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Drosophila WASH is required for integrin-mediated cell adhesion, cell motility and lysosomal neutralization

Nagel, Benedikt M., Bechtold, Meike, Rodriguez, Luis Garcia, Bogdan, Sven·2017·Journal of Cell Science
DOI 10.1242/jcs.193086
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Abstract

The Wiskott-Aldrich syndrome protein and SCAR homolog (WASH; also known as Washout in flies) is a conserved actin-nucleation-promoting factor controlling Arp2/3 complex activity in endosomal sorting and recycling. Previous studies have identified WASH as an essential regulator in Drosophila development. Here, we show that homozygous wash mutant flies are viable and fertile. We demonstrate that Drosophila WASH has conserved functions in integrin receptor recycling and lysosome neutralization. WASH generates actin patches on endosomes and lysosomes, thereby mediating both aforementioned functions. Consistently, loss of WASH function results in cell spreading and cell migration defects of macrophages, and an increased lysosomal acidification that affects efficient phagocytic and autophagic clearance. WASH physically interacts with the vacuolar (V)-ATPase subunit Vha55 that is crucial to establish and maintain lysosome acidification. As a consequence, starved flies that lack WASH function show a dramatic increase in acidic autolysosomes, causing a reduced lifespan. Thus, our data highlight a conserved role for WASH in the endocytic sorting and recycling of membrane proteins, such as integrins and the V-ATPase, that increase the likelihood of survival under nutrient deprivation.

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Research works printed but not linked: 59

  1. Bischof, 2007, An optimized transgenesis system for Drosophila using germ-line-specific phiC31 integrases, Proc. Natl. Acad. Sci. USA, 104, 3312, 10.1073/pnas.0611511104 · DOI
  2. Bogdan, 2004, Sra-1 interacts with Kette and Wasp and is required for neuronal and bristle development in Drosophila, Development, 131, 3981, 10.1242/dev.01274 · DOI
  3. Bretscher, 1992, Circulating integrins: alpha 5 beta 1, alpha 6 beta 4 and Mac-1, but not alpha 3 beta 1, alpha 4 beta 1 or LFA-1, EMBO J., 11, 405, 10.1002/j.1460-2075.1992.tb05068.x · DOI
  4. Brinkmann, 2016, WHAMY is a novel actin polymerase promoting myoblast fusion, macrophage cell motility and sensory organ development in Drosophila, J. Cell Sci., 129, 604, 10.1242/jcs.179325 · DOI
  5. Carnell, 2011, Actin polymerization driven by WASH causes V-ATPase retrieval and vesicle neutralization before exocytosis, J. Cell Biol., 193, 831, 10.1083/jcb.201009119 · DOI · Paper page
  6. Comber, 2013, A dual role for the betaPS integrin myospheroid in mediating Drosophila embryonic macrophage migration, J. Cell Sci., 126, 3475, 10.1242/jcs.129700 · DOI
  7. Davies, 1996, Analysis and inactivation of vha55, the gene encoding the vacuolar ATPase B-subunit in Drosophila melanogaster reveals a larval lethal phenotype, J. Biol. Chem., 271, 30677, 10.1074/jbc.271.48.30677 · DOI
  8. Derivery, 2010, Evolutionary conservation of the WASH complex, an actin polymerization machine involved in endosomal fission, Commun. Integr. Biol., 3, 227, 10.4161/cib.3.3.11185 · DOI
  9. Derivery, 2009, The Arp2/3 activator WASH controls the fission of endosomes through a large multiprotein complex, Dev. Cell, 17, 712, 10.1016/j.devcel.2009.09.010 · DOI · Paper page
  10. Derivery, 2012, Actin polymerization controls the organization of WASH domains at the surface of endosomes, PLoS ONE, 7, e39774, 10.1371/journal.pone.0039774 · DOI · Paper page
  11. Dong, 2013, Rab9 and retromer regulate retrograde trafficking of luminal protein required for epithelial tube length control, Nat. Commun., 4, 1358, 10.1038/ncomms2347 · DOI
  12. Duleh, 2010, WASH and the Arp2/3 complex regulate endosome shape and trafficking, Cytoskeleton, 67, 193, 10.1002/cm.20437 · DOI · Paper page
  13. Duleh, 2012, Regulation of integrin trafficking, cell adhesion, and cell migration by WASH and the Arp2/3 complex, Cytoskeleton, 69, 1047, 10.1002/cm.21069 · DOI · Paper page
  14. Du, 2006, The SzA mutations of the B subunit of the Drosophila vacuolar H+ ATPase identify conserved residues essential for function in fly and yeast, J. Cell Sci., 119, 2542, 10.1242/jcs.02983 · DOI
  15. Evans, 2013, SCAR/WAVE-mediated processing of engulfed apoptotic corpses is essential for effective macrophage migration in Drosophila, Cell Death Differ., 20, 709, 10.1038/cdd.2012.166 · DOI
  16. Fricke, 2009, Drosophila Cip4/Toca-1 integrates membrane trafficking and actin dynamics through WASP and SCAR/WAVE, Curr. Biol., 19, 1429, 10.1016/j.cub.2009.07.058 · DOI
  17. Gomez, 2009, A FAM21-containing WASH complex regulates retromer-dependent sorting, Dev. Cell, 17, 699, 10.1016/j.devcel.2009.09.009 · DOI · Paper page
  18. Gomez, 2012, Trafficking defects in WASH-knockout fibroblasts originate from collapsed endosomal and lysosomal networks, Mol. Biol. Cell, 23, 3215, 10.1091/mbc.E12-02-0101 · DOI · Paper page
  19. Harbour, 2012, Recruitment of the endosomal WASH complex is mediated by the extended ‘tail’ of Fam21 binding to the retromer protein Vps35, The Biochemical journal, 442, 209, 10.1042/BJ20111761 · DOI · Paper page
  20. Jani, 2007, Zasp is required for the assembly of functional integrin adhesion sites, J. Cell Biol., 179, 1583, 10.1083/jcb.200707045 · DOI
  21. Jia, 2010, WASH and WAVE actin regulators of the Wiskott-Aldrich syndrome protein (WASP) family are controlled by analogous structurally related complexes, Proc. Natl. Acad. Sci. USA, 107, 10442, 10.1073/pnas.0913293107 · DOI · Paper page
  22. Jordens, 2005, Rab proteins, connecting transport and vesicle fusion, Traffic, 6, 1070, 10.1111/j.1600-0854.2005.00336.x · DOI
  23. King, 2013, WASH is required for lysosomal recycling and efficient autophagic and phagocytic digestion, Mol. Biol. Cell, 24, 2714, 10.1091/mbc.E13-02-0092 · DOI
  24. Kolonko, 2014, WASH-driven actin polymerization is required for efficient mycobacterial phagosome maturation arrest, Cell Microbiol., 16, 232, 10.1111/cmi.12217 · DOI · Paper page
  25. Levine, 2015, Beclin orthologs: integrative hubs of cell signaling, membrane trafficking, and physiology, Trends Cell Biol., 25, 533, 10.1016/j.tcb.2015.05.004 · DOI
  26. Lammel, 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, 10.1242/dev.101352 · DOI
  27. Linardopoulou, 2007, Human subtelomeric WASH genes encode a new subclass of the WASP family, PLoS Genet., 3, e237, 10.1371/journal.pgen.0030237 · DOI
  28. Liu, 2009, Wash functions downstream of Rho and links linear and branched actin nucleation factors, Development, 136, 2849, 10.1242/dev.035246 · DOI
  29. Luzio, 2007, Lysosomes: fusion and function, Nat. Rev. Mol. Cell Biol., 8, 622, 10.1038/nrm2217 · DOI
  30. Maxson, 2014, The vacuolar-type H(+)-ATPase at a glance - more than a proton pump, J. Cell Sci., 127, 4987, 10.1242/jcs.158550 · DOI
  31. Moreira, 2013, Drosophila integrin adhesion complexes are essential for hemocyte migration in vivo, Biol. Open, 2, 795, 10.1242/bio.20134564 · DOI
  32. Parkhurst, 1991, wimp, a dominant maternal-effect mutation, reduces transcription of a specific subset of segmentation genes in Drosophila, Genes Dev., 5, 341, 10.1101/gad.5.3.341 · DOI
  33. Piotrowski, 2013, WASH knockout T cells demonstrate defective receptor trafficking, proliferation, and effector function, Molecular and cellular biology, 33, 958, 10.1128/MCB.01288-12 · DOI · Paper page
  34. Priya, 2015, Molecular insights into Rab7-mediated endosomal recruitment of core retromer: deciphering the role of Vps26 and Vps35, Traffic, 16, 68, 10.1111/tra.12237 · DOI
  35. Pryor, 2009, Delivery of endocytosed membrane proteins to the lysosome, Biochi. Biophys. Acta, 1793, 615, 10.1016/j.bbamcr.2008.12.022 · DOI
  36. Rainero, 2013, Late endosomal and lysosomal trafficking during integrin-mediated cell migration and invasion: cell matrix receptors are trafficked through the late endosomal pathway in a way that dictates how cells migrate, Bioessays, 35, 523, 10.1002/bies.201200160 · DOI
  37. Rodriguez-Mesa, 2012, Developmental expression of Drosophila Wiskott-Aldrich Syndrome family proteins, Dev. Dyn., 241, 608, 10.1002/dvdy.23742 · DOI
  38. Rogers, 2003, Molecular requirements for actin-based lamella formation in Drosophila S2 cells, J. Cell Biol., 162, 1079, 10.1083/jcb.200303023 · DOI
  39. Russell, 2014, Autophagy regulation by nutrient signaling, Cell Res., 24, 42, 10.1038/cr.2013.166 · DOI
  40. Sander, 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, 10.1016/j.ejcb.2013.09.003 · DOI
  41. Seaman, 2014, Analysis of the Retromer complex-WASH complex interaction illuminates new avenues to explore in Parkinson disease, Commun. Integr. Biol., 7, e29483, 10.4161/cib.29483 · DOI
  42. Seaman, 2009, Membrane recruitment of the cargo-selective retromer subcomplex is catalysed by the small GTPase Rab7 and inhibited by the Rab-GAP TBC1D5, J. Cell Sci., 122, 2371, 10.1242/jcs.048686 · DOI · Paper page
  43. Seaman, 2013, Retromer-mediated endosomal protein sorting: all WASHed up!, Trends Cell Biol., 23, 522, 10.1016/j.tcb.2013.04.010 · DOI
  44. Shravage, 2013, Atg6 is required for multiple vesicle trafficking pathways and hematopoiesis in Drosophila, Development, 140, 1321, 10.1242/dev.089490 · DOI
  45. Sinenko, 2004, Increased expression of Drosophila tetraspanin, Tsp68C, suppresses the abnormal proliferation of ytr-deficient and Ras/Raf-activated hemocytes, Oncogene, 23, 9120, 10.1038/sj.onc.1208156 · DOI
  46. Stephan, 2008, Abi induces ectopic sensory organ formation by stimulating EGFR signaling, Mech. Dev., 125, 183, 10.1016/j.mod.2007.12.002 · DOI
  47. Stramer, 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, 10.1083/jcb.200405120 · DOI · Paper page
  48. Tanaka, 2008, The endocytic pathway acts downstream of Oskar in Drosophila germ plasm assembly, Development, 135, 1107, 10.1242/dev.017293 · DOI
  49. Veltman, 2010, WASP family proteins: their evolution and its physiological implications, Mol. Biol. Cell, 21, 2880, 10.1091/mbc.E10-04-0372 · DOI
  50. Verboon, 2015, Wash functions downstream of Rho1 GTPase in a subset of Drosophila immune cell developmental migrations, Mol. Biol. Cell, 26, 1665, 10.1091/mbc.E14-08-1266 · DOI
  51. Wirawan, 2012, Beclin1: a role in membrane dynamics and beyond, Autophagy, 8, 6, 10.4161/auto.8.1.16645 · DOI
  52. Wood, 2007, Drosophila melanogaster embryonic haemocytes: masters of multitasking, Nat. Rev. Mol. Cell Biol., 8, 542, 10.1038/nrm2202 · DOI
  53. Xia, 2013, WASH inhibits autophagy through suppression of Beclin 1 ubiquitination, EMBO J., 32, 2685, 10.1038/emboj.2013.189 · DOI
  54. Xia, 2014, RNF2 is recruited by WASH to ubiquitinate AMBRA1 leading to downregulation of autophagy, Cell Res., 24, 943, 10.1038/cr.2014.85 · DOI
  55. Xie, 2007, Autophagosome formation: core machinery and adaptations, Nat. Cell Biol., 9, 1102, 10.1038/ncb1007-1102 · DOI
  56. Zavodszky, 2014, Mutation in VPS35 associated with Parkinson's disease impairs WASH complex association and inhibits autophagy, Nat. Commun., 5, 3828, 10.1038/ncomms4828 · DOI · Paper page
  57. Zavodszky, 2014, VPS35 Parkinson mutation impairs autophagy via WASH, Cell Cycle, 13, 2155, 10.4161/cc.29734 · DOI
  58. Zech, 2011, The Arp2/3 activator WASH regulates alpha5beta1-integrin-mediated invasive migration, J. Cell Sci., 124, 3753, 10.1242/jcs.080986 · DOI · Paper page
  59. Zobel, 2013, A high resolution view of the fly actin cytoskeleton lacking a functional WAVE complex, J. Microsc., 251, 224, 10.1111/jmi.12020 · DOI

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Metadata

Authors
Nagel, B. M., Bechtold, M., Rodriguez, L. G., & Bogdan, S.
Venue
Journal of Cell Science
Publisher
The Company of Biologists
Published
2017-01-15
Volume
130
Issue
2
Pages
344-359
ISSN
  • 1477-9137
  • 0021-9533
DOI
10.1242/jcs.193086
Cited by
43
References
2
Language
en
Licence
www.biologists.com/user-licence-1-1/ (vor, 181 d)
Funders
Deutsche Forschungsgemeinschaft (BO 1890/1 BO 1890/2 BO 1890/3 BO 1890/4)

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