Cofilin-induced Cooperative Conformational Changes of Actin Subunits Revealed Using Cofilin-actin Fusion Protein

Overview

Journal Sci Rep

Specialty Science

Date 2016 Feb 5

PMID 26842224

Citations 9

Authors

Nobuhisa Umeki

Keiko Hirose

Taro Q P Uyeda

Affiliations

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Abstract

To investigate cooperative conformational changes of actin filaments induced by cofilin binding, we engineered a fusion protein made of Dictyostelium cofilin and actin. The filaments of the fusion protein were functionally similar to actin filaments bound with cofilin in that they did not bind rhodamine-phalloidin, had quenched fluorescence of pyrene attached to Cys374 and showed enhanced susceptibility of the DNase loop to cleavage by subtilisin. Quantitative analyses of copolymers made of different ratios of the fusion protein and control actin further demonstrated that the fusion protein affects the structure of multiple neighboring actin subunits in copolymers. Based on these and other recent related studies, we propose a mechanism by which conformational changes induced by cofilin binding is propagated unidirectionally to the pointed ends of the filaments, and cofilin clusters grow unidirectionally to the pointed ends following this path. Interestingly, the fusion protein was unable to copolymerize with control actin at pH 6.5 and low ionic strength, suggesting that the structural difference between the actin moiety in the fusion protein and control actin is pH-sensitive.

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References

Ngo K, Kodera N, Katayama E, Ando T, Uyeda T . Cofilin-induced unidirectional cooperative conformational changes in actin filaments revealed by high-speed atomic force microscopy. Elife. 2015; 4. PMC: 4337605. DOI: 10.7554/eLife.04806. View

van Rheenen J, Song X, van Roosmalen W, Cammer M, Chen X, DesMarais V . EGF-induced PIP2 hydrolysis releases and activates cofilin locally in carcinoma cells. J Cell Biol. 2007; 179(6):1247-59. PMC: 2140025. DOI: 10.1083/jcb.200706206. View

Bonet C, Ternent D, Maciver S . Rapid formation and high diffusibility of actin-cofilin cofilaments at low pH. Eur J Biochem. 2000; 267(11):3378-84. DOI: 10.1046/j.1432-1327.2000.01372.x. View

Galkin V, Orlova A, Lukoyanova N, Wriggers W, Egelman E . Actin depolymerizing factor stabilizes an existing state of F-actin and can change the tilt of F-actin subunits. J Cell Biol. 2001; 153(1):75-86. PMC: 2185532. DOI: 10.1083/jcb.153.1.75. View

Dedova I, Dedov V, Nosworthy N, Hambly B, Dos Remedios C . Cofilin and DNase I affect the conformation of the small domain of actin. Biophys J. 2002; 82(6):3134-43. PMC: 1302102. DOI: 10.1016/S0006-3495(02)75655-5. View

Blondin L, Sapountzi V, Maciver S, Lagarrigue E, Benyamin Y, Roustan C . A structural basis for the pH-dependence of cofilin. F-actin interactions. Eur J Biochem. 2002; 269(17):4194-201. DOI: 10.1046/j.1432-1033.2002.03101.x. View

Yokoyama K, Hiratuka Y, Akimaru E, Hirose K, Uyeda T, Suzuki M . Design and functional analysis of actomyosin motor domain chimera proteins. Biochem Biophys Res Commun. 2002; 299(5):825-31. DOI: 10.1016/s0006-291x(02)02758-4. View

Bobkov A, Muhlrad A, Shvetsov A, Benchaar S, Scoville D, Almo S . Cofilin (ADF) affects lateral contacts in F-actin. J Mol Biol. 2004; 337(1):93-104. DOI: 10.1016/j.jmb.2004.01.014. View

Dedova I, Nikolaeva O, Mikhailova V, Dos Remedios C, Levitsky D . Two opposite effects of cofilin on the thermal unfolding of F-actin: a differential scanning calorimetric study. Biophys Chem. 2004; 110(1-2):119-28. DOI: 10.1016/j.bpc.2004.01.009. View

10.

Muhlrad A, Kudryashov D, Peyser Y, Bobkov A, Almo S, Reisler E . Cofilin induced conformational changes in F-actin expose subdomain 2 to proteolysis. J Mol Biol. 2004; 342(5):1559-67. DOI: 10.1016/j.jmb.2004.08.010. View

11.

Loscalzo J, Reed G, Weber A . Conformational change and cooperativity in actin filaments free of tropomyosin. Proc Natl Acad Sci U S A. 1975; 72(9):3412-5. PMC: 433003. DOI: 10.1073/pnas.72.9.3412. View

12.

Kouyama T, Mihashi K . Fluorimetry study of N-(1-pyrenyl)iodoacetamide-labelled F-actin. Local structural change of actin protomer both on polymerization and on binding of heavy meromyosin. Eur J Biochem. 1981; 114(1):33-8. View

13.

Miki M, Wahl P, Auchet J . Fluorescence anisotropy of labeled F-actin: influence of divalent cations on the interaction between F-actin and myosin heads. Biochemistry. 1982; 21(15):3661-5. DOI: 10.1021/bi00258a021. View

14.

Yonezawa N, Nishida E, Sakai H . pH control of actin polymerization by cofilin. J Biol Chem. 1985; 260(27):14410-2. View

15.

Yonezawa N, Nishida E, Maekawa S, Sakai H . Studies on the interaction between actin and cofilin purified by a new method. Biochem J. 1988; 251(1):121-7. PMC: 1148972. DOI: 10.1042/bj2510121. View

16.

Orlova A, Egelman E . Cooperative rigor binding of myosin to actin is a function of F-actin structure. J Mol Biol. 1997; 265(5):469-74. DOI: 10.1006/jmbi.1996.0761. View

17.

Smith L, Fiebig K, Schwalbe H, Dobson C . The concept of a random coil. Residual structure in peptides and denatured proteins. Fold Des. 1996; 1(5):R95-106. DOI: 10.1016/S1359-0278(96)00046-6. View

18.

McGough A, Pope B, Chiu W, Weeds A . Cofilin changes the twist of F-actin: implications for actin filament dynamics and cellular function. J Cell Biol. 1997; 138(4):771-81. PMC: 2138052. DOI: 10.1083/jcb.138.4.771. View

19.

Maciver S, Pope B, Whytock S, Weeds A . The effect of two actin depolymerizing factors (ADF/cofilins) on actin filament turnover: pH sensitivity of F-actin binding by human ADF, but not of Acanthamoeba actophorin. Eur J Biochem. 1998; 256(2):388-97. DOI: 10.1046/j.1432-1327.1998.2560388.x. View

20.

Visegrady B, Lorinczy D, Hild G, Somogyi B, Nyitrai M . A simple model for the cooperative stabilisation of actin filaments by phalloidin and jasplakinolide. FEBS Lett. 2004; 579(1):6-10. DOI: 10.1016/j.febslet.2004.11.023. View