Addressing the Molecular Mechanism of Longitudinal Lamin Assembly Using Chimeric Fusions

. 2020 Jul 07 ; 9 (7) : . [epub] 20200707

Jazyk angličtina Země Švýcarsko Médium electronic

Typ dokumentu časopisecké články, práce podpořená grantem

Perzistentní odkaz   https://www.medvik.cz/link/pmid32645958

The molecular architecture and assembly mechanism of intermediate filaments have been enigmatic for decades. Among those, lamin filaments are of particular interest due to their universal role in cell nucleus and numerous disease-related mutations. Filament assembly is driven by specific interactions of the elementary dimers, which consist of the central coiled-coil rod domain flanked by non-helical head and tail domains. We aimed to investigate the longitudinal 'head-to-tail' interaction of lamin dimers (the so-called ACN interaction), which is crucial for filament assembly. To this end, we prepared a series of recombinant fragments of human lamin A centred around the N- and C-termini of the rod. The fragments were stabilized by fusions to heterologous capping motifs which provide for a correct formation of parallel, in-register coiled-coil dimers. As a result, we established crystal structures of two N-terminal fragments one of which highlights the propensity of the coiled-coil to open up, and one C-terminal rod fragment. Additional studies highlighted the capacity of such N- and C-terminal fragments to form specific complexes in solution, which were further characterized using chemical cross-linking. These data yielded a molecular model of the ACN complex which features a 6.5 nm overlap of the rod ends.

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Turgay Y., Medalia O. The structure of lamin filaments in somatic cells as revealed by cryo-electron tomography. Nucleus. 2017;8:475–481. doi: 10.1080/19491034.2017.1337622. PubMed DOI PMC

Collas P., Lund E.G., Oldenburg A.R. Closing the (nuclear) envelope on the genome: How nuclear lamins interact with promoters and modulate gene expression. BioEssays. 2014;36:75–83. doi: 10.1002/bies.201300138. PubMed DOI

Frock R.L., Kudlow B.A., Evans A.M., Jameson S.A., Hauschka S.D., Kennedy B.K. Lamin A/C and emerin are critical for skeletal muscle satellite cell differentiation. Genes Dev. 2006;20:486–500. doi: 10.1101/gad.1364906. PubMed DOI PMC

Maynard S., Keijzers G., Akbari M., Ezra M.B., Hall A., Morevati M., Scheibye-Knudsen M., Gonzalo S., Bartek J., Bohr V.A. Lamin A/C promotes DNA base excision repair. Nucleic Acids Res. 2019;47:11709–11728. doi: 10.1093/nar/gkz912. PubMed DOI PMC

Qi R., Xu N., Wang G., Ren H., Li S., Lei J., Lin Q., Wang L., Gu X., Zhang H., et al. The lamin-A/C-LAP2α-BAF1 protein complex regulates mitotic spindle assembly and positioning. J. Cell Sci. 2015;128:2830–2841. doi: 10.1242/jcs.164566. PubMed DOI

Shumaker D.K., Solimando L., Sengupta K., Shimi T., Adam S.A., Grunwald A., Strelkov S.V., Aebi U., Cardoso M.C., Goldman R.D. The highly conserved nuclear lamin Ig-fold binds to PCNA: Its role in DNA replication. J. Cell Biol. 2008;181:269–280. doi: 10.1083/jcb.200708155. PubMed DOI PMC

Shimi T., Pfleghaar K., Kojima S.I., Pack C.G., Solovei I., Goldman A.E., Adam S.A., Shumaker D.K., Kinjo M., Cremer T., et al. The A- and B-type nuclear lamin networks: Microdomains involved in chromatin organization and transcription. Genes Dev. 2008;22:3409–3421. doi: 10.1101/gad.1735208. PubMed DOI PMC

Kang S.M., Yoon M.H., Park B.J. Laminopathies; Mutations on single gene and various human genetic diseases. BMB Rep. 2018;51:327–337. doi: 10.5483/BMBRep.2018.51.7.113. PubMed DOI PMC

Broers J.L.V., Ramaekers F.C.S. The role of the nuclear lamina in cancer and apoptosis. Adv. Exp. Med. Biol. 2014;773:27–48. PubMed

de Toledo M., Lopez-Mejia I.C., Cavelier P., Pratlong M., Barrachina C., Gromada X., Annicotte J.-S., Tazi J., Chavey C. Lamin C Counteracts Glucose Intolerance in Aging, Obesity and Diabetes Through β-Cell Adaptation. Diabetes. 2020;69:647–660. doi: 10.2337/db19-0377. PubMed DOI

Pradhan R., Jayakrishnan Nallappa M., Sengupta K. Lamin A/C modulates spatial organization and function of the Hsp70 gene locus via Nuclear Myosin I (NM1) J.Cell. Sci. 2020;133 doi: 10.1242/jcs.236265. jcs:236265. PubMed DOI

Lilina A.V., Chernyatina A.A., Guzenko D., Strelkov S.V. Lateral A11 type tetramerization in lamins. J. Struct. Biol. 2020;209:107404. doi: 10.1016/j.jsb.2019.10.006. PubMed DOI

Lupas A.N., Bassler J. Coiled Coils—A Model System for the 21st Century. Trends Biochem. Sci. 2017;42:130–140. doi: 10.1016/j.tibs.2016.10.007. PubMed DOI

Chernyatina A.A., Guzenko D., Strelkov S.V. Intermediate filament structure: The bottom-up approach. Curr. Opin. Cell Biol. 2015;32:65–72. doi: 10.1016/j.ceb.2014.12.007. PubMed DOI

Ahn J., Jo I., Kang S.M., Hong S., Kim S., Jeong S., Kim Y.H., Park B.J., Ha N.C. Structural basis for lamin assembly at the molecular level. Nat. Commun. 2019;10:3757. doi: 10.1038/s41467-019-11684-x. PubMed DOI PMC

Weber K., Geisler N. Intermediate Filaments: Structural Conservation and Divergence. Ann. N. Y. Acad. Sci. 1985;455:126–143. doi: 10.1111/j.1749-6632.1985.tb50408.x. PubMed DOI

Heitlinger E., Peter M., Lustig A., Villiger W., Nigg E.A., Aebi U. The role of the head and tail domain in lamin structure and assembly: Analysis of bacterially expressed chicken Lamin A and truncated B2 lamins. J. Struct. Biol. 1992;108:74–91. doi: 10.1016/1047-8477(92)90009-Y. PubMed DOI

Hess J.F., Budamagunta M.S., Aziz A., FitzGerald P.G., Voss J.C. Electron paramagnetic resonance analysis of the vimentin tail domain reveals points of order in a largely disordered region and conformational adaptation upon filament assembly. Protein Sci. 2013;22:47–55. doi: 10.1002/pro.2182. PubMed DOI PMC

Lee C.H., Coulombe P.A. Self-organization of keratin intermediate filaments into cross-linked networks. J. Cell Biol. 2009;186:409–421. doi: 10.1083/jcb.200810196. PubMed DOI PMC

Geisler N., Schünemann J., Weber K., Häner M., Aebi U. Assembly and architecture of invertebrate cytoplasmic intermediate filaments reconcile features of vertebrate cytoplasmic and nuclear lamin-type intermediate filaments. J. Mol. Biol. 1998;282:601–617. doi: 10.1006/jmbi.1998.1995. PubMed DOI

Heitlinger E., Peter M., Lustig A., Nigg E.A. Expression of Chicken Lamin B2 in Escherichia coli: Characterization of its Structure, Assembly, and Molecular Interactions. Cell. 1991;113:485–495. doi: 10.1083/jcb.113.3.485. PubMed DOI PMC

Aebi U., Julie C., Buble L., Gerace L. The nuclear lamina is a meshwork of intermediate-type filaments. Nature. 1986;324:698–699. doi: 10.1038/323560a0. PubMed DOI

Turgay Y., Eibauer M., Goldman A.E., Shimi T., Khayat M., Ben-Harush K., Dubrovsky-Gaupp A., Sapra K.T., Goldman R.D., Medalia O. The molecular architecture of lamins in somatic cells. Nature. 2017;543:261–264. doi: 10.1038/nature21382. PubMed DOI PMC

Stuurman N., Heins S., Aebi U., Mü M.E. Nuclear Lamins: Their Structure, Assembly, and Interactions. J. Struct. Biol. 1998;122:42–66. doi: 10.1006/jsbi.1998.3987. PubMed DOI

Ben-Harush K., Wiesel N., Frenkiel-Krispin D., Moeller D., Soreq E., Aebi U., Herrmann H., Gruenbaum Y., Medalia O. The Supramolecular Organization of the C. elegans Nuclear Lamin Filament. J. Mol. Biol. 2009;386:1392–1402. doi: 10.1016/j.jmb.2008.12.024. PubMed DOI

Foeger N., Wiesel N., Lotsch D., Mücke N., Kreplak L., Aebi U., Gruenbaum Y., Herrmann H. Solubility properties and specific assembly pathways of the B-type lamin from Caenorhabditis elegans. J. Struct. Biol. 2006;155:340–350. doi: 10.1016/j.jsb.2006.03.026. PubMed DOI

Isobe K., Gohara R., Ueda T., Takasaki Y., Ando S. The Last Twenty Residues in the Head Domain of Mouse Lamin A Contain Important Structural Elements for Formation of Head-to-Tail Polymers in Vitro. Biosci. Biotechnol. Biochem. 2007;71:1252–1259. doi: 10.1271/bbb.60674. PubMed DOI

Strelkov S.V., Herrmann H., Geisler N., Lustig A., Ivaninskii S., Zimbelmann R., Burkhard P., Aebi U. Divide-and-conquer crystallographic approach towards an atomic structure of intermediate filaments. J. Mol. Biol. 2001;306:773–781. doi: 10.1006/jmbi.2001.4442. PubMed DOI

Chernyatina A.A., Hess J.F., Guzenko D., Voss J.C., Strelkov S.V. How to Study Intermediate Filaments in Atomic Detail. Methods Enzymol. 2016;568:3–33. PubMed

Meier M., Padilla G.P., Herrmann H., Wedig T., Hergt M., Patel T.R., Stetefeld J., Aebi U., Burkhard P. Vimentin Coil 1A-A Molecular Switch Involved in the Initiation of Filament Elongation. J. Mol. Biol. 2009;390:245–261. doi: 10.1016/j.jmb.2009.04.067. PubMed DOI

Strelkov S.V., Herrmann H., Geisler N., Wedig T., Zimbelmann R., Aebi U., Burkhard P. Conserved segments 1A and 2B of the intermediate filament dimer: Their atomic structures and role in filament assembly. EMBO J. 2002;21:1255–1266. doi: 10.1093/emboj/21.6.1255. PubMed DOI PMC

Kapinos L.E., Burkhard P., Herrmann H., Aebi U., Strelkov S.V., Müller M. Simultaneous Formation of Right- and Left-handed Anti-parallel Coiled-coil Interfaces by a Coil2 Fragment of Human Lamin A. J. Mol. Biol. 2011;408:135–146. doi: 10.1016/j.jmb.2011.02.037. PubMed DOI

Tao Y., Strelkov S.V., Mesyanzhinov V.V., Rossmann M.G. Structure of bacteriophage T4 fibritin: A segmented coiled coil and the role of the C-terminal domain. Structure. 1997;5:789–798. doi: 10.1016/S0969-2126(97)00233-5. PubMed DOI

O’Shea E.K., Klemm J.D., Kim P.S., Alber T. X-ray structure of the GCN4 leucine zipper, a two-stranded, parallel coiled coil. Science. 1991;254:539–544. PubMed

Morais M.C., Kanamarul S., Badasso M.O., Koti J.S., Owen B.A.L., McMurray C.T., Anderson D.L., Rossmann M.G. Bacteriophage φ29 scaffolding protein gp7 before and after prohead assembly. Nat. Struct. Biol. 2003;10:572–576. doi: 10.1038/nsb939. PubMed DOI

Slep K.C., Rogers S.L., Elliott S.L., Ohkura H., Kolodziej P.A., Vale R.D. Structural determinants for EB1-mediated recruitment of APC and spectraplakins to the microtubule plus end. J. Cell Biol. 2005;168:587–598. doi: 10.1083/jcb.200410114. PubMed DOI PMC

Frye J., Klenchin V.A., Rayment I. Structure of the tropomyosin overlap complex from chicken smooth muscle: Insight into the diversity of N-terminal recognition. Biochemistry. 2010;49:4908–4920. doi: 10.1021/bi100349a. PubMed DOI PMC

Taylor K.C., Buvoli M., Korkmaz E.N., Buvoli A., Zheng Y., Heinze N.T., Cui Q., Leinwand L.A., Rayment I. Skip residues modulate the structural properties of the myosin rod and guide thick filament assembly. Proc. Natl. Acad. Sci. USA. 2015;112:E3806–E3815. doi: 10.1073/pnas.1505813112. PubMed DOI PMC

Korkmaz E.N., Taylor K.C., Andreas M.P., Ajay G., Heinze N.T., Cui Q., Rayment I. A composite approach towards a complete model of the myosin rod. Proteins Struct. Funct. Bioinform. 2016;84:172–189. doi: 10.1002/prot.24964. PubMed DOI PMC

Kapinos L.E., Schumacher J., Mücke N., Machaidze G., Burkhard P., Aebi U., Strelkov S.V., Herrmann H. Characterization of the Head-to-Tail Overlap Complexes Formed by Human Lamin A, B1 and B2 ‘Half-minilamin’ Dimers. J. Mol. Biol. 2010;396:719–731. doi: 10.1016/j.jmb.2009.12.001. PubMed DOI

Kochin V., Shimi T., Torvaldson E., Adam S.A., Goldman A., Pack C.G., Melo-Cardenas J., Imanishi S.Y., Goldman R.D., Eriksson J.E. Interphase phosphorylation of lamin A. J. Cell Sci. 2014;127:2683–2696. doi: 10.1242/jcs.141820. PubMed DOI PMC

Weeks S.D., Drinker M., Loll P.J. Ligation independent cloning vectors for expression of SUMO fusions. Protein Expr. Purif. 2007;53:40–50. doi: 10.1016/j.pep.2006.12.006. PubMed DOI PMC

Studier F.W. Protein production by auto-induction in high density shaking cultures. Protein Expr. Purif. 2005;41:207–234. doi: 10.1016/j.pep.2005.01.016. PubMed DOI

Studier F.W. Stable expression clones and auto-induction for protein production in E. Coli. Methods Mol. Biol. 2014;1091:17–32. PubMed

Kabsch W. XDS. Acta Crystallogr. Sect. D Biol. Crystallogr. 2010;66:125–132. doi: 10.1107/S0907444909047337. PubMed DOI PMC

Panjikar S., Parthasarathy V., Lamzin V.S., Weiss M.S., Tucker P.A. Auto-Rickshaw: An automated crystal structure determination platform as an efficient tool for the validation of an X-ray diffraction experiment. Acta Crystallogr. Sect. D Biol. Crystallogr. 2005;61:449–457. doi: 10.1107/S0907444905001307. PubMed DOI

Sheldrick G.M. A short history of SHELX. Acta Crystallogr. Sect. A Found. Crystallogr. 2008;64:112–122. doi: 10.1107/S0108767307043930. PubMed DOI

Read R.J., McCoy A.J. Using SAD data in Phaser. Acta Crystallogr. Sect. D Biol. Crystallogr. 2011;67:338–344. doi: 10.1107/S0907444910051371. PubMed DOI PMC

Cowtan K. The Buccaneer software for automated model building. 1. Tracing protein chains. Acta Crystallogr. Sect. D Biol. Crystallogr. 2006;62:1002–1011. doi: 10.1107/S0907444906022116. PubMed DOI

Winter G. Xia2: An expert system for macromolecular crystallography data reduction. J. Appl. Crystallogr. 2010;43:186–190. doi: 10.1107/S0021889809045701. DOI

Winter G., Waterman D.G., Parkhurst J.M., Brewster A.S., Gildea R.J., Gerstel M., Fuentes-Montero L., Vollmar M., Michels-Clark T., Young I.D., et al. DIALS: Implementation and evaluation of a new integration package. Acta Crystallogr. Sect. D Struct. Biol. 2018;74:85–97. doi: 10.1107/S2059798317017235. PubMed DOI PMC

Evans P. Scaling and assessment of data quality. Acta Crystallogr. Sect. D Biol. Crystallogr. 2006;62:72–82. doi: 10.1107/S0907444905036693. PubMed DOI

Evans P.R., Murshudov G.N. How good are my data and what is the resolution? Acta Crystallogr. Sect. D Biol. Crystallogr. 2013;69:1204–1214. doi: 10.1107/S0907444913000061. PubMed DOI PMC

Vagin A., Teplyakov A. Molecular replacement with MOLREP. Acta Crystallogr. Sect. D Biol. Crystallogr. 2010;66:22–25. doi: 10.1107/S0907444909042589. PubMed DOI

Emsley P., Lohkamp B., Scott W.G., Cowtan K. Features and development of Coot. Acta Crystallogr. Sect. D Biol. Crystallogr. 2010;66:486–501. doi: 10.1107/S0907444910007493. PubMed DOI PMC

Vagin A.A., Steiner R.A., Lebedev A.A., Potterton L., McNicholas S., Long F., Murshudov G.N. REFMAC5 dictionary: Organization of prior chemical knowledge and guidelines for its use. Acta Crystallogr. Sect. D Biol. Crystallogr. 2004;60:2184–2195. doi: 10.1107/S0907444904023510. PubMed DOI

Bricogne G., Blanc E., Brand M., Flensburg C., Keller P., Paciorek W., Roversi P., Sharff A., Smart O.S., Vonrhein C., et al. BUSTER. United Kingdom Glob. Phasing Ltd.; Cambridge, UK: 2017.

Strelkov S.V., Burkhard P. Analysis of α-helical coiled coils with the program TWISTER reveals a structural mechanism for stutter compensation. J. Struct. Biol. 2002;137:54–64. doi: 10.1006/jsbi.2002.4454. PubMed DOI

Candiano G., Bruschi M., Musante L., Santucci L., Ghiggeri G.M., Carnemolla B., Orecchia P., Zardi L., Righetti P.G. Blue silver: A very sensitive colloidal Coomassie G-250 staining for proteome analysis. Electrophoresis. 2004;25:1327–1333. doi: 10.1002/elps.200305844. PubMed DOI

Rozbeský D., Rosůlek M., Kukačka Z., Chmelík J., Man P., Novák P. Impact of Chemical Cross-Linking on Protein Structure and Function. Anal. Chem. 2018;90:1104–1113. doi: 10.1021/acs.analchem.7b02863. PubMed DOI

Fiala J., Kukačka Z., Novák P. Influence of cross-linker polarity on selectivity towards lysine side chains. J. Proteomics. 2020;218 doi: 10.1016/j.jprot.2020.103716. PubMed DOI

Götze M., Pettelkau J., Schaks S., Bosse K., Ihling C.H., Krauth F., Fritzsche R., Kühn U., Sinz A. StavroX-A software for analyzing crosslinked products in protein interaction studies. J. Am. Soc. Mass Spectrom. 2012;23:76–87. doi: 10.1007/s13361-011-0261-2. PubMed DOI

Iacobucci C., Götze M., Ihling C.H., Piotrowski C., Arlt C., Schäfer M., Hage C., Schmidt R., Sinz A. A cross-linking/mass spectrometry workflow based on MS-cleavable cross-linkers and the MeroX software for studying protein structures and protein–protein interactions. Nat. Protoc. 2018;13:2864–2889. doi: 10.1038/s41596-018-0068-8. PubMed DOI

Strelkov S.V., Schumacher J., Burkhard P., Aebi U., Herrmann H., Mu M.E. Crystal Structure of the Human Lamin A Coil 2B Dimer: Implications for the Head-to-tail Association of Nuclear Lamins. J. Mol. Biol. 2004;343:1067–1080. doi: 10.1016/j.jmb.2004.08.093. PubMed DOI

Heo L., Lee H., Seok C. GalaxyRefineComplex: Refinement of protein-protein complex model structures driven by interface repacking. Sci. Rep. 2016;6:1–10. doi: 10.1038/srep32153. PubMed DOI PMC

Ko J., Park H., Heo L., Seok C. GalaxyWEB server for protein structure prediction and refinement. Nucleic Acids Res. 2012;40:294–297. doi: 10.1093/nar/gks493. PubMed DOI PMC

Kraatz S.H.W., Bianchi S., Steinmetz M.O. Combinatorial use of disulfide bridges and native sulfur-SAD phasing for rapid structure determination of coiled-coils. Biosci. Rep. 2018;38:1–11. doi: 10.1042/BSR20181073. PubMed DOI PMC

Guzenko D., Strelkov S.V. Optimal data-driven parameterization of coiled coils. J. Struct. Biol. 2018;204:125–129. doi: 10.1016/j.jsb.2018.07.001. PubMed DOI

Doig A.J., Baldwin R.L. N- and C-capping preferences for all 20 amino acids in α-helical peptides. Protein Sci. 1995;4:1325–1336. doi: 10.1002/pro.5560040708. PubMed DOI PMC

Makarov A.A., Zou J., Houston D.R., Spanos C., Solovyova A.S., Cardenal-Peralta C., Rappsilber J., Schirmer E.C. Lamin A molecular compression and sliding as mechanisms behind nucleoskeleton elasticity. Nat. Commun. 2019;10:3056. doi: 10.1038/s41467-019-11063-6. PubMed DOI PMC

Rappsilber J. The beginning of a beautiful friendship: Cross-linking/mass spectrometry and modelling of proteins and multi-protein complexes. J. Struct. Biol. 2011;173:530–540. doi: 10.1016/j.jsb.2010.10.014. PubMed DOI PMC

Krissinel E., Henrick K. Inference of Macromolecular Assemblies from Crystalline State. J. Mol. Biol. 2007;372:774–797. doi: 10.1016/j.jmb.2007.05.022. PubMed DOI

Herrmann H., Aebi U. Intermediate Filaments: Molecular Structure, Assembly Mechanism, and Integration Into Functionally Distinct Intracellular Scaffolds. Annu. Rev. Biochem. 2004;73:749–789. doi: 10.1146/annurev.biochem.73.011303.073823. PubMed DOI

Kaus-Drobek M., Mücke N., Szczepanowski R.H., Wedig T., Czarnocki-Cieciura M., Polakowska M., Herrmann H., Wysłouch-Cieszyńska A., Dadlez M. Vimentin S-glutathionylation at Cys328 inhibits filament elongation and induces severing of mature filaments in vitro. FEBS J. 2020 doi: 10.1111/febs.15321. PubMed DOI PMC

Simon D.N., Zastrow M.S., Wilson K.L. Direct actin binding to A- and B-type lamin tails and actin filament bundling by the lamin A tail. Nucleus. 2010;1:264–272. doi: 10.4161/nucl.11799. PubMed DOI PMC

Samson C., Petitalot A., Celli F., Herrada I., Ropars V., Le Du M.-H., Nhiri N., Jacquet E., Arteni A.-A., Buendia B., et al. Structural analysis of the ternary complex between lamin A/C, BAF and emerin identifies an interface disrupted in autosomal recessive progeroid diseases. Nucleic Acids Res. 2018;46:10460–10473. doi: 10.1093/nar/gky736. PubMed DOI PMC

Simon D.N., Wilson K.L. Partners and post-translational modifications of nuclear lamins. Chromosoma. 2013;122:13–31. doi: 10.1007/s00412-013-0399-8. PubMed DOI PMC

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