Deletion mutagenesis of the amino-terminal head domain of vimentin reveals dispensability of large internal regions for intermediate filament assembly and stability

Experimental Cell Research

Volumn 279, Issue 2, 2002, Pages 344-353

  Shoeman, Robert L ^a   Hartig, Roland ^a   Berthel, Monika ^a   Traub, Peter ^a  

^a MAX PLANCK INSTITUTE FOR BIOPHYSICAL CHEMISTRY   (Germany)

Author keywords

Assembly; Confocal laser scanning microscopy; Deletion mutagenesis; Electron microscopy; Intermediate filament; Vimentin

Indexed keywords

CELL PROTEIN; MUTANT PROTEIN; VIMENTIN;

AMINO TERMINAL SEQUENCE; ARTICLE; BINDING SITE; DELETION MUTANT; ESCHERICHIA COLI; EUKARYOTIC CELL; IN VITRO STUDY; IN VIVO STUDY; INTERMEDIATE FILAMENT; MUTAGENESIS; NONHUMAN; PLASMID; PRIORITY JOURNAL; PROTEIN ASSEMBLY; PROTEIN DOMAIN; PROTEIN EXPRESSION; PROTEIN INTERACTION; PROTEIN POLYMERIZATION; PROTEIN PROTEIN INTERACTION; PROTEIN STABILITY; RECOMBINANT DNA TECHNOLOGY; WASTE; WILD TYPE;

EID: 0036403823     PISSN: 00144827     EISSN: None     Source Type: Journal    
DOI: 10.1006/excr.2002.5618     Document Type: Article

References (65)

1. Herrmann, H., and Aebi, U. (1998). Structure, assembly, and dynamics of intermediate filaments. In "Subcellular Biochemistry, Vol. 31: Intermediate Filaments" (H. Herrmann and J. R. Harris, Eds.), pp. 319-362, Plenum Press, New York.
2. Herrmann, H., and Aebi, U. (2000). Intermediate filaments and their associates: Multi-talented structural elements specifying cytoarchitecture and cytodynamics. Curr. Opin. Cell Biol. 12, 79-90.
3. Fuchs, E., and Weber, K. (1994). Intermediate filaments: structure, dynamics, function, and disease. Ann. Rev. Biochem. 63, 345-382.
4. Parry, D. A., Crewther, W. G., Fraser, R. D., and MacRae, T. P. (1977). Structure of alpha-keratin: Structural implication of the amino acid sequences of the type I and type II chain segments. J. Mol. Biol. 113, 449-454.
5. McLachlan, A. D., and Stewart, M. (1982). Periodic charge distribution in the intermediate filament proteins desmin and vimentin. J. Mol. Biol. 162, 693-698.
6. Meng, J. J., Khan, S., and Ip, W. (1994). Charge interactions in the rod domain drive formation of tetramers during intermediate filament assembly. J. Biol. Chem. 269, 18679-18685.
7. Hatzfeld, M., and Weber, K. (1991). Modulation of keratin intermediate filament assembly by single amino acid exchanges in the consensus sequence at the C-terminal end of the rod domain. J. Cell Sci. 99, 351-362.
8. Raats, J. M., Gerards, W. L., Schreuder, M. I., Grund, C., Henderik, J. B., Hendriks, I. L., Ramaekers, F. C., and Bloemendal, H. (1992). Biochemical and structural aspects of transiently and stably expressed mutant desmin in vimentin-free and vimentin-containing cells. Eur. J. Cell Biol. 58, 108-127.
9. Steinert, P. M. and Bale, S. J. (1993). Genetic skin diseases caused by mutations in keratin intermediate filaments. Trends Genet. 9, 280-284.
10. Fuchs, E. (1996). The cytoskeleton and disease: Genetic disorders of intermediate filaments. Ann. Rev. Genet. 30, 197-231.
11. Lazarides, E. (1980). Intermediate filaments as mechanical integrators of cellular space. Nature 283, 249-256.
12. Steinert, P. M., Steven, A. S., and Roop, D. R. (1985). The molecular biology of intermediate filaments. Cell 42, 411-419.
13. Raats, J. M. H., and Bloemendal, H. (1992). The role of protein domains in the assembly process of intermediate filaments. Prog. Nucleic Acid Res. Mol. Biol. 43, 67-86.
14. Heins, S., and Aebi, U. (1994). Making heads and tails of intermediate filament assembly, dynamics and networks. Curr. Opin. Cell Biol. 6, 25-33.
15. Rogers, K. R., Eckelt, A., Nimmrich, V., Janssen, K. P., Schliwa, M., Herrmann, H., and Franke, W. W. (1995). Truncation mutagenesis of the non-alpha-helical carboxyterminal tail domain of vimentin reveals contributions to cellular localization but not to filament assembly. Eur. J. Cell Biol. 66, 136-150.
16. Traub, P., and Vorgias, C. E. (1983). Involvement of the N-terminal polypeptide of vimentin in the formation of intermediate filaments. J. Cell Sci. 63, 43-67.
17. Kaufmann, E., Weber, K., and Geisler, N. (1985). Intermediate filament forming ability of desmin derivatives lacking either the amino-terminal 67 or the carboxy-terminal 27 residues. J. Mol. Biol. 185, 733-742.
18. Gill, S. R., Wong, P. C., Monteiro, M. J., and Cleveland, D. W. (1990). Assembly properties of dominant and recessive mutations in the small mouse neurofilament (NF-L) subunit. J. Cell Biol. 111, 2005-2019.
19. Raats, J. M., Pieper, F. R., Vree Egberts, W. T., Verrijp, K. N., Ramaekers, F. C., and Bloemendal, H. (1990). Assembly of amino-terminally deleted desmin in vimentin-free cells. J. Cell Biol. 111, 1971-1985.
20. Hatzfeld, M., and Burba, M. (1994). Function of type I and type II keratin head domains: Their role in dimer, tetramer and filament formation. J. Cell Sci. 107, 1959-1972.
21. Herrmann, H., Haner, M., Brettel, M., Muller, S. A., Goldie, K. N., Fedtke, B., Lustig, A., Franke, W. W., and Aebi, U. (1996). Structure and assembly properties of the intermediate filament protein vimentin: The role of its head, rod and tail domains. J. Mol. Biol. 264, 933-953.
22. Traub, P., Scherbarth, A., Wiegers, W., and Shoeman, R. L. (1992). Salt-stable interaction of the amino-terminal head region of vimentin with the α-helical rod domain of cytoplasmic intermediate filament proteins and its relevance to protofilament structure and filament formation and stability. J. Cell Sci. 101, 363-381.
23. Kouklis, P. D., Traub, P., and Georgatos, S. D. (1992). Involvement of the consensus sequence motif at coil 2b in the assembly and stability of vimentin filaments. J. Cell Sci. 102, 31-41.
24. Herrmann, H., Hofmann, I., and Franke, W. W. (1992). Identification of a nonapeptide motif in the vimentin head domain involved in intermediate filament assembly. J. Mol. Biol. 223, 637-650.
25. Hatzfeld, M., Dodemont, H., Plessmann, U., and Weber, K. (1992). Truncation of recombinant vimentin by ompT. Identification of a short motif in the head domain necessary for assembly of type III intermediate filament proteins. FEBS Lett. 302, 239-242.
26. Beuttenmüller, M., Chen, M., Janetzko, A., Kühn, S., and Traub, P. (1994). Structural elements of the amino-terminal head domain of vimentin essential for intermediate filament formation in vivo and in vitro. Exp. Cell Res. 213, 128-142.
27. Eriksson, J. E., Opal, P., and Goldman, R. D. (1992). Intermediate filament dynamics. Curr. Opin. Cell Biol. 4, 99-104.
28. Inagaki, M., Matsuoka, Y., Tsujimura, K., Ando, S., Tokui, T., Takahashi, T., and Inagaki, M. (1996). Dynamic property of intermediate filaments: Regulation by phosphorylation. BioEssays 18, 481-487.
29. Gohara, R., Tang, D., Inada, H., Inagaki, M., Takasaki, Y., and Ando, S. (2001). Phosphorylation of vimentin head domain inhibits interaction with the carboxyl-terminal end of alpha-helical rod domain studied by surface plasmon resonance measurements. FEBS Lett. 489, 182-186.
30. Traub, P., Mothes, E., Shoeman, R. L., Schröder, R., and Scherbarth, A. (1992). Binding of nucleic acids to intermediate filaments of the vimentin type and their effects on filament formation and stability. J. Biomol. Struct. Dyn. 10, 505-531.
31. Perides, G., Scherbarth, A., and Traub, P. (1986). Influence of phospholipids on the formation and stability of vimentin-type intermediate filaments. Eur. J. Cell Biol. 42, 268-280.
32. Quinlan, R., Hutchison, C., and Lane, B. (1995). "Intermediate Filament Proteins. Protein, Profile 2." pp. 795-952. Academic Press, London.
33. Sharp, G., Osborn, M., and Weber, K. (1982). Occurrence of two different intermediate filament proteins in the same filament in situ within a human glioma cell line. An immunoelectron microscopical study. Exp. Cell Res. 141, 385-395.
34. Quinlan, R. A., and Franke, W. W. (1983). Molecular interactions in intermediate-sized filaments revealed by chemical cross-linking. Heteropolymers of vimentin and glial filament protein in cultured human glioma cells. Eur. J. Biochem. 132, 477-484.
35. Wang, E., Cairncross, J. G., and Liem, R. K. (1984). Identification of glial filament protein and vimentin in the same intermediate filament system in human glioma cells. Proc. Natl. Acad. of Sci. USA 81, 2102-2106.
36. Shoeman, R. L., Hartig, R., and Traub, P. (1999). Characterization of the nucleic acid binding region of the intermediate filament protein vimentin by fluorescence polarization. Biochemistry 38, 16802-16809.
37. Shoeman, R. L., Hüttermann, C., Hartig, R., and Traub, P. (2001). Amino-terminal polypeptides of vimentin are responsible for the changes in nuclear architecture associated with human immunodeficiency virus type 1 protease activity in tissue culture cells. Mol. Biol. Cell 12, 143-154.
38. Kouklis, P. D., Hatzfeld, M., Brunkener, M., Weber, K., and Georgatos, S. D. (1993). In vitro assembly properties of vimentin mutagenized at the β-site tail motif. J. Cell Sci. 106, 919-928.
39. Hartig, R., Shoeman, R. L., Janetzko, A., Tolstonog, G., and Traub, P. (1998). DNA-mediated transport of the intermediate filament protein vimentin into the nucleus of cultured cells. J. Cell Sci. 111, 3573-3584.
40. Hartig, R., Huang, Y., Janetzko, A., Shoeman, R., Grüb, S., and Traub P. (1997). Binding of fluorescence- and gold-labeled oligodeoxyribonucleotides to cytoplasmic intermediate filaments in epithelial and fibroblast cells. Exp. Cell Res. 233, 169-186.
41. Djabali, K., Piron, G., de Néchaus, B., and Portier, M.-M. (1999). αB-crystallin interactions with cytoplasmic intermediate filament bundles during mitosis. Exp. Cell Res. 253, 649-662.
42. Lu, X., Quinlan, R. A., Steel, J. B., and Lane, E. B. (1993). Network incorporation of intermediate filament molecules differs between preexisting and newly assembling filaments. [erratum appears in Exp. Cell Res. 211, 424 (1994)]. Exp. Cell Res. 208, 218-225.
43. Andreoli, J. M., and Trevor, K. T. (1994). Fate of a headless vimentin protein in stable cell cultures: Soluble and cytoskeletal forms. Exp. Cell Res. 214, 177-188.
44. Strelkov, S. V., Herrmann, H., Geisler, N., Lustig, A., Ivaninskii, S., Zimbelmann, R., Burkhard, P., and Aebi, U. (2001). Divide-and-conquer crystallographic approach towards an atomic structure of intermediate filaments. J. Mol. Biol. 306, 773-781.
45. Hofmann, I., and Herrmann, H. (1992). Interference in vimentin assembly in vitro by synthetic peptides derived from the vimentin head domain. J. Cell Sci. 101, 687-700.
46. Geisler, N., Hatzfeld, M., and Weber, K. (1989). Phosphorylation in vitro of vimentin by protein kinases A and C is restricted to the head domain. Identification of the phosphoserine sites and their influence on filament formation. Eur. J. Biochem. 183, 441-447.
47. Wiegers, W., Höner, B., and Traub, P. (1991). Microinjection of intermediate filament proteins into living cells with and without preexisting intermediate filament network. Cell Biol. Int. 15, 287-296.
48. Chen, W. J., and Liem, R. K. (1994). The endless story of the glial fibrillary acidic protein. J. Cell Sci. 107, 2299-2311.
49. Wang, Q., Tolstonog, G. V., Shoeman, R., and Traub, P. (2001). Sites of nucleic acid binding in type I-IV intermediate filament subunit proteins. Biochemistry 40, 10342-10349.
50. Tolstonog, G. V., Wang, X., Shoeman, R., and Traub, P. (2000). Intermediate filaments reconstituted from vimentin, desmin, and glial fibrillary acidic protein selectively bind repetitive and mobile DNA sequences from a mixture of mouse genomic DNA fragments. DNA Cell Biol. 19, 647-677.
51. Wang, Q., Shoeman, R., and Traub, P. (2000). Identification of the amino acid residues of the amino terminus of vimentin responsible for DNA binding by enzymatic and chemical sequencing and analysis by MALDI-TOF. Biochemistry 39, 6645-6651.
52. Perides, G., Harter, C., and Traub, P. (1987). Electrostatic and hydrophobic interactions of the intermediate filament protein vimentin and its amino terminus with lipid bilayers. J. Biol. Chem. 262, 13742-13749.
53. Inagaki, M., Gonda, Y., Nishizawa, K., Kitamura, S., Sato, C., Ando, S., Tanabe, K., Kikuchi, K., Tsuiki, S., and Nishi, Y. (1990). Phosphorylation sites linked to glial filament disassembly in vitro locate in a non-α-helical head domain. J. Biol. Chem. 265, 4722-4729.
54. Huang, H.-Y., Graves, D. J., Robson, R. M., and Huiatt, T. W. (1993). ADP-ribosylation of the intermediate filament protein desmin by ADP-ribosyl-transferase. FASEB J. 7, A1078.
55. Haltiwanger, R. S., Kelly, W. G., Roquemore, E. P., Blomberg, M. A., Dong, L.-Y. D., Kreppel, L. Chou, T.-Y., and Hart, G. W. (1992). Glycosylation of nuclear and cytoplasmic proteins is ubiquitous and dynamic. Biochem. Soc. Transact. 20, 264-269.
56. Bravo, R., Small, J. V., Fey, S., Larsen, P. M., and Cellis, J. E. (1982). Architecture and polypeptide composition of HeLa cytoskeletons. Modification and cytoarchitecture polypeptides during mitosis. J. Mol. Biol. 154, 121-143.
57. Shoeman, R. L., Höner, B., Stoller, T. J., Kesselmeier, C., Miedel, M. C., Traub, P., and Graves, M. C. (1990). Human immunodeficiency virus type 1 protease cleaves the intermediate filament proteins vimentin, desmin, and glial fibrillary acidic protein. Proc. Natl. Acad. Sci. USA 87, 6336-6340.
58. Lindhofer, H., Nitschko, H., Wachinger, G., and von der Helm, K. (1993). Human immunodeficiency virus (HIV) proteinase in HIV-infected cell culture: Dual intracelluar effects in the absence or presence of inhibitor. In "Proteolysis and Protein Turnover" (J. S. Bond, and A. J. Barret, Eds.), pp. 219-224, Portland Press, London.
59. 2+-dependent deimination-induced disassembly of intermediate filaments involves specific modification of the amino-terminal head domain. J. Biol. Chem. 264, 18119-18127.
60. Traub, P., and Shoeman, R. L. (1994). Intermediate filament proteins: Cytoskeletal elements with gene-regulatory function? Int. Rev. Cytol. 154, 1-103.
61. Traub, P., and Shoeman, R. L. (1994). Intermediate filament and related proteins: Potential activators of nucleosomes during transcription initiation and elongation? BioEssays 16, 349-355.
62. Tolstonog, G. V., Mothes, E., Shoeman, R. L., and Traub, P. (2001). Isolation of SDS-stable complexes of the intermediate filament protein vimentin with repetitive, mobile, nuclear matrix attachment region and mitochondrial DNA sequence elements from cultured mouse and human fibroblasts. DNA Cell Biol. 20, 531-554.
63. Wang, X., Tolstonog, G., Shoeman, R. L., and Traub, P. (1996). Selective binding of specific mouse genomic DNA fragments by mouse vimentin filaments in vitro. DNA Cell Biol. 15, 209-225.
64. Colucci-Guyon, E., Portier, M.-M., Dunia, I., Paulin, D., Pournin, S., and Babinet, C. (1994). Mice lacking vimentin develop and reproduce without an obvious phenotype. Cell 79, 679-694.
65. Tolstonog, G. V., Shoeman, R. L., Traub, U., and Traub, P. (2001). Role of the intermediate filament protein vimentin in delaying senescence and in the spontaneous immortalization of mouse embryo fibroblasts. DNA Cell Biol. 20, 509-530.