Skip to main content
Log in

Drosophila as a Model System Used for Searching the Genes, Signaling Pathways, and Mechanisms Controlling Cytoskeleton Formation

  • REVIEWS
  • Published:
Russian Journal of Developmental Biology Aims and scope Submit manuscript

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.

This is a preview of subscription content, log in via an institution to check access.

Access this article

Price excludes VAT (USA)
Tax calculation will be finalised during checkout.

Instant access to the full article PDF.

Fig. 1.
Fig. 2.

Similar content being viewed by others

REFERENCES

  1. Abmayr, S.M. and Pavlath, G.K., Myoblast fusion: lessons from flies and mice, Development, 2012, vol. 139, no. 4, pp. 641–656.

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  2. 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.

    Article  CAS  PubMed  Google Scholar 

  3. 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.

    Article  CAS  PubMed  Google Scholar 

  4. 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.

    Article  CAS  PubMed  Google Scholar 

  5. 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.

    Article  CAS  PubMed  Google Scholar 

  6. 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.

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  7. 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.

    Article  CAS  Google Scholar 

  8. 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.

    Article  CAS  PubMed  Google Scholar 

  9. 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.

    Article  CAS  Google Scholar 

  10. 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.

    CAS  PubMed  Google Scholar 

  11. 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.

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  12. 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.

    Article  CAS  PubMed  Google Scholar 

  13. 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.

    Article  CAS  PubMed  Google Scholar 

  14. Fabian, L. and Brill, J.A., Drosophila spermiogenesis: big things come from little packages, Spermatogenesis, 2012, vol. 2, pp. 197–212.

    Article  PubMed  PubMed Central  Google Scholar 

  15. 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.

    Article  CAS  PubMed  Google Scholar 

  16. 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.

    Article  CAS  PubMed  Google Scholar 

  17. 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.

    Article  CAS  PubMed  Google Scholar 

  18. 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.

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  19. Haigo, S.L. and Bilder, D., Global tissue revolutions in a morphogenetic movement controlling elongation, Science, 2011, vol. 331, pp. 1071–1074.

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  20. 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.

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  21. 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.

    Article  CAS  PubMed  Google Scholar 

  22. 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.

    Article  CAS  PubMed  Google Scholar 

  23. 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.

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  24. 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.

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  25. 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.

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  26. 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.

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  27. 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.

    Article  CAS  PubMed  Google Scholar 

  28. 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.

    Article  CAS  PubMed  Google Scholar 

  29. 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.

    Article  CAS  PubMed  Google Scholar 

  30. 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.

    Article  CAS  PubMed  Google Scholar 

  31. 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.

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  32. Lye, C.M. and Sanson, B., Tension and epithelial morphogenesis in Drosophila early embryos, Curr. Top Dev. Biol., 2011, vol. 95, pp. 145–187.

    Article  PubMed  Google Scholar 

  33. 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.

    Article  CAS  PubMed  Google Scholar 

  34. 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.

    Article  CAS  PubMed  Google Scholar 

  35. 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.

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  36. 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.

    Article  CAS  PubMed  Google Scholar 

  37. Mohr, S.E. and Perrimon, N., RNAi screening: new approaches, understandings, and organisms, Wiley Interdiscip. Rev. RNA, 2012, vol. 3, pp. 145–158.

    Article  CAS  PubMed  Google Scholar 

  38. 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.

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  39. Ng, J., Nardine, T., Harms, M., et al., Rac GTPases control axon growth, guidance and branching, Nature, 2002, vol. 416, pp. 442–447.

    Article  CAS  PubMed  Google Scholar 

  40. 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.

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  41. Nusslein-Volhard, C. and Wieschaus, E., Mutations affecting segment number and polarity in Drosophila, Nature, 1980, vol. 287, pp. 795–801.

    Article  CAS  PubMed  Google Scholar 

  42. 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.

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  43. 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.

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  44. 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.

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  45. Rauzi, M., Lenne, P.F., and Lecuit, T., Planar polarized actomyosin contractile flows control epithelial junction remodeling, Nature, 2010, vol. 468, pp. 1110–1114.

    Article  CAS  PubMed  Google Scholar 

  46. Rebollo, E., Karkali, K., Mangione, F., et al., Live imaging in Drosophila: the optical and genetic toolkits, Methods, 2014, vol. 68, pp. 48–59.

    Article  CAS  PubMed  Google Scholar 

  47. 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.

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  48. 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.

    Article  CAS  Google Scholar 

  49. 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.

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  50. 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.

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  51. Roper, K., Anisotropy of crumbs and aPKC drives myosin cable assembly during tube formation, Dev. Cell, 2012, vol. 23, pp. 939–953.

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  52. Roper, K., Supracellular actomyosin assemblies during development, Bioarchitecture, 2013, vol. 3, pp. 45–49.

    Article  PubMed  PubMed Central  Google Scholar 

  53. 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.

    Article  CAS  PubMed  Google Scholar 

  54. 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.

    Article  CAS  PubMed  Google Scholar 

  55. 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.

  56. 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.

    Article  CAS  Google Scholar 

  57. 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.

    Article  Google Scholar 

  58. 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.

    Article  PubMed  Google Scholar 

  59. 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.

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  60. 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.

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  61. 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.

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  62. 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.

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  63. Wangler, M.F., Yamamoto, S., and Bellen, H.J., Fruit flies in biomedical research, Genetics, 2015, vol. 199, no. 3, pp. 639–653.

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  64. 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.

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  65. 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.

    Article  CAS  PubMed  Google Scholar 

  66. Xu, T. and Rubin, G.M., Analysis of genetic mosaics in developing and adult Drosophila tissues, Development, 1993, vol. 117, pp. 1223–1237.

    CAS  PubMed  Google Scholar 

  67. 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.

    Article  CAS  PubMed  Google Scholar 

Download references

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.

Author information

Authors and Affiliations

Authors

Corresponding author

Correspondence to O. B. Simonova.

Additional information

Translated by Ya. Lavrenchuk

Rights and permissions

Reprints and permissions

About this article

Check for updates. Verify currency and authenticity via CrossMark

Cite this article

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

Download citation

  • Received:

  • Revised:

  • Accepted:

  • Published:

  • Issue Date:

  • DOI: https://doi.org/10.1134/S1062360419010065

Keywords:

Navigation