WASH and the Arp2/3 complex regulate endosome shape and trafficking

Cytoskeleton

Volumn 67, Issue 3, 2010, Pages 193-206

  Duleh, Steve N ^a   Welch, Matthew D ^a  

^a UNIVERSITY OF CALIFORNIA   (United States)

Author keywords

Actin; Arp2 3 complex; Endocytosis; WASH

Indexed keywords

ACTIN; ACTIN RELATED PROTEIN 2; ACTIN RELATED PROTEIN 3; EARLY ENDOSOME ANTIGEN 1; F ACTIN; NEURAL WISKOTT ALDRICH SYNDROME PROTEIN; ACTIN BINDING PROTEIN; ACTIN RELATED PROTEIN 2-3 COMPLEX; EPIDERMAL GROWTH FACTOR; TRANSFERRIN; VESICULAR TRANSPORT PROTEIN; WASH PROTEIN, HUMAN;

ACTIN POLYMERIZATION; ANIMAL CELL; ARTICLE; CELL ELONGATION; CELL MATURATION; CELL MIGRATION; CELL SHAPE; CELL STRUCTURE; CONTROLLED STUDY; CYTOSOL; ENDOCYTOSIS; ENDOSOME; IN VITRO STUDY; NONHUMAN; NUCLEOTIDE SEQUENCE; PHAGOCYTOSIS; PRIORITY JOURNAL; ANIMAL; CHLOROCEBUS AETHIOPS; COS 1 CELL LINE; DRUG EFFECTS; HUMAN; METABOLISM; MOUSE; PHYSIOLOGY; PROTEIN TRANSPORT; TISSUE DISTRIBUTION; ULTRASTRUCTURE;

MAMMALIA;

ACTIN-RELATED PROTEIN 2-3 COMPLEX; ACTINS; ANIMALS; CERCOPITHECUS AETHIOPS; COS CELLS; ENDOCYTOSIS; ENDOSOMES; EPIDERMAL GROWTH FACTOR; HUMANS; MICE; MICROFILAMENT PROTEINS; PROTEIN TRANSPORT; TISSUE DISTRIBUTION; TRANSFERRIN; VESICULAR TRANSPORT PROTEINS; WISKOTT-ALDRICH SYNDROME PROTEIN, NEURONAL;

EID: 77949801905     PISSN: 19493584     EISSN: 19493592     Source Type: Journal    
DOI: 10.1002/cm.20437     Document Type: Article

References (55)

1. Barr FA, Gruneberg U. 2007. Cytokinesis: placing and making the final cut. Cell 131:847-860.
2. Benesch S, Lommel S, Steffen A, Stradal TE, Scaplehorn N, Way M, Wehland J, Rottner K. 2002. Phosphatidylinositol 4,5-biphosphate (PIP2)-induced vesicle movement depends on N-WASP and involves Nck, WIP, and Grb2. J Biol Chem 277:37771-37776.
3. Benesch S, Polo S, Lai FP, Anderson KI, Stradal TE, Wehland J, Rottner K. 2005. N-WASP deficiency impairs EGF internalization and actin assembly at clathrin-coated pits. J Cell Sci 118(Part 14):3103-3115.
4. Bolte S, Cordelieres FP. 2006. A guided tour into subcellular colocalization analysis in light microscopy. J Microsc 224(Part 3):213-232.
5. 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.
6. Ceresa BP, Lotscher M, Schmid SL. 2001. Receptor and membrane recycling can occur with unaltered efficiency despite dramatic Rab5(q79l)-induced changes in endosome geometry. J Biol Chem 276:9649-9654.
7. Chang FS, Stefan CJ, Blumer KJ. 2003. AWASp homolog powers actin polymerization-dependent motility of endosomes in vivo. Curr Biol 13:455-463.
8. Derivery E, Lombard B, Loew D, Gautreau A. 2009a. The Wave complex is intrinsically inactive. Cell Motil Cytoskeleton 66:777-790.
9. Derivery E, Sousa C, Gautier JJ, Lombard B, Loew D, Gautreau A. 2009b. The Arp2/3 activator WASH controls the fission of endosomes through a large multiprotein complex. Dev Cell 17:712-723.
10. 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.
11. Engqvist-Goldstein AE, Drubin DG. 2003. Actin assembly and endocytosis: from yeast to mammals. Annu Rev Cell Dev Biol 19:287-332.
12. Goley ED, Rodenbusch SE, Martin AC, Welch MD. 2004. Critical conformational changes in the Arp2/3 complex are induced by nucleotide and nucleation promoting factor. Mol Cell 16:269-279.
13. Goley ED, Welch MD. 2006. The ARP2/3 complex: An actin nucleator comes of age. Nat Rev Mol Cell Biol 7:713-726.
14. Gomez TS, Billadeau DD. 2009. A FAM21-containing WASH complex regulates retromer-dependent sorting. Dev Cell 17:699-711.
15. Gruenberg J. 2001. The endocytic pathway: A mosaic of domains. Nat Rev Mol Cell Biol 2:721-730.
16. Hanisch J, Ehinger J, Ladwein M, Rohde M, Derivery E, Bosse T, Steffen A, Bumann D, Misselwitz B, Hardt WD, Gautreau A, Stradal TE, Rottner K. 2009. Molecular dissection of Salmonella-induced membrane ruffling versus invasion. Cell Microbiol 12:84-98.
17. Harder T, Kellner R, Parton RG, Gruenberg J. 1997. Specific release of membrane-bound annexin II and cortical cytoskeletal elements by sequestration of membrane cholesterol. Mol Biol Cell 8:533-545.
18. Innocenti M, Gerboth S, Rottner K, Lai FP, Hertzog M, Stradal TE, Frittoli E, Didry D, Polo S, Disanza A, Benesch S, DiFiore PP, Carlier MF, Scita G. 2005. Abi1 regulates the activity of N-WASP and WAVE in distinct actin-based processes. Nat Cell Biol 7:969-976.
19. Ismail AM, Padrick SB, Chen B, Umetani J, Rosen MK. 2009. The WAVE regulatory complex is inhibited. Nat Struct Mol Biol 16:561-563.
20. Kaksonen M, Toret CP, Drubin DG. 2006. Harnessing actin dynamics for clathrin-mediated endocytosis. Nat Rev Mol Cell Biol 7:404-414.
21. Kim AS, Kakalis LT, Abdul-Manan N, Liu GA, Rosen MK. 2000. Autoinhibition and activation mechanisms of the Wiskott-Aldrich syndrome protein. Nature 404:151-158.
22. 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.
23. Liu R, Abreu-Blanco MT, Barry KC, Linardopoulou EV, Osborn GE, Parkhurst SM. 2009. Wash functions downstream of Rho and links linear and branched actin nucleation factors. Development 136:2849-2860.
24. 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.
25. Marchand JB, Kaiser DA, Pollard TD, Higgs HN. 2001. Interaction of WASP/Scar proteins with actin and vertebrate Arp2/3 complex. Nat Cell Biol 3:76-82.
26. Maxfield FR, McGraw TE. 2004. Endocytic recycling. Nat Rev Mol Cell Biol 5:121-132.
27. Mayran N, Parton RG, Gruenberg J. 2003. Annexin II regulates multivesicular endosome biogenesis in the degradation pathway of animal cells. Embo J 22:3242-3253.
28. Merrifield CJ, Qualmann B, Kessels MM, Almers W. 2004. Neural Wiskott Aldrich Syndrome Protein (N-WASP) and the Arp2/3 complex are recruited to sites of clathrin-mediated endocytosis in cultured fibroblasts. Eur J Cell Biol 83:13-18.
29. Miki H, Sasaki T, Takai Y, Takenawa T. 1998. Induction of filopodium formation by a WASP-related actin-depolymerizing protein N-WASP. Nature 391:93-96.
30. Miki H, Yamaguchi H, Suetsugu S, Takenawa T. 2000. IRSp53 is an essential intermediate between Rac and WAVE in the regulation of membrane ruffling. Nature 408:732-735.
31. Morel E, Parton RG, Gruenberg J. 2009. Annexin A2-dependent polymerization of actin mediates endosome biogenesis. Dev Cell 16:445-457.
32. Orth JD, Krueger EW, Weller SG, McNiven MA. 2006. A novel endocytic mechanism of epidermal growth factor receptor sequestration and internalization. Cancer Res 66:3603-3610.
33. Osborne A, Flett A, Smythe E. 2005. Endocytosis assays in intact and permeabilized cells. Curr Protoc Cell Biol 11:18.
34. Perrais D, Merrifield CJ. 2005. Dynamics of endocytic vesicle creation. Dev Cell 9:581-592.
35. Perret E, Lakkaraju A, Deborde S, Schreiner R, Rodriguez-Boulan E. 2005. Evolving endosomes: How many varieties and why?Curr Opin Cell Biol 17:423-434.
36. Pollard TD, Borisy GG. 2003. Cellular motility driven by assembly and disassembly of actin filaments. Cell 112:453-465.
37. Prehoda KE, Scott JA, Mullins RD, Lim WA. 2000. Integration of multiple signals through cooperative regulation of the N-WASP-Arp2/3 complex. Science 290:801-806.
38. Robertson AS, Smythe E, Ayscough KR. 2009. Functions of actin in endocytosis. Cell Mol Life Sci 66:2049-2065.
39. Rodal AA, Kozubowski L, Goode BL, Drubin DG, Hartwig JH. 2005. Actin and septin ultrastructures at the budding yeast cell cortex. Mol Biol Cell 16:372-384.
40. 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.
41. Rozelle AL, Machesky LM, Yamamoto M, Driessens MH, Insall RH, Roth MG, Luby-Phelps K, Marriott G, Hall A, Yin HL. 2000. Phosphatidylinositol 4,5-bisphosphate induces actin-based movement of raft-enriched vesicles through WASP-Arp2/3. Curr Biol 10:311-320.
42. Sigismund S, Argenzio E, Tosoni D, Cavallaro E, Polo S, Di Fiore PP. 2008. Clathrin-mediated internalization is essential for sustained EGFR signaling but dispensable for degradation. Dev Cell 15:209-219.
43. Sigismund S, Woelk T, Puri C, Maspero E, Tacchetti C, Transidico P, Di Fiore PP, Polo S. 2005. Clathrin-independent endocytosis of ubiquitinated cargos. Proc Natl Acad Sci USA 102:2760-2765.
44. Snapper SB, Takeshima F, Anton I, Liu CH, Thomas SM, Nguyen D, Dudley D, Fraser H, Purich D, Lopez-Ilasaca M, Klein C, Davidson L, Bronson R, Mulligan RC, Southwick F, Geha R, Goldberg MB, Rosen FS, Hartwig JH, Alt FW. 2001. N-WASP deficiency reveals distinct pathways for cell surface projections and microbial actin-based motility. Nat Cell Biol 3:897-904.
45. Soldati T, Schliwa M. 2006. Powering membrane traffic in endocytosis and recycling. Nat Rev Mol Cell Biol 7:897-908. (Pubitemid 44871416)
46. Stenmark H. 2009. Rab GTPases as coordinators of vesicle traffic. Nat Rev Mol Cell Biol 10:513-525.
47. Stradal TE, Rottner K, Disanza A, Confalonieri S, Innocenti M, Scita G. 2004. Regulation of actin dynamics by WASP and WAVE family proteins. Trends Cell Biol 14:303-311. (Pubitemid 38798179)
48. Stradal TE, Scita G. 2006. Protein complexes regulating Arp2/3-mediated actin assembly. Curr Opin Cell Biol 18:4-10. (Pubitemid 43107601)
49. Suetsugu S, Kurisu S, Oikawa T, Yamazaki D, Oda A, Takenawa T. 2006. Optimization of WAVE2 complex-induced actin polymerization by membrane-bound IRSp53. PIP(3), and Rac. J Cell Biol 173:571-585. (Pubitemid 43765203)
50. Takenawa T, Suetsugu S. 2007. TheWASP-WAVE protein network: Connecting the membrane to the cytoskeleton. Nat RevMol Cell Biol 8:37-48. (Pubitemid 46012013)
51. Taunton J, Rowning BA, Coughlin ML, Wu M, Moon RT, Mitchison TJ, Larabell CA. 2000. Actin-dependent propulsion of endosomes and lysosomes by recruitment of N-WASP. J Cell Biol 148:519-530.
52. Welch MD, DePace AH, Verma S, Iwamatsu A, Mitchison TJ. 1997. The human Arp2/3 complex is composed of evolutionarily conserved subunits and is localized to cellular regions of dynamic actin filament assembly. J Cell Biol 138:375-384. (Pubitemid 27323539)
53. Welch MD, Mullins RD. 2002. Cellular control of actin nucleation. Annu Rev Cell Dev Biol 18:247-288.
54. Yarar D, Waterman-Storer CM, Schmid SL. 2005. A dynamic actin cytoskeleton functions at multiple stages of clathrin-mediated endocytosis. Mol Biol Cell 16:964-975.
55. Zuchero JB, Coutts AS, Quinlan ME, Thangue NB, Mullins RD. 2009. p53-cofactor JMY is a multifunctional actin nucleation factor. Nat Cell Biol 11:451-459.