Distinct Roles for the Actin Nucleators Arp2/3 and hDia1 during NK-Mediated Cytotoxicity

Current Biology

Volumn 19, Issue 22, 2009, Pages 1886-1896

  Butler, Boyd ^a   Cooper, John A ^a  

^a WASHINGTON UNIVERSITY SCHOOL OF MEDICINE   (United States)

Author keywords

CELLBIO; CELLIMMUNO

Indexed keywords

ACTIN RELATED PROTEIN 2-3 COMPLEX; DIAPH1 PROTEIN, HUMAN; FIBRONECTIN; INTEGRIN; INTERCELLULAR ADHESION MOLECULE 1; SIGNAL TRANSDUCING ADAPTOR PROTEIN;

ARTICLE; CELL ADHESION; CYTOTOXICITY; HUMAN; IMMUNOLOGY; METABOLISM; NATURAL KILLER CELL; PHYSIOLOGY; SIGNAL TRANSDUCTION;

ACTIN-RELATED PROTEIN 2-3 COMPLEX; ADAPTOR PROTEINS, SIGNAL TRANSDUCING; CELL ADHESION; CYTOTOXICITY, IMMUNOLOGIC; FIBRONECTINS; HUMANS; INTEGRINS; INTERCELLULAR ADHESION MOLECULE-1; KILLER CELLS, NATURAL; SIGNAL TRANSDUCTION;

EID: 70450248424     PISSN: 09609822     EISSN: None     Source Type: Journal    
DOI: 10.1016/j.cub.2009.10.029     Document Type: Article

References (38)

1. Higgs H.N., and Pollard T.D. Regulation of actin filament network formation through ARP2/3 complex: Activation by a diverse array of proteins. Annu. Rev. Biochem. 70 (2001) 649-676
2. Pollard T.D. Regulation of actin filament assembly by arp2/3 complex and formins. Annu. Rev. Biophys. Biomol. Struct. 36 (2007) 451-477
3. Li F., and Higgs H.N. The mouse Formin mDia1 is a potent actin nucleation factor regulated by autoinhibition. Curr. Biol. 13 (2003) 1335-1340
4. Goode B.L., and Eck M.J. Mechanism and function of formins in the control of actin assembly. Annu. Rev. Biochem. 76 (2007) 593-627
5. Yang C., Czech L., Gerboth S., Kojima S., Scita G., and Svitkina T. Novel roles of formin mDia2 in lamellipodia and filopodia formation in motile cells. PLoS Biol. 5 (2007) e317
6. Chhabra E.S., and Higgs H.N. The many faces of actin: Matching assembly factors with cellular structures. Nat. Cell Biol. 9 (2007) 1110-1121
7. Orange J.S., Ramesh N., Remold-O'Donnell E., Sasahara Y., Koopman L., Byrne M., Bonilla F.A., Rosen F.S., Geha R.S., and Strominger J.L. Wiskott-Aldrich syndrome protein is required for NK cell cytotoxicity and colocalizes with actin to NK cell-activating immunologic synapses. Proc. Natl. Acad. Sci. USA 99 (2002) 11351-11356
8. Orange J.S., Harris K.E., Andzelm M.M., Valter M.M., Geha R.S., and Strominger J.L. The mature activating natural killer cell immunologic synapse is formed in distinct stages. Proc. Natl. Acad. Sci. USA 100 (2003) 14151-14156
9. Kirwan S.E., and Burshtyn D.N. Regulation of natural killer cell activity. Curr. Opin. Immunol. 19 (2007) 46-54
10. Carpen O., Virtanen I., Lehto V.P., and Saksela E. Polarization of NK cell cytoskeleton upon conjugation with sensitive target cells. J. Immunol. 131 (1983) 2695-2698
11. Burkhardt J.K., McIlvain J.M.J., Sheetz M.P., and Argon Y. Lytic granules from cytotoxic T cells exhibit kinesin-dependent motility on microtubules in vitro. J. Cell Sci. 104 (1993) 151-162
12. Stinchcombe J.C., Majorovits E., Bossi G., Fuller S., and Griffiths G.M. Centrosome polarization delivers secretory granules to the immunological synapse. Nature 443 (2006) 462-465
13. Ishizaki T., Morishima Y., Okamoto M., Furuyashiki T., Kato T., and Narumiya S. Coordination of microtubules and the actin cytoskeleton by the Rho effector mDia1. Nat. Cell Biol. 3 (2001) 8-14
14. Eng C.H., Huckaba T.M., and Gundersen G.G. The formin mDia regulates GSK3beta through novel PKCs to promote microtubule stabilization but not MTOC reorientation in migrating fibroblasts. Mol. Biol. Cell 17 (2006) 5004-5016
15. Bartolini F., Moseley J.B., Schmoranzer J., Cassimeris L., Goode B.L., and Gundersen G.G. The formin mDia2 stabilizes microtubules independently of its actin nucleation activity. J. Cell Biol. 181 (2008) 523-536
16. Gomez T.S., Kumar K., Medeiros R.B., Shimizu Y., Leibson P.J., and Billadeau D.D. Formins regulate the actin-related protein 2/3 complex-independent polarization of the centrosome to the immunological synapse. Immunity 26 (2007) 177-190
17. Wen Y., Eng C.H., Schmoranzer J., Cabrera-Poch N., Morris E.J., Chen M., Wallar B.J., Alberts A.S., and Gundersen G.G. EB1 and APC bind to mDia to stabilize microtubules downstream of Rho and promote cell migration. Nat. Cell Biol. 6 (2004) 820-830
18. Eisenmann K.M., West R.A., Hildebrand D., Kitchen S.M., Peng J., Sigler R., Zhang J., Siminovitch K.A., and Alberts A.S. T cell responses in mammalian diaphanous-related formin mDia1 knock-out mice. J. Biol. Chem. 282 (2007) 25152-25158
19. Shi Y., Zhang J., Mullin M., Dong B., Alberts A.S., and Siminovitch K.A. The mDial formin is required for neutrophil polarization, migration, and activation of the LARG/RhoA/ROCK signaling axis during chemotaxis. J. Immunol. 182 (2009) 3837-3845
20. Takeya R., Taniguchi K., Narumiya S., and Sumimoto H. The mammalian formin FHOD1 is activated through phosphorylation by ROCK and mediates thrombin-induced stress fibre formation in endothelial cells. EMBO J. 27 (2008) 618-628
21. Gasteier J.E., Schroeder S., Muranyi W., Madrid R., Benichou S., and Fackler O.T. FHOD1 coordinates actin filament and microtubule alignment to mediate cell elongation. Exp. Cell Res. 306 (2005) 192-202
22. Gasteier J.E., Madrid R., Krautkramer E., Schroder S., Muranyi W., Benichou S., and Fackler O.T. Activation of the Rac-binding partner FHOD1 induces actin stress fibers via a ROCK-dependent mechanism. J. Biol. Chem. 278 (2003) 38902-38912
23. Eisenmann K.M., Harris E.S., Kitchen S.M., Holman H.A., Higgs H.N., and Alberts A.S. Dia-interacting protein modulates formin-mediated actin assembly at the cell cortex. Curr. Biol. 17 (2007) 579-591
24. Carpen O. The role of microtubules in human natural killer cell-mediated cytotoxicity. Cell. Immunol. 106 (1987) 376-386
25. Goulimari P., Knieling H., Engel U., and Grosse R. LARG and mDia1 link Galpha12/13 to cell polarity and microtubule dynamics. Mol. Biol. Cell 19 (2008) 30-40
26. Morrison E.E. Action and interactions at microtubule ends. Cell. Mol. Life Sci. 64 (2007) 307-317
27. Lewkowicz E., Herit F., Le Clainche C., Bourdoncle P., Perez F., and Niedergang F. The microtubule-binding protein CLIP-170 coordinates mDia1 and actin reorganization during CR3-mediated phagocytosis. J. Cell Biol. 183 (2008) 1287-1298
28. Liao G., and Gundersen G.G. Kinesin is a candidate for cross-bridging microtubules and intermediate filaments. Selective binding of kinesin to detyrosinated tubulin and vimentin. J. Biol. Chem. 273 (1998) 9797-9803
29. Hammond J.W., Cai D., and Verhey K.J. Tubulin modifications and their cellular functions. Curr. Opin. Cell Biol. 20 (2008) 71-76
30. Schulze E., Asai D.J., Bulinski J.C., and Kirschner M. Posttranslational modification and microtubule stability. J. Cell Biol. 105 (1987) 2167-2177
31. Machesky L.M., Reeves E., Wientjes F., Mattheyse F.J., Grogan A., Totty N.F., Burlingame A.L., Hsuan J.J., and Segal A.W. Mammalian actin-related protein 2/3 complex localizes to regions of lamellipodial protrusion and is composed of evolutionarily conserved proteins. Biochem. J. 328 (1997) 105-112
32. Bailly M., Ichetovkin I., Grant W., Zebda N., Machesky L.M., Segall J.E., and Condeelis J. The F-actin side binding activity of the Arp2/3 complex is essential for actin nucleation and lamellipod extension. Curr. Biol. 11 (2001) 620-625
33. Weaver A.M., Karginov A.V., Kinley A.W., Weed S.A., Li Y., Parsons J.T., and Cooper J.A. Cortactin promotes and stabilizes Arp2/3-induced actin filament network formation. Curr. Biol. 11 (2001) 370-374
34. Nicholson-Dykstra S.M., and Higgs H.N. Arp2 depletion inhibits sheet-like protrusions but not linear protrusions of fibroblasts and lymphocytes. Cell Motil. Cytoskeleton 65 (2008) 904-922
35. Sakata D., Taniguchi H., Yasuda S., Adachi-Morishima A., Hamazaki Y., Nakayama R., Miki T., Minato N., and Narumiya S. Impaired T lymphocyte trafficking in mice deficient in an actin-nucleating protein, mDia1. J. Exp. Med. 204 (2007) 2031-2038
36. Hudson B.I., Kalea A.Z., Del Mar Arriero M., Harja E., Boulanger E., D'Agati V., and Schmidt A.M. Interaction of the RAGE cytoplasmic domain with diaphanous-1 is required for ligand-stimulated cellular migration through activation of Rac1 and Cdc42. J. Biol. Chem. 283 (2008) 34457-34468
37. Butler B., Kastendieck D.H., and Cooper J.A. Differently phosphorylated forms of the cortactin homolog HS1 mediate distinct functions in natural killer cells. Nat. Immunol. 9 (2008) 887-897
38. Kuhn J.R., and Poenie M. Dynamic polarization of the microtubule cytoskeleton during CTL-mediated killing. Immunity 16 (2002) 111-121