Order and disorder in intermediate filament proteins

FEBS Letters

Volumn 589, Issue 19, 2015, Pages 2464-2476

  Kornreich, Micha ^a   Avinery, Ram ^a   Malka Gibor, Eti ^a   Laser Azogui, Adi ^a   Beck, Roy ^a  

^a TEL AVIV UNIVERSITY   (Israel)

Author keywords

Cytoskeleton; Intermediate filament; Intrinsically disordered protein; Polymer brush; Self assembly

Indexed keywords

ALPHA INTERNEXIN; DESMIN; GLIAL FIBRILLARY ACIDIC PROTEIN; INTERMEDIATE FILAMENT PROTEIN; INTRINSICALLY DISORDERED PROTEIN; KERATIN; LAMIN; NESTIN; NEUROFILAMENT PROTEIN; PERIPHERIN; VIMENTIN; AMINO ACID; PROTEIN BINDING;

ALGORITHM; ALPHA HELIX; AMINO ACID SEQUENCE; AMINO TERMINAL SEQUENCE; CARBOXY TERMINAL SEQUENCE; CYTOSKELETON; HYDROPHOBICITY; INTERMEDIATE FILAMENT; PRIORITY JOURNAL; PROTEIN ASSEMBLY; PROTEIN CONFORMATION; PROTEIN DOMAIN; PROTEIN FUNCTION; PROTEIN MODIFICATION; PROTEIN PHOSPHORYLATION; PROTEIN PROTEIN INTERACTION; PROTEIN STRUCTURE; REVIEW; CHEMICAL MODEL; CHEMICAL PHENOMENA; CHEMICAL STRUCTURE; CHEMISTRY; HUMAN; METABOLISM; PROTEIN SECONDARY STRUCTURE; PROTEIN TERTIARY STRUCTURE;

AMINO ACIDS; CYTOSKELETON; HUMANS; HYDROPHOBIC AND HYDROPHILIC INTERACTIONS; INTERMEDIATE FILAMENT PROTEINS; MODELS, CHEMICAL; MODELS, MOLECULAR; PROTEIN BINDING; PROTEIN STRUCTURE, SECONDARY; PROTEIN STRUCTURE, TERTIARY;

EID: 84942296865     PISSN: 00145793     EISSN: 18733468     Source Type: Journal    
DOI: 10.1016/j.febslet.2015.07.024     Document Type: Review

References (202)

1. J.E. Eriksson, T. Dechat, B. Grin, B. Helfand, M. Mendez, H.M. Pallari, and R.D. Goldman Introducing intermediate filaments: from discovery to disease J. Clin. Invest. 119 2009 1763 1771
2. M.B. Omary, P.A. Coulombe, and W.H.I. McLean Intermediate filament proteins and their associated diseases N. Engl. J. Med. 351 2004 2087 2100
3. S. Kim, and P.A. Coulombe Intermediate filament scaffolds fulfill mechanical, organizational, and signaling functions in the cytoplasm Genes Dev. 21 2007 1581 1597
4. D. Toivola, G. Tao, A. Habtezion, J. Liao, and M. Omary Cellular integrity plus: organelle-related and protein-targeting functions of intermediate filaments Trends Cell Biol. 15 2005 608 617
5. I. Izawa, and M. Inagaki Regulatory mechanisms and functions of intermediate filaments: a study using site- and phosphorylation state-specific antibodies Cancer Sci. 97 2006 167 174
6. M.J. Hendrix, E.A. Seftor, Y.W. Chu, K.T. Trevor, and R.E. Seftor Role of intermediate filaments in migration, invasion and metastasis Cancer Metastasis Rev. 15 1996 507 525
7. S.A. Joosse, J. Hannemann, J. Spotter, A. Bauche, A. Andreas, V. Muller, and K. Pantel Changes in keratin expression during metastatic progression of breast cancer: impact on the detection of circulating tumor cells Clin. Cancer Res. 18 2012 993 1003
8. Z. Chen, J. Wang, L. Cai, B. Zhong, H. Luo, Y. Hao, W. Yu, B. Wang, C. Su, Y. Lei, A.E. Bella, A.P. Xiang, and T. Wang Role of the stem cell-associated intermediate filament nestin in malignant proliferation of non-small cell lung cancer PLoS One 9 2014 e85584
9. K. Narita, Y. Matsuda, M. Seike, Z. Naito, A. Gemma, and T. Ishiwata Nestin regulates proliferation, migration, invasion and stemness of lung adenocarcinoma Int. J. Oncol. 44 2014 1118 1130
10. A. Uchiumi, M. Yamashita, and Y. Katagata Downregulation of keratins 8, 18 and 19 influences invasiveness of human cultured squamous cell carcinoma and adenocarcinoma cells Exp. Ther. Med. 3 2012 443 448
11. M.H.-S. Chen, G.W.-C. Yip, G.M.-K. Tse, T. Moriya, P.C.-W. Lui, M.-L. Zin, B.-H. Bay, and P.-H. Tan Expression of basal keratins and vimentin in breast cancers of young women correlates with adverse pathologic parameters Mod. Pathol. 21 2008 1183 1191
12. I. Szeverenyi, A.J. Cassidy, W.C. Cheuk, B.T.K. Lee, J.E.A. Common, S.C. Ogg, H. Chen, Y.S. Shu, W.L.P. Goh, W.N. Kee, J.A. Simpson, L.C. Li, H.E. Goi, B. Li, D.P. Lunny, D. Chuon, A. Venkatesh, H.K. Kian, W.H.I. McLean, P.L. Yun, and E.B. Lane The human intermediate filament database: comprehensive information on a gene family involved in many human diseases Hum. Mutat. 29 2008 351 360
13. E. Lazarides Intermediate filaments: a chemically heterogeneous, developmentally regulated class of proteins Annu. Rev. Biochem. 51 1982 219 250
14. H. Herrmann, S.V. Strelkov, P. Burkhard, and U. Aebi Intermediate filaments: primary determinants of cell architecture and plasticity J. Clin. Invest. 119 2009 1772 1783
15. R.G. Oshima Intermediate filaments: a historical perspective Exp. Cell Res. 313 2007 1981 1994
16. H. Iwatsuki, and M. Suda Seven kinds of intermediate filament networks in the cytoplasm of polarized cells: structure and function Acta Histochem. Cytochem. 43 2010 19 31
17. J. Schweizer, P.E. Bowden, P.A. Coulombe, L. Langbein, E.B. Lane, T.M. Magin, L. Maltais, M.B. Omary, D.A.D. Parry, M.A. Rogers, and M.W. Wright New consensus nomenclature for mammalian keratins J. Cell Biol. 174 2006 169 174
18. R. Moll, M. Divo, and L. Langbein The human keratins: biology and pathology Histochem. Cell Biol. 129 2008 705 733
19. H.H. Bragulla, and D.G. Homberger Structure and functions of keratin proteins in simple, stratified, keratinized and cornified epithelia J. Anat. 2009 516 559
20. J. Ivaska, H.M. Pallari, J. Nevo, and J.E. Eriksson Novel functions of vimentin in cell adhesion, migration, and signaling Exp. Cell Res. 313 2007 2050 2062
21. J.M. Dave, and K.J. Bayless Vimentin as an integral regulator of cell adhesion and endothelial sprouting Microcirculation 21 2014 333 344
22. A. Yuan, T. Sasaki, A. Kumar, C.M. Peterhoff, M.V. Rao, R.K. Liem, J.-P. Julien, and R.A. Nixon Peripherin is a subunit of peripheral nerve neurofilaments: implications for differential vulnerability of CNS and peripheral nervous system axons J. Neurosci. 32 2012 8501 8508
23. K.H. Fliegner, M.P. Kaplan, T.L. Wood, J.E. Pintar, and R.K. Liem Expression of the gene for the neuronal intermediate filament protein alpha-internexin coincides with the onset of neuronal differentiation in the developing rat nervous system J. Comp. Neurol. 342 1994 161 173
24. Perrot, R., Eyer, J., 2013. Neurofilaments: properties, functions, and regulation. In: The cytoskeleton. Springer, 171-236.
25. A. Laser Azogui, M. Kornreich, E. Malka-Gibor, and R. Beck Neurofilament assembly and function during neuronal development Curr. Opin. Cell Biol. 32 2014 92 101
26. K. Michalczyk, and M. Ziman Nestin structure and predicted function in cellular cytoskeletal organisation Histol. Histopathol. 20 2005 665 671
27. M. Titeux, V. Brocheriou, Z. Xue, J. Gao, J.F. Pellissier, P. Guicheney, D. Paulin, and Z. Li Human synemin gene generates splice variants encoding two distinct intermediate filament proteins Eur. J. Biochem. 268 2001 6435 6448
28. S.E. Newey, E.V. Howman, C.P. Ponting, M.A. Benson, R. Nawrotzki, N.Y. Loh, K.E. Davies, and D.J. Blake Syncoilin, a novel member of the intermediate filament superfamily that interacts with alpha-dystrobrevin in skeletal muscle J. Biol. Chem. 276 2001 6645 6655
29. J. Zhang, M.-L. Bang, D.S. Gokhin, Y. Lu, L. Cui, X. Li, Y. Gu, N.D. Dalton, M.C. Scimia, K.L. Peterson, R.L. Lieber, and J. Chen Syncoilin is required for generating maximum isometric stress in skeletal muscle but dispensable for muscle cytoarchitecture Am. J. Physiol. Cell Physiol. 294 2008 C1175 C1182
30. D.a. Parry, and P.M. Steinert Intermediate filaments: molecular architecture, assembly, dynamics and polymorphism Q. Rev. Biophys. 32 1999 99 187
31. D.A.D. Parry, S.V. Strelkov, P. Burkhard, U. Aebi, and H. Herrmann Towards a molecular description of intermediate filament structure and assembly Exp. Cell Res. 313 2007 2204 2216
32. M. Guharoy, B. Szabo, S.C. Martos, S. Kosol, and P. Tompa Intrinsic structural disorder in cytoskeletal proteins Cytoskeleton 70 2013 550 571
33. S. Dhe-Paganon, E.D. Werner, Y.I. Chi, and S.E. Shoelson Structure of the globular tail of nuclear lamin J. Biol. Chem. 277 2002 17381 17384
34. R.D. Goldman, Y.H. Chou, V. Prahlad, and M. Yoon Intermediate filaments: dynamic processes regulating their assembly, motility, and interactions with other cytoskeletal systems FASEB J. 13 Suppl. 2 1999 S261 S265
35. H. Herrmann, and U. Aebi Intermediate filaments and their associates: multi-talented structural elements specifying cytoarchitecture and cytodynamics Curr. Opin. Cell Biol. 12 2000 79 90
36. A. Yuan, M.V. Rao, T. Sasaki, Y. Chen, A. Kumar, Veeranna, R.K.H. Liem, J. Eyer, A.C. Peterson, J.-P. Julien, and R.A. Nixon Alpha-internexin is structurally and functionally associated with the neurofilament triplet proteins in the mature CNS J. Neurosci. 26 2006 10006 10019
37. R. Beck, J. Deek, J.B. Jones, and C.R. Safinya Gel-expanded to gel-condensed transition in neurofilament networks revealed by direct force measurements Nat. Mater. 9 2010 40 46
38. H. Herrmann, M. Haner, M. Brettel, N.O. Ku, and U. Aebi Characterization of distinct early assembly units of different intermediate filament proteins J. Mol. Biol. 286 1999 1403 1420
39. Lowery, J., Kuczmarski, E.R., Herrmann, H., Goldman, R.D., 2015. Intermediate filaments play a pivotal role in regulating cell architecture and function. J. Biol. Chem. jbc.R115.640359.
40. R. Beck, J. Deek, and C.R. Safinya Structures and interactions in "bottlebrush" neurofilaments: the role of charged disordered proteins in forming hydrogel networks Biochem. Soc. Trans. 40 2012 1027 1031
41. H. Herrmann, and U. Aebi Intermediate filaments: molecular structure, assembly mechanism, and integration into functionally distinct intracellular Scaffolds Annu. Rev. Biochem. 73 2004 749 789
42. H. Herrmann, M. Haner, M. Brettel, S.A. Muller, K.N. Goldie, B. Fedtke, A. Lustig, W.W. Franke, and U. Aebi Structure and assembly properties of the intermediate filament protein vimentin: the role of its head, rod and tail domains J. Mol. Biol. 264 1996 933 953
43. R.L. Shoeman, R. Hartig, M. Berthel, and P. Traub Deletion mutagenesis of the amino-terminal head domain of vimentin reveals dispensability of large internal regions for intermediate filament assembly and stability Exp. Cell Res. 279 2002 344 353
44. M. Hatzfeld, and M. Burba Function of type I and type II keratin head domains: their role in dimer, tetramer and filament formation J. Cell Sci. 107 1994 1959 1972
45. S.R. Gill, P.C. Wong, M.J. Monteiro, and D.W. Cleveland Assembly properties of dominant and recessive mutations in the small mouse neurofilament (NF-L) subunit J. Cell Biol. 111 1990 2005 2019
46. S.S. Chin, P. Macioce, and R.K. Liem Effects of truncated neurofilament proteins on the endogenous intermediate filaments in transfected fibroblasts J. Cell Sci. 99 Pt 2 1991 335 350
47. N.T. Snider, S.V.W. Weerasinghe, J.A. Iniguez-Lluhf, H. Herrmann, and M.B. Omary Keratin hypersumoylation alters filament dynamics and is a marker for human liver disease and keratin mutation J. Biol. Chem. 286 2011 2273 2284
48. Y.Q. Zhang, and K.D. Sarge Sumoylation regulates lamin A function and is lost in lamin A mutants associated with familial cardiomyopathies J. Cell Biol. 182 2008 35 39
49. N.T. Snider, and M.B. Omary Post-translational modifications of intermediate filament proteins: mechanisms and functions Nat. Rev. Mol. Cell Biol. 15 2014 163 177
50. C.L. Hyder, H.M. Pallari, V. Kochin, and J.E. Eriksson Providing cellular signposts - post-translational modifications of intermediate filaments FEBS Lett. 582 2008 2140 2148
51. R.K. Sihag, M. Inagaki, T. Yamaguchi, T.B. Shea, and H.C. Pant Role of phosphorylation on the structural dynamics and function of types III and IV intermediate filaments Exp. Cell Res. 313 2007 2098 2109
52. M.B. Omary, N.O. Ku, G.Z. Tao, D.M. Toivola, and J. Liao "Heads and tails" of intermediate filament phosphorylation: multiple sites and functional insights Trends Biochem. Sci. 31 2006 383 394
53. H. Mitsuhashi, Y.K. Hayashi, C. Matsuda, S. Noguchi, S. Wakatsuki, T. Araki, and I. Nishino Specific phosphorylation of Ser458 of A-type lamins in LMNA-associated myopathy patients J. Cell Sci. 123 2010 3893 3900
54. D.L. Winter, D. Paulin, M. Mericskay, and Z. Li Posttranslational modifications of desmin and their implication in biological processes and pathologies Histochem. Cell Biol. 141 2014 1 16
55. D.M. Toivola, N.O. Ku, E.Z. Resurreccion, D.R. Nelson, T.L. Wright, and M.B. Omary Keratin 8 and 18 hyperphosphorylation is a marker of progression of human liver disease Hepatology 40 2004 459 466
56. P. Fickert, M. Trauner, A. Fuchsbichler, C. Stumptner, K. Zatloukal, and H. Denk Mallory body formation in primary biliary cirrhosis is associated with increased amounts and abnormal phosphorylation and ubiquitination of cytokeratins J. Hepatol. 38 2003 387 394
57. P. Rudrabhatla, P. Grant, H. Jaffe, M.J. Strong, and H.C. Pant Quantitative phosphoproteomic analysis of neuronal intermediate filament proteins (NF-M/H) in Alzheimer's disease by iTRAQ FASEB J. 24 2010 4396 4407
58. B.K. Binukumar, V. Shukla, N.D. Amin, P. Reddy, S. Skuntz, P. Grant, and H.C. Pant Topographic regulation of neuronal intermediate filaments by phosphorylation, role of peptidyl-prolyl isomerase 1: significance in neurodegeneration Histochem. Cell Biol. 140 2013 23 32
59. P. Rudrabhatla Regulation of neuronal cytoskeletal protein phosphorylation in neurodegenerative diseases J. Alzheimers Dis. 41 2014 671 684
60. J.M. Dale, and M.L. Garcia Neurofilament phosphorylation during development and disease: which came first, the phosphorylation or the accumulation? J. Amino Acids 2012 2012 382107 382116
61. Y.H. Chou, P. Opal, R.A. Quinlan, and R.D. Goldman The relative roles of specific N- and C-terminal phosphorylation sites in the disassembly of intermediate filament in mitotic BHK-21 cells J. Cell Sci. 109 1996 817 826
62. S. Heins, P.C. Wong, S. Muller, K. Goldie, D.W. Cleveland, and U. Aebi The rod domain of NF-L determines neurofilament architecture, whereas the end domains specify filament assembly and network formation J. Cell Biol. 123 1993 1517 1533
63. C. Huc, M. Escurat, K. Djabali, M. Derer, F. Landon, F. Gros, and M.M. Portier Phosphorylation of peripherin, an intermediate filament protein, in mouse neuroblastoma NIE 115 cell line and in sympathetic neurons Biochem. Biophys. Res. Commun. 160 1989 772 779
64. B.I. Giasson, and W.E. Mushynski Intermediate filament disassembly in cultured dorsal root ganglion neurons is associated with amino-terminal head domain phosphorylation of specific subunits J. Neurochem. 70 1998 1869 1875
65. S. Hisanaga, Y. Gonda, M. Inagaki, A. Ikai, and N. Hirokawa Effects of phosphorylation of the neurofilament L protein on filamentous structures Cell Regul. 1 1990 237 248
66. R.K. Sihag, and R.A. Nixon Identification of Ser-55 as a major protein kinase a phosphorylation site on the 70-kDa subunit of neurofilaments: early turnover during axonal transport J. Biol. Chem. 266 1991 18861 18867
67. R.K. Sihag, and R.A. Nixon In vivo phosphorylation of distinct domains of the 70-kilodalton neurofilament subunit involves different protein kinases J. Biol. Chem. 264 1989 457 464
68. S. Hisanaga, Y. Matsuoka, K. Nishizawa, T. Saito, M. Inagaki, and N. Hirokawa Phosphorylation of native and reassembled neurofilaments composed of NF-L, NF-M, and NF-H by the catalytic subunit of cAMP-dependent protein kinase Mol. Biol. Cell 5 1994 161 172
69. Y. Nakamura, R. Hashimoto, Y. Kashiwagi, S. Aimoto, E. Fukusho, N. Matsumoto, T. Kudo, and M. Takeda Major phosphorylation site (Ser55) of neurofilament L by cyclic AMP-dependent protein kinase in rat primary neuronal culture J. Neurochem. 74 2000 949 959
70. H. Mukai, M. Toshimori, H. Shibata, M. Kitagawa, M. Shimakawa, M. Miyahara, H. Sunakawa, and Y. Ono PKN associates and phosphorylates the head-rod domain of neurofilament protein J. Biol. Chem. 271 1996 9816 9822
71. B.J. Gibb, J.P. Brion, J. Brownlees, B.H. Anderton, and C.C. Miller Neuropathological abnormalities in transgenic mice harbouring a phosphorylation mutant neurofilament transgene J. Neurochem. 70 1998 492 500
72. J. Tanaka, M. Ogawara, S. Ando, M. Shibata, R. Yatani, M. Kusagawa, and M. Inagaki Phosphorylation of a 62 kd porcine alpha-internexin, a newly identified intermediate filament protein Biochem. Biophys. Res. Commun. 196 1993 115 123
73. G.Y. Ching, and R.K. Liem Analysis of the roles of the head domains of type IV rat neuronal intermediate filament proteins in filament assembly using domain-swapped chimeric proteins J. Cell Sci. 112 1999 2233 2240
74. M.K. Lee, Z. Xu, P.C. Wong, and D.W. Cleveland Neurofilaments are obligate heteropolymers in vivo J. Cell Biol. 122 1993 1337 1350
75. Y.l. Zheng, B.S. Li, Veeranna, and H.C. Pant Phosphorylation of the head domain of neurofilament protein (NF-M). A factor regulating topographic phosphorylation of NF-M tail domain KSP sites in neurons J. Biol. Chem. 278 2003 24026 24032
76. R.K. Sihag, H. Jaffe, R.A. Nixon, and X. Rong Serine-23 is a major protein kinase A phosphorylation site on the amino-terminal head domain of the middle molecular mass subunit of neurofilament proteins J. Neurochem. 72 1999 491 499
77. R. Perrot, R. Berges, A. Bocquet, and J. Eyer Review of the multiple aspects of neurofilament functions, and their possible contribution to neurodegeneration Mol. Neurobiol. 38 2008 27 65
78. J. Kushkuley, S. Metkar, W.K.H. Chan, S. Lee, and T.B. Shea Aluminum induces neurofilament aggregation by stabilizing cross-bridging of phosphorylated c-terminal sidearms Brain Res. 1322 2010 118 123
79. D.L.Y. Dong, Z.S. Xu, G.W. Hart, and D.W. Cleveland Cytoplasmic O-GlcNAc modification of the head domain and the KSP repeat motif of the neurofilament protein neurofilament-H J. Biol. Chem. 271 1996 20845 20852
80. Y. Deng, B. Li, F. Liu, K. Iqbal, I. Grundke-Iqbal, R. Brandt, and C.-X. Gong Regulation between O-GlcNAcylation and phosphorylation of neurofilament-M and their dysregulation in Alzheimer disease FASEB J. 22 2008 138 145
81. N. Lüdemann, A. Clement, V.H. Hans, J. Leschik, C. Behl, and R. Brandt O-glycosylation of the tail domain of neurofilament protein M in human neurons and in spinal cord tissue of a rat model of amyotrophic lateral sclerosis (ALS) J. Biol. Chem. 280 2005 31648 31658
82. F. Loschke, K. Seltmann, J.-E. Bouameur, and T.M. Magin Regulation of keratin network organization Curr. Opin. Cell Biol. 32C 2015 56 64
83. T. Busch, M. Armacki, T. Eiseler, G. Joodi, C. Temme, J. Jansen, G. von Wichert, M.B. Omary, J. Spatz, and T. Seufferlein Keratin 8 phosphorylation regulates keratin reorganization and migration of epithelial tumor cells J. Cell Sci. 125 2012 2148 2159
84. H. Alam, P. Gangadaran, A.V. Bhate, D.A. Chaukar, S.S. Sawant, R. Tiwari, J. Bobade, S. Kannan, A.K. D'cruz, S. Kane, and M.M. Vaidya Loss of keratin 8 phosphorylation leads to increased tumor progression and correlates with clinico-pathological parameters of OSCC patients PLoS One 6 2011 e27767
85. V.N. Uversky Intrinsically disordered proteins from A to Z Int. J. Biochem. Cell Biol. 43 2011 1090 1103
86. P. Kouklis, M. Hatzfeld, M. Brunkener, K. Weber, and S. Georgatos In vitro assembly properties of vimentin mutagenized at the beta-site tail motif J. Cell Sci. 106 1993 919 928
87. M.B. McCormick The roles of the rod end and the tail in vimentin IF assembly and IF network formation J. Cell Biol. 122 1993 395 407
88. O. Esue, A.A. Carson, Y. Tseng, and D. Wirtz A direct interaction between actin and vimentin filaments mediated by the tail domain of vimentin J. Biol. Chem. 281 2006 30393 30399
89. R.B. Cary, M.W. Klymkowsky, R.M. Evans, A. Domingo, J.A. Dent, and L.E. Backhus Vimentin's tail interacts with actin-containing structures in vivo J. Cell Sci. 107 1994 1609 1622
90. S.D. Georgatos, and G. Blobel Lamin B constitutes an intermediate filament attachment site at the nuclear envelope J. Cell Biol. 105 1987 117 125
91. C. Maison, H. Horstmann, and S.D. Georgatos Regulated docking of nuclear membrane vesicles to vimentin filaments during mitosis J. Cell Biol. 123 1993 1491 1505
92. J.F. Hess, M.S. Budamagunta, A. Aziz, P.G. FitzGerald, and J.C. Voss 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. 22 2013 47 55
93. P.D. Kouklis, T. Papamarcaki, A. Merdes, and S.D. Georgatos A potential role for the COOH-terminal domain in the lateral packing of type III intermediate filaments J. Cell Biol. 114 1991 773 786
94. D. Li, T. Tapscoft, O. Gonzalez, P.E. Burch, M.A. Quinones, W.A. Zoghbi, R. Hill, L.L. Bachinski, D.L. Mann, and R. Roberts Desmin mutation responsible for idiopathic dilated cardiomyopathy Circulation 100 1999 461 464
95. M.C. Dalakas, A. Dagvadorj, B. Goudeau, K.Y. Park, K. Takeda, M. Simon-Casteras, O. Vasconcelos, N. Sambuughin, A. Shatunov, J.W. Nagle, K. Sivakumar, P. Vicart, and L.G. Goldfarb Progressive skeletal myopathy, a phenotypic variant of desmin myopathy associated with desmin mutations Neuromuscul. Disord. 13 2003 252 258
96. E. Arbustini, M. Pasotti, A. Pilotto, C. Pellegrini, M. Grasso, S. Previtali, A. Repetto, O. Bellini, G. Azan, M. Scaffino, C. Campana, G. Piccolo, M. Vigano, and L. Tavazzi Desmin accumulation restrictive cardiomyopathy and atrioventricular block associated with desmin gene defects Eur. J. Heart Fail. 8 2006 477 483
97. D. Selcen, K. Ohno, and A.G. Engel Myofibrillar myopathy: clinical, morphological and genetic studies in 63 patients Brain 127 2004 439 451
98. M. Mavroidis, P. Panagopoulou, I. Kostavasili, N. Weisleder, and Y. Capetanaki A missense mutation in desmin tail domain linked to human dilated cardiomyopathy promotes cleavage of the head domain and abolishes its Z-disc localization FASEB J. 22 2008 3318 3327
99. H. Bär, B. Goudeau, S. Walde, M. Casteras-Simon, N. Mucke, A. Shatunov, Y.P. Goldberg, C. Clarke, J.L. Holton, B. Eymard, H.A. Katus, M. Fardeau, L. Goldfarb, P. Vicart, and H. Herrmann Conspicuous involvement of desmin tail mutations in diverse cardiac and skeletal myopathies Hum. Mutat. 28 2007 374 386
100. N. Uyama, L. Zhao, E. Van Rossen, Y. Hirako, H. Reynaert, D.H. Adams, Z. Xue, Z. Li, R. Robson, M. Pekny, and A. Geerts Hepatic stellate cells express synemin, a protein bridging intermediate filaments to focal adhesions Gut 55 2006 1276 1289
101. R.M. Bellin, T.W. Huiatt, D.R. Critchley, and R.M. Robson Synemin may function to directly link muscle cell intermediate filaments to both myofibrillar Z-lines and costameres J. Biol. Chem. 276 2001 32330 32337
102. C.-H. Lee, and P.A. Coulombe Self-organization of keratin intermediate filaments into cross-linked networks J. Cell Biol. 186 2009 409 421
103. O. Bousquet, L. Ma, S. Yamada, C. Gu, T. Idei, K. Takahashi, D. Wirtz, and P.A. Coulombe The nonhelical tail domain of keratin 14 promotes filament bundling and enhances the mechanical properties of keratin intermediate filaments in vitro J. Cell Biol. 155 2001 747 754
104. P.C. Stasiak, P.E. Purkis, I.M. Leigh, and E.B. Lane Keratin 19: predicted amino acid sequence and broad tissue distribution suggest it evolved from keratinocyte keratins J. Invest. Dermatol. 92 1989 707 716
105. E. Sprecher, A. Ishida-Yamamoto, O.M. Becker, L. Marekov, C.J. Miller, P.M. Steinert, K. Neldner, and G. Richard Evidence for novel functions of the keratin tail emerging from a mutation causing ichthyosis hystrix J. Invest. Dermatol. 116 2001 511 519
106. L.-H. Gu, and P.A. Coulombe Defining the properties of the nonhelical tail domain in type II keratin 5: insight from a bullous disease-causing mutation Mol. Biol. Cell 16 2005 1427 1438
107. C.R. Safinya, J. Deek, R. Beck, J.B. Jones, and Y. Li Assembly of biological nanostructures: isotropic and liquid crystalline phases of neurofilament hydrogels Annu. Rev. Condens. Matter Phys. 6 2015 113 136
108. D.M. Barry, W. Stevenson, B.G. Bober, P.J. Wiese, J.M. Dale, G.S. Barry, N.S. Byers, J.D. Strope, R. Chang, D.J. Schulz, S. Shah, N.A. Calcutt, Y. Gebremichael, and M.L. Garcia Expansion of neurofilament medium C terminus increases axonal diameter independent of increases in conduction velocity or myelin thickness J. Neurosci. 32 2012 6209 6219
109. M.L. Garcia, C.S. Lobsiger, S.B. Shah, T.J. Deerinck, J. Crum, D. Young, C.M. Ward, T.O. Crawford, T. Gotow, Y. Uchiyama, M.H. Ellisman, N.A. Calcutt, and D.W. Cleveland NF-M is an essential target for the myelin-directed "outside-in" signaling cascade that mediates radial axonal growth J. Cell Biol. 163 2003 1011 1020
110. U. Raviv, S. Giasson, N. Kampf, J.-F. Gohy, R. Jerome, and J. Klein Lubrication by charged polymers Nature 425 2003 163 165
111. N. Ayres Polymer brushes: applications in biomaterials and nanotechnology Polym. Chem. 1 2010 769 777
112. M.E. Welch, Y. Xu, H. Chen, N. Smith, M.E. Tague, H.D. Abruna, B. Baird, and C.K. Ober Polymer brushes as functional, patterned surfaces for nanobiotechnology J. Photopolym. Sci. Technol. 25 2012 53 56
113. M. Welch, A. Rastogi, and C. Ober Polymer brushes for electrochemical biosensors Soft Matter 7 2011 297 302
114. E.B.B. Zhulina, and F.A.M.A.M. Leermakers The polymer brush model of neurofilament projections: effect of protein composition Biophys. J. 98 2010 462 469
115. Rubinstein, M., Colby, R.H., 2003. Polymer physics. OUP, Oxford.
116. J.N. Bright, T.B. Woolf, and J.H. Hoh Predicting properties of intrinsically unstructured proteins Prog. Biophys. Mol. Biol. 76 2001 131 173
117. P. De Gennes Conformations of polymers attached to an interface Macromolecules 13 1980 1069 1075
118. S. Alexander Adsorption of chain molecules with a polar head a scaling description J. Phys. 38 1977 983 987
119. Strelkov, S.V., Kreplak, L., Herrmann, H., Aebi, U., 2004. Intermediate filament protein structure determination. In: Intermediate filament cytoskeleton. Academic Press, 25-43.
120. J.E. Kohn, I.S. Millett, J. Jacob, B. Zagrovic, T.M. Dillon, N. Cingel, R.S. Dothager, S. Seifert, P. Thiyagarajan, T.R. Sosnick, M.Z. Hasan, V.S. Pande, I. Ruczinski, S. Doniach, and K.W. Plaxco Random-coil behavior and the dimensions of chemically unfolded proteins Proc. Natl. Acad. Sci. U.S.A. 101 2004 12491 12496
121. N.C. Fitzkee, and G.D. Rose Reassessing random-coil statistics in unfolded proteins Proc. Natl. Acad. Sci. U.S.A. 101 2004 12497 12502
122. P. Bernadó, and D.I. Svergun Structural analysis of intrinsically disordered proteins by small-angle X-ray scattering Mol. Biosyst. 8 2012 151 167
123. E.B. Zhulina, T.M. Birshtein, and O.V. Borisov Theory of ionizable polymer brushes Macromolecules 28 1995 1491 1499
124. O.V. Borisov, E.B. Zhulina, and T.M. Birshtein Diagram of the states of a grafted polyelectrolyte layer Macromolecules 27 1994 4795 4803
125. C.M. Wijmans, and E.B. Zhulina Polymer brushes at curved surfaces Macromolecules 26 1993 7214 7224
126. N. Srinivasan, M. Bhagawati, B. Ananthanarayanan, and S. Kumar Stimuli-sensitive intrinsically disordered protein brushes Nat. Commun. 5 2014 5145
127. M.E. Brennich, S. Bauch, U. Vainio, T. Wedig, H. Herrmann, and S. Koster Impact of ion valency on the assembly of vimentin studied by quantitative small angle X-ray scattering Soft Matter 10 2014 2059
128. S. Komura, and S.A. Safran Scaling theory of mixed amphiphilic monolayers Eur. Phys. J. E 5 2001 337 351
129. A.M. Skvortsov, L.I. Klushin, and A.A. Gorbunov Long and short chains in a polymeric brush: a conformational transition Macromolecules 30 1997 1818 1827
130. E.B.B. Zhulina, and F.A.M.A.M. Leermakers Effect of the ionic strength and pH on the equilibrium structure of a neurofilament brush Biophys. J. 93 2007 1452 1463
131. F.A.M. Leermakers, and E.B. Zhulina How the projection domains of NF-L and α-internexin determine the conformations of NF-M and NF-H in neurofilaments Eur. Biophys. J. 39 2010 1323 1334
132. Kornreich, M., Malka-Gibor, E., Laser-Azogui, A., Doron, O., Herrmann, H., Beck, R., 2015. Composite bottlebrush mechanics: α-internexin fine-tunes neurofilament network properties. Soft Matter (Under review).
133. Jeong, S.M., Zhou, X., Zhulina, E.B., Jho, Y., 2014. Monte-Carlo simulation of neurofilament brush. Isr. J. Chem. doi: http://dx.doi.org/10.1002/ijch.201400085.
134. J. Lee, S. Kim, R. Chang, L. Jayanthi, and Y. Gebremichael Effects of molecular model, ionic strength, divalent ions, and hydrophobic interaction on human neurofilament conformation J. Chem. Phys. 138 2013 015103
135. M.J. Stevens, and J.H. Hoh Conformational dynamics of neurofilament side-arms J. Phys. Chem. B 114 2010 8879 8886
136. S.T. Milner Polymer brushes Science 251 1991 905 914
137. J.C. Le Guillou, and J. Zinn-Justin Critical exponents for the n-vector model in three dimensions from field theory Phys. Rev. Lett. 39 1977 95 98
138. L.J. Fetters, D.J. Lohse, D. Richter, T.A. Witten, and A. Zirkel Connection between polymer molecular weight, density, chain dimensions, and melt viscoelastic properties Macromolecules 27 1994 4639 4647
139. G.J. Fleer, M.A. Cohen Stuart, J.M.H.M. Scheutjens, T. Cosgrove, and B. Vincent Polymers at interfaces 1993 Chapman & Hall London
140. M.J. Stevens, and J.H. Hoh Interactions between planar grafted neurofilament side-arms J. Phys. Chem. B 115 2011 7541 7549
141. L. Jayanthi, W. Stevenson, Y. Kwak, R. Chang, and Y. Gebremichael Conformational properties of interacting neurofilaments: Monte Carlo simulations of cylindrically grafted apposing neurofilament brushes J. Biol. Phys. 39 2013 343 362
142. V.N. Uversky, J.R. Gillespie, and A.L. Fink Why are "natively unfolded" proteins unstructured under physiologic conditions? Proteins Struct. Funct. Bioinformatics 41 2000 415 427
143. C.N. Magnan, and P. Baldi SSpro/ACCpro 5: almost perfect prediction of protein secondary structure and relative solvent accessibility using profiles, machine learning and structural similarity Bioinformatics 30 2014 2592 2597
144. D.T. Jones, and D. Cozzetto DISOPRED3: precise disordered region predictions with annotated protein-binding activity Bioinformatics 31 2014 857 863
145. D.W.A. Buchan, F. Minneci, T.C.O. Nugent, K. Bryson, and D.T. Jones Scalable web services for the PSIPRED Protein Analysis Workbench Nucleic Acids Res. 41 2013
146. P. Strnad, V. Usachov, C. Debes, F. Grater, D.A.D. Parry, and M.B. Omary Unique amino acid signatures that are evolutionarily conserved distinguish simple-type, epidermal and hair keratins J. Cell Sci. 124 2011 4221 4232
147. L.N. Jones, M. Simon, N.R. Watts, F.P. Booy, a.C. Steven, and D.a.D. Parry Intermediate filament structure: hard α-keratin Biophys. Chem. 68 1997 83 93
148. H. Fraga, R. Grana-Montes, R. Illa, G. Covaleda, and S. Ventura Association between foldability and aggregation propensity in small disulfide-rich proteins Antioxid. Redox Signal. 21 2014 368 383
149. X. Feng, and P.a. Coulombe A role for disulfide bonding in keratin intermediate filament organization and dynamics in skin keratinocytes J. Cell Biol. 209 2015 59 72
150. H. Wang, D.a.D. Parry, L.N. Jones, W.W. Idler, L.N. Marekov, and P.M. Steinert In vitro assembly and structure of trichocyte keratin intermediate filaments: a novel role for stabilization by disulfide bonding J. Cell Biol. 151 2000 1459 1468
151. S. Kumar, X. Yin, B.D. Trapp, J.H. Hoh, and M.E. Paulaitis Relating interactions between neurofilaments to the structure of axonal neurofilament distributions through polymer brush models Biophys. J. 82 2002 2360 2372
152. J.F. Leterrier, J. Kas, J. Hartwig, R. Vegners, and P.A. Janmey Mechanical effects of neurofilament cross-bridges. Modulation by phosphorylation, lipids, and interactions with F-actin J. Biol. Chem. 271 1996 15687 15694
153. S. Rammensee, P.A. Janmey, and A.R. Bausch Mechanical and structural properties of in vitro neurofilament hydrogels Eur. Biophys. J. 36 2007 661 668
154. E. Van Rossen, Z. Liu, D. Blijweert, N. Eysackers, I. Mannaerts, B. Schroyen, A. El Taghdouini, B. Edwards, K.E. Davies, and E. Sokal Syncoilin is an intermediate filament protein in activated hepatic stellate cells Histochem. Cell Biol. 141 2014 85 99
155. S. Song, A. Landsbury, R. Dahm, Y. Liu, Q. Zhang, and R.A. Quinlan Functions of the intermediate filament cytoskeleton in the eye lens J. Clin. Invest. 119 2009 1837 1848
156. L. Almagor, R. Avinery, J.A. Hirsch, and R. Beck Structural flexibility of CaV1.2 and CaV2.2 I-II proximal linker fragments in solution Biophys. J. 104 2013 2392 2400
157. A. Aziz, J.F. Hess, M.S. Budamagunta, P.G. Fitzgerald, and J.C. Voss Head and Rod 1 interactions in Vimentin. Identification of contact sites, structure and changes with phosphorylation using site-directed spin labeling and electron paramagnetic resonance J. Biol. Chem. 284 2009 7330 7338
158. A. Aziz, J.F. Hess, M.S. Budamagunta, J.C. Voss, and P.G. FitzGerald Site-directed spin labeling and electron paramagnetic resonance determination of vimentin head domain structure J. Biol. Chem. 285 2010 15278 15285
159. J. Kyte, and R.F. Doolittle A simple method for displaying the hydropathic character of a protein J. Mol. Biol. 157 1982 105 132
160. D. Szklarczyk, A. Franceschini, S. Wyder, K. Forslund, D. Heller, J. Huerta-Cepas, M. Simonovic, A. Roth, A. Santos, K.P. Tsafou, M. Kuhn, P. Bork, L.J. Jensen, and C. von Mering STRING v10: protein-protein interaction networks, integrated over the tree of life Nucleic Acids Res. 2014 D447 D452
161. F. Huber, A. Boire, M.P. Lopez, and G.H. Koenderink Cytoskeletal crosstalk: when three different personalities team up Curr. Opin. Cell Biol. 32 2015 39 47
162. S. Köster, D.A. Weitz, R.D. Goldman, U. Aebi, and H. Herrmann Intermediate filament mechanics in vitro and in the cell: from coiled coils to filaments, fibers and networks Curr. Opin. Cell Biol. 32 2015 82 91
163. S. Kumar, and J.H. Hoh Modulation of repulsive forces between neurofilaments by sidearm phosphorylation Biochem. Biophys. Res. Commun. 324 2004 489 496
164. H.G. Brown, and J.H. Hoh Entropic exclusion by neurofilament sidearms: a mechanism for maintaining interfilament spacing Biochemistry 36 1997 15035 15040
165. J. Deek, P.J. Chung, J. Kayser, A.R. Bausch, and C.R. Safinya Neurofilament sidearms modulate parallel and crossed-filament orientations inducing nematic to isotropic and re-entrant birefringent hydrogels Nat. Commun. 4 2013 2224
166. J.B. Jones, and C.R. Safinya Interplay between liquid crystalline and isotropic gels in self-assembled neurofilament networks Biophys. J. 95 2008 823 835
167. S. Pregent, A. Lichtenstein, R. Avinery, A. Laser-Azogui, F. Patolsky, and R. Beck Probing the interactions of intrinsically disordered proteins using nanoparticle tags Nano Lett. 15 2015 3080 3087
168. E.B. Zhulina, and M. Rubinstein Ionic strength dependence of polyelectrolyte brush thickness Soft Matter 8 2012 9376 9383
169. S. Hisanaga, and N. Hirokawa The effects of dephosphorylation on the structure of the projections of neurofilament J. Neurosci. 9 1989 959 966
170. H. Aranda-Espinoza, P. Carl, J.F. Leterrier, P. Janmey, and D.E. Discher Domain unfolding in neurofilament sidearms: effects of phosphorylation and ATP FEBS Lett. 531 2002 397 401
171. J. Eyer, and J.F. Leterrier Influence of the phosphorylation state of neurofilament proteins on the interactions between purified filaments in vitro Biochem. J. 252 1988 655 660
172. J.P. Gou, T. Gotow, P.A. Janmey, and J.F. Leterrier Regulation of neurofilament interactions in vitro by natural and synthetic polypeptides sharing Lys-Ser-Pro sequences with the heavy neurofilament subunit NF-H: neurofilament crossbridging by antiparallel sidearm overlapping Med. Biol. Eng. Comput. 36 1998 371 387
173. D.M. Barry, C. Carpenter, C. Yager, B. Golik, K.J. Barry, H. Shen, O. Mikse, L.S. Eggert, D.J. Schulz, and M.L. Garcia Variation of the neurofilament medium KSP repeat sub-domain across mammalian species: implications for altering axonal structure J. Exp. Biol. 213 2010 128 136
174. Y.C. Lin, C.P. Broedersz, A.C. Rowat, T. Wedig, H. Herrmann, F.C. MacKintosh, and D.A. Weitz Divalent cations crosslink vimentin intermediate filament tail domains to regulate network mechanics J. Mol. Biol. 399 2010 637 644
175. Y.-C. Lin, N.Y. Yao, C.P. Broedersz, H. Herrmann, F.C. MacKintosh, and D.A. Weitz Origins of elasticity in intermediate filament networks Phys. Rev. Lett. 104 2010 058101
176. C. Dammann, and S. Koster Dynamics of counterion-induced attraction between vimentin filaments followed in microfluidic drops Lab Chip 14 2014 2681 2687
177. P. Pawelzyk, H. Herrmann, and N. Willenbacher Mechanics of intermediate filament networks assembled from keratins K8 and K18 Soft Matter 9 2013 8871
178. P. Pawelzyk, N. Mucke, H. Herrmann, and N. Willenbacher Attractive interactions among intermediate filaments determine network mechanics in vitro PLoS One 9 2014 e93194
179. M. Schopferer, H. Bar, B. Hochstein, S. Sharma, N. Mucke, H. Herrmann, and N. Willenbacher Desmin and vimentin intermediate filament networks: their viscoelastic properties investigated by mechanical rheometry J. Mol. Biol. 388 2009 133 143
180. H. Bär, M. Schopferer, S. Sharma, B. Hochstein, N. Mucke, H. Herrmann, and N. Willenbacher Mutations in desmin's carboxy-terminal "tail" domain severely modify filament and network mechanics J. Mol. Biol. 397 2010 1188 1198
181. Kornreich, M.H., Malka-Gibor, E., Laser-Azogui, A., Doron, O., Herrmann, H., Beck, R. 2015. Composite bottlebrush mechanics: α-internexin fine-tunes neurofilament network properties. Soft Matter (Under review).
182. C. Storm, J.J. Pastore, F.C. MacKintosh, T.C. Lubensky, and P.A. Janmey Nonlinear elasticity in biological gels Nature 435 2005 191 194
183. Q. Wen, and P.A. Janmey Polymer physics of the cytoskeleton Curr. Opin. Solid State Mater. Sci. 15 2011 177 182
184. N.Y. Yao, C.P. Braedersz, Y.C. Lin, K.E. Kasza, F.C. MacKintosh, and D.A. Weitz Elasticity in ionically cross-linked neurofilament networks Biophys. J. 98 2010 2147 2153
185. C.P. Broedersz, and F.C. Mackintosh Modeling semiflexible polymer networks Rev. Mod. Phys. 86 2014 995 1036
186. K. Kroy, and J. Glaser The glassy wormlike chain New J. Phys. 9 2007 416
187. J.F. Leterrier, and J. Eyer Properties of highly viscous gels formed by neurofilaments in vitro. A possible consequence of a specific inter-filament cross-bridging Biochem. J. 245 1987 93 101
188. L. Kreplak, H. Bar, J.F. Leterrier, H. Herrmann, and U. Aebi Exploring the mechanical behavior of single intermediate filaments J. Mol. Biol. 354 2005 569 577
189. L. Kreplak, H. Herrmann, and U. Aebi Tensile properties of single desmin intermediate filaments Biophys. J. 94 2008 2790 2799
190. J. Block, V. Schroeder, P. Pawelzyk, N. Willenbacher, and S. Koster Physical properties of cytoplasmic intermediate filaments Biochim. Biophys. Acta - Mol. Cell Res. 2015
191. H. Herrmann, M. Haner, M. Brettel, S.A. Muller, K.N. Goldie, B. Fedtke, A. Lustig, W.W. Franke, and U. Aebi Structure and assembly properties of the intermediate filament protein vimentin: the role of its head, rod and tail domains J. Mol. Biol. 264 1996 933 953
192. R. Beck, J. Deek, M.C. Choi, T. Ikawa, O. Watanabe, E. Frey, P. Pincus, and C.R. Safinya Unconventional salt trend from soft to stiff in single neurofilament biopolymers Langmuir 26 2010 18595 18599
193. B. Ramm, J. Stigler, M. Hinczewski, D. Thirumalai, H. Herrmann, G. Woehlke, and M. Rief Sequence-resolved free energy profiles of stress-bearing vimentin intermediate filaments Proc. Natl. Acad. Sci. 111 2014 11359 11364
194. A.A. Chernyatina, D. Guzenko, and S.V. Strelkov Intermediate filament structure: the bottom-up approach Curr. Opin. Cell Biol. 32 2015 65 72
195. D.A.D. Parry, and A.C.T. North Hard α-keratin intermediate filament chains: substructure of the N-and C-terminal domains and the predicted structure and function of the C-terminal domains of type I and type II chains J. Struct. Biol. 122 1998 67 75
196. C.S. Clemen, H. Herrmann, S.V. Strelkov, and R. Schroder Desminopathies: pathology and mechanisms Acta Neuropathol. 125 2013 47 75
197. M. Guo, A.J. Ehrlicher, M.H. Jensen, M. Renz, J.R. Moore, R.D. Goldman, J. Lippincott-Schwartz, F.C. Mackintosh, and D.A. Weitz Probing the stochastic, motor-driven properties of the cytoplasm using force spectrum microscopy Cell 158 2014 822 832
198. M. Guo, A.J. Ehrlicher, S. Mahammad, H. Fabich, M.H. Jensen, J.R. Moore, J.J. Fredberg, R.D. Goldman, and D.A. Weitz The role of vimentin intermediate filaments in cortical and cytoplasmic mechanics Biophys. J. 105 2013 1562 1568
199. Y.-L. Wang, and D.E. Discher Cell mechanics 2007 Academic Press
200. B. Fabry, G.N. Maksym, J.P. Butler, M. Glogauer, D. Navajas, and J.J. Fredberg Scaling the microrheology of living cells Phys. Rev. Lett. 87 2001 148102
201. D. Weihs, T.G. Mason, and M.A. Teitell Bio-microrheology: a frontier in microrheology Biophys. J. 91 2006 4296 4305
202. R. Apweiler The universal protein resource (UniProt) in 2010 Nucleic Acids Res. 38 2009