Abstract—
The regulatory factors and biochemical properties of the actin cytoskeleton are widely studied in vitro and in cell cultures. However, it is still unclear how these factors work in vivo and create an incredible variety of cytoskeleton structures during the organism’s development. Firstly, for the full understanding of formation and functioning of cytoskeleton structures, we need to determine all factors that regulate the structure composition. Secondly, we need to investigate the spatial and temporal mechanisms that provide the coordination of these factors and their activity. Thirdly, we need to know how the regulating factors and structures controlled by them are involved in the development dynamics. This review discusses the innovation methods that made Drosophila a valuable tool for the investigation of these issues.
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REFERENCES
Abmayr, S.M. and Pavlath, G.K., Myoblast fusion: lessons from flies and mice, Development, 2012, vol. 139, no. 4, pp. 641–656.
Aigouy, B., Farhadifar, R., Staple, D.B., et al., Cell flow reorients the axis of planar polarity in the wing epithelium of Drosophila, Cell, 2010, vol. 142, pp. 773–786.
Bertet, C., Sulak, L., and Lecuit, T., Myosin-dependent junction remodelling controls planar cell intercalation and axis elongation, Nature, 2004, vol. 429, pp. 667–671.
Blankenship, J.T., Backovic, S.T., Sanny, J.S., et al., Multicellular rosette formation links planar cell polarity to tissue morphogenesis, Dev. Cell, 2006, vol. 11, pp. 459–470.
Bosveld, F., Bonnet, I., Guirao, B., et al., Mechanical control of morphogenesis by Fat/Dachsous/Four-jointed planar cell polarity pathway, Science, 2012, vol. 336, no. 6082, pp. 724–727.
Cai, D., Chen, S.C., Prasad, M., et al., Mechanical feedback through E-cadherin promotes direction sensing during collective cell migration, Cell, 2014, vol. 157, pp. 1146–1159.
Caussinus, E., Kanca, O., and Affolter, M., Fluorescent fusion protein knockout mediated by anti-GFP nanobody, Nat. Struct. Mol. Biol., 2012, vol. 19, pp. 117–121.
Cavey, M., Rauzi, M., Lenne, P.F., et al., A two-tiered mechanism for stabilization and immobilization of E-cadherin, Nature, 2008, vol. 453, pp. 751–756.
Chen, B.C., Legant, W.R., Wang, K., et al., Lattice light-sheet microscopy: imaging molecules to embryos at high spatiotemporal resolution, Science, 2014, vol. 46, no. 6208, p. 1257998.
Chou, T.B., Noll, E., and Perrimon, N., Autosomal P[ovoD1] dominant female-sterile insertions in Drosophila and their use in generating germ-line chimeras, Development, 1993, vol. 119, pp. 1359–1369.
DeRosier, D.J. and Tilney, L.G., F-actin bundles are derivatives of microvilli: what does this tell us about how bundles might form?, J. Cell Biol., 2000, vol. 148, pp. 1–6.
Desai, R., Sarpal, R., Ishiyama, N., et al., Monomeric alpha-catenin links cadherin to the actin cytoskeleton, Nat. Cell Biol., 2013, vol. 15, pp. 261–273.
Dietzl, G., Chen, D., Schnorrer, F., et al., A genome-wide transgenic RNAi library for conditional gene inactivation in Drosophila, Nature, 2007, vol. 448, no. 7150, pp. 151–156.
Fabian, L. and Brill, J.A., Drosophila spermiogenesis: big things come from little packages, Spermatogenesis, 2012, vol. 2, pp. 197–212.
Fabrowski, P., Necakov, A.S., Mumbauer, S., et al., Tubular endocytosis drives remodelling of the apical surface during epithelial morphogenesis in Drosophila, Nat. Commun., 2013, vol. 4, p. 2244.
Founounou, N., Loyer, N., and Le Borgne, R., Septins regulate the contractility of the actomyosin ring to enable adherens junction remodeling during cytokinesis of epithelial cells, Dev. Cell, 2013, vol. 24, pp. 242–255.
Guillot, C. and Lecuit, T., Adhesion disengagement uncouples intrinsic and extrinsic forces to drive cytokinesis in epithelial tissues, Dev. Cell, 2013, vol. 24, pp. 227–241.
Haglund, K., Nezis, I.P., and Stenmark, H., Structure and functions of stable intercellular bridges formed by incomplete cytokinesis during development, Commun. Integr. Biol., 2011, vol. 4, pp. 1–9.
Haigo, S.L. and Bilder, D., Global tissue revolutions in a morphogenetic movement controlling elongation, Science, 2011, vol. 331, pp. 1071–1074.
He, L., Wang, X., Tang, H.L., et al., Tissue elongation requires oscillating contractions of a basal actomyosin network, Nat. Cell Biol., 2010, vol. 12, pp. 1133–1142.
Herszterg, S., Leibfried, A., Bosveld, F., et al., Interplay between the dividing cell and its neighbors regulates adherens junction formation during cytokinesis in epithelial tissue, Dev. Cell, 2013, vol. 24, pp. 256–270.
Hudson, A.M. and Cooley, L., Understanding the function of actin-binding proteins through genetic analysis of Drosophila oogenesis, Annu. Rev. Genet., 2002, vol. 36, pp. 455–488.
Keller, P.J., Schmidt, A.D., Santella, A., et al., Fast, high-contrast imaging of animal development with scanned light sheet-based structured-illumination microscopy, Nat. Methods, 2010, vol. 7, pp. 637–642.
Kiger, A.A., Baum, B., Jones, S., et al., A functional genomic analysis of cell morphology using RNA interference, J. Biol., 2003, vol. 2, p. 27.
Kim, J.H., Cho, A., Yin, H., et al., Psidin, a conserved protein that regulates protrusion dynamics and cell migration, Genes Dev., 2011, vol. 25, pp. 730–741.
Kim, J.H., Jin, P., Duan, R., and Chen, E.H., Mechanisms of myoblast fusion during muscle development, Curr. Opin. Genet. Dev., 2015, vol. 32, pp. 162–170.
Kremers, G.J., Gilbert, S.G., Cranfill, P.J., et al., Fluorescent proteins at a glance, J. Cell Sci., 2011, vol. 124, pp. 157–160.
Lee, T. and Luo, L., Mosaic analysis with a repressible cell marker (MARCM) for Drosophila neural development, Trends Neurosci., 2001, vol. 24, pp. 251–254.
Linder, S., Wiesner, C., and Himmel, M., Degrading devices: invadosomes in proteolytic cell invasion, Annu. Rev. Cell Dev. Biol., 2011, vol. 27, pp. 185–211.
Liu, J., Li, C., Yu, Z., et al., Efficient and specific modifications of the Drosophila genome by means of an easy TALEN strategy, J. Genet. Genomics, 2012, vol. 39, pp. 209–215.
Luxton, G.W., Gomes, E.R., Folker, E.S., et al., Linear arrays of nuclear envelope proteins harness retrograde actin flow for nuclear movement, Science, 2010, vol. 329, pp. 956–959.
Lye, C.M. and Sanson, B., Tension and epithelial morphogenesis in Drosophila early embryos, Curr. Top Dev. Biol., 2011, vol. 95, pp. 145–187.
Marek, K.W. and Davis, G.W., Transgenically encoded protein photoinactivation (FlAsH–FALI): acute inactivation of synaptotagmin I, Neuron, 2002, vol. 36, pp. 805–813.
Martin, A.C., Kaschube, M., and Wieschaus, E.F., Pulsed contractions of an actin–myosin network drive apical constriction, Nature, 2009, vol. 457, pp. 495–499.
Mavrakis, M., Rikhy, R., and Lippincott-Schwartz, J., Plasma membrane polarity and compartmentalization are established before cellularization in the fly embryo, Dev. Cell, 2009, vol. 16, pp. 93–104.
McGuire, S.E., Le, P.T., Osborn, A.J., et al., Spatiotemporal rescue of memory dysfunction in Drosophila, Science, 2003, vol. 302, pp. 1765–1768.
Mohr, S.E. and Perrimon, N., RNAi screening: new approaches, understandings, and organisms, Wiley Interdiscip. Rev. RNA, 2012, vol. 3, pp. 145–158.
Montell, D.J., Yoon, W.H., and Starz-Gaiano, M., Group choreography: mechanisms orchestrating the collective movement of border cells, Nat. Rev. Mol. Cell Biol., 2012, vol. 13, pp. 631–645.
Ng, J., Nardine, T., Harms, M., et al., Rac GTPases control axon growth, guidance and branching, Nature, 2002, vol. 416, pp. 442–447.
Ni, J.Q., Zhou, R., Czech, B., et al., A genome-scale shRNA resource for transgenic RNAi in Drosophila, Nat. Methods, 2011, vol. 8, pp. 405–407.
Nusslein-Volhard, C. and Wieschaus, E., Mutations affecting segment number and polarity in Drosophila, Nature, 1980, vol. 287, pp. 795–801.
Pfender, S., Kuznetsov, V., Pleiser, S., et al., Spire-type actin nucleators cooperate with formin-2 to drive asymmetric oocyte division, Curr. Biol., 2011, vol. 21, pp. 955–960.
Port, F., Chen, H.M., Lee, T., et al., Optimized CRISPR/Cas tools for efficient germline and somatic genome engineering in Drosophila, Proc. Natl. Acad. Sci. U. S. A., 2014, vol. 111, pp. E2967–E2976.
Ramel, D., Wang, X., Laflamme, C., et al., Rab11 regulates cell-cell communication during collective cell movements, Nat. Cell Biol., 2013, vol. 15, pp. 317–324.
Rauzi, M., Lenne, P.F., and Lecuit, T., Planar polarized actomyosin contractile flows control epithelial junction remodeling, Nature, 2010, vol. 468, pp. 1110–1114.
Rebollo, E., Karkali, K., Mangione, F., et al., Live imaging in Drosophila: the optical and genetic toolkits, Methods, 2014, vol. 68, pp. 48–59.
Ren, X., Sun, J., Housden, B.E., et al., Optimized gene editing technology for Drosophila melanogaster using germ line-specific Cas9, Proc. Natl. Acad. Sci. U. S. A., 2013, vol. 110, no. 47, pp. 19012–19017.
Rodal, A.A., Del Signore, S.J., and Martin, A.C., Drosophila comes of age as a model system for understanding the function of cytoskeletal proteins in cells, tissues, and organisms, Cytoskeleton (Hoboken, NJ), 2015, vol. 72, no. 5, pp. 207–224.
Rogers, S.L., Wiedemann, U., Stuurman, N., et al., Molecular requirements for actin-based lamella formation in Drosophila S2 cells, J. Cell Biol., 2003, vol. 162, pp. 1079–1088.
Rohn, J.L., Sims, D., Liu, T., et al., Comparative RNAi screening identifies a conserved core metazoan actinome by phenotype, J. Cell Biol., 2011, vol. 194, pp. 789–805.
Roper, K., Anisotropy of crumbs and aPKC drives myosin cable assembly during tube formation, Dev. Cell, 2012, vol. 23, pp. 939–953.
Roper, K., Supracellular actomyosin assemblies during development, Bioarchitecture, 2013, vol. 3, pp. 45–49.
Schachtner, H., Calaminus, S.D., Thomas, S.G., et al., Podosomes in adhesion, migration, mechanosensing and matrix remodeling, Cytoskeleton (Hoboken), 2013, vol. 70, pp. 572–589.
Schmid, A., Hallermann, S., Kittel, R.J., et al., Activity-dependent site-specific changes of glutamate receptor composition in vivo, Nat. Neurosci., 2008, vol. 11, pp. 659–666.
Schupbach, T. and Wieschaus, E., Female sterile mutations on the second chromosome of Drosophila melanogaster. I. Maternal effect mutations, Genetics, 1989, vol. 121, no. 1, pp. 101–117.
Simoes, S., Blankenship, J.T., Weitz, O., et al., Rho-kinase directs Bazooka/Par-3 planar polarity during Drosophila axis elongation, Dev. Cell, 2010, vol. 19, pp. 377–388.
Simonova, O.B. and Burdina, N.V., Morphogenetic movement of cells in embryogenesis of Drosophila melanogaster: mechanism and genetic control, Russ. J. Dev. Biol., 2009, vol. 40, no. 5, pp. 283–299.
Solon, J., Kaya-Copur, A., Colombelli, J., et al., Pulsed forces timed by a ratchet-like mechanism drive directed tissue movement during dorsal closure, Cell, 2009, vol. 137, pp. 1331–1342.
Sopko, R., Foos, M., Vinayagam, A., et al., Combining genetic perturbations and proteomics to examine kinase-phosphatase networks in Drosophila embryos, Dev. Cell, 2014, vol. 31, pp. 114–127.
Tilney, L.G. and DeRosier, D.J., How to make a curved Drosophila bristle using straight actin bundles, Proc. Natl. Acad. Sci. U. S. A., 2005, vol. 102, pp. 18785–18792.
Venken, K.J., Simpson, J.H., and Bellen, H.J., Genetic manipulation of genes and cells in the nervous system of the fruit fly, Neuron, 2011, vol. 72, pp. 202–230.
Wang, X., He, L., Wu, Y.I., et al., Light-mediated activation reveals a key role for Rac in collective guidance of cell movement in vivo, Nat. Cell Biol., 2010, vol. 12, pp. 591–597.
Wangler, M.F., Yamamoto, S., and Bellen, H.J., Fruit flies in biomedical research, Genetics, 2015, vol. 199, no. 3, pp. 639–653.
Weil, T.T., Parton, R.M., Herpers, B., et al., Drosophila patterning is established by differential association of mRNAs with P bodies, Nat. Cell Biol., 2012, vol. 14, no. 12, pp. 1305–1313.
Winter, P.W. and Shroff, H., Faster fluorescence microscopy: advances in high speed biological imaging, Curr. Opin. Chem. Biol., 2014, vol. 20, pp. 46–53.
Xu, T. and Rubin, G.M., Analysis of genetic mosaics in developing and adult Drosophila tissues, Development, 1993, vol. 117, pp. 1223–1237.
Zhang, J., Fonovic, M., Suyama, K., et al., Rab35 controls actin bundling by recruiting fascin as an effector protein, Science, 2009, vol. 325, pp. 1250–1254.
ACKNOWLEDGMENTS
This work was supported by the Russian Foundation for Basic Research, project nos. 16-04-00829-a and 18-34-00162 mol-a and by the federal budget for the Koltsov Institute of Developmental Biology, project no. 0108-2019-0001.
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Vorontsova, Y.E., Zavoloka, E.L., Cherezov, R.O. et al. Drosophila as a Model System Used for Searching the Genes, Signaling Pathways, and Mechanisms Controlling Cytoskeleton Formation. Russ J Dev Biol 50, 1–8 (2019). https://doi.org/10.1134/S1062360419010065
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DOI: https://doi.org/10.1134/S1062360419010065