF2 regulates actin organization and contractility in the Drosophila blastoderm embryo. J. Cell Biol. 168, 575-585.
31. Peifer, M. and Wieschaus, E. (1990). The segment polarity gene armadillo encodes a functionally modular protein that is the Drosophila bomolog of human plakoglobin. Cell 63, 1167-1176.
32. Pesacreta, T. C., Byers, T. J., Dubreull, R., Kiehart, D. P. and Branton, D. (1989). Drosophila spectrin: the membrane skeleton during embryogenesis. J. Cell Biol. 108, 1697-1709.
33. Postner, M. A. and Wieschaus, E. F. (1994). The nullo protein is a component of the actin-myosin network that mediates cellularization in Drosophila melanogaster embryos. J. Cell Sci. 107, 1863-1873.
34. Rose, L. S. and Wieschaus, E. (1992). The Drosophila cellularization gene nullo produces a blastoderm-specific transcript whose levels respond to the nucleocytoplasmic ratio. Genes Dev. 6, 1255-1268.
35. Royou, A., Field, C., Sisson, J. C., Sullivan, W. and Karess, R. (2004). Reassessing the role and dynamics of nommuscle myosin II during furrow formation in early Drosophila embryos. Mol. Biol. Cell 15, 838-850.
36. Schejter, E. D. and Wieschaus, E. (1993). Functional elements of the cytoskeleton in the early Drosophila embryo. Annu. Rev. Cell Biol. 9, 67-99.
37. Schmidt, K. and Nichols, B. J. (2004). A barrier to lateral diffusion in the cleavage furrow of dividing mammalian cells. Curr. Biol. 14, 1002-1006.
38. Schupbach, T. and Wieschaus, E. (1989). Female sterile mutations on the second chromosome of Drosophila melanogaster. I. Material effect mutations. Genetics 121, 101-117.
39. Seveau, S., Eddy, R. J., Maxfield, F. R. and Pierini, L. M. (2001). Cytoskeleton-dependent membrane domain segregation during neutrophil polarization. Mol. Biol. Cell 12, 3550-3562.
40. Shapiro, L., Fannon, A. M., Kwong, P. D., Thompson, A., Lehmann, M. S., Grubel, G., Legrand, J. F., Als-Nielsen, J., Colman, D. R. and Hendrickson, W. A. (1995). Structural basis of cell-cell adhesion by cadherins. Nature 374, 327-337.
41. Sokac, A. M. and Wieschaus, E. (2008). Local actin-dependent endocytosis is zygotically controlled to initiate Drosophila cellularization. Dev. Cell (in press).
42. Sullivan, W., Ashburner, M. and Hawley, R. S. (ed.) (2000). Drosophila Protocols. Cold Spring Harbor, NY: Cold Spring Harbor Laboratory Press.
43. Takeds, T., Kawate, T. and Chang, F. (2004). Organization of a sterol-rich membrane domain by cdc15p during cytokinesis in fission yeast. Nat. Cell Biol. 6, 1142-1144.
44. Thomas, G. H. and Williams, J. A. (1999). Dynamic rearrangement of the spectrin membrane skeleton during the generation of epithelial polarity in Drosophila. J. Cell Sci. 112, 2843-2852.
45. Thomas, J. H. and Wieschaus, E. (2004). src64 and tec29 ate required for microfilament contraction during Drosophila cellularization. Development 131, 863-871.
46. Tolwinski, N. S. and Wieschaus, E. (2001). Armadillo nuclear import is regulated by cytoplasmic anchor Axin and nuclear anchor dTCF/ Pan. Development 128, 2107-2117.
47. Townsley, E. M. and Bienz, M. (2000). Actin-dependent membrane association of a Drosophila epithelial APC protein and its effect on junctional Armadillo. Curr. Biol. 10, 1339-1348.
48. Valentijn, K. M., Gumkowski, F. D. and Jamieson, J. D. (1999). The subapical actin cytoskeleton regulates secretion and membrane retrieval in pancreatic acinar cells. J. Cell Sci. 112, 81-96.
49. Wachtler, V., Rajagopalan, S. and Balasubramanian, M. K. (2003). Sterol-rich plasma membrane domains in the fission yeast Schizosaccharomyces pombe. J. Cell Sci. 116, 867-874.
50. Warn, R. M. and Magrath, R. (1983). F-actin distribution during the cellularization of the Drosophila embryo visualized with FL-phalloidin. Exp. Cell Res. 143, 103-114.
51. Warn, R. M., Bullard, B. and Magrath, R. (1980). Changes in the distribution of cortical myosin during the cellularization of the Drosophila embryo. J. Embryol. Exp. Morphol. 57, 167-176.
52. Wieschaus, E. (1996). Embryonic transcription and the control of developmental pathways. Genetics 142, 5-10.
53. Wieschaus, E. and Sweeton, D. (1988). Requirements for X-linked zygotic gene activity during cellularization of early Drosophila embryos. Development 104, 483-493.
54. Winckler, B. and Mellman, I. (1999). Neuronal polarity: controlling the sorting and diffusion of membrane components. Neuron 23, 637-640.
55. Winckler, B., Forscher, P. and Mellman, I. (1999). A diffusion barrier maintains distribution of membrane proteins in polarized neurons. Nature 397, 698-701.
56. Wu, M., Holowka, D., Craighead, H. G. and Baird, B. (2004). Visualization of plasma membrane compartmentalization with patterned lipid bilayers. Proc. Natl. Acad. Sci. USA 101, 13798-13803.