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    Vimentin Intermediate Filament Formation: In Vitro Measurement and Mathematical Modeling of the Filament Length Distribution during Assembly†
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    ‡ Department of Mathematics, 342 Machray Hall, University of Manitoba, Winnipeg, MB, Canada R3L 2N2
    § Division of Biophysics of Macromolecules
    ∥ Division of Molecular Genetics
    German Cancer Research Center (DKFZ), Im Neuenheimer Feld 580, Heidelberg D-69120, Germany
    ⊥ Department of Internal Medicine I, University Hospital Ulm, D-89070 Ulm, Germany
    *Corresponding authors. E-mail: [email protected]; [email protected]
    #These authors contributed equally to this work
    ▽Current address: Research Group Microenvironment of Tumor Cell Invasion, German Cancer Research Center (DKFZ), Im Neuenheimer Feld 280, Heidelberg D-69120, Germany.
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    Langmuir

    Cite this: Langmuir 2009, 25, 15, 8817–8823
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    https://doi.org/10.1021/la900509r
    Published May 13, 2009
    Copyright © 2009 American Chemical Society
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    Abstract

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    The salt-induced in vitro assembly of cytoplasmic intermediate filament (IF) proteins such as vimentin is characterized by a very rapid lateral association of soluble tetrameric subunits into 60-nm-long full-width “unit-length” filaments (ULFs). We have demonstrated for this prototype IF protein that filament elongation occurs by the longitudinal annealing of ULFs into short IFs. These IFs further longitudinally anneal and thus constitute a progressively elongating filament population that over time yields filaments of several μm in length. Previously, we provided a mathematical model for the kinetics of the assembly process based on the average length distribution of filaments as determined by time-lapse electron and atomic force microscopy. Thereby, we were able to substantiate the concept that end-to-end-annealing of both ULFs and short filaments is obligatory for the formation of long IFs (Kirmse, R.; Portet, S.; Mücke, N. Aebi, U.; Herrmann, H.; Langowski, J. J. Biol. Chem.2007, 282, 18563−18572). As the next step in understanding the mechanics of IF formation, we have expanded our mathematical model to describe the quantitative aspects of IF assembly by taking into account geometry constraints as well as the diffusion properties of rodlike linear aggregates. Thereby, we have developed a robust model for the time-dependent filament length distribution of IFs under standard conditions.

    Copyright © 2009 American Chemical Society

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    Part of the Molecular and Polymer Gels; Materials with Self-Assembled Fibrillar Networks special issue.

    Cited By

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    This article is cited by 45 publications.

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    23. Norbert Mücke, Stefan Winheim, Holger Merlitz, Jan Buchholz, Jörg Langowski, Harald Herrmann, . In Vitro Assembly Kinetics of Cytoplasmic Intermediate Filaments: A Correlative Monte Carlo Simulation Study. PLOS ONE 2016, 11 (6) , e0157451. https://doi.org/10.1371/journal.pone.0157451
    24. Soufi Nafeey, Ines Martin, Tatiana Felder, Paul Walther, Edward Felder. Branching of keratin intermediate filaments. Journal of Structural Biology 2016, 194 (3) , 415-422. https://doi.org/10.1016/j.jsb.2016.03.023
    25. Oliva Saldanha, Martha E. Brennich, Manfred Burghammer, Harald Herrmann, Sarah Köster. The filament forming reactions of vimentin tetramers studied in a serial-inlet microflow device by small angle x-ray scattering. Biomicrofluidics 2016, 10 (2) https://doi.org/10.1063/1.4943916
    26. Karen M. Ridge, Dale Shumaker, Amélie Robert, Caroline Hookway, Vladimir I. Gelfand, Paul A. Janmey, Jason Lowery, Ming Guo, David A. Weitz, Edward Kuczmarski, Robert D. Goldman. Methods for Determining the Cellular Functions of Vimentin Intermediate Filaments. 2016, 389-426. https://doi.org/10.1016/bs.mie.2015.09.036
    27. I. Martin, M. Moch, T. Neckernuss, S. Paschke, H. Herrmann, O. Marti. Both monovalent cations and plectin are potent modulators of mechanical properties of keratin K8/K18 networks. Soft Matter 2016, 12 (33) , 6964-6974. https://doi.org/10.1039/C6SM00977H
    28. Johanna Block, Viktor Schroeder, Paul Pawelzyk, Norbert Willenbacher, Sarah Köster. Physical properties of cytoplasmic intermediate filaments. Biochimica et Biophysica Acta (BBA) - Molecular Cell Research 2015, 1853 (11) , 3053-3064. https://doi.org/10.1016/j.bbamcr.2015.05.009
    29. Ines Martin, Anke Leitner, Paul Walther, Harald Herrmann, Othmar Marti. Model-based analysis of keratin intermediate filament assembly. Journal of Physics D: Applied Physics 2015, 48 (37) , 375401. https://doi.org/10.1088/0022-3727/48/37/375401
    30. Gimena dos Santos, Micah R. Rogel, Margaret A. Baker, James R. Troken, Daniela Urich, Luisa Morales-Nebreda, Joseph A. Sennello, Mikhail A. Kutuzov, Albert Sitikov, Jennifer M. Davis, Anna P. Lam, Paul Cheresh, David Kamp, Dale K. Shumaker, G. R. Scott Budinger, Karen M. Ridge. Vimentin regulates activation of the NLRP3 inflammasome. Nature Communications 2015, 6 (1) https://doi.org/10.1038/ncomms7574
    31. Bernd Nöding, Harald Herrmann, Sarah Köster. Direct Observation of Subunit Exchange along Mature Vimentin Intermediate Filaments. Biophysical Journal 2014, 107 (12) , 2923-2931. https://doi.org/10.1016/j.bpj.2014.09.050
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    33. Martha E. Brennich, Susanne Bauch, Ulla Vainio, Tatjana Wedig, Harald Herrmann, Sarah Köster. Impact of ion valency on the assembly of vimentin studied by quantitative small angle X-ray scattering. Soft Matter 2014, 10 (12) , 2059-2068. https://doi.org/10.1039/C3SM52532E
    34. Stéphanie Portet. Dynamics of in vitro intermediate filament length distributions. Journal of Theoretical Biology 2013, 332 , 20-29. https://doi.org/10.1016/j.jtbi.2013.04.004
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    36. Jayne L. Elliott, Ming Der Perng, Alan R. Prescott, Karin A. Jansen, Gijsje H. Koenderink, Roy A. Quinlan. The specificity of the interaction between α B-crystallin and desmin filaments and its impact on filament aggregation and cell viability. Philosophical Transactions of the Royal Society B: Biological Sciences 2013, 368 (1617) , 20120375. https://doi.org/10.1098/rstb.2012.0375
    37. Christian Dammann, Bernd Nöding, Sarah Köster. Vimentin networks at tunable ion-concentration in microfluidic drops. Biomicrofluidics 2012, 6 (2) https://doi.org/10.1063/1.4705103
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    39. P.A. Janmey, F.C. MacKintosh. Polymers of the Cytoskeleton. 2012, 183-200. https://doi.org/10.1016/B978-0-444-53349-4.00249-1
    40. Tanja Lichtenstern, Norbert Mücke, Ueli Aebi, Monika Mauermann, Harald Herrmann. Complex formation and kinetics of filament assembly exhibited by the simple epithelial keratins K8 and K18. Journal of Structural Biology 2012, 177 (1) , 54-62. https://doi.org/10.1016/j.jsb.2011.11.003
    41. Robert D. Goldman, Megan M. Cleland, S.N. Prasanna Murthy, Saleemulla Mahammad, Edward R. Kuczmarski. Inroads into the structure and function of intermediate filament networks. Journal of Structural Biology 2012, 177 (1) , 14-23. https://doi.org/10.1016/j.jsb.2011.11.017
    42. Stefan Winheim, Aaron R. Hieb, Marleen Silbermann, Eva-Maria Surmann, Tatjana Wedig, Harald Herrmann, Jörg Langowski, Norbert Mücke, . Deconstructing the Late Phase of Vimentin Assembly by Total Internal Reflection Fluorescence Microscopy (TIRFM). PLoS ONE 2011, 6 (4) , e19202. https://doi.org/10.1371/journal.pone.0019202
    43. A. John McKinnon, Duane P. Harland. A concerted polymerization-mesophase separation model for formation of trichocyte intermediate filaments and macrofibril templates. 1: Relating phase separation to structural development. Journal of Structural Biology 2011, 173 (2) , 229-240. https://doi.org/10.1016/j.jsb.2010.11.019
    44. Martha Elisabeth Brennich, Jens-Friedrich Nolting, Christian Dammann, Bernd Nöding, Susanne Bauch, Harald Herrmann, Thomas Pfohl, Sarah Köster. Dynamics of intermediate filament assembly followed in micro-flow by small angle X-ray scattering. Lab on a Chip 2011, 11 (4) , 708. https://doi.org/10.1039/c0lc00319k
    45. Yi-Chia Lin, Chase P. Broedersz, Amy C. Rowat, Tatjana Wedig, Harald Herrmann, Frederick C. MacKintosh, David A. Weitz. Divalent Cations Crosslink Vimentin Intermediate Filament Tail Domains to Regulate Network Mechanics. Journal of Molecular Biology 2010, 399 (4) , 637-644. https://doi.org/10.1016/j.jmb.2010.04.054
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    Langmuir

    Cite this: Langmuir 2009, 25, 15, 8817–8823
    Click to copy citationCitation copied!
    https://doi.org/10.1021/la900509r
    Published May 13, 2009
    Copyright © 2009 American Chemical Society
    Request reuse permissions

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