Towards a molecular description of intermediate filament structure and assembly

Experimental Cell Research

Volumn 313, Issue 10, 2007, Pages 2204-2216

  Parry, David A D ^a   Strelkov, Sergei V ^b   Burkhard, Peter ^c   Aebi, Ueli ^d   Herrmann, Harald ^e  

^a MASSEY UNIVERSITY   (New Zealand)

^b UNIVERSITY OF LEUVEN   (Belgium)

^c UNIVERSITY OF CONNECTICUT   (United States)

^d UNIVERSITY OF BASEL   (Switzerland)

^e GERMAN CANCER RESEARCH CENTER DKFZ   (Germany)

Author keywords

Assembly; Intermediate filaments; Keratin; Polymorphism; Small angle X ray scattering; Vimentin

Indexed keywords

HETERODIMER; KERATIN; VIMENTIN;

CELL STRUCTURE; CRYOELECTRON MICROSCOPY; HUMAN; INTERMEDIATE FILAMENT; MOLECULAR MODEL; NONHUMAN; PRIORITY JOURNAL; PROTEIN ANALYSIS; PROTEIN ASSEMBLY; PROTEIN DOMAIN; RADIATION SCATTERING; REVIEW; STRUCTURE ANALYSIS; X RAY CRYSTALLOGRAPHY;

METAZOA;

EID: 34249750035     PISSN: 00144827     EISSN: None     Source Type: Journal    
DOI: 10.1016/j.yexcr.2007.04.009     Document Type: Review

References (61)

1. Ishikawa H., Bischoff R., and Holtzer H. Mitosis and intermediate-sized filaments in developing skeletal muscle. J. Cell Biol. 38 (1968) 538-555
2. Herrmann H., Häner M., Brettel M., Muller S.A., Goldie K.N., Fedtke B., Lustig A., Franke W.W., and Aebi U. 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
3. Mücke N., Wedig T., Bürer A., Marekov L.N., Steinert P.M., Langowski J., Aebi U., and Herrmann H. Molecular and biophysical characterization of assembly-starter units of human vimentin. J. Mol. Biol. 340 (2004) 97-114
4. Reichenzeller M., Burzlaff A., Lichter P., and Herrmann H. In vivo observation of a nuclear channel-like system: evidence for a distinct interchromosomal domain compartment in interphase cells. J. Struct. Biol. 129 (2000) 175-185
5. Eichner R., Rew P., Engel A., and Aebi U. Human epidermal keratin filaments: studies on their structure and assembly. Ann. N. Y. Acad. Sci. 455 (1985) 381-402
6. Engel A., Eichner R., and Aebi U. Polymorphism of reconstituted human epidermal keratin filaments: determination of their mass-per-length and width by scanning transmission electron microscopy (STEM). J. Ultrastruct. Res. 90 (1985) 323-335
7. Parry D.A., and Steinert P.M. Intermediate Filament Structure (1995), Springer Verlag, New York/Berlin/Heidelberg
8. Steinert P.M., Marekov L.N., Fraser R.D., and Parry D.A. Keratin intermediate filament structure. Crosslinking studies yield quantitative information on molecular dimensions and mechanism of assembly. J. Mol. Biol. 230 (1993) 436-452
9. Steinert P.M., Marekov L.N., and Parry D.A. Conservation of the structure of keratin intermediate filaments: molecular mechanism by which different keratin molecules integrate into preexisting keratin intermediate filaments during differentiation. Biochemistry 32 (1993) 10046-10056
10. Steinert P.M., Marekov L.N., and Parry D.A. 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. 268 (1993) 24916-24925
11. Steinert P.M., Marekov L.N., and Parry D.A. Molecular parameters of type IV alpha-internexin and type IV-type III alpha-internexin-vimentin copolymer intermediate filaments. J. Biol. Chem. 274 (1999) 1657-1666
12. Steinert P.M., Chou Y.H., Prahlad V., Parry D.A., Marekov L.N., Wu K.C., Jang S.I., and Goldman R.D. A high molecular weight intermediate filament-associated protein in BHK-21 cells is nestin, a type VI intermediate filament protein. Limited co-assembly in vitro to form heteropolymers with type III vimentin and type IV alpha-internexin. J. Biol. Chem. 274 (1999) 9881-9890
13. Parry D.A., Marekov L.N., and Steinert P.M. Subfilamentous protofibril structures in fibrous proteins: cross-linking evidence for protofibrils in intermediate filaments. J. Biol. Chem. 276 (2001) 39253-39258
14. Geisler N., Schunemann J., Weber K., Häner M., and Aebi U. Assembly and architecture of invertebrate cytoplasmic intermediate filaments reconcile features of vertebrate cytoplasmic and nuclear lamin-type intermediate filaments. J. Mol. Biol. 282 (1998) 601-617
15. Herrmann H., Häner M., Brettel M., Ku N.O., and Aebi U. Characterization of distinct early assembly units of different intermediate filament proteins. J. Mol. Biol. 286 (1999) 1403-1420
16. Herrmann H., and Aebi U. Intermediate filament assembly: fibrillogenesis is driven by decisive dimer-dimer interactions. Curr. Opin. Struct. Biol. 8 (1998) 177-185
17. Herrmann H., and Aebi U. Intermediate filaments: molecular structure, assembly mechanism, and integration into functionally distinct intracellular Scaffolds. Annu. Rev. Biochem. 73 (2004) 749-789
18. Strelkov S.V., Herrmann H., Geisler N., Wedig T., Zimbelmann R., Aebi U., and Burkhard P. Conserved segments 1A and 2B of the intermediate filament dimer: their atomic structures and role in filament assembly. EMBO J. 21 (2002) 1255-1266
19. Mehrani T., Wu K.C., Morasso M.I., Bryan J.T., Marekov L.N., Parry D.A., and Steinert P.M. Residues in the 1A rod domain segment and the linker L2 are required for stabilizing the A11 molecular alignment mode in keratin intermediate filaments. J. Biol. Chem. 276 (2001) 2088-2097
20. Kammerer R.A., Schulthess T., Landwehr R., Lustig A., Engel J., Aebi U., and Steinmetz M.O. An autonomous folding unit mediates the assembly of two-stranded coiled coils. Proc. Natl. Acad. Sci. U. S. A. 95 (1998) 13419-13424
21. Strelkov S.V., Herrmann H., Geisler N., Lustig A., Ivaninskii S., Zimbelmann R., Burkhard P., and Aebi U. Divide-and-conquer crystallographic approach towards an atomic structure of intermediate filaments. J. Mol. Biol. 306 (2001) 773-781
22. Wang H., Parry D.A., Jones L.N., Idler W.W., Marekov L.N., and Steinert P.M. 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
23. Parry D.A., Marekov L.N., Steinert P.M., and Smith T.A. A role for the 1A and L1 rod domain segments in head domain organization and function of intermediate filaments: structural analysis of trichocyte keratin. J. Struct. Biol. 137 (2002) 97-108
24. Strelkov S.V., Herrmann H., and Aebi U. Molecular architecture of intermediate filaments. BioEssays 25 (2003) 243-251
25. Smith T.A., Strelkov S.V., Burkhard P., Aebi U., and Parry D.A. Sequence comparisons of intermediate filament chains: evidence of a unique functional/structural role for coiled-coil segment 1A and linker L1. J. Struct. Biol. 137 (2002) 128-145
26. Steinert P.M., and Roop D.R. Molecular and cellular biology of intermediate filaments. Annu. Rev. Biochem. 57 (1988) 593-625
27. Aebi U., Cohn J., Buhle L., and Gerace L. The nuclear lamina is a meshwork of intermediate-type filaments. Nature 323 (1986) 560-564
28. Heitlinger E., Peter M., Lustig A., Villiger W., Nigg E.A., and 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. 108 (1992) 74-89
29. Stuurman N., Heins S., and Aebi U. Nuclear lamins: their structure, assembly, and interactions. J. Struct. Biol. 122 (1998) 42-66
30. Parry D.A. Hendecad repeat in segment 2A and linker L2 of intermediate filament chains implies the possibility of a right-handed coiled-coil structure. J. Struct. Biol. 155 (2006) 370-374
31. Stetefeld J., Jenny M., Schulthess T., Landwehr R., Engel J., and Kammerer R.A. Crystal structure of a naturally occurring parallel right-handed coiled coil tetramer. Nat. Struct. Biol. 7 (2000) 772-776
32. Ozbek S., Muller J.F., Figgemeier E., and Stetefeld J. Favourable mediation of crystal contacts by cocoamidopropylbetaine (CAPB). Acta Crystallogr., D Biol. Crystallogr. 61 (2005) 477-480
33. Harbury P.B., Plecs J.J., Tidor B., Alber T., and Kim P.S. High-resolution protein design with backbone freedom. Science 282 (1998) 1462-1467
34. Hess J.F., Budamagunta M.S., Shipman R.L., FitzGerald P.G., and Voss J.C. Characterization of the linker 2 region in human vimentin using site-directed spin labeling and electron paramagnetic resonance. Biochemistry 45 (2006) 11737-11743
35. Bär H., Mücke N., Kostareva A., Sjoberg G., Aebi U., and Herrmann H. Severe muscle disease-causing desmin mutations interfere with in vitro filament assembly at distinct stages. Proc. Natl. Acad. Sci. U. S. A. 102 (2005) 15099-15104
36. Herrmann H., Strelkov S.V., Feja B., Rogers K.R., Brettel M., Lustig A., Häner M., Parry D.A., Steinert P.M., Burkhard P., and Aebi U. The intermediate filament protein consensus motif of helix 2B: its atomic structure and contribution to assembly. J. Mol. Biol. 298 (2000) 817-832
37. Strelkov S.V., Schumacher J., Burkhard P., Aebi U., and Herrmann H. Crystal structure of the human lamin A coil 2B dimer: implications for the head-to-tail association of nuclear lamins. J. Mol. Biol. 343 (2004) 1067-1080
38. Strelkov S.V., and Burkhard P. Analysis of alpha-helical coiled coils with the program TWISTER reveals a structural mechanism for stutter compensation. J. Struct. Biol. 137 (2002) 54-64
39. Brown J.H., Cohen C., and Parry D.A. Heptad breaks in alpha-helical coiled coils: stutters and stammers. Proteins 26 (1996) 134-145
40. Parry D.A., Smith T.A., Rogers M.A., and Schweizer J. Human hair keratin-associated proteins: sequence regularities and structural implications. J. Struct. Biol. 155 (2006) 361-369
41. Sokolova A.V., Kreplak L., Wedig T., Mücke N., Svergun D.I., Herrmann H., Aebi U., and Strelkov S.V. Monitoring intermediate filament assembly by small-angle X-ray scattering reveals the molecular architecture of assembly intermediates. Proc. Natl. Acad. Sci. U. S. A. 103 (2006) 16206-16211
42. Rafik M.E., Briki F., Burghammer M., and Doucet J. In vivo formation steps of the hard alpha-keratin intermediate filament along a hair follicle: evidence for structural polymorphism. J. Struct. Biol. 154 (2006) 79-88
43. R.D.B. Fraser, D.A.D. Parry, Structural changes in the trichocyte intermediate filaments accompanying the transition from the reduced to the oxidized form, J. Struct. Biol. (in press), doi:10.1016/j.jsb.2007.02.001.
44. Fraser R.D., and Macrae T.P. Structural organization in feather keratin. J. Mol. Biol. 16 (1963) 272-280
45. Fraser R.D., MacRae T.P., and Miller A. X-ray diffraction patterns of alpha-fibrous proteins. J. Mol. Biol. 14 (1965) 432-442
46. Franke W.W., Schiller D.L., and Grund C. Protofilamentous and annular structures as intermediates during reconstitution of cytokeratin filaments in vitro. Biol. Cell 46 (1982) 257-268
47. Herrmann H., Wedig T., Porter R.M., Lane E.B., and Aebi U. Characterization of early assembly intermediates of recombinant human keratins. J. Struct. Biol. 137 (2002) 82-96
48. Ip W., Hartzer M.K., Pang Y.Y., and Robson R.M. Assembly of vimentin in vitro and its implications concerning the structure of intermediate filaments. J. Mol. Biol. 183 (1985) 365-375
49. Ip W., Heuser J.E., Pang Y.Y., Hartzer M.K., and Robson R.M. Subunit structure of desmin and vimentin protofilaments and how they assemble into intermediate filaments. Ann. N. Y. Acad. Sci. 455 (1985) 185-199
50. Abumuhor I.A., Spencer P.H., and Cohlberg J.A. The pathway of assembly of intermediate filaments from recombinant alpha-internexin. J. Struct. Biol. 123 (1998) 187-198
51. Herrmann H., and Aebi U. Intermediate filament assembly: temperature sensitivity and polymorphism. Cell. Mol. Life Sci. 55 (1999) 1416-1431
52. K.N., Goldie, T., Wedig, A., Mitra, U., Aebi, H., Herrmann, A. Hoenger, Dissecting the 3-D structure of vimentin intermediate filaments by cryo-electron tomography, J. Struct. Biol. (in press), doi:10.1016/j.jsb.2006.12.007.
53. Franke W.W., Zerban H., Grund C., and Schmid E. Electron microscopy of vimentin filaments and associated whisker structures in thin sections and freeze-fractures. Biol. Cell 41 (1981) 173-178
54. Koch M.H., Vachette P., and Svergun D.I. Small-angle scattering: a view on the properties, structures and structural changes of biological macromolecules in solution. Q. Rev. Biophys. 36 (2003) 147-227
55. Petoukhov M.V., Monie T.P., Allain F.H., Matthews S., Curry S., and Svergun D.I. Conformation of polypyrimidine tract binding protein in solution. Structure 14 (2006) 1021-1027
56. Smith T.A., Steinert P.M., and Parry D.A. Modeling effects of mutations in coiled-coil structures: case study using epidermolysis bullosa simplex mutations in segment 1a of K5/K14 intermediate filaments. Proteins 55 (2004) 1043-1052
57. Kaminska A., Strelkov S.V., Goudeau B., Olive M., Dagvadorj A., Fidzianska A., Simon-Casteras M., Shatunov A., Dalakas M.C., Ferrer I., Kwiecinski H., Vicart P., and Goldfarb L.G. Small deletions disturb desmin architecture leading to breakdown of muscle cells and development of skeletal or cardioskeletal myopathy. Hum. Genet. 114 (2004) 306-313
58. Pruszczyk P., Kostera-Pruszczyk A., Shatunov A., Goudeau B., Draminska A., Takeda K., Sambuughin N., Vicart P., Strelkov S.V., Goldfarb L.G., and Kaminska A. Restrictive cardiomyopathy with atrioventricular conduction block resulting from a desmin mutation. Int. J. Cardiol. 117 (2007) 244-253
59. Bär H., Mücke N., Katus H.A., Aebi U., and Herrmann H. Assembly defects of desmin disease mutants carrying deletions in the alpha-helical rod domain are rescued by wild type protein. J. Struct. Biol. 158 (2007) 107-115
60. Bar H., Fischer D., Goudeau B., Kley R.A., Clemen C.S., Vicart P., Herrmann H., Vorgerd M., and Schroder R. Pathogenic effects of a novel heterozygous R350P desmin mutation on the assembly of desmin intermediate filaments in vivo and in vitro. Hum. Mol. Genet. 14 (2005) 1251-1260
61. Bar H., Mucke N., Ringler P., Muller S.A., Kreplak L., Katus H.A., Aebi U., and Herrmann H. Impact of disease mutations on the desmin filament assembly process. J. Mol. Biol. 360 (2006) 1031-1042