Biochemical characterization of actin assembly mechanisms with ALS-associated profilin variants

Aguda, 2006, The structural basis of actin interaction with multiple WH2/B-thymosin motif-containing proteins, Structure, 14, 469, 10.1016/j.str.2005.12.011 Ajroud-Driss, 2015, Sporadic and hereditary amyotrophic lateral sclerosis (ALS), Biochim. Et. Biophys. Acta, 1852, 679, 10.1016/j.bbadis.2014.08.010 Alkam, 2017, Profilin1 biology and its mutation, actin(g) in disease, Cell. Mol. Life Sci., 74, 967, 10.1007/s00018-016-2372-1 Aydin, 2018, Gating mechanisms during actin filament elongation by formins, eLife, 7, 10.7554/eLife.37342 Blanchoin, 2014, Actin dynamics, architecture, and mechanics in cell motility, Physiol. Rev., 94, 235, 10.1152/physrev.00018.2013 Boopathy, 2015, Structural basis for mutation-induced destabilization of profilin 1 in ALS, Proc. Natl. Acad. Sci. USA, 112, 7984, 10.1073/pnas.1424108112 Bowerman, 2009, SMN, profilin IIa and plastin 3: a link between the deregulation of actin dynamics and SMA pathogenesis, Mol. Cell. Neurosci., 42, 66, 10.1016/j.mcn.2009.05.009 Breitsprecher, 2013, Formins at a glance, J. Cell. Sci., 126, 1, 10.1242/jcs.107250 Breitsprecher, 2012, Rocket launcher mechanism of collaborative actin assembly defined by single-molecule imaging, Science, 336, 1164, 10.1126/science.1218062 Cao, 2018, Modulation of formin processivity by profilin and mechanical tension, eLife, 7, 10.7554/eLife.34176 Castellanos-Montiel, 2020, The neglected genes of ALS: cytoskeletal dynamics impact synaptic degeneration in ALS, Front. Cell. Neurosci., 14, 10.3389/fncel.2020.594975 Chesarone, 2010, Unleashing formins to remodel the actin and microtubule cytoskeletons, Nat. Rev. Mol. Cell Biol., 11, 62, 10.1038/nrm2816 Cleveland, 2001, From charcot to lou gehrig: deciphering selective motor neuron death in als, Nat. Rev. Neurosci., 2, 806, 10.1038/35097565 Cooper, 1984, Acanthamoeba castellanii capping protein: properties, mechanism of action, immunologic cross-reactivity, and localization, J. Cell Biol., 99, 217, 10.1083/jcb.99.1.217 Courtemanche, 2018, Mechanisms of formin-mediated actin assembly and dynamics, Biophys. Rev., 10, 1553, 10.1007/s12551-018-0468-6 Courtemanche, 2013, Interaction of profilin with the barbed end of actin filaments, Biochemistry, 52, 6456, 10.1021/bi400682n Courtemanche, 2012, Determinants of Formin Homology 1 (FH1) domain function in actin filament elongation by formins, J. Biol. Chem., 287, 7812, 10.1074/jbc.M111.322958 Da Silva, 2003, RhoA/ROCK regulation of neuritogenesis via profilin IIa-mediated control of actin stability, J. Cell Biol., 162, 1267, 10.1083/jcb.200304021 Davey, 2020, Profilin: many facets of a small protein, Biophys. Rev., 12, 827, 10.1007/s12551-020-00723-3 Del Poggetto, 2016, Biophysical analysis of three novel profilin-1 variants associated with amyotrophic lateral sclerosis indicates a correlation between their aggregation propensity and the structural features of their globular state, Biol. Chem., 397, 927, 10.1515/hsz-2016-0154 Ezezika, 2009, Incompatibility with formin Cdc12p prevents human profilin from substituting for fission yeast profilin: insights from crystal structures of fission yeast profilin, J. Biol. Chem., 284, 2088, 10.1074/jbc.M807073200 Ferron, 2007, Structural basis for the recruitment of profilin-actin complexes during filament elongation by Ena/VASP, EMBO J., 26, 4597, 10.1038/sj.emboj.7601874 Figley, 2014, Profilin 1 associates with stress granules and ALS-linked mutations alter stress granule dynamics, J. Neurosci., 34, 8083, 10.1523/JNEUROSCI.0543-14.2014 Freischmidt, 2015, Profilin 1 with the amyotrophic lateral sclerosis associated mutation T109M displays unaltered actin binding and does not affect the actin cytoskeleton, BMC Neurosci., 16, 77, 10.1186/s12868-015-0214-y Funk, 2019, Profilin and formin constitute a pacemaker system for robust actin filament growth, Elife, 8, 10.7554/eLife.50963 Giampetruzzi, 2019, Modulation of actin polymerization affects nucleocytoplasmic transport in multiple forms of amyotrophic lateral sclerosis, Nat. Commun., 10, 3827, 10.1038/s41467-019-11837-y Goldschmidt-Clermont, 1992, The control of actin nucleotide exchange by thymosin beta 4 and profilin. A potential regulatory mechanism for actin polymerization in cells, Mol. Biol. Cell, 3, 1015, 10.1091/mbc.3.9.1015 Gregory, 2020, Genetics of amyotrophic lateral sclerosis, Curr. Genet. Med. Rep., 8, 121, 10.1007/s40142-020-00194-8 Harker, 2019, Ena/VASP processive elongation is modulated by avidity on actin filaments bundled by the filopodia cross-linker fascin, Mol. Biol. Cell, 30, 851, 10.1091/mbc.E18-08-0500 Henty-Ridilla, 2015, Global resource distribution: allocation of actin building blocks by profilin, Dev. Cell, 32, 5, 10.1016/j.devcel.2014.12.022 Henty-Ridilla, 2017, Profilin directly promotes microtubule growth through residues mutated in amyotrophic lateral sclerosis, Curr. Biol., 27, 3535, 10.1016/j.cub.2017.10.002 Henty-Ridilla, 2016, Accelerated actin filament polymerization from microtubule plus ends, Science, 352, 1004, 10.1126/science.aaf1709 Homa, 2021, Formin Cdc12’s specific actin assembly properties are tailored for cytokinesis in fission yeast, Biophys. J., 120, 2984, 10.1016/j.bpj.2021.06.023 Jacquemet, 2019, Filopodome mapping identifies p130Cas as a mechanosensitive regulator of filopodia stability, Curr. Biol., 29, 202, 10.1016/j.cub.2018.11.053 Jégou, 2011, Individual actin filaments in a microfluidic flow reveal the mechanism of ATP hydrolysis and give insight into the properties of profilin, PLoS Biol., 9, 10.1371/journal.pbio.1001161 Kaiser, 1989, Characterization of renatured profilin purified by urea elution from poly-L-proline agarose columns, Cell Motil. Cytoskelet., 14, 251, 10.1002/cm.970140211 Kiaei, 2018, ALS-causing mutations in profilin-1 alter its conformational dynamics: a computational approach to explain propensity for aggregation, Sci. Rep., 8, 13102, 10.1038/s41598-018-31199-7 Kovar, 2006, Control of the assembly of ATP- and ADP-actin by formins and profilin, Cell, 124, 423, 10.1016/j.cell.2005.11.038 Krishnan, 2009, Structure and functions of profilins, Biophys. Rev., 1, 71, 10.1007/s12551-009-0010-y Kursula, 2008, High-resolution structural analysis of mammalian profilin 2a complex formation with two physiological ligands: the formin homology 1 domain of mDia1 and the proline-rich domain of VASP, J. Mol. Biol., 375, 270, 10.1016/j.jmb.2007.10.050 Lambrechts, 2006, Profilin-I-ligand interactions influence various aspects of neuronal differentiation, J. Cell Sci., 119, 1570, 10.1242/jcs.02884 Lee, 2013, Dynamic localization of G-actin during membrane protrusion in neuronal motility, Curr. Biol., 23, 1046, 10.1016/j.cub.2013.04.057 Lim, 2016, ALS-causing mutations significantly perturb the self-assembly and interaction with nucleic acid of the intrinsically disordered prion-like domain of TDP-43, PLoS Biol., 14, 10.1371/journal.pbio.1002338 Ling, 2013, Converging mechanisms in ALS and FTD: disrupted RNA and protein homeostasis, Neuron, 79, 416, 10.1016/j.neuron.2013.07.033 Lu, 2001, Profilin binding to poly-L-proline and actin monomers along with ability to catalyze actin nucleotide exchange is required for viability of fission yeast, Mol. Biol. Cell, 12, 1161, 10.1091/mbc.12.4.1161 Michaelsen-Preusse, 2016, Neuronal profilins in health and disease: relevance for spine plasticity and Fragile X syndrome, Proc. Natl. Acad. Sci. U. S. A., 113, 3365, 10.1073/pnas.1516697113 Moens, 2015, Profilin-1 mediated cell-cycle arrest: searching for drug targets, Cell Cycle, 14, 3669, 10.1080/15384101.2015.1086204 Muller, 2005, Sequence and comparative genomic analysis of actin-related proteins, Mol. Biol. Cell, 16, 5736, 10.1091/mbc.e05-06-0508 Murk, 2021, Profilin isoforms in health and disease – all the same but different, Front. Cell Dev. Biol., 9, 10.3389/fcell.2021.681122 Nejedlá, 2021, The actin regulator profilin 1 is functionally associated with the mammalian centrosome, Life Sci. Alliance, 4, 10.26508/lsa.202000655 Nejedla, 2017, A fluorophore fusion construct of human profilin i with non-compromised poly(l-proline) binding capacity suitable for imaging, J. Mol. Biol., 429, 964, 10.1016/j.jmb.2017.01.004 Nejedla, 2016, Profilin connects actin assembly with microtubule dynamics, Mol. Biol. Cell, 27, 2381, 10.1091/mbc.e15-11-0799 Neuhoff, 2005, The actin-binding protein profilin I is localized at synaptic sites in an activity-regulated manner, Eur. J. Neurosci., 21, 15, 10.1111/j.1460-9568.2004.03814.x Paul, 2008, The role of the FH1 domain and profilin in formin-mediated actin-filament elongation and nucleation, Curr. Biol., 18, 9, 10.1016/j.cub.2007.11.062 Pereira, 2019, In silico analysis of PFN1 related to amyotrophic lateral sclerosis, PLoS ONE, 14, 10.1371/journal.pone.0215723 Pernier, 2016, Profilin interaction with actin filament barbed end Ccontrols dynamic instability, capping, branching, and motility, Dev. Cell, 36, 201, 10.1016/j.devcel.2015.12.024 Pimm, 2021, New twists in actin-microtubule interactions, Mol. Biol. Cell, 32, 211, 10.1091/mbc.E19-09-0491 Pimm, 2020, Profilin choreographs actin and microtubules in cells and cancer, Int. Rev. Cell Mol. Biol., 355, 155, 10.1016/bs.ircmb.2020.05.005 Pimm, M.L., Liu, X., Tuli, F., Lojko, A., Henty-Ridilla, J.L., 2021. Visualizing functional human profilin in cells and in vitro applications. bioRxiv 2021.09.01.458557. 〈https://doi.org/10.1101/2021.09.01.458557〉. Pinto‐Costa, 2019, Profilin as a dual regulator of actin and microtubule dynamics, Cytoskelet. cm, 21586 Pinto-Costa, 2020, Profilin 1 delivery tunes cytoskeletal dynamics toward CNS axon regeneration, J. Clin. Investig., 130, 2024, 10.1172/JCI125771 Pohl, 2019, Cellular quality control by the ubiquitin-proteasome system and autophagy, Science, 366, 818, 10.1126/science.aax3769 Pollard, 2000, Molecular mechanisms controlling actin filament dynamics in nonmuscle cells, Annu. Rev. Biophys. Biomol. Struct., 29, 545, 10.1146/annurev.biophys.29.1.545 Rosenbloom, 2021, Mechanism of actin filament nucleation, Biophys. J., 120, 4399, 10.1016/j.bpj.2021.09.006 Rotty, 2015, Profilin-1 serves as a gatekeeper for actin assembly by Arp2/3-dependent and -independent pathways, Dev. Cell, 32, 54, 10.1016/j.devcel.2014.10.026 Sadr, 2021, Detection of structural and conformational changes in ALS-causing mutant profilin-1 with hydrogen/deuterium exchange mass spectrometry and bioinformatics techniques, Metab. Brain Dis., 37, 229, 10.1007/s11011-021-00763-y Schindelin, 2012, Fiji: an open-source platform for biological-image analysis, Nat. Methods, 9, 676, 10.1038/nmeth.2019 Schmidt, 2021, ALS-linked PFN1 variants exhibit loss and gain of functions in the context of formin-induced actin polymerization, Proc. Natl. Acad. Sci. USA, 118, 10.1073/pnas.2024605118 Schutt, 1993, The structure of crystalline profilin [beta]-actin, Nature, 365, 810, 10.1038/365810a0 Skruber, 2018, Reconsidering an active role for G-actin in cytoskeletal regulation, J. Cell. Sci., 131, 10.1242/jcs.203760 Skruber, 2020, Arp2/3 and Mena/VASP Require Profilin 1 for Actin network assembly at the leading edge, Curr. Biol., 30, 2651, 10.1016/j.cub.2020.04.085 Smith, 2013, Three-color single molecule imaging shows WASP detachment from Arp2/3 complex triggers actin filament branch formation, Elife, 2, 10.7554/eLife.01008 Spudich, 1971, The regulation of rabbit skeletal muscle contraction. I. Biochemical studies of the interaction of the tropomyosin-troponin complex with actin and the proteolytic fragments of myosin, J. Biol. Chem., 246, 4866, 10.1016/S0021-9258(18)62016-2 Stüven, 2003, Exportin 6: a novel nuclear export receptor that is specific for profilin.actin complexes, EMBO J., 22, 5928, 10.1093/emboj/cdg565 Suarez, 2015, Profilin regulates F-actin network homeostasis by favoring formin over Arp2/3 complex, Dev. Cell, 32, 43, 10.1016/j.devcel.2014.10.027 Suarez, 2016, Internetwork competition for monomers governs actin cytoskeleton organization, Nat. Rev. Mol. Cell Biol., 17, 799, 10.1038/nrm.2016.106 Suetsugu, 1998, The essential role of profilin in the assembly of actin for microspike formation, EMBO J., 17, 6516, 10.1093/emboj/17.22.6516 Van Damme, 2017, Modelling amyotrophic lateral sclerosis: progress and possibilities, Dis. Model Mech., 10, 537, 10.1242/dmm.029058 Witke, 1998, In mouse brain profilin I and profilin II associate with regulators of the endocytic pathway and actin assembly, EMBO J., 17, 967, 10.1093/emboj/17.4.967 Wittenmayer, 2004, Tumor suppressor activity of profilin requires a functional actin binding site, Mol. Biol. Cell, 15, 1600, 10.1091/mbc.e03-12-0873 Wu, 2012, Mutations in the profilin 1 gene cause familial amyotrophic lateral sclerosis, Nature, 488, 499, 10.1038/nature11280 Zimmermann, 2017, Mechanoregulated inhibition of formin facilitates contractile actomyosin ring assembly, Nat. Commun., 8, 703, 10.1038/s41467-017-00445-3 Zweifel, 2020, Competition for delivery of profilin-actin to barbed ends limits the rate of formin-mediated actin filament elongation, J. Biol. Chem., 295, 4513, 10.1074/jbc.RA119.012000 Zweifel, 2021, Nucleation limits the lengths of actin filaments assembled by formin, Biophys. J., 120, 4442, 10.1016/j.bpj.2021.09.003