Coordinating the cytoskeleton and endocytosis for regulated plasma membrane growth in the early Drosophila embryo

BioArchitecture

Volumn 4, Issue 2, 2014, Pages 68-74

  Lee, Donghoon M ^a   Harris, Tony J C ^a  

^a UNIVERSITY OF TORONTO   (Canada)

Author keywords

Actin; Amphiphysin; Cellularization; Cytohesin; Cytoskeleton; Drosophila; Endocytosis; Plasma membrane; Rho1; Steppke

Indexed keywords

ACTIN RELATED PROTEIN 2; ACTIN RELATED PROTEIN 3; AMPHIPHYSIN; ARF PROTEIN; CLATHRIN; DIAPHANOUS; DYNAMIN; MYOSIN ADENOSINE TRIPHOSPHATASE; MYOSIN II; RHO GUANINE NUCLEOTIDE DISSOCIATION INHIBITOR 1; RHO GUANINE NUCLEOTIDE EXCHANGE FACTOR; RHO GUANINE NUCLEOTIDE EXCHANGE FACTOR 2; UNCLASSIFIED DRUG; DROSOPHILA PROTEIN; GUANINE NUCLEOTIDE EXCHANGE FACTOR;

CELL COMPARTMENTALIZATION; CELL GROWTH; CELL MEMBRANE; CENTROSOME; CYTOKINESIS; CYTOSKELETON; DROSOPHILA; ENDOCYTOSIS; ENZYME ACTIVITY; ENZYME MECHANISM; ENZYME REGULATION; MEMBRANE STRUCTURE; MOLECULAR INTERACTION; NONHUMAN; NOTE; ANIMAL; BLASTODERM; CYTOLOGY; DROSOPHILA MELANOGASTER; EMBRYOLOGY; GENETICS; METABOLISM; PHYSIOLOGY;

ANIMALS; BLASTODERM; CYTOSKELETON; DROSOPHILA MELANOGASTER; DROSOPHILA PROTEINS; ENDOCYTOSIS; GUANINE NUCLEOTIDE EXCHANGE FACTORS;

EID: 84922480995     PISSN: 19490992     EISSN: 1949100X     Source Type: Journal    
DOI: 10.4161/bioa.28949     Document Type: Note

References (49)

1. Mooren OL, Galletta BJ, Cooper JA. Roles for actin assembly in endocytosis. Annu Rev Biochem 2012; 81:661-86; PMID:22663081; http://dx.doi. org/10.1146/annurev-biochem-060910-094416
2. Anitei M, Hoflack B. Bridging membrane and cytoskeleton dynamics in the secretory and endocytic pathways. Nat Cell Biol 2012; 14:11-9; PMID:22193159; http://dx.doi.org/10.1038/ ncb2409
3. Aghamohammadzadeh S, Ayscough KR. Differential requirements for actin during yeast and mammalian endocytosis. Nat Cell Biol 2009; 11:1039-42; PMID:19597484; http://dx.doi.org/10.1038/ ncb1918
4. Gauthier NC, Masters TA, Sheetz MP. Mechanical feedback between membrane tension and dynamics. Trends Cell Biol 2012; 22:527-35; PMID:22921414; http://dx.doi.org/10.1016/j.tcb.2012.07.005
5. Boulant S, Kural C, Zeeh JC, Ubelmann F, Kirchhausen T. Actin dynamics counteract membrane tension during clathrin-mediated endocytosis. Nat Cell Biol 2011; 13:1124-31; PMID:21841790; http:// dx.doi.org/10.1038/ncb2307
6. Kaur S, Fielding AB, Gassner G, Carter NJ, Royle SJ. An unmet actin requirement explains the mitotic inhibition of clathrin-mediated endocytosis. Elife 2014; 3:e00829; PMID:24550251; http://dx.doi. org/10.7554/eLife.00829
7. Lee DM, Harris TJ. An Arf-GEF regulates antagonism between endocytosis and the cytoskeleton for Drosophila blastoderm development. Curr Biol 2013; 23:2110-20; PMID:24120639; http://dx.doi. org/10.1016/j.cub.2013.08.058
8. Lecuit T. Junctions and vesicular trafficking during Drosophila cellularization. J Cell Sci 2004; 117:3427-33; PMID:15252125; http://dx.doi.org/10.1242/ jcs.01312
9. Mazumdar A, Mazumdar M. How one becomes many: blastoderm cellularization in Drosophila melanogaster. Bioessays 2002; 24:1012-22; PMID:12386932; http://dx.doi.org/10.1002/ bies.10184
10. Harris TJ, Sawyer JK, Peifer M. How the cytoskeleton helps build the embryonic body plan: models of morphogenesis from Drosophila. Curr Top Dev Biol 2009; 89:55-85; PMID:19737642; http://dx.doi. org/10.1016/S0070-2153(09)89003-0
11. Foe VE, Alberts BM. Studies of nuclear and cytoplasmic behaviour during the five mitotic cycles that precede gastrulation in Drosophila embryogenesis. J Cell Sci 1983; 61:31-70; PMID:6411748
12. Lecuit T, Wieschaus E. Polarized insertion of new membrane from a cytoplasmic reservoir during cleavage of the Drosophila embryo. J Cell Biol 2000; 150:849-60; PMID:10953008; http://dx.doi. org/10.1083/jcb.150.4.849
13. Frescas D, Mavrakis M, Lorenz H, Delotto R, Lippincott-Schwartz J. The secretory membrane system in the Drosophila syncytial blastoderm embryo exists as functionally compartmentalized units around individual nuclei. J Cell Biol 2006; 173:219-30; PMID:16636144; http://dx.doi. org/10.1083/jcb.200601156
14. Papoulas O, Hays TS, Sisson JC. The golgin Lava lamp mediates dynein-based Golgi movements during Drosophila cellularization. Nat Cell Biol 2005; 7:612-8; PMID:15908943; http://dx.doi. org/10.1038/ncb1264
15. Murthy M, Teodoro RO, Miller TP, Schwarz TL., Sec5, a member of the exocyst complex, mediates Drosophila embryo cellularization. Development 2010; 137:2773-83; PMID:20630948; http://dx.doi. org/10.1242/dev.048330
16. Burgess RW, Deitcher DL, Schwarz TL. The synaptic protein syntaxin1 is required for cellularization of Drosophila embryos. J Cell Biol 1997; 138:861-75; PMID:9265652; http://dx.doi.org/10.1083/ jcb.138.4.861
17. Pelissier A, Chauvin JP, Lecuit T. Trafficking through Rab11 endosomes is required for cellularization during Drosophila embryogenesis. Curr Biol 2003; 13:1848-57; PMID:14588240; http://dx.doi. org/10.1016/j.cub.2003.10.023
18. Figard L, Xu H, Garcia HG, Golding I, Sokac AM. The plasma membrane flattens out to fuel cell-surface growth during Drosophila cellularization. Dev Cell 2013; 27:648-55; PMID:24316147; http://dx.doi. org/10.1016/j.devcel.2013.11.006
19. von Dassow G. Concurrent cues for cytokinetic furrow induction in animal cells. Trends Cell Biol 2009; 19:165-73; PMID:19285868; http://dx.doi. org/10.1016/j.tcb.2009.01.008
20. Crest J, Concha-Moore K, Sullivan W. RhoGEF and positioning of rappaport-like furrows in the early Drosophila embryo. Curr Biol 2012; 22:2037-41; PMID:23022066; http://dx.doi.org/10.1016/j. cub.2012.08.046
21. Acharya S, Laupsien P, Wenzl C, Yan S, Großhans J. Function and dynamics of slam in furrow formation in early Drosophila embryo. Dev Biol 2014; 386:371-84; PMID:24368071; http://dx.doi.org/10.1016/j. ydbio.2013.12.022
22. Zallen JA, Cohen Y, Hudson AM, Cooley L, Wieschaus E, Schejter ED. SCAR is a primary regulator of Arp2/3-dependent morphological events in Drosophila. J Cell Biol 2002; 156:689-701; PMID:11854309; http://dx.doi.org/10.1083/ jcb.200109057
23. Stevenson V, Hudson A, Cooley L, Theurkauf WE. Arp2/3-dependent pseudocleavage [correction of psuedocleavage] furrow assembly in syncytial Drosophila embryos. Curr Biol 2002; 12:705-11; PMID:12007413; http://dx.doi.org/10.1016/ 0960-9822(02)00807-2
24. Padash Barmchi M, Rogers S, Häcker U. DRhoGEF2 regulates actin organization and contractility in the Drosophila blastoderm embryo. J Cell Biol 2005; 168:575-85; PMID:15699213; http://dx.doi. org/10.1083/jcb.200407124
25. Grosshans J, Wenzl C, Herz HM, Bartoszewski S, Schnorrer F, Vogt N, Schwarz H, Müller HA. RhoGEF2 and the formin Dia control the formation of the furrow canal by directed actin assembly during Drosophila cellularisation. Development 2005; 132:1009-20; PMID:15689371; http://dx.doi. org/10.1242/dev.01669
26. Afshar K, Stuart B, Wasserman SA. Functional analysis of the Drosophila diaphanous FH protein in early embryonic development. Development 2000; 127:1887-97; PMID:10751177
27. Royou A, Sullivan W, Karess R. Cortical recruitment of nonmuscle myosin II in early syncytial Drosophila embryos: its role in nuclear axial expansion and its regulation by Cdc2 activity. J Cell Biol 2002; 158:127-37; PMID:12105185; http://dx.doi. org/10.1083/jcb.200203148
28. Zaccai M, Lipshitz HD. Role of Adducin-like (hu-li tai shao) mRNA and protein localization in regulating cytoskeletal structure and function during Drosophila Oogenesis and early embryogenesis. Dev Genet 1996; 19:249-57; PMID:8952067; ht t p : / / d x . d o i . o r g /10 .10 0 2 / ( S ICI )152 0 -6408(1996)19:3<249::AID-DVG8>3.0.CO;2-9
29. Field CM, Coughlin M, Doberstein S, Marty T, Sullivan W. Characterization of anillin mutants reveals essential roles in septin localization and plasma membrane integrity. Development 2005; 132:2849-60; PMID:15930114; http://dx.doi. org/10.1242/dev.01843
30. Adam JC, Pringle JR, Peifer M. Evidence for functional differentiation among Drosophila septins in cytokinesis and cellularization. Mol Biol Cell 2000; 11:3123-35; PMID:10982405; http://dx.doi. org/10.1091/mbc.11.9.3123
31. Thomas JH, Wieschaus E. src64 and tec29 are required for microfilament contraction during Drosophila cellularization. Development 2004; 131:863-71; PMID:14736750; http://dx.doi. org/10.1242/dev.00989
32. Cao J, Albertson R, Riggs B, Field CM, Sullivan W. Nuf, a Rab11 effector, maintains cytokinetic furrow integrity by promoting local actin polymerization. J Cell Biol 2008; 182:301-13; PMID:18644888; http://dx.doi.org/10.1083/jcb.200712036
33. Wenzl C, Yan S, Laupsien P, Grosshans J. Localization of RhoGEF2 during Drosophila cellularization is developmentally controlled by Slam. Mech Dev 2010; 127:371-84; PMID:20060902; http://dx.doi. org/10.1016/j.mod.2010.01.001
34. Simpson L, Wieschaus E. Zygotic activity of the nullo locus is required to stabilize the actin-myosin network during cellularization in Drosophila. Development 1990; 110:851-63; PMID:2088725
35. Sokac AM, Wieschaus E. Zygotically controlled F-actin establishes cortical compartments to stabilize furrows during Drosophila cellularization. J Cell Sci 2008; 121:1815-24; PMID:18460582; http://dx.doi. org/10.1242/jcs.025171
36. Sokac AM, Wieschaus E. Local actin-dependent endocytosis is zygotically controlled to initiate Drosophila cellularization. Dev Cell 2008; 14:775-86; PMID:18477459; http://dx.doi.org/10.1016/j. devcel.2008.02.014
37. Daumke O, Roux A, Haucke V. BAR domain scaffolds in dynamin-mediated membrane fission. Cell 2014; 156:882-92; PMID:24581490; http:// dx.doi.org/10.1016/j.cell.2014.02.017
38. Georgiou M, Marinari E, Burden J, Baum B. Cdc42, Par6, and aPKC regulate Arp2/3-mediated endocytosis to control local adherens junction stability. Curr Biol 2008; 18:1631-8; PMID:18976918; http:// dx.doi.org/10.1016/j.cub.2008.09.029
39. Leibfried A, Fricke R, Morgan MJ, Bogdan S, Bellaiche Y. Drosophila Cip4 and WASp define a branch of the Cdc42-Par6-aPKC pathway regulating E-cadherin endocytosis. Curr Biol 2008; 18:1639-48; PMID:18976911; http://dx.doi.org/10.1016/j. cub.2008.09.063
40. Yan S, Lv Z, Winterhoff M, Wenzl C, Zobel T, Faix J, Bogdan S, Grosshans J. The F-BAR protein Cip4/Toca-1 antagonizes the formin Diaphanous in membrane stabilization and compartmentalization. J Cell Sci 2013; 126:1796-805; PMID:23424199; http://dx.doi.org/10.1242/jcs.118422
41. Su J, Chow B, Boulianne GL, Wilde A. The BAR domain of amphiphysin is required for cleavage furrow tip-tubule formation during cellularization in Drosophila embryos. Mol Biol Cell 2013; 24:1444-53; PMID:23447705; http://dx.doi.org/10.1091/ mbc.E12-12-0878
42. Leventis PA, Chow BM, Stewart BA, Iyengar B, Campos AR, Boulianne GL. Drosophila Amphiphysin is a post-synaptic protein required for normal locomotion but not endocytosis. Traffic 2001; 2:839-50; PMID:11733051; http://dx.doi. org/10.1034/j.1600-0854.2001.21113.x.
43. Gillingham AK, Munro S. The small Gproteins of the Arffamily and theirregulators.AnnuRevCell Dev Biol 2007;23:579-611; PMID:17506703;h t t p : / / d x . d o i . o r g / 1 0 . 11 4 6 / a n n u r e v . cellbio.23.090506.123209
44. Donaldson JG, Jackson CL. ARF family G proteins and their regulators: roles in membrane transport, development and disease. Nat Rev Mol Cell Biol 2011; 12:362-75; PMID:21587297; http://dx.doi. org/10.1038/nrm3117
45. Fuss B, Becker T, Zinke I, Hoch M. The cytohesin Steppke is essential for insulin signalling in Drosophila. Nature 2006; 444:945-8; PMID:17167488; http:// dx.doi.org/10.1038/nature05412
46. Hahn I, Fuss B, Peters A, Werner T, Sieberg A, Gosejacob D, Hoch M. The Drosophila Arf GEF Steppke controls MAPK activation in EGFR signaling. J Cell Sci 2013; 126:2470-9; PMID:23549788; http://dx.doi.org/10.1242/jcs.120964
47. Schejter ED, Wieschaus E. bottleneck acts as a regulator of the microfilament network governing cellularization of the Drosophila embryo. Cell 1993; 75:373-85; PMID:8402919; http://dx.doi. org/10.1016/0092-8674(93)80078-S
48. Reversi A, Loeser E, Subramanian D, Schultz C, De Renzis S. Plasma membrane phosphoinositide balance regulates cell shape during Drosophila embryo morphogenesis. J Cell Biol 2014; (Forthcoming)
49. Burke TA, Christensen JR, Barone E, Suarez C, Sirotkin V, Kovar DR. Homeostatic actin cytoskeleton networks are regulated by assembly factor competition for monomers. Curr Biol 2014; 24:579-85; PMID:24560576; http://dx.doi. org/10.1016/j.cub.2014.01.072