Abstract
ADF/cofilins disassemble the actin filament and contribute to a wide range of actin dynamics. These proteins are regulated by several factors, including phosphorylation, pH and mechanical forces. Although the cofilin-decorated actin filament structure was published recently, the mechanisms of these regulating factors remain unclear. Models that describe regulation based on the latest structural data and research will be discussed. Aspects about the interaction between actin and cofilin that require further investigation are also discussed.
This is a preview of subscription content, log in via an institution to check access.
Similar content being viewed by others
References
Abe H, Obinata T, Minamide LS, Bamburg JR (1996) Xenopus laevis actin-depolymerizing factor/cofilin: a phosphorylation-regulated protein essential for development. J Cell Biol 132:871–885
Aggeli D et al (2014) Coordination of the filament stabilizing versus destabilizing activities of cofilin through its secondary binding site on actin. Cytoskeleton (Hoboken) 71:361–379. https://doi.org/10.1002/cm.21178
Bernstein BW, Painter WB, Chen H, Minamide LS, Abe H, Bamburg JR (2000) Intracellular pH modulation of ADF/cofilin proteins. Cell Motil Cytoskelet 47:319–336
Bobkov AA, Muhlrad A, Pavlov DA, Kokabi K, Yilmaz A, Reisler E (2006) Cooperative effects of cofilin (ADF) on actin structure suggest allosteric mechanism of cofilin function. J Mol Biol 356:325–334. https://doi.org/10.1016/j.jmb.2005.11.072
Carlier MF et al (1997) Actin depolymerizing factor (ADF/cofilin) enhances the rate of filament turnover: implication in actin-based motility. J Cell Biol 136:1307–1322
Dumpich M, Mannherz HG, Theiss C (2015) VEGF signaling regulates cofilin and the Arp2/3-complex within the axonal growth cone. Curr Neurovasc Res 12:293–307
Durer ZA, Kudryashov DS, Sawaya MR, Altenbach C, Hubbell W, Reisler E (2012) Structural states and dynamics of the D-loop in actin. Biophys J 103:930–939. https://doi.org/10.1016/j.bpj.2012.07.030
Egelman EH, Francis N, DeRosier DJ (1982) F-actin is a helix with a random variable twist. Nature 298:131–135
Elam WA et al (2017) Phosphomimetic S3D cofilin binds but only weakly severs actin filaments. J Biol Chem 292:19565–19579. https://doi.org/10.1074/jbc.m117.808378
Fass J, Gehler S, Sarmiere P, Letourneau P, Bamburg JR (2004) Regulating filopodial dynamics through actin-depolymerizing factor/cofilin. Anat Sci Int 79:173–183. https://doi.org/10.1111/j.1447-073x.2004.00087.x
Gressin L, Guillotin A, Guerin C, Blanchoin L, Michelot A (2015) Architecture dependence of actin filament network disassembly. Curr Biol 25:1437–1447. https://doi.org/10.1016/j.cub.2015.04.011
Hayakawa K, Tatsumi H, Sokabe M (2011) Actin filaments function as a tension sensor by tension-dependent binding of cofilin to the filament. J Cell Biol 195:721–727. https://doi.org/10.1083/jcb.201102039
Holmes KC, Popp D, Gebhard W, Kabsch W (1990) Atomic model of the actin filament. Nature 347:44–49
Huehn A, Cao W, Elam WA, Liu X, De La Cruz EM, Sindelar CV (2018) The actin filament twist changes abruptly at boundaries between bare and cofilin-decorated segments. J Biol Chem 293:5377–5383. https://doi.org/10.1074/jbc.AC118.001843
Humphrey W, Dalke A, Schulten K (1996) VMD: visual molecular dynamics. J Mol Graph 14(33–38):27–38
Kabsch W, Mannherz HG, Suck D, Pai EF, Holmes KC (1990) Atomic structure of the actin: DNase I complex. Nature 347:37–44
Kanellos G, Frame MC (2016) Cellular functions of the ADF/cofilin family at a glance. J Cell Sci 129:3211–3218. https://doi.org/10.1242/jcs.187849
Klejnot M et al (2013) Analysis of the human cofilin 1 structure reveals conformational changes required for actin binding. Acta Crystallogr Sect D 69:1780–1788. https://doi.org/10.1107/S0907444913014418
Kremneva E, Makkonen MH, Skwarek-Maruszewska A, Gateva G, Michelot A, Dominguez R, Lappalainen P (2014) Cofilin-2 controls actin filament length in muscle sarcomeres. Dev Cell 31:215–226. https://doi.org/10.1016/j.devcel.2014.09.002
Loisel TP, Boujemaa R, Pantaloni D, Carlier MF (1999) Reconstitution of actin-based motility of Listeria and Shigella using pure proteins. Nature 401:613–616
Matsushita S, Inoue Y, Hojo M, Sokabe M, Adachi T (2011) Effect of tensile force on the mechanical behavior of actin filaments. J Biomech 44:1776–1781. https://doi.org/10.1016/j.jbiomech.2011.04.012
Mizuno H, Higashida C, Yuan Y, Ishizaki T, Narumiya S, Watanabe N (2011) Rotational movement of the formin mDia1 along the double helical strand of an actin filament. Science. 331:80–83. https://doi.org/10.1126/science.1197692
Mizuno H, Tanaka K, Yamashiro S, Narita A, Watanabe N (2018) Helical rotation of the diaphanous-related formin mDia1 generates actin filaments resistant to cofilin. Proc Natl Acad Sci USA 115:E5000–E5007. https://doi.org/10.1073/pnas.1803415115
Nagaoka R, Abe H, Obinata T (1996) Site-directed mutagenesis of the phosphorylation site of cofilin: its role in cofilin-actin interaction and cytoplasmic localization. Cell Motil Cytoskelet 35:200–209
Nakano K, Mabuchi I (2006) Actin-depolymerizing protein Adf1 is required for formation and maintenance of the contractile ring during cytokinesis in fission yeast. Mol Biol Cell 17:1933–1945. https://doi.org/10.1091/mbc.e05-09-0900
Ngo KX, Kodera N, Katayama E, Ando T, Uyeda TQ (2015) Cofilin-induced unidirectional cooperative conformational changes in actin filaments revealed by high-speed atomic force microscopy. eLife. https://doi.org/10.7554/elife.04806
Ngo KX et al (2016) Allosteric regulation by cooperative conformational changes of actin filaments drives mutually exclusive binding with cofilin and myosin. Sci Rep 6:35449. https://doi.org/10.1038/srep35449
Nishizaka T, Yagi T, Tanaka Y, Ishiwata S (1993) Right-handed rotation of an actin filament in an in vitro motile system. Nature 361:269–271. https://doi.org/10.1038/361269a0
Nomura K, Hayakawa K, Tatsumi H, Ono S (2016) Actin-interacting protein 1 promotes disassembly of actin-depolymerizing factor/cofilin-bound actin filaments in a pH-dependent manner. J Biol Chem 291:5146–5156. https://doi.org/10.1074/jbc.m115.713495
Oda T, Iwasa M, Aihara T, Maeda Y, Narita A (2009) The nature of the globular- to fibrous-actin transition. Nature 457:441–445
Oda T, Takeda S, Narita A, Maeda Y (2019) Structural polymorphism of actin. J Mol Biol 1:2–3. https://doi.org/10.1016/j.jmb.2019.05.048
Ono S (2007) Mechanism of depolymerization and severing of actin filaments and its significance in cytoskeletal dynamics. Int Rev Cytol 258:1–82. https://doi.org/10.1016/S0074-7696(07)58001-0
Otterbein LR, Graceffa P, Dominguez R (2001) The crystal structure of uncomplexed actin in the ADP state. Science 293:708–711. https://doi.org/10.1126/science.1059700
Phillips JC et al (2005) Scalable molecular dynamics with NAMD. J Comput Chem 26:1781–1802
Pollard TD, Borisy GG (2003) Cellular motility driven by assembly and disassembly of actin filaments. Cell 112:453–465
Pope BJ, Zierler-Gould KM, Kuhne R, Weeds AG, Ball LJ (2004) Solution structure of human cofilin: actin binding, pH sensitivity, and relationship to actin-depolymerizing factor. J Biol Chem 279:4840–4848. https://doi.org/10.1074/jbc.m310148200
Saunders MG, Tempkin J, Weare J, Dinner AR, Roux B, Voth GA (2014) Nucleotide regulation of the structure and dynamics of G-actin. Biophys J 106:1710–1720. https://doi.org/10.1016/j.bpj.2014.03.012
Tanaka K, Takeda S, Mitsuoka K, Oda T, Kimura-Sakiyama C, Maeda Y, Narita A (2018) Structural basis for cofilin binding and actin filament disassembly. Nat Commun 9:1860. https://doi.org/10.1038/s41467-018-04290-w
Tojkander S, Gateva G, Lappalainen P (2012) Actin stress fibers–assembly, dynamics and biological roles. J Cell Sci 125:1855–1864. https://doi.org/10.1242/jcs.098087
von der Ecken J, Muller M, Lehman W, Manstein DJ, Penczek PA, Raunser S (2015) Structure of the F-actin-tropomyosin complex. Nature 519:114–117. https://doi.org/10.1038/nature14033
Wang F, Sampogna RV, Ware BR (1989) pH dependence of actin self-assembly. Biophys J 55:293–298. https://doi.org/10.1016/s0006-3495(89)82804-8
Wioland H, Guichard B, Senju Y, Myram S, Lappalainen P, Jegou A, Romet-Lemonne G (2017) ADF/cofilin accelerates actin dynamics by severing filaments and promoting their depolymerization at both ends. Curr Biol 27(1956–1967):e1957. https://doi.org/10.1016/j.cub.2017.05.048
Wioland H, Jegou A, Romet-Lemonne G (2019a) Quantitative variations with pH of actin depolymerizing factor/cofilin’s multiple actions on actin filaments. Biochemistry 58:40–47. https://doi.org/10.1021/acs.biochem.8b01001
Wioland H, Jegou A, Romet-Lemonne G (2019b) Torsional stress generated by ADF/cofilin on cross-linked actin filaments boosts their severing. Proc Natl Acad Sci USA 116:2595–2602. https://doi.org/10.1073/pnas.1812053116
Yeoh S, Pope B, Mannherz HG, Weeds A (2002) Determining the differences in actin binding by human ADF and cofilin. J Mol Biol 315:911–925. https://doi.org/10.1006/jmbi.2001.5280
Yonezawa N, Nishida E, Sakai H (1985) pH control of actin polymerization by cofilin. J Biol Chem 260:14410–14412
Zhou GL, Zhang H, Field J (2014) Mammalian CAP (Cyclase-associated protein) in the world of cell migration: roles in actin filament dynamics and beyond. Cell Adhes Migr 8:55–59. https://doi.org/10.4161/cam.27479
Zimmerle CT, Frieden C (1988) Effect of pH on the mechanism of actin polymerization. Biochemistry 27:7766–7772
Acknowledgements
This research was supported by JSPS KAKENHI (18H02410). The author thanks the Edanz Group (www.edanzediting.com/ac) for editing a draft of this manuscript.
Author information
Authors and Affiliations
Corresponding author
Ethics declarations
Conflict of interest
The author declares no competing interests.
Additional information
Publisher's Note
Springer Nature remains neutral with regard to jurisdictional claims in published maps and institutional affiliations.
Rights and permissions
About this article
Cite this article
Narita, A. ADF/cofilin regulation from a structural viewpoint. J Muscle Res Cell Motil 41, 141–151 (2020). https://doi.org/10.1007/s10974-019-09546-6
Received:
Accepted:
Published:
Issue Date:
DOI: https://doi.org/10.1007/s10974-019-09546-6