Dynamin regulates metaphase furrow formation and plasma membrane compartmentalization in the syncytial Drosophila embryo

Biology Open

Volumn 4, Issue 3, 2015, Pages 301-311

  Rikhy, Richa ^a,c   Mavrakis, Manos ^b   Lippincott Schwartz, Jennifer ^a  

^a EUNICE KENNEDY SHRIVER NATIONAL INSTITUTE OF CHILD HEALTH AND HUMAN DEVELOPMENT   (United States)

^b AIX MARSEILLE UNIVERSITÉ   (France)

^c INDIAN INSTITUTE OF SCIENCE EDUCATION AND RESEARCH   (India)

Author keywords

Actin; Compartmentalization; Drosophila; Dynamin; Endocytosis; Polarity; Syncytium

Indexed keywords

ACTIN; CLATHRIN; CORTACTIN; DYNAMIN; MOESIN;

ARTICLE; CELL COMPARTMENTALIZATION; CELL CYCLE REGULATION; CELL MEMBRANE; CELL MEMBRANE FURROW; CONTROLLED STUDY; DIFFUSION; DROSOPHILA; EMBRYO; EMBRYO DEVELOPMENT; ENDOCYTOSIS; INTERPHASE; MEMBRANE STRUCTURE; METAPHASE; MORPHOGENESIS; MUTANT DROSOPHILA; NONHUMAN; NUCLEAR DIVISION; PROPHASE; PROTEIN FUNCTION; REGULATORY MECHANISM; TEMPERATURE;

EID: 84979765679     PISSN: None     EISSN: 20466390     Source Type: Journal    
DOI: 10.1242/bio.20149936     Document Type: Article

References (55)

1. Achiriloaie, M., Barylko, B. and Albanesi, J. P. (1999). Essential role of the dynamin pleckstrin homology domain in receptor-mediated endocytosis. Mol. Cell. Biol. 19, 1410-1415.
2. Adam, J. C., Pringle, J. R. and Peifer, M. (2000). Evidence for functional differentiation among Drosophila septins in cytokinesis and cellularization. Mol. Biol. Cell 11, 3123-3135.
3. Afshar, K., Stuart, B. and Wasserman, S. A. (2000). Functional analysis of the Drosophila diaphanous FH protein in early embryonic development. Development 127, 1887-1897.
4. Babu, P., Bryan, J. D., Panek, H. R., Jordan, S. L., Forbrich, B. M., Kelley, S. C., Colvin, R. T. and Robinson, L. C. (2002). Plasma membrane localization of the Yck2p yeast casein kinase 1 isoform requires the C-terminal extension and secretory pathway function. J. Cell Sci. 115, 4957-4968.
5. Bhat, M. A., Izaddoost, S., Lu, Y., Cho, K. O., Choi, K. W. and Bellen, H. J. (1999). Discs Lost, a novel multi-PDZ domain protein, establishes and maintains epithelial polarity. Cell 96, 833-845.
6. Cao, J., Albertson, R., Riggs, B., Field, C. M. and Sullivan, W. (2008). Nuf, a Rab11 effector, maintains cytokinetic furrow integrity by promoting local actin polymerization. J. Cell Biol. 182, 301-313.
7. Caudron, F. and Barral, Y. (2009). Septins and the lateral compartmentalization of eukaryotic membranes. Dev. Cell 16, 493-506.
8. Chua, J., Rikhy, R. and Lippincott-Schwartz, J. (2009). Dynamin 2 orchestrates the global actomyosin cytoskeleton for epithelial maintenance and apical constriction. Proc. Natl. Acad. Sci. USA 106, 20770-20775.
9. 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.
10. Daly, R. J. (2004). Cortactin signalling and dynamic actin networks. Biochem. J. 382, 13-25.
11. Damke, H., Baba, T., Warnock, D. E. and Schmid, S. L. (1994). Induction of mutant dynamin specifically blocks endocytic coated vesicle formation. J. Cell Biol. 127, 915-934.
12. Damke, H., Baba, T., van der Bliek, A. M. and Schmid, S. L. (1995). Clathrinindependent pinocytosis is induced in cells overexpressing a temperaturesensitive mutant of dynamin. J. Cell Biol. 131, 69-80.
13. Damke, H., Binns, D. D., Ueda, H., Schmid, S. L. and Baba, T. (2001). Dynamin GTPase domain mutants block endocytic vesicle formation at morphologically distinct stages. Mol. Biol. Cell 12, 2578-2589.
14. Fabrowski, P., Necakov, A. S., Mumbauer, S., Loeser, E., Reversi, A., Streichan, S., Briggs, J. A. G. and De Renzis, S. (2013). Tubular endocytosis drives remodelling of the apical surface during epithelial morphogenesis in Drosophila. Nat. Commun. 4, 2244.
15. 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.
16. 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.
17. Foe, V. E. and Alberts, B. M. (1983). Studies of nuclear and cytoplasmic behaviour during the five mitotic cycles that precede gastrulation in Drosophila embryogenesis. J. Cell Sci. 61, 31-70.
18. Frescas, D., Mavrakis, M., Lorenz, H., Delotto, R. and Lippincott-Schwartz, J. (2006). The secretory membrane system in the Drosophila syncytial blastoderm embryo exists as functionally compartmentalized units around individual nuclei. J. Cell Biol. 173, 219-230.
19. Hagedorn, E. J., Bayraktar, J. L., Kandachar, V. R., Bai, T., Englert, D. M. and Chang, H. C. (2006). Drosophila melanogaster auxilin regulates the internalization of Delta to control activity of the Notch signaling pathway. J. Cell Biol. 173, 443-452.
20. Huang, H.-R., Chen, Z. J., Kunes, S., Chang, G.-D. and Maniatis, T. (2010). Endocytic pathway is required for Drosophila Toll innate immune signaling. Proc. Natl. Acad. Sci. USA 107, 8322-8327.
21. Kalpin, R. F., Daily, D. R. and Sullivan, W. (1994). Use of dextran beads for live analysis of the nuclear division and nuclear envelope breakdown/reformation cycles in the Drosophila embryo. Biotechniques 17, 730, 732-733.
22. Karr, T. L. and Alberts, B. M. (1986). Organization of the cytoskeleton in early Drosophila embryos. J. Cell Biol. 102, 1494-1509.
23. Kellogg, D. R., Mitchison, T. J. and Alberts, B. M. (1988). Behaviour of microtubules and actin filaments in living Drosophila embryos. Development 103, 675-686.
24. Kellogg, D. R., Field, C. M. and Alberts, B. M. (1989). Identification of microtubule-associated proteins in the centrosome, spindle, and kinetochore of the early Drosophila embryo. J. Cell Biol. 109, 2977-2991.
25. Kiehart, D. P., Galbraith, C. G., Edwards, K. A., Rickoll, W. L. and Montague, R. A. (2000). Multiple forces contribute to cell sheet morphogenesis for dorsal closure in Drosophila. J. Cell Biol. 149, 471-490.
26. Kinoshita, M., Field, C. M., Coughlin, M. L., Straight, A. F. and Mitchison, T. J. (2002). Self- and actin-templated assembly of Mammalian septins. Dev. Cell 3, 791-802.
27. Koenig, J. H. and Ikeda, K. (1989). Disappearance and reformation of synaptic vesicle membrane upon transmitter release observed under reversible blockage of membrane retrieval. J. Neurosci. 9, 3844-3860.
28. Le, T. L., Yap, A. S. and Stow, J. L. (1999). Recycling of E-cadherin: a potential mechanism for regulating cadherin dynamics. J. Cell Biol. 146, 219-232.
29. Lloyd, T. E., Atkinson, R., Wu, M. N., Zhou, Y., Pennetta, G. and Bellen, H. J. (2002). Hrs regulates endosome membrane invagination and tyrosine kinase receptor signaling in Drosophila. Cell 108, 261-269.
30. Macia, E., Ehrlich, M., Massol, R., Boucrot, E., Brunner, C. and Kirchhausen, T. (2006). Dynasore, a cell-permeable inhibitor of dynamin. Dev. Cell 10, 839-850.
31. 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.
32. Mavrakis, M., Rikhy, R. and Lippincott-Schwartz, J. (2008). Fluorescence imaging techniques for studying Drosophila embryo development. Curr. Protoc. Cell Biol. 39, 4.18.1-4.18.43.
33. Mavrakis, M., Rikhy, R. and Lippincott-Schwartz, J. (2009). Plasma membrane polarity and compartmentalization are established before cellularization in the fly embryo. Dev. Cell 16, 93-104.
34. McNiven, M. A., Kim, L., Krueger, E. W., Orth, J. D., Cao, H. and Wong, T. W. (2000). Regulated interactions between dynamin and the actin-binding protein cortactin modulate cell shape. J. Cell Biol. 151, 187-198.
35. Mettlen, M., Pucadyil, T., Ramachandran, R. and Schmid, S. L. (2009). Dissecting dynamin's role in clathrin-mediated endocytosis. Biochem. Soc. Trans. 37, 1022-1026.
36. Miller, K. G., Karr, T. L., Kellogg, D. R., Mohr, I. J., Walter, M. and Alberts, B. M. (1985). Studies on the cytoplasmic organization of early Drosophila embryos. Cold Spring Harb. Symp. Quant. Biol. 50, 79-90.
37. Mooren, O. L. and Schafer, D. A. (2009). Constricting membranes at the nano and micro scale. Proc. Natl. Acad. Sci. USA 106, 20559-20560.
38. Nakayama, Y., Shivas, J. M., Poole, D. S., Squirrell, J. M., Kulkoski, J. M., Schleede, J. B. and Skop, A. R. (2009). Dynamin participates in the maintenance of anterior polarity in the Caenorhabditis elegans embryo. Dev. Cell 16, 889-900.
39. Narayanan, R., Leonard, M., Song, B. D., Schmid, S. L. and Ramaswami, M. (2005). An internal GAP domain negatively regulates presynaptic dynamin in vivo: a two-step model for dynamin function. J. Cell Biol. 169, 117-126.
40. Oda, H. and Tsukita, S. (2001). Real-time imaging of cell-cell adherens junctions reveals that Drosophila mesoderm invagination begins with two phases of apical constriction of cells. J. Cell Sci. 114, 493-501.
41. Pelissier, A., Chauvin, J.-P. and Lecuit, T. (2003). Trafficking through Rab11 endosomes is required for cellularization during Drosophila embryogenesis. Curr. Biol. 13, 1848-1857.
42. Poodry, C. A. and Edgar, L. (1979). Reversible alteration in the neuromuscular junctions of Drosophila melanogaster bearing a temperature-sensitive mutation, shibire. J. Cell Biol. 81, 520-527.
43. 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.
44. Riggs, B., Rothwell, W., Mische, S., Hickson, G. R. X., Matheson, J., Hays, T. S., Gould, G. W. and Sullivan, W. (2003). Actin cytoskeleton remodeling during early Drosophila furrow formation requires recycling endosomal components Nuclear-fallout and Rab11. J. Cell Biol. 163, 143-154.
45. Rothwell, W. F., Fogarty, P., Field, C. M. and Sullivan, W. (1998). Nuclear-fallout, a Drosophila protein that cycles from the cytoplasm to the centrosomes, regulates cortical microfilament organization. Development 125, 1295-1303.
46. Royle, S. J., Bright, N. A. and Lagnado, L. (2005). Clathrin is required for the function of the mitotic spindle. Nature 434, 1152-1157.
47. Royou, A., Field, C., Sisson, J. C., Sullivan, W. and Karess, R. (2004). Reassessing the role and dynamics of nonmuscle myosin II during furrow formation in early Drosophila embryos. Mol. Biol. Cell 15, 838-850.
48. Shivas, J. M., Morrison, H. A., Bilder, D. and Skop, A. R. (2010). Polarity and endocytosis: reciprocal regulation. Trends Cell Biol. 20, 445-452.
49. Silverman-Gavrila, R. V., Hales, K. G. and Wilde, A. (2008). Anillin-mediated targeting of peanut to pseudocleavage furrows is regulated by the GTPase Ran. Mol. Biol. Cell 19, 3735-3744.
50. Sokac, A. M. and Wieschaus, E. (2008). Local actin-dependent endocytosis is zygotically controlled to initiate Drosophila cellularization. Dev. Cell 14, 775-786.
51. Stevenson, V., Hudson, A., Cooley, L. and Theurkauf, W. E. (2002). Arp2/3-dependent pseudocleavage [correction of psuedocleavage] furrow assembly in syncytial Drosophila embryos. Curr. Biol. 12, 705-711.
52. Tepass, U., Gruszynski-DeFeo, E., Haag, T. A., Omatyar, L., Török, T. and Hartenstein, V. (1996). shotgun encodes Drosophila E-cadherin and is preferentially required during cell rearrangement in the neurectoderm and other morphogenetically active epithelia. Genes Dev. 10, 672-685.
53. Thompson, H. M., Skop, A. R., Euteneuer, U., Meyer, B. J. and McNiven, M. A. (2002). The large GTPase dynamin associates with the spindle midzone and is required for cytokinesis. Curr. Biol. 12, 2111-2117.
54. van der Bliek, A. M. and Meyerowitz, E. M. (1991). Dynamin-like protein encoded by the Drosophila shibire gene associated with vesicular traffic. Nature 351, 411-414.
55. van der Bliek, A. M., Redelmeier, T. E., Damke, H., Tisdale, E. J., Meyerowitz, E. M. and Schmid, S. L. (1993). Mutations in human dynamin block an intermediate stage in coated vesicle formation. J. Cell Biol. 122, 553-563.