Membrane-actin interactions in morphogenesis: Lessons learned from Drosophila cellularization

Chugh, 2018, The actin cortex at a glance, J. Cell Sci., 131, 10.1242/jcs.186254

Mazumdar, 2002, How one becomes many: blastoderm cellularization in Drosophila melanogaster, Bioessays, 24, 1012, 10.1002/bies.10184

Miura, 2003, A comparison of parthenogenetic and sexual embryogenesis of the pea aphid Acyrthosiphon pisum (Hemiptera: Aphidoidea), J. Exp. Zool. B Mol. Dev. Evol., 295, 59, 10.1002/jez.b.3

van der Zee, 2015, Innexin7a forms junctions that stabilize the basal membrane during cellularization of the blastoderm in Tribolium castaneum, Development, 142, 2173, 10.1242/dev.097113

Davis, 2002, Short, long, and beyond: molecular and embryological approaches to insect segmentation, Annu. Rev. Entomol., 47, 669, 10.1146/annurev.ento.47.091201.145251

Liu, 2005, Short and long germ segmentation: unanswered questions in the evolution of a developmental mode, Evol. Dev., 7, 629, 10.1111/j.1525-142X.2005.05066.x

Foe, 1983, Studies of nuclear and cytoplasmic behaviour during the five mitotic cycles that precede gastrulation in Drosophila embryogenesis, J. Cell Sci., 61, 31, 10.1242/jcs.61.1.31

Sullivan, 1993, Delays in anaphase initiation occur in individual nuclei of the syncytial Drosophila embryo, Mol. Biol. Cell, 4, 885, 10.1091/mbc.4.9.885

Takada, 2003, Drosophila checkpoint kinase 2 couples centrosome function and spindle assembly to genomic integrity, Cell, 113, 87, 10.1016/S0092-8674(03)00202-2

Edgar, 1986, Cell cycle control by the nucleo-cytoplasmic ratio in early Drosophila development, Cell, 44, 365, 10.1016/0092-8674(86)90771-3

Lu, 2009, Coupling of zygotic transcription to mitotic control at the Drosophila mid-blastula transition, Development, 136, 2101, 10.1242/dev.034421

McCleland, 2008, RNAi of mitotic cyclins in Drosophila uncouples the nuclear and centrosome cycle, Curr. Biol., 18, 245, 10.1016/j.cub.2008.01.041

Sung, 2013, Number of nuclear divisions in the Drosophila blastoderm controlled by onset of zygotic transcription, Curr. Biol., 23, 133, 10.1016/j.cub.2012.12.013

Deneke, 2016, Waves of Cdk1 activity in S phase synchronize the cell cycle in drosophila embryos, Dev. Cell, 38, 399, 10.1016/j.devcel.2016.07.023

Lefebvre, 2018, Flying the RNA Nest: Drosophila reveals novel insights into the transcriptome dynamics of early development, J. Dev. Biol., 6, 10.3390/jdb6010005

Langley, 2014, New insights into the maternal to zygotic transition, Development, 141, 3834, 10.1242/dev.102368

Tadros, 2009, The maternal-to-zygotic transition: a play in two acts, Development, 136, 3033, 10.1242/dev.033183

Krueger, 2019, Cross-linker-mediated regulation of actin network organization controls tissue morphogenesis, J. Cell Biol., 218, 2743, 10.1083/jcb.201811127

Sokac, 2008, Zygotically controlled F-actin establishes cortical compartments to stabilize furrows during Drosophila cellularization, J. Cell Sci., 121, 1815, 10.1242/jcs.025171

Zheng, 2013, The maternal-to-zygotic transition targets actin to promote robustness during morphogenesis, PLoS Genet., 9, 10.1371/journal.pgen.1003901

Ibnsouda, 1993, Relationship between expression of serendipity alpha and cellularisation of the Drosophila embryo as revealed by interspecific transformation, Development, 119, 471, 10.1242/dev.119.2.471

Lecuit, 2002, slam encodes a developmental regulator of polarized membrane growth during cleavage of the Drosophila embryo, Dev. Cell, 2, 425, 10.1016/S1534-5807(02)00141-7

Postner, 1994, The nullo protein is a component of the actin-myosin network that mediates cellularization in Drosophila melanogaster embryos, J. Cell Sci., 107, 1863, 10.1242/jcs.107.7.1863

Schejter, 1993, Bottleneck acts as a regulator of the microfilament network governing cellularization of the Drosophila embryo, Cell, 75, 373, 10.1016/0092-8674(93)80078-S

Schweisguth, 1990, The serendipity alpha gene encodes a membrane-associated protein required for the cellularization of the Drosophila embryo, Genes Dev., 4, 922, 10.1101/gad.4.6.922

Simpson, 1990, Zygotic activity of the nullo locus is required to stabilize the actin-myosin network during cellularization in Drosophila, Development, 110, 851, 10.1242/dev.110.3.851

Wieschaus, 1988, Requirements for X-linked zygotic gene activity during cellularization of early Drosophila embryos, Development, 104, 483, 10.1242/dev.104.3.483

Hunter, 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, 10.1083/jcb.150.2.391

Rose, 1992, The Drosophila cellularization gene nullo produces a blastoderm-specific transcript whose levels respond to the nucleocytoplasmic ratio, Genes Dev., 6, 1255, 10.1101/gad.6.7.1255

Blythe, 2015, Coordinating cell cycle remodeling with transcriptional activation at the Drosophila MBT, Curr. Top. Dev. Biol., 113, 113, 10.1016/bs.ctdb.2015.06.002

Hamm, 2018, Regulatory principles governing the maternal-to-zygotic transition: insights from Drosophila melanogaster, Open Biol., 8, 10.1098/rsob.180183

Liang, 2008, The zinc-finger protein Zelda is a key activator of the early zygotic genome in Drosophila, Nature, 456, 400, 10.1038/nature07388

Figard, 2013, The plasma membrane flattens out to fuel cell-surface growth during Drosophila cellularization, Dev. Cell, 27, 648, 10.1016/j.devcel.2013.11.006

Fullilove, 1971, Nuclear elongation and cytokinesis in Drosophila montana, Dev. Biol., 26, 560, 10.1016/0012-1606(71)90141-2

Schmidt, 2018, Dynamics of cortical domains in early Drosophila development, J. Cell Sci., 131, 10.1242/jcs.212795

Raff, 1989, Centrosomes, and not nuclei, initiate pole cell formation in Drosophila embryos, Cell, 57, 611, 10.1016/0092-8674(89)90130-X

Rothwell, 1999, The Drosophila centrosomal protein Nuf is required for recruiting Dah, a membrane associated protein, to furrows in the early embryo, J. Cell Sci., 112, 2885, 10.1242/jcs.112.17.2885

Pollard, 2019, Molecular mechanism of cytokinesis, Annu. Rev. Biochem., 88, 661, 10.1146/annurev-biochem-062917-012530

Bray, 1988, Cortical flow in animal cells, Science, 239, 883, 10.1126/science.3277283

DeBiasio, 1996, Myosin II transport, organization, and phosphorylation: evidence for cortical flow/solation-contraction coupling during cytokinesis and cell locomotion, Mol. Biol. Cell, 7, 1259, 10.1091/mbc.7.8.1259

Reymann, 2016, Cortical flow aligns actin filaments to form a furrow, Elife, 5, 10.7554/eLife.17807

Yumura, 2008, Multiple mechanisms for accumulation of myosin II filaments at the equator during cytokinesis, Traffic, 9, 2089, 10.1111/j.1600-0854.2008.00837.x

Benink, 2000, Analysis of cortical flow models in vivo, Mol. Biol. Cell, 11, 2553, 10.1091/mbc.11.8.2553

Canman, 1997, Microtubules suppress actomyosin-based cortical flow in Xenopus oocytes, J. Cell Sci., 110, 1907, 10.1242/jcs.110.16.1907

Mandato, 2000, Microtubule-actomyosin interactions in cortical flow and cytokinesis, Cell Motil. Cytoskelet., 45, 87, 10.1002/(SICI)1097-0169(200002)45:2<87::AID-CM1>3.0.CO;2-0

Afshar, 2000, Functional analysis of the Drosophila diaphanous FH protein in early embryonic development, Development, 127, 1887, 10.1242/dev.127.9.1887

Grosshans, 2005, RhoGEF2 and the formin Dia control the formation of the furrow canal by directed actin assembly during Drosophila cellularisation, Development, 132, 1009, 10.1242/dev.01669

Minestrini, 2003, Localization of Pavarotti-KLP in living Drosophila embryos suggests roles in reorganizing the cortical cytoskeleton during the mitotic cycle, Mol. Biol. Cell, 14, 4028, 10.1091/mbc.e03-04-0214

Padash Barmchi, 2005, DRhoGEF2 regulates actin organization and contractility in the Drosophila blastoderm embryo, J. Cell Biol., 168, 575, 10.1083/jcb.200407124

Sommi, 2010, A mitotic kinesin-6, Pav-KLP, mediates interdependent cortical reorganization and spindle dynamics in Drosophila embryos, J. Cell Sci., 123, 1862, 10.1242/jcs.064048

Lecuit, 2000, Polarized insertion of new membrane from a cytoplasmic reservoir during cleavage of the Drosophila embryo, J. Cell Biol., 150, 849, 10.1083/jcb.150.4.849

Harris, 2004, Adherens junction-dependent and -independent steps in the establishment of epithelial cell polarity in Drosophila, J. Cell Biol., 167, 135, 10.1083/jcb.200406024

Choi, 2013, Rap1 and Canoe/afadin are essential for establishment of apical-basal polarity in the Drosophila embryo, Mol. Biol. Cell, 24, 945, 10.1091/mbc.e12-10-0736

Yan, 2017, Slam protein dictates subcellular localization and translation of its own mRNA, PLoS Biol., 15, 10.1371/journal.pbio.2003315

Yan, 2018, Localization and translation control of slam in Drosophila cellularization, Fly, 12, 191, 10.1080/19336934.2018.1520574

Xue, 2016, -Back-to-back mechanisms drive actomyosin ring closure during Drosophila embryo cleavage, J. Cell Biol., 215, 335, 10.1083/jcb.201608025

Tepass, 2012, The apical polarity protein network in Drosophila epithelial cells: regulation of polarity, junctions, morphogenesis, cell growth, and survival, Annu. Rev. Cell Dev. Biol., 28, 655, 10.1146/annurev-cellbio-092910-154033

Lee, 2013, An Arf-GEF regulates antagonism between endocytosis and the cytoskeleton for Drosophila blastoderm development, Curr. Biol., 23, 2110, 10.1016/j.cub.2013.08.058

Liu, 2015, Stepping stone: a cytohesin adaptor for membrane cytoskeleton restraint in the syncytial Drosophila embryo, Mol. Biol. Cell, 26, 711, 10.1091/mbc.E14-11-1554

Su, 2013, The BAR domain of amphiphysin is required for cleavage furrow tip-tubule formation during cellularization in Drosophila embryos, Mol. Biol. Cell, 24, 1444, 10.1091/mbc.e12-12-0878

Zhao, 2017, Nanoscale manipulation of membrane curvature for probing endocytosis in live cells, Nat. Nanotechnol., 12, 750, 10.1038/nnano.2017.98

Figard, 2019, Cofilin-mediated actin stress response is maladaptive in heat-stressed embryos, Cell Rep., 26, 3493, 10.1016/j.celrep.2019.02.092

Harris, 2005, The positioning and segregation of apical cues during epithelial polarity establishment in Drosophila, J. Cell Biol., 170, 813, 10.1083/jcb.200505127

Muller, 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, 10.1083/jcb.134.1.149

Fabrowski, 2013, Renzis, Tubular endocytosis drives remodelling of the apical surface during epithelial morphogenesis in Drosophila, Nat. Commun., 4, 2244, 10.1038/ncomms3244

Chua, 2009, Dynamin 2 orchestrates the global actomyosin cytoskeleton for epithelial maintenance and apical constriction, Proc. Natl. Acad. Sci. U.S.A., 106, 20770, 10.1073/pnas.0909812106

Jha, 2018, Quantitative control of GPCR organization and signaling by endocytosis in epithelial morphogenesis, Curr. Biol., 28, 1570, 10.1016/j.cub.2018.03.068

Kowalczyk, 2021, Neural tube closure requires the endocytic receptor Lrp2 and its functional interaction with intracellular scaffolds, Development, 148, 10.1242/dev.195008

Lee, 2010, Endocytosis is required for efficient apical constriction during Xenopus gastrulation, Curr. Biol., 20, 253, 10.1016/j.cub.2009.12.021

Mateus, 2011, Endocytic and recycling endosomes modulate cell shape changes and tissue behaviour during morphogenesis in Drosophila, PLoS One, 6, 10.1371/journal.pone.0018729

Thottacherry, 2019, Spoiled for choice: diverse endocytic pathways function at the cell surface, Annu. Rev. Cell Dev. Biol., 35, 55, 10.1146/annurev-cellbio-100617-062710

West, 2016, Cadherin trafficking for tissue morphogenesis: control and consequences, Traffic, 17, 1233, 10.1111/tra.12407

Jewett, 2017, Planar polarized Rab35 functions as an oscillatory ratchet during cell intercalation in the Drosophila epithelium, Nat. Commun., 8, 476, 10.1038/s41467-017-00553-0

Chakrabarti, 2021, Multiple roles for actin in secretory and endocytic pathways, Curr. Biol., 31, R603, 10.1016/j.cub.2021.03.038

Sigismund, 2021, Fiore, Endocytosis in the context-dependent regulation of individual and collective cell properties, Nat. Rev. Mol. Cell Biol., 22, 625, 10.1038/s41580-021-00375-5

Xie, 2018, Membrane trafficking in morphogenesis and planar polarity, Traffic, 10.1111/tra.12580

Field, 2005, Characterization of anillin mutants reveals essential roles in septin localization and plasma membrane integrity, Development, 132, 2849, 10.1242/dev.01843

Mavrakis, 2014, Septins promote F-actin ring formation by crosslinking actin filaments into curved bundles, Nat. Cell Biol., 16, 322, 10.1038/ncb2921

Royou, 2004, Reassessing the role and dynamics of nonmuscle myosin II during furrow formation in early Drosophila embryos, Mol. Biol. Cell, 15, 838, 10.1091/mbc.e03-06-0440

Sharma, 2021, Spatiotemporal recruitment of RhoGTPase protein GRAF inhibits actomyosin ring constriction in Drosophila cellularization, Elife, 10, 10.7554/eLife.63535

Thomas, 2004, src64 and tec29 are required for microfilament contraction during Drosophila cellularization, Development, 131, 863, 10.1242/dev.00989

Figard, 2014, A membrane reservoir at the cell surface: unfolding the plasma membrane to fuel cell shape change, Bioarchitecture, 4, 39, 10.4161/bioa.29069

Cao, 2008, Nuf, a Rab11 effector, maintains cytokinetic furrow integrity by promoting local actin polymerization, J. Cell Biol., 182, 301, 10.1083/jcb.200712036

Murthy, 2010, Sec5, a member of the exocyst complex, mediates Drosophila embryo cellularization, Development, 137, 2773, 10.1242/dev.048330

Pelissier, 2003, Trafficking through Rab11 endosomes is required for cellularization during Drosophila embryogenesis, Curr. Biol., 13, 1848, 10.1016/j.cub.2003.10.023

Riggs, 2003, Actin cytoskeleton remodeling during early Drosophila furrow formation requires recycling endosomal components Nuclear-fallout and Rab11, J. Cell Biol., 163, 143, 10.1083/jcb.200305115

Zhang, 2000, Discontinuous actin hexagon, a protein essential for cortical furrow formation in Drosophila, is membrane associated and hyperphosphorylated, Mol. Biol. Cell, 11, 1011, 10.1091/mbc.11.3.1011

Zhang, 1996, Isolation and characterization of a Drosophila gene essential for early embryonic development and formation of cortical cleavage furrows, J. Cell Biol., 134, 923, 10.1083/jcb.134.4.923

Figard, 2016, Membrane supply and demand regulates F-Actin in a cell surface reservoir, Dev. Cell, 37, 267, 10.1016/j.devcel.2016.04.010

Frescas, 2006, The secretory membrane system in the Drosophila syncytial blastoderm embryo exists as functionally compartmentalized units around individual nuclei, J. Cell Biol., 173, 219, 10.1083/jcb.200601156

Sisson, 2000, Lava lamp, a novel peripheral golgi protein, is required for Drosophila melanogaster cellularization, J. Cell Biol., 151, 905, 10.1083/jcb.151.4.905

LaLonde, 2006, A role for Phospholipase D in Drosophila embryonic cellularization, BMC Dev. Biol., 6, 60, 10.1186/1471-213X-6-60

Lee, 2015, G protein interactions localize the Arf-GEF steppke for cleavage furrow regulation in drosophila, PLoS One, 10, 10.1371/journal.pone.0142562

Papoulas, 2005, The golgin Lava lamp mediates dynein-based Golgi movements during Drosophila cellularization, Nat. Cell Biol., 7, 612, 10.1038/ncb1264

Clark, 2014, Stresses at the cell surface during animal cell morphogenesis, Curr. Biol., 24, R484, 10.1016/j.cub.2014.03.059

Lecuit, 2004, Junctions and vesicular trafficking during Drosophila cellularization, J. Cell Sci., 117, 3427, 10.1242/jcs.01312

Pfenninger, 2009, Plasma membrane expansion: a neuron’s Herculean task, Nat. Rev. Neurosci., 10, 251, 10.1038/nrn2593

Prekeris, 2008, Breaking up is hard to do - membrane traffic in cytokinesis, J. Cell Sci., 121, 1569, 10.1242/jcs.018770

Rodrigues, 2019, Key roles of Arf small G proteins and biosynthetic trafficking for animal development, Small GTPases, 10, 403, 10.1080/21541248.2017.1304854

D’Angelo, 2019, In vivo force application reveals a fast tissue softening and external friction increase during early embryogenesis, Curr. Biol., 29, 1564, 10.1016/j.cub.2019.04.010

Doubrovinski, 2017, Measurement of cortical elasticity in Drosophila melanogaster embryos using ferrofluids, Proc. Natl. Acad. Sci. U.S.A., 114, 1051, 10.1073/pnas.1616659114

He, 2014, Apical constriction drives tissue-scale hydrodynamic flow to mediate cell elongation, Nature, 508, 392, 10.1038/nature13070

Wessel, 2015, The mechanical properties of early Drosophila embryos measured by high-speed video microrheology, Biophys. J., 108, 1899, 10.1016/j.bpj.2015.02.032

Chougule, 2016, Drak is required for actomyosin organization during drosophila cellularization, G3, 6, 819, 10.1534/g3.115.026401

Krajcovic, 2012, Assessing the critical period for Rho kinase activity during Drosophila ventral furrow formation, Dev. Dyn., 241, 1729, 10.1002/dvdy.23859

Mason, 2016, RhoA GTPase inhibition organizes contraction during epithelial morphogenesis, J. Cell Biol., 214, 603, 10.1083/jcb.201603077

Field, 1995, Anillin, a contractile ring protein that cycles from the nucleus to the cell cortex, J. Cell Biol., 131, 165, 10.1083/jcb.131.1.165

Carter, 2019, Actomyosin contraction during cellularization is regulated in part by Src64 control of Actin 5C protein levels, Genesis, 57, 10.1002/dvg.23297

Reversi, 2014, Plasma membrane phosphoinositide balance regulates cell shape during Drosophila embryo morphogenesis, J. Cell Biol., 205, 395, 10.1083/jcb.201309079

Chowdhary, 2020, Mitochondrial morphology and activity regulate furrow ingression and contractile ring dynamics in Drosophila cellularization, Mol. Biol. Cell, 31, 2331, 10.1091/mbc.E20-03-0177

Hunter, 2018, Oxidative stress orchestrates cell polarity to promote embryonic wound healing, Dev. Cell, 47, 377, 10.1016/j.devcel.2018.10.013

Agarwal, 2019, Principles of actomyosin regulation in vivo, Trends Cell Biol., 29, 150, 10.1016/j.tcb.2018.09.006

Blanchoin, 2014, Actin dynamics, architecture, and mechanics in cell motility, Physiol. Rev., 94, 235, 10.1152/physrev.00018.2013

Heer, 2017, Tension, contraction and tissue morphogenesis, Development, 144, 4249, 10.1242/dev.151282

Li, 2020, Excitable networks controlling cell migration during development and disease, Semin. Cell Dev. Biol., 100, 133, 10.1016/j.semcdb.2019.11.001

Schejter, 1993, Functional elements of the cytoskeleton in the early Drosophila embryo, Annu. Rev. Cell Biol., 9, 67, 10.1146/annurev.cb.09.110193.000435

Harris, 2009, How the cytoskeleton helps build the embryonic body plan: models of morphogenesis from Drosophila, Curr. Top. Dev. Biol., 89, 55, 10.1016/S0070-2153(09)89003-0

Rupprecht, 2017, Geometric constraints alter cell arrangements within curved epithelial tissues, Mol. Biol. Cell, 28, 3582, 10.1091/mbc.e17-01-0060

Blake-Hedges, 2019, Coordination of Embryogenesis by the Centrosome in Drosophila melanogaster, Results Probl. Cell Differ., 67, 277, 10.1007/978-3-030-23173-6_12

Callaini, 1988, Centrosome splitting during nuclear elongation in the Drosophila embryo, Exp. Cell Res, 178, 415, 10.1016/0014-4827(88)90410-7

Eisman, 2006, Centrosomin’s beautiful sister (cbs) encodes a GRIP-domain protein that marks Golgi inheritance and functions in the centrosome cycle in Drosophila, J. Cell Sci., 119, 3399, 10.1242/jcs.03088

Tillery, 2018, Centrosomal and non-centrosomal microtubule-organizing centers (MTOCs) in drosophila melanogaster, Cells, 7, 10.3390/cells7090121

Hampoelz, 2011, Microtubule-induced nuclear envelope fluctuations control chromatin dynamics in Drosophila embryos, Development, 138, 3377, 10.1242/dev.065706

Pilot, 2006, Developmental control of nuclear morphogenesis and anchoring by charleston, identified in a functional genomic screen of Drosophila cellularisation, Development, 133, 711, 10.1242/dev.02251

Hunter, 2002, Conserved domains of the Nullo protein required for cell-surface localization and formation of adherens junctions, Mol. Biol. Cell, 13, 146, 10.1091/mbc.01-08-0418

Grevengoed, 2003, Balancing different types of actin polymerization at distinct sites: roles for Abelson kinase and Enabled, J. Cell Biol., 163, 1267, 10.1083/jcb.200307026

Stevenson, 2002, Arp2/3-dependent pseudocleavage [correction of psuedocleavage] furrow assembly in syncytial Drosophila embryos, Curr. Biol., 12, 705, 10.1016/S0960-9822(02)00807-2

Rikhy, 2015, Dynamin regulates metaphase furrow formation and plasma membrane compartmentalization in the syncytial Drosophila embryo, Biol. Open, 4, 301, 10.1242/bio.20149936

Young, 1991, Dynamic changes in the distribution of cytoplasmic myosin during Drosophila embryogenesis, Development, 111, 1, 10.1242/dev.111.1.1

Nakamura, 2020, The kinesin-like protein Pavarotti functions noncanonically to regulate actin dynamics, J. Cell Biol., 219, 10.1083/jcb.201912117

Adam, 2000, Evidence for functional differentiation among Drosophila septins in cytokinesis and cellularization, Mol. Biol. Cell, 11, 3123, 10.1091/mbc.11.9.3123

Fares, 1995, Localization and possible functions of Drosophila septins, Mol. Biol. Cell, 6, 1843, 10.1091/mbc.6.12.1843

Rothwell, 1998, Nuclear-fallout, a Drosophila protein that cycles from the cytoplasm to the centrosomes, regulates cortical microfilament organization, Development, 125, 1295, 10.1242/dev.125.7.1295

Strong, 2011, Maternal and zygotic requirements for src64 during Drosophila cellularization, Genesis, 49, 912, 10.1002/dvg.20783

Burgess, 1997, The synaptic protein syntaxin1 is required for cellularization of Drosophila embryos, J. Cell Biol., 138, 861, 10.1083/jcb.138.4.861