Journal of Biomechanics
Volume 43, Issue 1 , Pages 15-22 , 5 January 2010

A multi-scale approach to understand the mechanobiology of intermediate filaments

  • Zhao Qin

      Affiliations

    • Laboratory for Atomistic and Molecular Mechanics, Department of Civil and Environmental Engineering, Massachusetts Institute of Technology, 77 Massachusetts Avenue, Room 1-235A&B, Cambridge, MA 02139, USA
    • Center for Materials Science and Engineering, Massachusetts Institute of Technology, 77 Massachusetts Avenue, Room 1-235A&B, Cambridge, MA 02139, USA
    • ,
  • Markus J. Buehler

      Affiliations

    • Laboratory for Atomistic and Molecular Mechanics, Department of Civil and Environmental Engineering, Massachusetts Institute of Technology, 77 Massachusetts Avenue, Room 1-235A&B, Cambridge, MA 02139, USA
    • Center for Materials Science and Engineering, Massachusetts Institute of Technology, 77 Massachusetts Avenue, Room 1-235A&B, Cambridge, MA 02139, USA
    • ,
  • Laurent Kreplak

      Affiliations

    • Department of Physics and Atmospheric Science, Dalhousie University, Halifax, Canada, NS B3 H 3J5
    • Corresponding Author InformationCorresponding author. Tel.: +19024948435; fax: +19024945191.

,Accepted 21 August 2009.

References 

  1. Ackbarow T, Chen X, et al. Hierarchies, multiple energy barriers, and robustness govern the fracture mechanics of alpha-helical and beta-sheet protein domains. Proc. Natl. Acad. Sci. USA. 2007;104(42):16410–16415
  2. Ackbarow T, Sen D, et al. Alpha-helical protein networks are self protective and flaw tolerant. PLoS ONE. 2009;4(6):e6015
  3. Benjamin M, Archer CW, et al. Cytoskeleton of cartilage cells. Microsc. Res. Tech. 1994;28(5):372–377
  4. Bertaud J, Qin Z, et al. Atomistically informed mesoscale model of alpha-helical protein domains. Int. J. Multiscale Comput. Eng. 2009;7(3):237–250
  5. Bhattacharya R, Gonzalez AM, et al. Recruitment of vimentin to the cell surface by {beta}3 integrin and plectin mediates adhesion strength. J. Cell Sci. 2009;
  6. Bloom S, Lockard VG, et al. Intermediate filament-mediated stretch-induced changes in chromatin: a hypothesis for growth initiation in cardiac myocytes. J. Mol. Cell Cardiol. 1996;28(10):2123–2127
  7. Bordeleau F, Bessard J, et al. Keratin contribution to cellular mechanical stress response at focal adhesions as assayed by laser tweezers. Biochem. Cell Biol. 2008;86(4):352–359
  8. Buehler MJ, Ackbarow T. Fracture mechanics of protein materials. Mater. Today. 2007;10(9):46–58
  9. Buehler MJ, Yung YC. Deformation and failure of protein materials in physiologically extreme conditions and disease. Nat. Mater. 2009;8(3):175–188
  10. Cavazza B, Cuniberti C, et al. Self-assembly of fibrin monomer. a light scattering and electron microscopic investigation. Ital. J. Biochem. 1981;30(1):75–89
  11. Cohen TV, Hernandez L, et al. Functions of the nuclear envelope and lamina in development and disease. Biochem. Soc. Trans. 2008;36(Pt 6):1329–1334
  12. Colombelli J, Besser A, et al. Mechanosensing in actin stress fibers revealed by a close correlation between force and protein localization. J. Cell Sci. 2009;122(Pt 10):1665–1679
  13. Crisp M, Liu Q, et al. Coupling of the nucleus and cytoplasm: role of the LINC complex. J. Cell Biol. 2006;172(1):41–53
  14. Deguchi S, Ohashi T, et al. Evaluation of tension in actin bundle of endothelial cells based on preexisting strain and tensile properties measurements. Mol. Cell Biomech. 2005;2(3):125–133
  15. Deguchi S, Ohashi T, et al. Tensile properties of single stress fibers isolated from cultured vascular smooth muscle cells. J. Biomech. 2006;39(14):2603–2610
  16. Djabali K, Piron G, et al. alphaB-crystallin interacts with cytoplasmic intermediate filament bundles during mitosis. Exp. Cell Res. 1999;253(2):649–662
  17. Fabry B, Maksym GN, et al. Scaling the microrheology of living cells. Phys. Rev. Lett. 2001;87(14):148102
  18. Flitney EW, Kuczmarski ER, et al. Insights into the mechanical properties of epithelial cells: the effects of shear stress on the assembly and remodeling of keratin intermediate filaments. FASEB J. 2009;23(7):2110–2119
  19. Fuchs E, Weber K. Intermediate filaments: structure, dynamics, function, and disease. Annu. Rev. Biochem. 1994;63:345–382
  20. Fudge D, Russell D, et al. The intermediate filament network in cultured human keratinocytes is remarkably extensible and resilient. PLoS ONE. 2008;3(6):e2327
  21. Fudge DS, Gardner KH, et al. The mechanical properties of hydrated intermediate filaments: insights from hagfish slime threads. Biophys. J. 2003;85(3):2015–2027
  22. Gardel ML, Sabass B, et al. Traction stress in focal adhesions correlates biphasically with actin retrograde flow speed. J. Cell Biol. 2008;183(6):999–1005
  23. Garrod D, Chidgey M. Desmosome structure, composition and function. Biochim. Biophys. Acta. 2008;1778(3):572–587
  24. Georgakopoulou S, Moller D, et al. Near-UV circular dichroism reveals structural transitions of vimentin subunits during intermediate filament assembly. J. Mol. Biol. 2009;386(2):544–553
  25. Haddad LA, Smith N, et al. The TSC1 tumor suppressor hamartin interacts with neurofilament-L and possibly functions as a novel integrator of the neuronal cytoskeleton. J. Biol. Chem. 2002;277(46):44180–44186
  26. Head MW, Hurwitz L, et al. AlphaB-crystallin regulates intermediate filament organization in situ. Neuroreport. 2000;11(2):361–365
  27. Hegele RA. Lamin mutations come of age. Nat. Med. 2003;9(6):644–645
  28. Hegele RA. Phenomics, lamin A/C, and metabolic disease. J. Clin. Endocrinol. Metab. 2007;92(12):4566–4568
  29. Helmke BP, Goldman RD, et al. Rapid displacement of vimentin intermediate filaments in living endothelial cells exposed to flow. Circ. Res. 2000;86(7):745–752
  30. Helmke BP, Thakker DB, et al. Spatiotemporal analysis of flow-induced intermediate filament displacement in living endothelial cells. Biophys. J. 2001;80(1):184–194
  31. Herrmann H, Bar H, et al. Intermediate filaments: from cell architecture to nanomechanics. Nat. Rev. Mol. Cell Biol. 2007;8(7):562–573
  32. Herrmann H, Haner M, et al. Characterization of distinct early assembly units of different intermediate filament proteins. J. Mol. Biol. 1999;286(5):1403–1420
  33. Herrmann H, Haner M, et al. Structure and assembly properties of the intermediate filament protein vimentin: the role of its head, rod and tail domains. J. Mol. Biol. 1996;264(5):933–953
  34. Hess JF, Budamagunta MS, et al. Structural characterization of human vimentin rod 1 and the sequencing of assembly steps in intermediate filament formation in vitro using site-directed spin labeling and electron paramagnetic resonance. J. Biol. Chem. 2004;279(43):44841–44846
  35. Hyder CL, Pallari HM, et al. Providing cellular signposts—post-translational modifications of intermediate filaments. FEBS Lett. 2008;582(14):2140–2148
  36. Ingber DE. Cellular tensegrity: defining new rules of biological design that govern the cytoskeleton. J. Cell Sci. 1993;104(Pt 3):613–627
  37. Ishikawa H, Bischoff R, et al. Mitosis and intermediate-sized filaments in developing skeletal muscle. J. Cell Biol. 1968;38:538–555
  38. Keten S, Buehler MJ. Geometric confinement governs the rupture strength of H-bond assemblies at a critical length scale. Nano Lett. 2008;8(2):743–748
  39. Kim S, Coulombe PA. Intermediate filament scaffolds fulfill mechanical, organizational, and signaling functions in the cytoplasm. Genes Dev. 2007;21(13):1581–1597
  40. Kim S, Kellner J, et al. Interaction between the keratin cytoskeleton and eEF1Bgamma affects protein synthesis in epithelial cells. Nat. Struct. Mol. Biol. 2007;14(10):982–983
  41. Kirmse R, Portet S, et al. A quantitative kinetic model for the in vitro assembly of intermediate filaments from tetrameric vimentin. J. Biol. Chem. 2007;282(25):18563–18572
  42. Kreplak L, Aebi U, et al. Molecular mechanisms underlying the assembly of intermediate filaments. Exp. Cell Res. 2004;301(1):77–83
  43. Kreplak L, Bar H. Severe myopathy mutations modify the nanomechanics of desmin intermediate filaments. J. Mol. Biol. 2009;385(4):1043–1051
  44. Kreplak L, Bar H, et al. Exploring the mechanical behavior of single intermediate filaments. J. Mol. Biol. 2005;354(3):569–577
  45. Kreplak L, Doucet J, et al. New aspects of the alpha-helix to beta-sheet transition in stretched hard alpha-keratin fibers. Biophys. J. 2004;87(1):640–647
  46. Kreplak L, Franbourg A, et al. A new deformation model of hard alpha-keratin fibers at the nanometer scale: implications for hard alpha-keratin intermediate filament mechanical properties. Biophys. J. 2002;82(4):2265–2274
  47. Kreplak L, Fudge D. Biomechanical properties of intermediate filaments: from tissues to single filaments and back. Bioessays. 2007;29(1):26–35
  48. Kreplak L, Herrmann H, et al. Tensile properties of single desmin intermediate filaments. Biophys. J. 2008;94(7):2790–2799
  49. Lazarides E. Intermediate filaments as mechanical integrators of cellular space. Nature. 1980;283(5744):249–256
  50. Lazaridis T, Karplus M. Effective energy function for proteins in solution. Proteins. 1999;35(2):133–152
  51. Lewis MK, Nahirney PC, et al. Concentric intermediate filament lattice links to specialized Z-band junctional complexes in sonic muscle fibers of the type I male midshipman fish. J. Struct. Biol. 2003;143(1):56–71
  52. Lin L, Holbro T, et al. Molecular interaction between human tumor marker protein p150, the largest subunit of eIF3, and intermediate filament protein K7. J. Cell Biochem. 2001;80(4):483–490
  53. Mogensen MM, Henderson CG, et al. Keratin filament deployment and cytoskeletal networking in a sensory epithelium that vibrates during hearing. Cell Motil. Cytoskeleton. 1998;41(2):138–153
  54. Mucke N, Kreplak L, et al. Assessing the flexibility of intermediate filaments by atomic force microscopy. J. Mol. Biol. 2004;335(5):1241–1250
  55. Mucke N, Wedig T, et al. Molecular and biophysical characterization of assembly-starter units of human vimentin. J. Mol. Biol. 2004;340(1):97–114
  56. Na S, Chowdhury F, et al. Plectin contributes to mechanical properties of living cells. Am. J. Physiol. Cell Physiol. 2009;296(4):C868–C877
  57. Nievers MG, Schaapveld RQ, et al. Biology and function of hemidesmosomes. Matrix Biol. 1999;18(1):5–17
  58. Olins AL, Hoang TV, et al. The LINC-less granulocyte nucleus. Eur. J. Cell Biol. 2009;88(4):203–214
  59. Omary MB, Coulombe PA, et al. Intermediate filament proteins and their associated diseases. N. Engl. J. Med. 2004;351(20):2087–2100
  60. Omary MB, Ku NO, et al. “Heads and tails” of intermediate filament phosphorylation: multiple sites and functional insights. Trends Biochem. Sci. 2006;31(7):383–394
  61. Pallari HM, Eriksson JE. Intermediate filaments as signaling platforms. Sci. STKE. 2006;2006(366):pe53
  62. Parry DA, Strelkov SV, et al. Towards a molecular description of intermediate filament structure and assembly. Exp. Cell Res. 2007;313(10):2204–2216
  63. Qin Z, Cranford S, et al. Robustness-strength performance of hierachical alpha-helical protein filaments. Int. J. Appl. Mech. 2009;1(1):85–112
  64. Qin, Z., Kreplak, L., et al., 2009b. Hierarchical structure controls nanomechanical properties of vimentin intermediate filaments, PLoS ONE, doi: 10.1371/journal.pone.000729
  65. Qin Z, Kreplak L, et al. Nanomechanical properties of vimentin intermediate filament dimers. Nanotechnology. 2009;20(42):425101
  66. Ridge KM, Linz L, et al. Keratin 8 phosphorylation by protein kinase C delta regulates shear stress-mediated disassembly of keratin intermediate filaments in alveolar epithelial cells. J. Biol. Chem. 2005;280(34):30400–30405
  67. Root DD, Yadavalli VK, et al. Coiled-coil nanomechanics and uncoiling and unfolding of the superhelix and alpha-helices of myosin. Biophys. J. 2006;90(8):2852–2866
  68. Schwaiger I, Sattler C, et al. The myosin coiled-coil is a truly elastic protein structure. Nat. Mater. 2002;1(4):232–235
  69. Seifert GJ, Lawson D, et al. Immunolocalization of the intermediate filament-associated protein plectin at focal contacts and actin stress fibers. Eur. J. Cell Biol. 1992;59(1):138–147
  70. Sivaramakrishnan S, DeGiulio JV, et al. Micromechanical properties of keratin intermediate filament networks. Proc. Natl. Acad. Sci. USA. 2008;105(3):889–894
  71. Sivaramakrishnan S, Schneider JL, et al. Shear stress induced reorganization of the keratin intermediate filament network requires phosphorylation by PKC {zeta}. Mol. Biol. Cell. 2009;20(11):2755–2765
  72. Smith TA, Strelkov SV, et al. Sequence comparisons of intermediate filament chains: evidence of a unique functional/structural role for coiled-coil segment 1A and linker L1. J. Struct. Biol. 2002;137(1–2):128–145
  73. Sokolova AV, Kreplak L, et al. Monitoring intermediate filament assembly by small-angle X-ray scattering reveals the molecular architecture of assembly intermediates. Proc. Natl. Acad. Sci. USA. 2006;103(44):16206–16211
  74. Staple D, Loparic M, et al. Stretching, unfolding, and deforming protein filaments adsorbed at solid-liquid interfaces using the tip of an atomic-force microscope. Phys. Rev. Lett. 2009;102:128302
  75. Steinert PM, Marekov LN, et al. Diversity of intermediate filament structure. Evidence that the alignment of coiled-coil molecules in vimentin is different from that in keratin intermediate filaments.. J. Biol. Chem. 1993;268(33):24916–24925
  76. Stewart-Hutchinson PJ, Hale CM, et al. Structural requirements for the assembly of LINC complexes and their function in cellular mechanical stiffness. Exp. Cell Res. 2008;314(8):1892–1905
  77. Strelkov SV, Herrmann H, et al. Molecular architecture of intermediate filaments. Bioessays. 2003;25(3):243–251
  78. Strelkov SV, Herrmann H, et al. Divide-and-conquer crystallographic approach towards an atomic structure of intermediate filaments. J. Mol. Biol. 2001;306(4):773–781
  79. Sylvius N, Tesson F. Lamin A/C and cardiac diseases. Curr. Opin. Cardiol. 2006;21(3):159–165
  80. Traub P, Bauer C, et al. Colocalization of single ribosomes with intermediate filaments in puromycin-treated and serum-starved mouse embryo fibroblasts. Biol. Cell. 1998;90(4):319–337
  81. Troyanovsky SM, Eshkind LG, et al. Contributions of cytoplasmic domains of desmosomal cadherins to desmosome assembly and intermediate filament anchorage. Cell. 1993;72(4):561–574
  82. Tzima E. Stress response role of small GTPases in endothelial Cytoskeletal dynamics and the shear. Circ. Res. 2006;98:176–185
  83. van der Kooi AJ, Bonne G, et al. Lamin A/C mutations with lipodystrophy, cardiac abnormalities, and muscular dystrophy. Neurology. 2002;59(4):620–623
  84. Vlcek S, Foisner R. Lamins and lamin-associated proteins in aging and disease. Curr. Opin. Cell Biol. 2007;19(3):298–304
  85. Wang K, McCarter R, et al. Viscoelasticity of the sarcomere matrix of skeletal muscles. The titin–myosin composite filament is a dual-stage molecular spring. Biophys. J. 1993;64(4):1161–1177
  86. Wang K, Ramirez-Mitchell R. A network of transverse and longitudinal intermediate filaments is associated with sarcomeres of adult vertebrate skeletal muscle. J. Cell Biol. 1983;96(2):562–570
  87. Wang N, Butler JP, et al. Mechanotransduction across the cell surface and through the cytoskeleton. Science. 1993;260(5111):1124–1127
  88. Wang N, Stamenovic D. Contribution of intermediate filaments to cell stiffness, stiffening, and growth. Am. J. Physiol. Cell Physiol. 2000;279(1):C188–C194
  89. Wang N, Stamenovic D. Mechanics of vimentin intermediate filaments. J. Muscle Res. Cell Motil. 2002;23(5–6):535–540
  90. Wilhelmsen K, Litjens SH, et al. Nesprin-3, a novel outer nuclear membrane protein, associates with the cytoskeletal linker protein plectin. J. Cell Biol. 2005;171(5):799–810
  91. Winter L, Abrahamsberg C, et al. Plectin isoform 1b mediates mitochondrion-intermediate filament network linkage and controls organelle shape. J. Cell Biol. 2008;181(6):903–911
  92. Yuan L, Veis A. The self-assembly of collagen molecules. Biopolymers. 1973;12(6):1437–1444
  93. Zhu Y, Boglomovas J, et al. Single molecule force spectroscopy of cardiac titin's N2B element-effects of the molecular chaperone alpha B-crystallin with disease causing mutations. J. Biol. Chem. 2009;284(20):13914–13923

PII: S0021-9290(09)00495-3

doi: 10.1016/j.jbiomech.2009.09.004

Journal of Biomechanics
Volume 43, Issue 1 , Pages 15-22 , 5 January 2010

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