MDia1-3 in mammalian filopodia

Communicative and Integrative Biology

Volumn 5, Issue 4, 2012, Pages 340-344

  Goh, Wah Ing ^a,b   Ahmed, Sohail ^a,b  

^a INSTITUTE OF MEDICAL BIOLOGY   (Singapore)

^b Immunos ^*  (Singapore)

Author keywords

Actin; Cell morphology; Filopodia; Formins; MDia; Rho GTPases

Indexed keywords

MAMMALIA;

EID: 84869746159     PISSN: 19420889     EISSN: 19420889     Source Type: Journal    
DOI: 10.4161/cib.20214     Document Type: Article

References (56)

1. Mellor H. The role of formins in filopodia formation. Biochim Biophys Acta 2009; 1803:191-200.
2. Young KG, Copeland JW. Formins in cell signaling. Biochim Biophys Acta 2010; 1803:183-90.
3. Higgs HN. Formin proteins: a domain-based approach. Trends Biochem Sci 2005; 30:342-53; http://dx.doi.org/10.1016/j.tibs.2005.04.014
4. Takeya R, Taniguchi K, Narumiya S, Sumimoto H. The mammalian formin FHOD1 is activated through phosphorylation by ROCK and mediates thrombininduced stress fibre formation in endothelial cells. EMBO J 2008; 27:618-28; http:// dx.doi.org/10.1038/emboj.2008.7
5. Ramalingam N, Zhao H, Breitsprecher D, Lappalainen P, Faix J, Schleicher M. Phospholipids regulate localization and activity of mDia1 formin. Eur J Cell Biol 2010; 89:723-32; http://dx.doi. org/10.1016/j.ejcb.2010.06.001
6. Liu W, Sato A, Khadka D, Bharti R, Diaz H, Runnels LW, et al. Mechanism of activation of the Formin protein Daam1. Proc Natl Acad Sci U S A 2008; 105:210-5; http://dx.doi.org/10. 1073/pnas.0707277105
7. Goh WI, Sudhaharan T, Lim KB, Sem KP, Lau CL, Ahmed S. Rif-mDia1 interaction is involved in filopodium formation independent of Cdc42 and Rac effectors. J Biol Chem 2011; 286:13681-94; http://dx.doi.org/10.1074/jbc.M110.182683
8. Yang C, Czech L, Gerboth S, Kojima S, Scita G, Svitkina T. Novel roles of formin mDia2 in lamellipodia and filopodia formation in motile cells. PLoS Biol 2007; 5:e317; http://dx.doi.org/10. 1371/journal.pbio.0050317
9. Pellegrin S, Mellor H. The Rho family GTPase Rif induces filopodia through mDia2. Curr Biol 2005; 15:129-33; http://dx.doi.org/10. 1016/j.cub.2005.01.011
10. Yasuda S, Oceguera-Yanez F, Kato T, Okamoto M, Yonemura S, Terada Y, et al. Cdc42 and mDia3 regulate microtubule attachment to kinetochores. Nature 2004; 428:767-71; http:// dx.doi.org/10.1038/nature02452
11. Watanabe N, Kato T, Fujita A, Ishizaki T, Narumiya S. Cooperation between mDia1 and ROCK in Rhoinduced actin reorganization. Nat Cell Biol 1999; 1:136-43; http://dx.doi.org/10. 1038/11056
12. Hotulainen P, Lappalainen P. Stress fibers are generated by two distinct actin assembly mechanisms in motile cells. J Cell Biol 2006; 173:383-94; http://dx.doi.org/10.1083/jcb.200511093
13. Wallar BJ, Deward AD, Resau JH, Alberts AS. RhoB and the mammalian Diaphanous-related formin mDia2 in endosome trafficking. Exp Cell Res 2007; 313:560-71; http://dx.doi.org/10.1016/j. yexcr.2006.10.033
14. Watanabe S, Ando Y, Yasuda S, Hosoya H, Watanabe N, Ishizaki T, et al. mDia2 induces the actin scaffold for the contractile ring and stabilizes its position during cytokinesis in NIH 3T3 cells. Mol Biol Cell 2008; 19:2328-38; http://dx.doi.org/10. 1091/mbc.E07-10-1086
15. Zaoui K, Honoré S, Isnardon D, Braguer D, Badache A. Memo-RhoA-mDia1 signaling controls microtubules, the actin network, and adhesion site formation in migrating cells. J Cell Biol 2008; 183:401-8; http://dx.doi.org/10.1083/jcb.200805107
16. Goh WI, Lim KB, Sudhaharan T, Sem KP, Bu W, Chou AM, et al. mDia1 and WAVE2 proteins interact directly with IRSp53 in filopodia and are involved in filopodium formation. J Biol Chem 2012; 287:4702-14; http://dx.doi.org/10.1074/jbc. M111.305102
17. Urban E, Jacob S, Nemethova M, Resch GP, Small JV. Electron tomography reveals unbranched networks of actin filaments in lamellipodia. Nat Cell Biol 2010; 12:429-35; http://dx.doi.org/10. 1038/ncb2044
18. Lizárraga F, Poincloux R, Romao M, Montagnac G, Le Dez G, Bonne I, et al. Diaphanous-related formins are required for invadopodia formation and invasion of breast tumor cells. Cancer Res 2009; 69:2792-800; http://dx.doi.org/10.1158/0008-5472.CAN-08-3709
19. Hotulainen P, LlanoO, Smirnov S, Tanhuanpää K, Faix J, Rivera C, et al. Defining mechanisms of actin polymerization and depolymerization during dendritic spine morphogenesis. J Cell Biol 2009; 185:323-39; http://dx.doi.org/10.1083/jcb.200809046
20. Colucci-Guyon E, Niedergang F, Wallar BJ, Peng J, Alberts AS, Chavrier P. A role for mammalian diaphanous-related formins in complement receptor (CR3)-mediated phagocytosis in macrophages. Curr Biol 2005; 15:2007-12; http://dx. doi.org/10.1016/j.cub.2005.09.051
21. Peng J, Wallar BJ, Flanders A, Swiatek PJ, Alberts AS. Disruption of the Diaphanous-related formin Drf1 gene encoding mDia1 reveals a role for Drf3 as an effector for Cdc42. Curr Biol 2003; 13:534-45; http://dx.doi.org/10.1016/S0960-9822(03) 00170-2
22. Block J, Stradal TE, Hänisch J, Geffers R, Köstler SA, Urban E, et al. Filopodia formation induced by active mDia2/Drf3. J Microsc 2008; 231:506-17; http://dx.doi.org/10.1111/j.1365-2818. 2008.02063.x
23. Faix J, Breitsprecher D, Stradal TE, Rottner K. Filopodia: Complex models for simple rods. Int J Biochem Cell Biol 2009; 41:1656-64; http://dx.doi.org/10.1016/j.biocel.2009. 02.012
24. Kovar DR, Harris ES, Mahaffy R, Higgs HN, Pollard TD. Control of the assembly of ATP- and ADP-actin by formins and profilin. Cell 2006; 124:423-35; http://dx.doi.org/10.1016/j.cell. 2005.11.038
25. Medalia O, Beck M, Ecke M, Weber I, Neujahr R, Baumeister W, et al. Organization of actin networks in intact filopodia. Curr Biol 2007; 17:79-84; http://dx.doi.org/10.1016/j.cub.2006.11. 022
26. Lim KB, Bu W, Goh WI, Koh E, Ong SH, Pawson T, et al. The Cdc42 effector IRSp53 generates filopodia by coupling membrane protrusion with actin dynamics. J Biol Chem 2008; 283:20454-72; http://dx.doi.org/10.1074/jbc.M710185200
27. Fan L, Pellegrin S, Scott A, Mellor H. The small GTPase Rif is an alternative trigger for the formation of actin stress fibers in epithelial cells. J Cell Sci 2010; 123:1247-52; http://dx.doi.org/10. 1242/jcs.061754
28. Tominaga T, Sahai E, Chardin P, McCormick F, Courtneidge SA, Alberts AS. Diaphanous-related formins bridge Rho GTPase and Src tyrosine kinase signaling. Mol Cell 2000; 5:13-25; http://dx.doi.org/10.1016/S1097-2765(00)80399-8
29. Nemethova M, Auinger S, Small JV. Building the actin cytoskeleton: filopodia contribute to the construction of contractile bundles in the lamella. J Cell Biol 2008; 180:1233-44; http://dx.doi.org/10. 1083/jcb.200709134
30. Vetterkind S, Miki H, Takenawa T, Klawitz I, Scheidtmann KH, Preuss U. The rat homologue of Wiskott-Aldrich syndrome protein (WASP)-interacting protein (WIP) associates with actin filaments, recruits N-WASP from the nucleus, and mediates mobilization of actin from stress fibers in favor of filopodia formation. J Biol Chem 2002; 277:87-95; http:// dx.doi.org/10.1074/jbc.M104555200
31. Ryu JR, Echarri A, Li R, Pendergast AM. Regulation of cell-cell adhesion by Abi/Diaphanous complexes. Mol Cell Biol 2009; 29:1735-48; http:// dx.doi.org/10.1128/MCB.01483-08
32. Wen Y, Eng CH, Schmoranzer J, Cabrera-Poch N, Morris EJ, Chen M, et al. EB1 and APC bind to mDia to stabilize microtubules downstream of Rho and promote cell migration. Nat Cell Biol 2004; 6:820-30; http://dx.doi.org/10.1038/ ncb1160
33. Lewkowicz E, Herit F, Le Clainche C, Bourdoncle P, Perez F, Niedergang F. The microtubule-binding protein CLIP-170 coordinates mDia1 and actin reorganization during CR3-mediated phagocytosis. J Cell Biol 2008; 183:1287-98; http://dx.doi.org/10.1083/jcb.200807023
34. Satoh S, Tominaga T. mDia-interacting protein acts downstream of Rho-mDia and modifies Src activation and stress fiber formation. J Biol Chem 2001; 276: 39290-4; http://dx.doi.org/10. 1074/jbc.M107026200
35. Eisenmann KM, Harris ES, Kitchen SM, Holman HA, Higgs HN, Alberts AS. Dia-interacting protein modulates formin-mediated actin assembly at the cell cortex. Curr Biol 2007; 17:579-91; http:// dx.doi.org/10.1016/j.cub.2007.03.024
36. Aspenström P, Richnau N, Johansson AS. The diaphanous-related formin DAAM1 collaborates with the Rho GTPases RhoA and Cdc42, CIP4 and Src in regulating cell morphogenesis and actin dynamics. Exp Cell Res 2006; 312:2180-94; http:// dx.doi.org/10.1016/j.yexcr.2006.03.013
37. Brandt DT, Marion S, Griffiths G, Watanabe T, Kaibuchi K, Grosse R. Dia1 and IQGAP1 interact in cell migration and phagocytic cup formation. J Cell Biol 2007; 178:193-200; http://dx.doi. org/10.1083/jcb.200612071
38. Fujiwara T, Mammoto A, Kim Y, Takai Y. Rho small G-protein-dependent binding of mDia to an Src homology 3 domain-containing IRSp53/BAIAP2. Biochem Biophys Res Commun 2000; 271:626-9; http://dx.doi.org/10.1006/bbrc. 2000.2671
39. Tominaga T, Meng W, Togashi K, Urano H, Alberts AS, Tominaga M. The Rho GTPase effector protein, mDia, inhibits the DNA binding ability of the transcription factor Pax6 and changes the pattern of neurite extension in cerebellar granule cells through its binding to Pax6. J Biol Chem 2002; 277:47686-91; http://dx.doi.org/10.1074/jbc. M207539200
40. Eng CH, Huckaba TM, Gundersen GG. The formin mDia regulates GSK3beta through novel PKCs to promote microtubule stabilization but not MTOC reorientation in migrating fibroblasts. Mol Biol Cell 2006; 17:5004-16; http://dx.doi. org/10.1091/mbc.E05-10-0914
41. Rundle DR, Gorbsky G, Tsiokas L. PKD2 interacts and co-localizes with mDia1 to mitotic spindles of dividing cells: role of mDia1 IN PKD2 localization to mitotic spindles. J Biol Chem 2004; 279:29728-39; http://dx.doi.org/10.1074/jbc. M400544200
42. Xie Y, Tan EJ, Wee S, Manser E, Lim L, Koh CG. Functional interactions between phosphatase POPX2 and mDia modulate RhoA pathways. J Cell Sci 2008; 121:514-21; http://dx.doi.org/10. 1242/jcs.013557
43. Watanabe N, Madaule P, Reid T, Ishizaki T, Watanabe G, Kakizuka A, et al. p140mDia, a mammalian homolog of Drosophila diaphanous, is a target protein for Rho small GTPase and is a ligand for profilin. EMBO J 1997; 16:3044-56; http:// dx.doi.org/10.1093/emboj/16.11.3044
44. Yamana N, Arakawa Y, Nishino T, Kurokawa K, Tanji M, Itoh RE, et al. The Rho-mDia1 pathway regulates cell polarity and focal adhesion turnover in migrating cells through mobilizing Apc and c-Src. Mol Cell Biol 2006; 26:6844-58; http://dx.doi. org/10.1128/MCB.00283-06
45. Grosse R, Copeland JW, Newsome TP, Way M, Treisman R. A role for VASP in RhoA-Diaphanous signalling to actin dynamics and SRF activity. EMBO J 2003; 22:3050-61; http://dx.doi. org/10.1093/emboj/cdg287
46. Watanabe S, Okawa K, Miki T, Sakamoto S, Morinaga T, Segawa K, et al. Rho and anillin-dependent control of mDia2 localization and function in cytokinesis. Mol Biol Cell 2010; 21:3193-204; http://dx.doi.org/10.1091/mbc.E10-04-0324
47. Alberts AS, Bouquin N, Johnston LH, Treisman R. Analysis of RhoA-binding proteins reveals an interaction domain conserved in heterotrimeric G protein beta subunits and the yeast response regulator protein Skn7. J Biol Chem 1998; 273:8616-22; http://dx.doi.org/10.1074/jbc.273.15.8616
48. Destaing O, Saltel F, Gilquin B, Chabadel A, Khochbin S, Ory S, et al. A novel Rho-mDia2-HDAC6 pathway controls podosome patterning through microtubule acetylation in osteoclasts. J Cell Sci 2005; 118:2901-11; http://dx.doi.org/10.1242/jcs.02425
49. Miki T, Okawa K, Sekimoto T, Yoneda Y, Watanabe S, Ishizaki T, et al. mDia2 shuttles between the nucleus and the cytoplasm through the importin-alpha/betaand CRM1-mediated nuclear transport mechanism. J Biol Chem 2009; 284:5753-62; http://dx.doi.org/10.1074/jbc.M806191200
50. Sun H, Schlondorff JS, Brown EJ, Higgs HN, Pollak MR. Rho activation of mDia formins is modulated by an interaction with inverted formin 2 (INF2). Proc Natl Acad Sci U S A 2011; 108:2933-8; http://dx.doi.org/10.1073/pnas. 1017010108
51. Ji P, Jayapal SR, Lodish HF. Enucleation of cultured mouse fetal erythroblasts requires Rac GTPases and mDia2. Nat Cell Biol 2008; 10:314-21; http://dx.doi.org/10.1038/ncb1693
52. DeWard AD, Alberts AS. Ubiquitin-mediated degradation of the formin mDia2 upon completion of cell division. J Biol Chem 2009; 284:20061-9; http://dx.doi.org/10.1074/jbc.M109.000885
53. Beli P, Mascheroni D, Xu D, Innocenti M. WAVE and Arp2/3 jointly inhibit filopodium formation by entering into a complex with mDia2. Nat Cell Biol 2008; 10:849-57; http://dx.doi.org/10. 1038/ncb1745
54. Cheng L, Mao Y. mDia3-EB1-APC: A connection between kinetochores and microtubule plus ends. Commun Integr Biol 2011; 4:480-2
55. Behnen M, Murk K, Kursula P, Cappallo-Obermann H, Rothkegel M, Kierszenbaum AL, et al. Testisexpressed profilins 3 and 4 show distinct functional characteristics and localize in the acroplaxome-manchette complex in spermatids. BMC Cell Biol 2009; 10:34; http://dx.doi.org/10.1186/ 1471-2121-10-34
56. Zhang SM, Miao SY, Wang LF, Koide SS. Evidence for the binding of a human sperm component with diaphanous protein. Arch Androl 2001; 46:29-35; http://dx.doi.org/10.1080/ 01485010150211128