Actin-capping protein promotes microtubule stability by antagonizing the actin activity of mDia1

Molecular Biology of the Cell

Volumn 23, Issue 20, 2012, Pages 4032-4040

  Bartolini, Francesca ^a   Ramalingam, Nagendran ^a   Gundersen, Gregg G ^a  

^a NewYork Presbyterian Hospital   (United States)

Author keywords

[No Author keywords available]

Indexed keywords

ACTIN; ACTIN CAPPING PROTEIN; PROTEIN MDIA1; REGULATOR PROTEIN; UNCLASSIFIED DRUG;

ACTIN FILAMENT; ACTIN POLYMERIZATION; ARTICLE; FIBROBLAST; HUMAN; MICROTUBULE; NONHUMAN; PRIORITY JOURNAL; PROTEIN DOMAIN; PROTEIN FUNCTION; PROTEIN LOCALIZATION; PROTEIN PROTEIN INTERACTION;

ACTIN CAPPING PROTEINS; ACTINS; ANIMALS; BICYCLO COMPOUNDS, HETEROCYCLIC; CARRIER PROTEINS; DEPSIPEPTIDES; GENES, DOMINANT; GLUTAMIC ACID; INTEGRINS; MICE; MICROTUBULE-ASSOCIATED PROTEINS; MICROTUBULES; NIH 3T3 CELLS; RHO GTP-BINDING PROTEINS; SIGNAL TRANSDUCTION; THIAZOLIDINES; TYROSINE;

EID: 84867477942     PISSN: 10591524     EISSN: 19394586     Source Type: Journal    
DOI: 10.1091/mbc.E12-05-0338     Document Type: Article

References (42)

1. Balzer EM, Whipple RA, Cho EH, Matrone MA, Martin SS (2010). Antimitotic chemotherapeutics promote adhesive responses in detached and circulating tumor cells. Breast Cancer Res Treat 121, 65-78.
2. Bartolini F, Gundersen GG (2010). Formins and microtubules. Biochim Biophys Acta 1803, 164-173.
3. Bartolini F, Moseley JB, Schmoranzer J, Cassimeris L, Goode BL, Gundersen GG (2008). The formin mDia2 stabilizes microtubules independently of its actin nucleation activity. J Cell Biol 181, 523-536. (Pubitemid 351645041)
4. Bradke F, Dotti CG (1999). The role of local actin instability in axon formation. Science 283, 1931-1934.
5. Cheng L, Zhang J, Ahmad S, Rozier L, Yu H, Deng H, Mao Y (2011). Aurora B regulates formin mDia3 in achieving metaphase chromosome alignment. Dev Cell 20, 342-352.
6. Chesarone M, Gould CJ, Moseley JB, Goode BL (2009). Displacement of formins from growing barbed ends by bud14 is critical for actin cable architecture and function. Dev Cell 16, 292-302.
7. Chesarone-Cataldo M, Guerin C, Yu JH, Wedlich-Soldner R, Blanchoin L, Goode BL (2011). The myosin passenger protein smy1 controls actin cable structure and dynamics by acting as a formin damper. Dev Cell 21, 217-230.
8. Cook TA, Nagasaki T, Gundersen GG (1998). Rho guanosine triphosphatase mediates the selective stabilization of microtubules induced by lysophosphatidic acid. J Cell Biol 141, 175-185. (Pubitemid 28182650)
9. Cooper JA, Pollard TD (1985). Effect of capping protein on the kinetics of actin polymerization. Biochemistry 24, 793-799. (Pubitemid 15142262)
10. Cooper JA, Sept D (2008). New insights into mechanism and regulation of actin capping protein. Int Rev Cell Mol Biol 267, 183-206.
11. Dunn S, Morrison EE, Liverpool TB, Molina-Paris C, Cross RA, Alonso MC, Peckham M (2008). Differential trafficking of Kif5c on tyrosinated and detyrosinated microtubules in live cells. J Cell Sci 121, 1085-1095. (Pubitemid 351639427)
12. Eng CH, Huckaba TM, Gundersen GG (2006). The formin mDia regulates GSK3β through novel PKCs to promote microtubule stabilization but not MTOC reorientation in migrating fibroblasts. Mol Biol Cell 17, 5004-5016. (Pubitemid 44907346)
13. Enomoto T (1996). Microtubule disruption induces the formation of actin stress fibers and focal adhesions in cultured cells: possible involvement of the rho signal cascade. Cell Struct Funct 21, 317-326.
14. Gaillard J, Ramabhadran V, Neumanne E, Gurel P, Blanchoin L, Vantard M, Higgs HN (2011). Differential interactions of the formins INF2, mDia1, and mDia2 with microtubules. Mol Biol Cell 22, 4575-4587.
15. Goode BL, Eck MJ (2007). Mechanism and function of formins in the control of actin assembly. Annu Rev Biochem 76, 593-627.
16. Goulimari P, Kitzing TM, Knieling H, Brandt DT, Offermanns S, Grosse R (2005). Gα12/13 is essential for directed cell migration and localized Rho-Dia1 function. J Biol Chem 280, 42242-42251. (Pubitemid 43023195)
17. Gundersen GG, Bulinski JC (1988). Selective stabilization of microtubules oriented toward the direction of cell migration. Proc Natl Acad Sci USA 85, 5946-5950.
18. Gundersen GG, Gomes ER, Wen Y (2004). Cortical control of microtubule stability and polarization. Curr Opin Cell Biol 16, 106-112. (Pubitemid 38368160)
19. Gundersen GG, Kalnoski MH, Bulinski JC (1984). Distinct populations of microtubules: tyrosinated and nontyrosinated alpha tubulin are distributed differently in vivo. Cell 38, 779-789. (Pubitemid 15176108)
20. Gundersen GG, Khawaja S, Bulinski JC (1987). Postpolymerization detyrosination of alpha tubulin: a mechanism for subcellular differentiation of microtubules. J Cell Biol 105, 251-264.
21. Gundersen GG, Kim I, Chapin CJ (1994). Induction of stable microtubules in 3T3 fibroblasts by TGF-β and serum. J Cell Sci 107, 645-659. (Pubitemid 24091869)
22. Gurland G, Gundersen GG (1995). Stable, detyrosinated microtubules function to localize vimentin intermediate filaments in fibroblasts. J Cell Biol 131, 1275-1290.
23. Higashida C, Miyoshi T, Fujita A, Oceguera-Yanez F, Monypenny J, Andou Y, Narumiya S, Watanabe N (2004). Actin polymerization-driven molecular movement of mDia1 in living cells. Science 303, 2007-2010. (Pubitemid 38393274)
24. Higashida C, Suetsugu S, Tsuji T, Monypenny J, Narumiya S, Watanabe N (2008). G-actin regulates rapid induction of actin nucleation by mDia1 to restore cellular actin polymers. J Cell Sci 121, 3403-3412.
25. Infante AS, Stein MS, Zhai Y, Borisy GG, Gundersen GG (2000). Detyrosinated (Glu) microtubules are stabilized by an ATP-sensitive plus-end cap. J Cell Sci 113, 3907-3919. (Pubitemid 32194516)
26. Kato T, Watanabe N, Morishima Y, Fujita A, Ishizaki T, Narumiya S (2001). Localization of a mammalian homolog of diaphanous, mDia1, to the mitotic spindle in HeLa cells. J Cell Sci 114, 775-784. (Pubitemid 32237150)
27. Khawaja S, Gundersen GG, Bulinski JC (1988). Enhanced stability of microtubules enriched in detyrosinated tubulin is not a direct function of detyrosination level. J Cell Biol 106, 141-149. (Pubitemid 18051401)
28. Kreitzer G, Liao G, Gundersen GG (1999). Detyrosination of tubulin regulates the interaction of intermediate filaments with microtubules in vivo via a kinesin-dependent mechanism. Mol Biol Cell 10, 1105-1118. (Pubitemid 29193734)
29. Li R, Gundersen GG (2008). Beyond polymer polarity: how the cytoskeleton builds a polarized cell. Nat Rev Mol Cell Biol 9, 860-873.
30. Lin SX, Gundersen GG, Maxfield FR (2002). Export from pericentriolar endocytic recycling compartment to cell surface depends on stable, detyrosinated (glu) microtubules and kinesin. Mol Biol Cell 13, 96-109. (Pubitemid 34106061)
31. Mejillano MR, Kojima S, Applewhite DA, Gertler FB, Svitkina TM, Borisy GG (2004). Lamellipodial versus filopodial mode of the actin nanomachinery: pivotal role of the filament barbed end. Cell 118, 363-373. (Pubitemid 39061116)
32. Okada K, Bartolini F, Deaconescu AM, Moseley JB, Dogic Z, Grigorieff N, Gundersen GG, Goode BL (2010). Adenomatous polyposis coli protein nucleates actin assembly and synergizes with the formin mDia1. J Cell Biol 189, 1087-1096.
33. Palazzo AF, Cook TA, Alberts AS, Gundersen GG (2001). mDia mediates Rho-regulated formation and orientation of stable microtubules. Nat Cell Biol 3, 723-729. (Pubitemid 32734250)
34. Palazzo AF, Eng CH, Schlaepfer DD, Marcantonio EE, Gundersen GG (2004). Localized stabilization of microtubules by integrin- and FAK-facilitated Rho signaling. Science 303, 836-839. (Pubitemid 38174661)
35. Reed NA, Cai D, Blasius TL, Jih GT, Meyhofer E, Gaertig J, Verhey KJ (2006). Microtubule acetylation promotes kinesin-1 binding and transport. Curr Biol 16, 2166-2172. (Pubitemid 44692098)
36. Ren XD, Kiosses WB, Schwartz MA (1999). Regulation of the small GTP-binding protein Rho by cell adhesion and the cytoskeleton. EMBO J 18, 578-585. (Pubitemid 29057242)
37. Rosales-Nieves AE, Johndrow JE, Keller LC, Magie CR, Pinto-Santini DM, Parkhurst SM (2006). Coordination of microtubule and microfilament dynamics by Drosophila Rho1, Spire and Cappuccino. Nat Cell Biol 8, 367-376.
38. Rundle DR, Gorbsky G, Tsiokas L (2004). 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 279, 29728-29739. (Pubitemid 38915856)
39. Watanabe S, Ando Y, Yasuda S, Hosoya H, Watanabe N, Ishizaki T, Narumiya S (2008). mDia2 induces the actin scaffold for the contractile ring and stabilizes its position during cytokinesis in NIH 3T3 cells. Mol Biol Cell 19, 2328-2338.
40. Webster DR, Gundersen GG, Bulinski JC, Borisy GG (1987). Differential turnover of tyrosinated and detyrosinated microtubules. Proc Natl Acad Sci USA 84, 9040-9044.
41. Wen Y, Eng CH, Schmoranzer J, Cabrera-Poch N, Morris EJ, Chen M, Wallar BJ, Alberts AS, Gundersen GG (2004). EB1 and APC bind to mDia to stabilize microtubules downstream of Rho and promote cell migration. Nat Cell Biol 6, 820-830. (Pubitemid 39207247)
42. Yang C, Czech L, Gerboth S, Kojima S, Scita G, Svitkina T (2007). Novel roles of formin mDia2 in lamellipodia and filopodia formation in motile cells. PLoS Biol 5, e317.