Skip to main content
SpringerLink
Log in
Book cover

The Actin Cytoskeleton pp 285–310Cite as

Molecular Control of Actin Dynamics In Vivo: Insights from Drosophila

  • Chapter
  • First Online:

Part of the book series: Handbook of Experimental Pharmacology ((HEP,volume 235))

Abstract

The actin cytoskeleton provides mechanical support for cells and generates forces to drive cell shape changes and cell migration in morphogenesis. Molecular understanding of actin dynamics requires a genetically traceable model system that allows interdisciplinary experimental approaches to elucidate the regulatory network of cytoskeletal proteins in vivo. Here, we will discuss some examples of how advances in Drosophila genetics and high-resolution imaging techniques contribute to the discovery of new actin functions, signaling pathways, and mechanisms of actin regulation in vivo.

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

Chapter
USD   29.95
Price excludes VAT (USA)
  • Available as PDF
  • Read on any device
  • Instant download
  • Own it forever
eBook
USD   229.00
Price excludes VAT (USA)
  • Available as EPUB and PDF
  • Read on any device
  • Instant download
  • Own it forever
Softcover Book
USD   299.99
Price excludes VAT (USA)
  • Compact, lightweight edition
  • Dispatched in 3 to 5 business days
  • Free shipping worldwide - see info
Hardcover Book
USD   299.99
Price excludes VAT (USA)
  • Durable hardcover edition
  • Dispatched in 3 to 5 business days
  • Free shipping worldwide - see info

Tax calculation will be finalised at checkout

Purchases are for personal use only

Learn about institutional subscriptions

References

  • Bai J, Uehara Y, Montell DJ (2000) Regulation of invasive cell behavior by taiman, a Drosophila protein related to AIB1, a steroid receptor coactivator amplified in breast cancer. Cell 103:1047–1058

    Article  CAS  PubMed  Google Scholar 

  • Bastock R, St Johnston D (2008) Drosophila oogenesis. Curr Biol 18:R1082–R1087

    Article  CAS  PubMed  Google Scholar 

  • Bastock R, St Johnston D (2011) Oogenesis: matrix revolutions. Curr Biol 21:R231–R233

    Article  CAS  PubMed  Google Scholar 

  • Bear JE, Rawls JF, Saxe CL 3rd (1998) SCAR, a WASP-related protein, isolated as a suppressor of receptor defects in late Dictyostelium development. J Cell Biol 142:1325–1335

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Beccari S, Teixeira L, Rorth P (2002) The JAK/STAT pathway is required for border cell migration during Drosophila oogenesis. Mech Dev 111:115–123

    Article  CAS  PubMed  Google Scholar 

  • Bechtold M, Schultz J, Bogdan S (2014) FHOD proteins in actin dynamics—a formin’ class of its own. Small GTPases 5:11

    Article  PubMed  Google Scholar 

  • Ben-Yaacov S, Le Borgne R, Abramson I, Schweisguth F, Schejter ED (2001) Wasp, the Drosophila Wiskott-Aldrich syndrome gene homologue, is required for cell fate decisions mediated by Notch signaling. J Cell Biol 152:1–13

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Berger S, Schafer G, Kesper DA, Holz A, Eriksson T, Palmer RH, Beck L, Klambt C, Renkawitz-Pohl R, Onel SF (2008) WASP and SCAR have distinct roles in activating the Arp2/3 complex during myoblast fusion. J Cell Sci 121:1303–1313

    Article  CAS  PubMed  Google Scholar 

  • Bier E (2005) Drosophila, the golden bug, emerges as a tool for human genetics. Nat Rev Genet 6:9–23

    Article  CAS  PubMed  Google Scholar 

  • Bilder D, Haigo SL (2012) Expanding the morphogenetic repertoire: perspectives from the Drosophila egg. Dev Cell 22:12–23

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Bogdan S, Klambt C (2003) Kette regulates actin dynamics and genetically interacts with Wave and Wasp. Development 130:4427–4437

    Article  CAS  PubMed  Google Scholar 

  • Bogdan S, Stephan R, Lobke C, Mertens A, Klambt C (2005) Abi activates WASP to promote sensory organ development. Nat Cell Biol 7:977–984

    Article  CAS  PubMed  Google Scholar 

  • Borghese L, Fletcher G, Mathieu J, Atzberger A, Eades WC, Cagan RL, Rorth P (2006) Systematic analysis of the transcriptional switch inducing migration of border cells. Dev Cell 10:497–508

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Bouma G, Burns S, Thrasher AJ (2007) Impaired T-cell priming in vivo resulting from dysfunction of WASp-deficient dendritic cells. Blood 110:4278–4284

    Article  CAS  PubMed  Google Scholar 

  • Bouma G, Mendoza-Naranjo A, Blundell MP, de Falco E, Parsley KL, Burns SO, Thrasher AJ (2011) Cytoskeletal remodeling mediated by WASp in dendritic cells is necessary for normal immune synapse formation and T-cell priming. Blood 118:2492–2501

    Article  CAS  PubMed  Google Scholar 

  • Brand AH, Perrimon N (1993) Targeted gene expression as a means of altering cell fates and generating dominant phenotypes. Development 118:401–415

    CAS  PubMed  Google Scholar 

  • Brinkmann K, Winterhoff M, Onel SF, Schultz J, Faix J, Bogdan S (2016) WHAMY is a novel actin polymerase promoting myoblast fusion, macrophage cell motility and sensory organ development in Drosophila. J Cell Sci 129:604–620

    Article  CAS  PubMed  Google Scholar 

  • Bruckner K, Kockel L, Duchek P, Luque CM, Rorth P, Perrimon N (2004) The PDGF/VEGF receptor controls blood cell survival in Drosophila. Dev Cell 7:73–84

    Article  PubMed  Google Scholar 

  • Bugyi B, Carlier MF (2010) Control of actin filament treadmilling in cell motility. Annu Rev Biophys 39:449–470

    Article  CAS  PubMed  Google Scholar 

  • Caceres R, Abou-Ghali M, Plastino J (2015) Reconstituting the actin cytoskeleton at or near surfaces in vitro. Biochim Biophys Acta 1853:3006–3014

    Article  CAS  PubMed  Google Scholar 

  • Cai D, Chen SC, Prasad M, He L, Wang X, Choesmel-Cadamuro V, Sawyer JK, Danuser G, Montell DJ (2014) Mechanical feedback through E-cadherin promotes direction sensing during collective cell migration. Cell 157:1146–1159

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Cameron JM, Gabrielsen M, Chim YH, Munro J, McGhee EJ, Sumpton D, Eaton P, Anderson KI, Yin HB, Olson MF (2015) Polarized cell motility induces hydrogen peroxide to inhibit cofilin via cysteine oxidation. Curr Biol 25:1520–1525

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Campellone KG, Webb NJ, Znameroski EA, Welch MD (2008) WHAMM is an Arp2/3 complex activator that binds microtubules and functions in ER to Golgi transport. Cell 134:148–161

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Campellone KG, Welch MD (2010) A nucleator arms race: cellular control of actin assembly. Nat Rev Mol Cell Biol 11:237–251

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Cestra G, Toomre D, Chang S, De Camilli P (2005) The Abl/Arg substrate ArgBP2/nArgBP2 coordinates the function of multiple regulatory mechanisms converging on the actin cytoskeleton. Proc Natl Acad Sci U S A 102:1731–1736

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Cetera M, Horne-Badovinac S (2015) Round and round gets you somewhere: collective cell migration and planar polarity in elongating Drosophila egg chambers. Curr Opin Genet Dev 32:10–15

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Cetera M, Ramirez-San Juan GR, Oakes PW, Lewellyn L, Fairchild MJ, Tanentzapf G, Gardel ML, Horne-Badovinac S (2014) Epithelial rotation promotes the global alignment of contractile actin bundles during Drosophila egg chamber elongation. Nat Commun 5:5511

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Chen EH (2011) Invasive podosomes and myoblast fusion. Curr Top Membr 68:235–258

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Chen Z, Borek D, Padrick SB, Gomez TS, Metlagel Z, Ismail AM, Umetani J, Billadeau DD, Otwinowski Z, Rosen MK (2010) Structure and control of the actin regulatory WAVE complex. Nature 468:533–538

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Chen B, Brinkmann K, Chen Z, Pak CW, Liao Y, Shi S, Henry L, Grishin NV, Bogdan S, Rosen MK (2014a) The WAVE regulatory complex links diverse receptors to the actin cytoskeleton. Cell 156:195–207

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Chen XJ, Squarr AJ, Stephan R, Chen B, Higgins TE, Barry DJ, Martin MC, Rosen MK, Bogdan S, Way M (2014b) Ena/VASP proteins cooperate with the WAVE complex to regulate the actin cytoskeleton. Dev Cell 30:569–584

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Cho NK, Keyes L, Johnson E, Heller J, Ryner L, Karim F, Krasnow MA (2002) Developmental control of blood cell migration by the Drosophila VEGF pathway. Cell 108:865–876

    Article  CAS  PubMed  Google Scholar 

  • Cooper JA, Schafer DA (2000) Control of actin assembly and disassembly at filament ends. Curr Opin Cell Biol 12:97–103

    Article  CAS  PubMed  Google Scholar 

  • Cotta-de-Almeida V, Westerberg L, Maillard MH, Onaldi D, Wachtel H, Meelu P, Chung UI, Xavier R, Alt FW, Snapper SB (2007) Wiskott Aldrich syndrome protein (WASP) and N-WASP are critical for T cell development. Proc Natl Acad Sci U S A 104:15424–15429

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • D’Ambrosio MV, Vale RD (2010) A whole genome RNAi screen of Drosophila S2 cell spreading performed using automated computational image analysis. J Cell Biol 191:471–478

    Article  PubMed  PubMed Central  CAS  Google Scholar 

  • Derry JM, Ochs HD, Francke U (1994) Isolation of a novel gene mutated in Wiskott-Aldrich syndrome. Cell 79:following 922

    Google Scholar 

  • Devriendt K, Kim AS, Mathijs G, Frints SG, Schwartz M, Van Den Oord JJ, Verhoef GE, Boogaerts MA, Fryns JP, You D, Rosen MK, Vandenberghe P (2001) Constitutively activating mutation in WASP causes X-linked severe congenital neutropenia. Nat Genet 27:313–317

    Article  CAS  PubMed  Google Scholar 

  • Dietzl G, Chen D, Schnorrer F, Su KC, Barinova Y, Fellner M, Gasser B, Kinsey K, Oppel S, Scheiblauer S et al (2007) A genome-wide transgenic RNAi library for conditional gene inactivation in Drosophila. Nature 448:151–156

    Article  CAS  PubMed  Google Scholar 

  • Dong B, Kakihara K, Otani T, Wada H, Hayashi S (2013) Rab9 and retromer regulate retrograde trafficking of luminal protein required for epithelial tube length control. Nat Commun 4:1358

    Article  PubMed  PubMed Central  CAS  Google Scholar 

  • Duchek P, Rorth P (2001) Guidance of cell migration by EGF receptor signaling during Drosophila oogenesis. Science 291:131–133

    Article  CAS  PubMed  Google Scholar 

  • Duchek P, Somogyi K, Jekely G, Beccari S, Rorth P (2001) Guidance of cell migration by the Drosophila PDGF/VEGF receptor. Cell 107:17–26

    Article  CAS  PubMed  Google Scholar 

  • Eden S, Rohatgi R, Podtelejnikov AV, Mann M, Kirschner MW (2002) Mechanism of regulation of WAVE1-induced actin nucleation by Rac1 and Nck. Nature 418:790–793

    Article  CAS  PubMed  Google Scholar 

  • Evans IR, Ghai PA, Urbancic V, Tan KL, Wood W (2013) SCAR/WAVE-mediated processing of engulfed apoptotic corpses is essential for effective macrophage migration in Drosophila. Cell Death Differ 20:709–720

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Firat-Karalar EN, Welch MD (2011) New mechanisms and functions of actin nucleation. Curr Opin Cell Biol 23:4–13

    Article  CAS  PubMed  Google Scholar 

  • Fricke R, Gohl C, Dharmalingam E, Grevelhorster A, Zahedi B, Harden N, Kessels M, Qualmann B, Bogdan S (2009) Drosophila Cip4/Toca-1 integrates membrane trafficking and actin dynamics through WASP and SCAR/WAVE. Curr Biol 19:1429–1437

    Article  CAS  PubMed  Google Scholar 

  • Frugtniet B, Jiang WG, Martin TA (2015) Role of the WASP and WAVE family proteins in breast cancer invasion and metastasis. Breast Cancer (Dove Med Press) 7:99–109

    CAS  PubMed Central  Google Scholar 

  • Fulga TA, Rorth P (2002) Invasive cell migration is initiated by guided growth of long cellular extensions. Nat Cell Biol 4:715–719

    Article  CAS  PubMed  Google Scholar 

  • Gardberg M, Kaipio K, Lehtinen L, Mikkonen P, Heuser VD, Talvinen K, Iljin K, Kampf C, Uhlen M, Grenman R, Koivisto M, Carpen O (2013) FHOD1, a formin upregulated in epithelial-mesenchymal transition, participates in cancer cell migration and invasion. PLoS One 8, e74923

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Gates J (2012) Drosophila egg chamber elongation Insights into how tissues and organs are shaped. Fly 6:213–227

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Godt D, Tepass U (2009) Breaking a temporal barrier: signalling crosstalk regulates the initiation of border cell migration. Nat Cell Biol 11:536–538

    Article  CAS  PubMed  Google Scholar 

  • Goulding NJ (2004) The molecular complexity of glucocorticoid actions in inflammation – a four-ring circus. Curr Opin Pharmacol 4:629–636

    Article  CAS  PubMed  Google Scholar 

  • Gruenbaum-Cohen Y, Harel I, Umansky KB, Tzahor E, Snapper SB, Shilo BZ, Schejter ED (2012) The actin regulator N-WASp is required for muscle-cell fusion in mice. Proc Natl Acad Sci U S A 109:11211–11216

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Gustafsson MG, Shao L, Carlton PM, Wang CJ, Golubovskaya IN, Cande WZ, Agard DA, Sedat JW (2008) Three-dimensional resolution doubling in wide-field fluorescence microscopy by structured illumination. Biophys J 94:4957–4970

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Hadjieconomou D, Rotkopf S, Alexandre C, Bell DM, Dickson BJ, Salecker I (2011) Flybow: genetic multicolor cell labeling for neural circuit analysis in Drosophila melanogaster. Nat Methods 8:260–266

    Article  CAS  PubMed  Google Scholar 

  • Haigo SL, Bilder D (2011) Global tissue revolutions in a morphogenetic movement controlling elongation. Science 331:1071–1074

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Haralalka S, Shelton C, Cartwright HN, Katzfey E, Janzen E, Abmayr SM (2011) Asymmetric Mbc, active Rac1 and F-actin foci in the fusion-competent myoblasts during myoblast fusion in Drosophila. Development 138:1551–1562

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • He L, Wang X, Montell DJ (2011) Shining light on Drosophila oogenesis: live imaging of egg development. Curr Opin Genet Dev 21:612–619

    Article  CAS  PubMed  Google Scholar 

  • Horne-Badovinac S, Bilder D (2005) Mass transit: epithelial morphogenesis in the Drosophila egg chamber. Dev Dyn 232:559–574

    Article  CAS  PubMed  Google Scholar 

  • Ibarra N, Pollitt A, Insall RH (2005) Regulation of actin assembly by SCAR/WAVE proteins. Biochem Soc Trans 33:1243–1246

    Article  CAS  PubMed  Google Scholar 

  • Imai K, Nonoyama S, Ochs HD (2003) WASP (Wiskott-Aldrich syndrome protein) gene mutations and phenotype. Curr Opin Allergy Clin Immunol 3:427–436

    Article  CAS  PubMed  Google Scholar 

  • Jang AC, Chang YC, Bai J, Montell D (2009) Border-cell migration requires integration of spatial and temporal signals by the BTB protein Abrupt. Nat Cell Biol 11:569–579

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Jin Y, Mazza C, Christie JR, Giliani S, Fiorini M, Mella P, Gandellini F, Stewart DM, Zhu Q, Nelson DL, Notarangelo LD, Ochs HD (2004) Mutations of the Wiskott-Aldrich syndrome protein (WASP): hotspots, effect on transcription, and translation and phenotype/genotype correlation. Blood 104:4010–4019

    Article  CAS  PubMed  Google Scholar 

  • Jurmeister S, Baumann M, Balwierz A, Keklikoglou I, Ward A, Uhlmann S, Zhang JD, Wiemann S, Sahin O (2012) MicroRNA-200c represses migration and invasion of breast cancer cells by targeting actin-regulatory proteins FHOD1 and PPM1F. Mol Cell Biol 32:633–651

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Kanca O, Caussinus E, Denes AS, Percival-Smith A, Affolter M (2014) Raeppli: a whole-tissue labeling tool for live imaging of Drosophila development. Development 141:472–480

    Article  CAS  PubMed  Google Scholar 

  • Kiger AA, Baum B, Jones S, Jones MR, Coulson A, Echeverri C, Perrimon N (2003) A functional genomic analysis of cell morphology using RNA interference. J Biol 2:27

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Kollmar M, Lbik D, Enge S (2012) Evolution of the eukaryotic ARP2/3 activators of the WASP family: WASP, WAVE, WASH, and WHAMM, and the proposed new family members WAWH and WAML. BMC Res Notes 5:88

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Koronakis V, Hume PJ, Humphreys D, Liu T, Horning O, Jensen ON, McGhie EJ (2011) WAVE regulatory complex activation by cooperating GTPases Arf and Rac1. Proc Natl Acad Sci U S A 108:14449–14454

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Krause M, Gautreau A (2014) Steering cell migration: lamellipodium dynamics and the regulation of directional persistence. Nat Rev Mol Cell Biol 15:577–590

    Article  CAS  PubMed  Google Scholar 

  • Krzemien J, Dubois L, Makki R, Meister M, Vincent A, Crozatier M (2007) Control of blood cell homeostasis in Drosophila larvae by the posterior signalling centre. Nature 446:325–328

    Article  CAS  PubMed  Google Scholar 

  • Kunda P, Craig G, Dominguez V, Baum B (2003) Abi, Sra1, and Kette control the stability and localization of SCAR/WAVE to regulate the formation of actin-based protrusions. Curr Biol 13:1867–1875

    Article  CAS  PubMed  Google Scholar 

  • Lammel U, Bechtold M, Risse B, Berh D, Fleige A, Bunse I, Jiang X, Klambt C, Bogdan S (2014) The Drosophila FHOD1-like formin Knittrig acts through Rok to promote stress fiber formation and directed macrophage migration during the cellular immune response. Development 141:1366–1380

    Article  CAS  PubMed  Google Scholar 

  • Leng Y, Zhang J, Badour K, Arpaia E, Freeman S, Cheung P, Siu M, Siminovitch K (2005) Abelson-interactor-1 promotes WAVE2 membrane translocation and Abelson-mediated tyrosine phosphorylation required for WAVE2 activation. Proc Natl Acad Sci U S A 102:1098–1103

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Linardopoulou EV, Parghi SS, Friedman C, Osborn GE, Parkhurst SM, Trask BJ (2007) Human subtelomeric WASH genes encode a new subclass of the WASP family. PLoS Genet 3, e237

    Article  PubMed  PubMed Central  CAS  Google Scholar 

  • Liu R, Abreu-Blanco MT, Barry KC, Linardopoulou EV, Osborn GE, Parkhurst SM (2009a) Wash functions downstream of Rho and links linear and branched actin nucleation factors. Development 136:2849–2860

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Liu T, Sims D, Baum B (2009b) Parallel RNAi screens across different cell lines identify generic and cell type-specific regulators of actin organization and cell morphology. Genome Biol 10:R26

    Article  PubMed  PubMed Central  CAS  Google Scholar 

  • Loisel TP, Boujemaa R, Pantaloni D, Carlier MF (1999) Reconstitution of actin-based motility of Listeria and Shigella using pure proteins. Nature 401:613–616

    Article  CAS  PubMed  Google Scholar 

  • Machesky LM, Gould KL (1999) The Arp2/3 complex: a multifunctional actin organizer. Curr Opin Cell Biol 11:117–121

    Article  CAS  PubMed  Google Scholar 

  • Machesky LM, Insall RH (1998) Scar1 and the related Wiskott-Aldrich syndrome protein, WASP, regulate the actin cytoskeleton through the Arp2/3 complex. Curr Biol 8:1347–1356

    Article  CAS  PubMed  Google Scholar 

  • Machesky LM, Atkinson SJ, Ampe C, Vandekerckhove J, Pollard TD (1994) Purification of a cortical complex containing two unconventional actins from Acanthamoeba by affinity chromatography on profilin-agarose. J Cell Biol 127:107–115

    Article  CAS  PubMed  Google Scholar 

  • Maillard MH, Cotta-de-Almeida V, Takeshima F, Nguyen DD, Michetti P, Nagler C, Bhan AK, Snapper SB (2007) The Wiskott-Aldrich syndrome protein is required for the function of CD4(+)CD25(+)Foxp3(+) regulatory T cells. J Exp Med 204:381–391

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Markus R, Laurinyecz B, Kurucz E, Honti V, Bajusz I, Sipos B, Somogyi K, Kronhamn J, Hultmark D, Ando I (2009) Sessile hemocytes as a hematopoietic compartment in Drosophila melanogaster. Proc Natl Acad Sci U S A 106:4805–4809

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Massarwa R, Carmon S, Shilo BZ, Schejter ED (2007) WIP/WASp-based actin-polymerization machinery is essential for myoblast fusion in Drosophila. Dev Cell 12:557–569

    Article  CAS  PubMed  Google Scholar 

  • McDonald JA, Montell DJ (2005) Analysis of cell migration using Drosophila as a model system. Methods Mol Biol 294:175–202

    PubMed  Google Scholar 

  • McDonald JA, Pinheiro EM, Montell DJ (2003) PVF1, a PDGF/VEGF homolog, is sufficient to guide border cells and interacts genetically with Taiman. Development 130:3469–3478

    Article  CAS  PubMed  Google Scholar 

  • McDonald JA, Pinheiro EM, Kadlec L, Schupbach T, Montell DJ (2006) Multiple EGFR ligands participate in guiding migrating border cells. Dev Biol 296:94–103

    Article  CAS  PubMed  Google Scholar 

  • McMahon A, Supatto W, Fraser SE, Stathopoulos A (2008) Dynamic analyses of Drosophila gastrulation provide insights into collective cell migration. Science 322:1546–1550

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Miki H, Miura K, Takenawa T (1996) N-WASP, a novel actin-depolymerizing protein, regulates the cortical cytoskeletal rearrangement in a PIP2-dependent manner downstream of tyrosine kinases. EMBO J 15:5326–5335

    PubMed  PubMed Central  Google Scholar 

  • Moeller MJ, Soofi A, Braun GS, Li X, Watzl C, Kriz W, Holzman LB (2004) Protocadherin FAT1 binds Ena/VASP proteins and is necessary for actin dynamics and cell polarization. EMBO J 23:3769–3779

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Mohr S, Bakal C, Perrimon N (2010) Genomic screening with RNAi: results and challenges. Annu Rev Biochem 79:37–64

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Montell DJ (2003) Border-cell migration: the race is on. Nat Rev Mol Cell Bio 4:13–24

    Article  CAS  Google Scholar 

  • Montell DJ, Rorth P, Spradling AC (1992) Slow border cells, a locus required for a developmentally regulated cell migration during oogenesis, encodes Drosophila C/EBP. Cell 71:51–62

    Article  CAS  PubMed  Google Scholar 

  • Montell DJ, Yoon WH, Starz-Gaiano M (2012) Group choreography: mechanisms orchestrating the collective movement of border cells. Nat Rev Mol Cell Biol 13:631–645

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Moreira S, Stramer B, Evans I, Wood W, Martin P (2010) Prioritization of competing damage and developmental signals by migrating macrophages in the Drosophila embryo. Curr Biol 20:464–470

    Article  CAS  PubMed  Google Scholar 

  • Moreira CG, Jacinto A, Prag S (2013) Drosophila integrin adhesion complexes are essential for hemocyte migration in vivo. Biol Open 2:795–801

    Article  PubMed  PubMed Central  CAS  Google Scholar 

  • Mukherjee P, Gildor B, Shilo BZ, VijayRaghavan K, Schejter ED (2011) The actin nucleator WASp is required for myoblast fusion during adult Drosophila myogenesis. Development 138:2347–2357

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Niethammer P, Grabher C, Look AT, Mitchison TJ (2009) A tissue-scale gradient of hydrogen peroxide mediates rapid wound detection in zebrafish. Nature 459:996–999

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Ni JQ, Liu LP, Binari R, Hardy R, Shim HS, Cavallaro A, Booker M, Pfeiffer BD, Markstein M, Wang H et al (2009) A Drosophila resource of transgenic RNAi lines for neurogenetics. Genetics 182:1089–1100

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Oikawa T, Yamaguchi H, Itoh T, Kato M, Ijuin T, Yamazaki D, Suetsugu S, Takenawa T (2004) PtdIns(3,4,5)P3 binding is necessary for WAVE2-induced formation of lamellipodia. Nat Cell Biol 6:420–426

    Article  CAS  PubMed  Google Scholar 

  • Pocha SM, Montell DJ (2014) Cellular and molecular mechanisms of single and collective cell migrations in Drosophila: themes and variations. Annu Rev Genet 48:295–318

    Article  CAS  PubMed  Google Scholar 

  • Pollard TD, Borisy GG (2003) Cellular motility driven by assembly and disassembly of actin filaments. Cell 112:453–465

    Article  CAS  PubMed  Google Scholar 

  • Pollard TD, Cooper JA (2009) Actin, a central player in cell shape and movement. Science 326:1208–1212

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Poulter NS, Pollitt AY, Davies A, Malinova D, Nash GB, Hannon MJ, Pikramenou Z, Rappoport JZ, Hartwig JH, Owen DM, Thrasher AJ, Watson SP, Thomas SG (2015) Platelet actin nodules are podosome-like structures dependent on Wiskott-Aldrich syndrome protein and ARP2/3 complex. Nat Commun 6:7254

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Rajan A, Tien AC, Haueter CM, Schulze KL, Bellen HJ (2009) The Arp2/3 complex and WASp are required for apical trafficking of Delta into microvilli during cell fate specification of sensory organ precursors. Nat Cell Biol 11:815–824

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Ramond E, Meister M, Lemaitre B (2015) From embryo to adult: hematopoiesis along the Drosophila life cycle. Dev Cell 33:367–368

    Article  CAS  PubMed  Google Scholar 

  • Razzell W, Evans IR, Martin P, Wood W (2013) Calcium flashes orchestrate the wound inflammatory response through DUOX activation and hydrogen peroxide release. Curr Biol 23:424–429

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Recher M, Burns SO, de la Fuente MA, Volpi S, Dahlberg C, Walter JE, Moffitt K, Mathew D, Honke N, Lang PA, Patrizi L, Falet H, Keszei M, Mizui M, Csizmadia E, Candotti F, Nadeau K, Bouma G, Delmonte OM, Frugoni F, Fomin AB, Buchbinder D, Lundequist EM, Massaad MJ, Tsokos GC, Hartwig J, Manis J, Terhorst C, Geha RS, Snapper S, Lang KS, Malley R, Westerberg L, Thrasher AJ, Notarangelo LD (2012) B cell-intrinsic deficiency of the Wiskott-Aldrich syndrome protein (WASp) causes severe abnormalities of the peripheral B-cell compartment in mice. Blood 119:2819–2828

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Regan JC, Brandao AS, Leitao AB, Mantas Dias AR, Sucena E, Jacinto A, Zaidman-Remy A (2013) Steroid hormone signaling is essential to regulate innate immune cells and fight bacterial infection in Drosophila. PLoS Pathog 9, e1003720

    Article  PubMed  PubMed Central  CAS  Google Scholar 

  • Reiter LT, Potocki L, Chien S, Gribskov M, Bier E (2001) A systematic analysis of human disease-associated gene sequences in Drosophila melanogaster. Genome Res 11:1114–1125

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Rieder LE, Larschan EN (2014) Wisdom from the fly. Trends Genet 30:479–481

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Robinson DN, Cooley L (1997) Genetic analysis of the actin cytoskeleton in the Drosophila ovary. Annu Rev Cell Dev Biol 13:147–170

    Article  CAS  PubMed  Google Scholar 

  • Rogers SL, Wiedemann U, Stuurman N, Vale RD (2003) Molecular requirements for actin-based lamella formation in Drosophila S2 cells. J Cell Biol 162:1079–1088

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Rohatgi R, Ma L, Miki H, Lopez M, Kirchhausen T, Takenawa T, Kirschner MW (1999) The interaction between N-WASP and the Arp2/3 complex links Cdc42-dependent signals to actin assembly. Cell 97:221–231

    Article  CAS  PubMed  Google Scholar 

  • Rohn JL, Sims D, Liu T, Fedorova M, Schock F, Dopie J, Vartiainen MK, Kiger AA, Perrimon N, Baum B (2011) Comparative RNAi screening identifies a conserved core metazoan actinome by phenotype. J Cell biol 194:789–805

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Rorth P (2012) Fellow travellers: emergent properties of collective cell migration. EMBO Rep 13:984–991

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Rosales-Nieves AE, Gonzalez-Reyes A (2014) Genetics and mechanisms of ovarian cancer: parallels between Drosophila and humans. Semin Cell Dev Biol 28:104–109

    Article  CAS  PubMed  Google Scholar 

  • Rotkopf S, Hamberg Y, Aigaki T, Snapper SB, Shilo BZ, Schejter ED (2011) The WASp-based actin polymerization machinery is required in somatic support cells for spermatid maturation and release. Development 138:2729–2739

    Article  CAS  PubMed  Google Scholar 

  • Rottner K, Stradal TE (2011) Actin dynamics and turnover in cell motility. Curr Opin Cell Biol 23:569–578

    Article  CAS  PubMed  Google Scholar 

  • Routley CE, Ashcroft GS (2009) Effect of estrogen and progesterone on macrophage activation during wound healing. Wound Repair Regen 17:42–50

    Article  PubMed  Google Scholar 

  • Sadhukhan S, Sarkar K, Taylor M, Candotti F, Vyas YM (2014) Nuclear role of WASp in gene transcription is uncoupled from its ARP2/3-dependent cytoplasmic role in actin polymerization. J Immunol 193:150–160

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Sampson CJ, Amin U, Couso JP (2013) Activation of Drosophila hemocyte motility by the ecdysone hormone. Biol Open 2:1412–1420

    Article  PubMed  PubMed Central  CAS  Google Scholar 

  • Sander M, Squarr AJ, Risse B, Jiang X, Bogdan S (2013) Drosophila pupal macrophages—a versatile tool for combined ex vivo and in vivo imaging of actin dynamics at high resolution. Eur J Cell Biol 92:349–354

    Article  CAS  PubMed  Google Scholar 

  • Sarkar K, Sadhukhan S, Han SS, Vyas YM (2014) Disruption of hSWI/SNF complexes in T cells by WAS mutations distinguishes X-linked thrombocytopenia from Wiskott-Aldrich syndrome. Blood 124:3409–3419

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Sens KL, Zhang S, Jin P, Duan R, Zhang G, Luo F, Parachini L, Chen EH (2010) An invasive podosome-like structure promotes fusion pore formation during myoblast fusion. J Cell Biol 191:1013–1027

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Shilagardi K, Li S, Luo F, Marikar F, Duan R, Jin P, Kim JH, Murnen K, Chen EH (2013) Actin-propelled invasive membrane protrusions promote fusogenic protein engagement during cell-cell fusion. Science 340:359–363

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Silver DL, Montell DJ (2001) Paracrine signaling through the JAK/STAT pathway activates invasive behavior of ovarian epithelial cells in Drosophila. Cell 107:831–841

    Article  CAS  PubMed  Google Scholar 

  • Silver DL, Geisbrecht ER, Montell DJ (2005) Requirement for JAK/STAT signaling throughout border cell migration in Drosophila. Development 132:3483–3492

    Article  CAS  PubMed  Google Scholar 

  • Snapper SB, Rosen FS, Mizoguchi E, Cohen P, Khan W, Liu CH, Hagemann TL, Kwan SP, Ferrini R, Davidson L, Bhan AK, Alt FW (1998) Wiskott-Aldrich syndrome protein-deficient mice reveal a role for WASP in T but not B cell activation. Immunity 9:81–91

    Article  CAS  PubMed  Google Scholar 

  • Squarr AJ, Brinkmann K, Chen B, Steinbacher T, Ebnet K, Rosen MK, Bogdan S (2016) Fat2 acts through the WAVE regulatory complex to drive collective cell migration during tissue rotation. J Cell Biol 212:591–603

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Starz-Gaiano M, Montell DJ (2004) Genes that drive invasion and migration in Drosophila. Curr Opin Genet Dev 14:86–91

    Article  CAS  PubMed  Google Scholar 

  • Stephan R, Grevelhorster A, Wenderdel S, Klambt C, Bogdan S (2008) Abi induces ectopic sensory organ formation by stimulating EGFR signaling. Mech Dev 125:183–195

    Article  CAS  PubMed  Google Scholar 

  • Stephan R, Gohl C, Fleige A, Klambt C, Bogdan S (2011) Membrane-targeted WAVE mediates photoreceptor axon targeting in the absence of the WAVE complex in Drosophila. Mol Biol Cell 22:4079–4092

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Stewart DM, Tian L, Nelson DL (1999) Mutations that cause the Wiskott-Aldrich syndrome impair the interaction of Wiskott-Aldrich syndrome protein (WASP) with WASP interacting protein. J Immunol 162:5019–5024

    CAS  PubMed  Google Scholar 

  • Stramer B, Wood W, Galko MJ, Redd MJ, Jacinto A, Parkhurst SM, Martin P (2005) Live imaging of wound inflammation in Drosophila embryos reveals key roles for small GTPases during in vivo cell migration. J Cell Biol 168:567–573

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Sturner T, Tavosanis G (2016) Rotating for elongation: Fat2 whips for the race. J Cell Biol 212:487–489

    Article  PubMed  PubMed Central  CAS  Google Scholar 

  • Suetsugu S, Hattori M, Miki H, Tezuka T, Yamamoto T, Mikoshiba K, Takenawa T (2002) Sustained activation of N-WASP through phosphorylation is essential for neurite extension. Dev Cell 3:645–658

    Article  CAS  PubMed  Google Scholar 

  • Supatto W, McMahon A, Fraser SE, Stathopoulos A (2009) Quantitative imaging of collective cell migration during Drosophila gastrulation: multiphoton microscopy and computational analysis. Nat Protoc 4:1397–1412

    Article  PubMed  PubMed Central  CAS  Google Scholar 

  • Takenawa T (2005) From N-WASP to WAVE: key molecules for regulation of cortical actin organization. Novartis Found Symp 269:3–10; discussion 10–15, 30–14 passim

    Google Scholar 

  • Tal T, Vaizel-Ohayon D, Schejter ED (2002) Conserved interactions with cytoskeletal but not signaling elements are an essential aspect of Drosophila WASp function. Dev Biol 243:260–271

    Article  CAS  PubMed  Google Scholar 

  • Tang H, Li A, Bi J, Veltman DM, Zech T, Spence HJ, Yu X, Timpson P, Insall RH, Frame MC, Machesky LM (2013) Loss of Scar/WAVE complex promotes N-WASP- and FAK-dependent invasion. Curr Biol 23:107–117

    Article  CAS  PubMed  Google Scholar 

  • Tanner K, Mori H, Mroue R, Bruni-Cardoso A, Bissell MJ (2012) Coherent angular motion in the establishment of multicellular architecture of glandular tissues. Proc Natl Acad Sci U S A 109:1973–1978

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Taylor MD, Sadhukhan S, Kottangada P, Ramgopal A, Sarkar K, D’Silva S, Selvakumar A, Candotti F, Vyas YM (2010) Nuclear role of WASp in the pathogenesis of dysregulated TH1 immunity in human Wiskott-Aldrich syndrome. Sci Transl Med 2:37ra44

    Google Scholar 

  • Thrasher AJ, Burns SO (2010) WASP: a key immunological multitasker. Nat Rev Immunol 10:182–192

    Article  CAS  PubMed  Google Scholar 

  • Tsuboi S (2007) Requirement for a complex of Wiskott-Aldrich syndrome protein (WASP) with WASP interacting protein in podosome formation in macrophages. J Immunol 178:2987–2995

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Veltman DM, Insall RH (2010) WASP family proteins: their evolution and its physiological implications. Mol Biol Cell 21:2880–2893

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Vignaud T, Blanchoin L, Thery M (2012) Directed cytoskeleton self-organization. Trends Cell Biol 22:671–682

    Article  CAS  PubMed  Google Scholar 

  • Villa A, Notarangelo L, Macchi P, Mantuano E, Cavagni G, Brugnoni D, Strina D, Patrosso MC, Ramenghi U, Sacco MG et al (1995) X-linked thrombocytopenia and Wiskott-Aldrich syndrome are allelic diseases with mutations in the WASP gene. Nat Genet 9:414–417

    Article  CAS  PubMed  Google Scholar 

  • Wang XJ, Bo JY, Bridges T, Dugan KD, Pan TC, Chodosh LA, Montell DJ (2006) Analysis of cell migration using whole-genome expression profiling of migratory cells in the Drosophila ovary. Dev Cell 10:483–495

    Article  CAS  PubMed  Google Scholar 

  • Wang X, He L, Wu YI, Hahn KM, Montell DJ (2010) Light-mediated activation reveals a key role for Rac in collective guidance of cell movement in vivo. Nat Cell Biol 12:591–597

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Wang H, Lacoche S, Huang L, Xue B, Muthuswamy SK (2013) Rotational motion during three-dimensional morphogenesis of mammary epithelial acini relates to laminin matrix assembly. Proc Natl Acad Sci U S A 110:163–168

    Article  CAS  PubMed  Google Scholar 

  • Wangler MF, Yamamoto S, Bellen HJ (2015) Fruit flies in biomedical research. Genetics 199:639–653

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Weiss C, Schultz J (2015) Identification of divergent WH2 motifs by HMM-HMM alignments. BMC Res Notes 8:18

    Article  PubMed  PubMed Central  Google Scholar 

  • Wood W, Faria C, Jacinto A (2006) Distinct mechanisms regulate hemocyte chemotaxis during development and wound healing in Drosophila melanogaster. J Cell Biol 173:405–416

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Xia P, Wang S, Du Y, Zhao Z, Shi L, Sun L, Huang G, Ye B, Li C, Dai Z, Hou N, Cheng X, Sun Q, Li L, Yang X, Fan Z (2013) WASH inhibits autophagy through suppression of Beclin 1 ubiquitination. EMBO J 32:2685–2696

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Xiao X, Mruk DD, Tang EI, Massarwa R, Mok KW, Li N, Wong CK, Lee WM, Snapper SB, Shilo BZ, Schejter ED, Cheng CY (2014) N-wasp is required for structural integrity of the blood-testis barrier. PLoS Genet 10, e1004447

    Article  PubMed  PubMed Central  CAS  Google Scholar 

  • Yan C, Martinez-Quiles N, Eden S, Shibata T, Takeshima F, Shinkura R, Fujiwara Y, Bronson R, Snapper SB, Kirschner MW, Geha R, Rosen FS, Alt FW (2003) WAVE2 deficiency reveals distinct roles in embryogenesis and Rac-mediated actin-based motility. EMBO J 22:3602–3612

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Yoo SK, Freisinger CM, LeBert DC, Huttenlocher A (2012) Early redox, Src family kinase, and calcium signaling integrate wound responses and tissue regeneration in zebrafish. J Cell Biol 199:225–234

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Yu X, Zech T, McDonald L, Gonzalez EG, Li A, Macpherson I, Schwarz JP, Spence H, Futo K, Timpson P, Nixon C, Ma Y, Anton IM, Visegrady B, Insall RH, Oien K, Blyth K, Norman JC, Machesky LM (2012) N-WASP coordinates the delivery and F-actin-mediated capture of MT1-MMP at invasive pseudopods. J Cell Biol 199:527–544

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Zallen JA, Cohen Y, Hudson AM, Cooley L, Wieschaus E, Schejter ED (2002) SCAR is a primary regulator of Arp2/3-dependent morphological events in Drosophila. J Cell Biol 156:689–701

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Zobel T, Bogdan S (2013) A high resolution view of the fly actin cytoskeleton lacking a functional WAVE complex. J Microsc 251:224–231

    Article  CAS  PubMed  Google Scholar 

  • Zuchero JB, Coutts AS, Quinlan ME, La Thangue NB, Mullins RD (2009) p53-cofactor JMY is a multifunctional actin nucleation factor. Nat Cell Biol 11:451–459

    Article  CAS  PubMed  PubMed Central  Google Scholar 

Download references

Acknowledgements

We thank Meike Bechtold and Christian Klämbt for critical reading of the manuscript. Our work is supported by a grant to S.B. from the cluster of excellence “Cells in Motion” (CIM), and by grants to S.B. from the Heisenberg Program of the Deutsche Forschungsgemeinschaft (DFG) and by the SPP1464 priority programme of the DFG.

Author information

Authors and Affiliations

  1. Institute for Neurobiology, University of Muenster, Badestrasse 9, 48149, Muenster, Germany

    Lena Brüser & Sven Bogdan

Authors
  1. Lena Brüser
    View author publications

    You can also search for this author in PubMed Google Scholar

  2. Sven Bogdan
    View author publications

    You can also search for this author in PubMed Google Scholar

Corresponding author

Correspondence to Sven Bogdan .

Editor information

Editors and Affiliations

  1. Cell Biology, Life Sciences, BRICS, TU Braunschweig, Braunschweig, Germany

    Brigitte M. Jockusch

Rights and permissions

Reprints and permissions

Copyright information

© 2016 Springer International Publishing Switzerland

About this chapter

Cite this chapter

Brüser, L., Bogdan, S. (2016). Molecular Control of Actin Dynamics In Vivo: Insights from Drosophila . In: Jockusch, B. (eds) The Actin Cytoskeleton. Handbook of Experimental Pharmacology, vol 235. Springer, Cham. https://doi.org/10.1007/164_2016_33

Download citation

Publish with us

Policies and ethics

Search

Navigation