Mechanism of actin filament severing and capping by gelsolin.

Journal

Nature structural & molecular biology
ISSN: 1545-9985
Titre abrégé: Nat Struct Mol Biol
Pays: United States
ID NLM: 101186374

Informations de publication

Date de publication:
24 Oct 2024
Historique:
received: 19 01 2024
accepted: 27 09 2024
medline: 25 10 2024
pubmed: 25 10 2024
entrez: 25 10 2024
Statut: aheadofprint

Résumé

Gelsolin is the prototypical member of a family of Ca

Identifiants

DOI: 10.1038/s41594-024-01412-5 PMID: 39448849
pubmed: 39448849
doi: 10.1038/s41594-024-01412-5
pii: 10.1038/s41594-024-01412-5
doi:

Types de publication

Journal Article

Langues

eng

Sous-ensembles de citation

IM

Informations de copyright

© 2024. The Author(s), under exclusive licence to Springer Nature America, Inc.

Références

Pollard, T. D. Actin and actin-binding proteins. Cold Spring Harb. Perspect. Biol. 8, a018226 (2016).
doi: 10.1101/cshperspect.a018226 pubmed: 26988969 pmcid: 4968159
Huehn, A. R. et al. Structures of cofilin-induced structural changes reveal local and asymmetric perturbations of actin filaments. Proc. Natl Acad. Sci. USA 117, 1478–1484 (2020).
doi: 10.1073/pnas.1915987117 pubmed: 31900364 pmcid: 6983403
Kotila, T. et al. Mechanism of synergistic actin filament pointed end depolymerization by cyclase-associated protein and cofilin. Nat. Commun. 10, 5320 (2019).
doi: 10.1038/s41467-019-13213-2 pubmed: 31757941 pmcid: 6876575
Shekhar, S., Chung, J., Kondev, J., Gelles, J. & Goode, B. L. Synergy between cyclase-associated protein and cofilin accelerates actin filament depolymerization by two orders of magnitude. Nat. Commun. 10, 5319 (2019).
doi: 10.1038/s41467-019-13268-1 pubmed: 31757952 pmcid: 6876572
Nag, S., Larsson, M., Robinson, R. C. & Burtnick, L. D. Gelsolin: the tail of a molecular gymnast. Cytoskeleton 70, 360–384 (2013).
doi: 10.1002/cm.21117 pubmed: 23749648
Haddad, J. G., Harper, K. D., Guoth, M., Pietra, G. G. & Sanger, J. W. Angiopathic consequences of saturating the plasma scavenger system for actin. Proc. Natl Acad. Sci. USA 87, 1381–1385 (1990).
doi: 10.1073/pnas.87.4.1381 pubmed: 2154744 pmcid: 53479
Burtnick, L. D. et al. The crystal structure of plasma gelsolin: implications for actin severing, capping, and nucleation. Cell 90, 661–670 (1997).
doi: 10.1016/S0092-8674(00)80527-9 pubmed: 9288746
Robinson, R. C. et al. Domain movement in gelsolin: a calcium-activated switch. Science 286, 1939–1942 (1999).
doi: 10.1126/science.286.5446.1939 pubmed: 10583954
Burtnick, L. D., Urosev, D., Irobi, E., Narayan, K. & Robinson, R. C. Structure of the N-terminal half of gelsolin bound to actin: roles in severing, apoptosis and FAF. EMBO J. 23, 2713–2722 (2004).
doi: 10.1038/sj.emboj.7600280 pubmed: 15215896 pmcid: 514944
Oda, T., Iwasa, M., Aihara, T., Maeda, Y. & Narita, A. The nature of the globular- to fibrous-actin transition. Nature 457, 441–445 (2009).
doi: 10.1038/nature07685 pubmed: 19158791
Carman, P. J., Barrie, K. R., Rebowski, G. & Dominguez, R. Structures of the free and capped ends of the actin filament. Science 380, 1287–1292 (2023).
doi: 10.1126/science.adg6812 pubmed: 37228182 pmcid: 10880383
Palmer, N. J., Barrie, K. R. & Dominguez, R. Mechanisms of actin filament severing and elongation by formins. Nature 632, 437–442 (2024).
doi: 10.1038/s41586-024-07637-0 pubmed: 38843827
Janmey, P. A. et al. Interactions of gelsolin and gelsolin-actin complexes with actin. Effects of calcium on actin nucleation, filament severing, and end blocking. Biochemistry 24, 3714–3723 (1985).
doi: 10.1021/bi00335a046 pubmed: 2994715
Yin, H. L., Hartwig, J. H., Maruyama, K. & Stossel, T. P. Ca
doi: 10.1016/S0021-9258(19)68818-6 pubmed: 6270098
Irobi, E., Burtnick, L. D., Urosev, D., Narayan, K. & Robinson, R. C. From the first to the second domain of gelsolin: a common path on the surface of actin? FEBS Lett. 552, 86–90 (2003).
doi: 10.1016/S0014-5793(03)00934-7 pubmed: 14527665
Dominguez, R. The WH2 domain and actin nucleation: necessary but insufficient. Trends Biochem. Sci. 41, 478–490 (2016).
doi: 10.1016/j.tibs.2016.03.004 pubmed: 27068179 pmcid: 4884163
Yin, H. L. & Stossel, T. P. Control of cytoplasmic actin gel-sol transformation by gelsolin, a calcium-dependent regulatory protein. Nature 281, 583–586 (1979).
doi: 10.1038/281583a0 pubmed: 492320
Way, M., Gooch, J., Pope, B. & Weeds, A. G. Expression of human plasma gelsolin in Escherichia coli and dissection of actin binding sites by segmental deletion mutagenesis. J. Cell Biol. 109, 593–605 (1989).
doi: 10.1083/jcb.109.2.593 pubmed: 2547804
Yin, H. L., Iida, K. & Janmey, P. A. Identification of a polyphosphoinositide-modulated domain in gelsolin which binds to the sides of actin filaments. J. Cell Biol. 106, 805–812 (1988).
doi: 10.1083/jcb.106.3.805 pubmed: 2831234
Bryan, J. Gelsolin has three actin-binding sites. J. Cell Biol. 106, 1553–1562 (1988).
doi: 10.1083/jcb.106.5.1553 pubmed: 2836434
Yu, F. X., Zhou, D. M. & Yin, H. L. Chimeric and truncated gCap39 elucidate the requirements for actin filament severing and end capping by the gelsolin family of proteins. J. Biol. Chem. 266, 19269–19275 (1991).
doi: 10.1016/S0021-9258(18)54993-0 pubmed: 1655780
Kwiatkowski, D. J., Janmey, P. A. & Yin, H. L. Identification of critical functional and regulatory domains in gelsolin. J. Cell Biol. 108, 1717–1726 (1989).
doi: 10.1083/jcb.108.5.1717 pubmed: 2541138
Way, M., Pope, B. & Weeds, A. G. Evidence for functional homology in the F-actin binding domains of gelsolin and alpha-actinin: implications for the requirements of severing and capping. J. Cell Biol. 119, 835–842 (1992).
doi: 10.1083/jcb.119.4.835 pubmed: 1331120
Selden, L. A. et al. Severing of F-actin by the amino-terminal half of gelsolin suggests internal cooperativity in gelsolin. Biophys. J. 75, 3092–3100 (1998).
doi: 10.1016/S0006-3495(98)77750-1 pubmed: 9826629 pmcid: 1299980
Pope, B., Way, M. & Weeds, A. G. Two of the three actin-binding domains of gelsolin bind to the same subdomain of actin. Implications of capping and severing mechanisms. FEBS Lett. 280, 70–74 (1991).
doi: 10.1016/0014-5793(91)80206-I pubmed: 1849098
McLaughlin, P. J., Gooch, J. T., Mannherz, H. G. & Weeds, A. G. Structure of gelsolin segment 1-actin complex and the mechanism of filament severing. Nature 364, 685–692 (1993).
doi: 10.1038/364685a0 pubmed: 8395021
McGough, A., Chiu, W. & Way, M. Determination of the gelsolin binding site on F-actin: implications for severing and capping. Biophys. J. 74, 764–772 (1998).
doi: 10.1016/S0006-3495(98)74001-9 pubmed: 9533689 pmcid: 1302557
Kothakota, S. et al. Caspase-3-generated fragment of gelsolin: effector of morphological change in apoptosis. Science 278, 294–298 (1997).
doi: 10.1126/science.278.5336.294 pubmed: 9323209
Pardee, J. D. & Spudich, J. A. Purification of muscle actin. Methods Enzymol. 85, 164–181 (1982).
doi: 10.1016/0076-6879(82)85020-9 pubmed: 7121269
Punjani, A., Rubinstein, J. L., Fleet, D. J. & Brubaker, M. A. cryoSPARC: algorithms for rapid unsupervised cryo-EM structure determination. Nat. Methods 14, 290–296 (2017).
doi: 10.1038/nmeth.4169 pubmed: 28165473
Bepler, T. et al. Positive-unlabeled convolutional neural networks for particle picking in cryo-electron micrographs. Nat. Methods 16, 1153–1160 (2019).
doi: 10.1038/s41592-019-0575-8 pubmed: 31591578 pmcid: 6858545
Tan, Y. Z. et al. Addressing preferred specimen orientation in single-particle cryo-EM through tilting. Nat. Methods 14, 793–796 (2017).
doi: 10.1038/nmeth.4347 pubmed: 28671674 pmcid: 5533649
Naydenova, K. & Russo, C. J. Measuring the effects of particle orientation to improve the efficiency of electron cryomicroscopy. Nat. Commun. 8, 629 (2017).
doi: 10.1038/s41467-017-00782-3 pubmed: 28931821 pmcid: 5607000
Casanal, A., Lohkamp, B. & Emsley, P. Current developments in Coot for macromolecular model building of electron cryo-microscopy and crystallographic data. Protein Sci. 29, 1069–1078 (2020).
doi: 10.1002/pro.3791 pubmed: 31730249 pmcid: 7096722
van Zundert, G. C. P., Moriarty, N. W., Sobolev, O. V., Adams, P. D. & Borrelli, K. W. Macromolecular refinement of X-ray and cryoelectron microscopy structures with Phenix/OPLS3e for improved structure and ligand quality. Structure 29, 913–921.e4 (2021).
doi: 10.1016/j.str.2021.03.011 pubmed: 33823127 pmcid: 8349848
Pettersen, E. F. et al. UCSF ChimeraX: structure visualization for researchers, educators, and developers. Protein Sci. 30, 70–82 (2021).
doi: 10.1002/pro.3943 pubmed: 32881101

Auteurs

Kyle R Barrie (KR)

Department of Physiology and Biochemistry and Molecular Biophysics Graduate Group, Perelman School of Medicine, University of Pennsylvania, Philadelphia, PA, USA.
ORCID: 0000-0003-0860-1639

Grzegorz Rebowski (G)

Department of Physiology and Biochemistry and Molecular Biophysics Graduate Group, Perelman School of Medicine, University of Pennsylvania, Philadelphia, PA, USA.
ORCID: 0000-0002-0766-6302

Roberto Dominguez (R)

Department of Physiology and Biochemistry and Molecular Biophysics Graduate Group, Perelman School of Medicine, University of Pennsylvania, Philadelphia, PA, USA. droberto@pennmedicine.upenn.edu.
ORCID: 0000-0003-3186-5229

Classifications MeSH