Self-assembly incompetence of synemin is related to the property of its head and rod domains

Biochemistry

Volumn 47, Issue 36, 2008, Pages 9531-9539

  Khanamiryan, Luiza ^a,b   Li, Zhenlin ^a,b   Paulin, Denise ^b   Xue, Zhigang ^a,b  

^a SORBONNE UNIVERSITÉ   (France)

^b CNRS   (France)

Author keywords

[No Author keywords available]

Indexed keywords

ABS RESINS; COMPUTER NETWORKS; ERROR ANALYSIS; NUCLEIC ACIDS;

FILAMENT NETWORKS; HELICAL RODS; VIMENTIN;

SELF ASSEMBLY;

CHIMERIC PROTEIN; VIMENTIN;

ARTICLE; CELL CULTURE; IMMUNOFLUORESCENCE; INTERMEDIATE FILAMENT; MUTAGENESIS; NUCLEOTIDE SEQUENCE; PRIORITY JOURNAL; TRANSIENT TRANSFECTION;

AMINO ACID MOTIFS; CELL LINE, TUMOR; HUMANS; INTERMEDIATE FILAMENT PROTEINS; MUTAGENESIS, SITE-DIRECTED; POINT MUTATION; PROTEIN STRUCTURE, TERTIARY; RECOMBINANT FUSION PROTEINS;

VERTEBRATA;

EID: 51549106904     PISSN: 00062960     EISSN: None     Source Type: Journal    
DOI: 10.1021/bi800912w     Document Type: Article

References (52)

1. Herrmann, H., and Aebi, U. (2004) Intermediate filaments: Molecular structure, assembly mechanism, and integration into functionally distinct intracellular scaffolds. Annu. Rev. Biochem. 73, 749-789.
2. Strelkov, S. V., Herrmann, H., and Aebi, U. (2003) Molecular architecture of intermediate filaments. BioEssays 25, 243-251.
3. Fuchs, E., and Weber, K. (1994) Intermediate filaments: Structure, dynamics, function, and disease. Annu. Rev. Biochem. 63, 345-382.
4. Dahlstrand, J., Zimmerman, L. B., McKay, R. D., and Lendahl, U. (1992) Characterization of the human nestin gene reveals a close evolutionary relationship to neurofilaments. J. Cell Sci. 103, 589-597.
5. Titeux, M., Brocheriou, V., Xue, Z., Gao, J., Pellissier, J. F., Guicheney, P., Paulin, D., and Li, Z. (2001) Human synemin gene generates splice variants encoding two distinct intermediate filament proteins. Eur. J. Biochem. 268, 6435-6449.
6. Steinert, P. M., Idler, W. W., Cabral, F., Gottesman, M. M., and Goldman, R. D. (1981) In vitro assembly of homopolymer and copolymer filaments from intermediate filament subunits of muscle and fibroblastic cells. Proc. Natl. Acad. Sci. U.S.A. 78, 3692-3696.
7. Heins, S., Wong, P. C., Muller, S., Goldie, K., Cleveland, D. W., and Aebi, U. (1993) The rod domain of NF-L determines neurofilament architecture, whereas the end domains specify filament assembly and network formation. J. Cell Biol. 123, 1517-1533.
8. Ip, W., Hartzer, M. K., Pang, Y. Y., and Robson, R. M. (1985) Assembly of vimentin in vitro and its implications concerning the structure of intermediate filaments. J. Mol. Biol. 183, 365-375.
9. Chadan, S., Moya, K. L., Portier, M. M., and Filliatreau, G. (1994) Identification of a peripherin dimer: Changes during axonal development and regeneration of the rat sciatic nerve. J. Neurochem. 62, 1894-1905.
10. Bellin, R. M., Sernett, S. W., Becker, B., Ip, W., Huiatt, T. W., and Robson, R. M. (1999) Molecular characteristics and interactions of the intermediate filament protein synemin. Interactions with α-actinin may anchor synemin-containing heterofilaments. J. Biol. Chem. 274, 29493-29499.
11. Marvin, M. J., Dahlstrand, J., Lendahl, U., and McKay, R. D. (1998) A rod end deletion in the intermediate filament protein nestin alters its subcellular localization in neuroepithelial cells of transgenic mice. J. Cell Sci. 111, 1951-1961.
12. Coulombe, P. A., and Fuchs, E. (1990) Elucidating the early stages of keratin filament assembly. J. Cell Biol. 111, 153-169.
13. Hatzfeld, M., and Weber, K. (1990) The coiled coil of in vitro assembled keratin filaments is a heterodimer of type I and II keratins: Use of site-specific mutagenesis and recombinant protein expression. J. Cell Biol. 110, 1199-1210.
14. Herrmann, H., Haner, M., Brettel, M., Ku, N. O., and Aebi, U. (1999) Characterization of distinct early assembly units of different intermediate filament proteins. J. Mol. Biol. 286, 1403-1420.
15. Herrmann, H., Strelkov, S. V., Feja, B., Rogers, K. R., Brettel, M., Lustig, A., Haner, M., Parry, D. A., Steinert, P. M., Burkhard, P., and Aebi, U. (2000) The intermediate filament protein consensus motif of helix 2B: Its atomic structure and contribution to assembly. J. Mol. Biol. 298, 817-832.
16. Geisler, N., Kaufmann, E., and Weber, K. (1985) Antiparallel orientation of the two double-stranded coiled-coils in the tetrameric protofilament unit of intermediate filaments. J. Mol. Biol. 182, 173-177.
17. Steinert, P. M., Marekov, L. N., Fraser, R. D., and Parry, D. A. (1993) Keratin intermediate filament structure. Crosslinking studies yield quantitative information on molecular dimensions and mechanism of assembly. J. Mol. Biol. 230, 436-452.
18. Parry, D. A. (2005) Microdissection of the sequence and structure of intermediate filament chains. Adv. Protein Chem. 70, 113-142.
19. 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.
20. Lu, X., and Lane, E. B. (1990) Retrovims-mediated transgenic keratin expression in cultured fibroblasts: Specific domain functions in keratin stabilization and filament formation. Cell 62, 681-696.
21. 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.
22. Izmiryan, A., Cheraud, Y., Khanamiryan, L., Leterrier, J. F., Federici, T., Peltekian, E., Moura-Neto, V., Paulin, D., Li, Z., and Xue, Z. G. (2006) Different expression of synemin isoforms in glia and neurons during nervous system development. Glia 54, 204-213.
23. Xue, Z. G., Cheraud, Y., Brocheriou, V., Izmiryan, A., Titeux, M., Paulin, D., and Li, Z. (2004) The mouse synemin gene encodes three intermediate filament proteins generated by alternative exon usage and different open reading frames. Exp. Cell Res. 298, 431-444.
24. Heins, S., and Aebi, U. (1994) Making heads and tails of intermediate filament assembly, dynamics and networks. Curr. Opin. Cell Biol. 6, 25-33.
25. 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.
26. Kreplak, L., Aebi, U., and Herrmann, H. (2004) Molecular mechanisms underlying the assembly of intermediate filaments. Exp. Cell Res. 301, 77-83.
27. Herrmann, H., and Aebi, U. (1998) Structure, assembly, and dynamics of intermediate filaments. Subcell. Biochem. 31, 319-362.
28. 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.
29. Riemer, D., and Weber, K. (1998) Common and variant properties of intermediate filament proteins from lower chordates and vertebrates: Two proteins from the tunicate Styela and the identification of a type III homologue. J. Cell Sci. 111, 2967-2975.
30. Shoeman, R. L., Hartig, R., Berthel, M., and Traub, P. (2002) 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, 344-353.
31. Hirokawa, N. (1982) Cross-linker system between neurofilaments, microtubules, and membranous organelles in frog axons revealed by the quick-freeze, deep-etching method. J. Cell Biol. 94, 129-142.
32. Gotow, T., Takeda, M., Tanaka, T., and Hashimoto, P. H. (1992) Macromolecular structure of reassembled neurofilaments as revealed by the quick-freeze deep-etch mica method: Difference between NF-M and NF-H subunits in their ability to form cross-bridges. Eur. J. Cell Biol. 58, 331-345.
33. Chen, J., Nakata, T., Zhang, Z., and Hirokawa, N. (2000) The C-terminal tail domain of neurofilament protein-H (NF-H) forms the crossbridges and regulates neurofilament bundle formation. J. Cell Sci. 113, 3861-3869.
34. Leterrier, J. F., Rusakov, D. A., Nelson, B. D., and Linden, M. (1994) Interactions between brain mitochondria and cytoskeleton: Evidence for specialized outer membrane domains involved in the association of cytoskeleton-associated proteins to mitochondria in situ and in vitro. Microsc. Res. Tech. 27, 233-261.
35. Miyasaka, H., Okabe, S., Ishiguro, K., Uchida, T., and Hirokawa, N. (1993) Interaction of the tail domain of high molecular weight subunits of neurofilaments with the COOH-terminal region of tubulin and its regulation by tau protein kinase II. J. Biol. Chem. 268, 22695-22702.
36. Frappier, T., Derancourt, J., and Pradel, L. A. (1992) Actin and neurofilament binding domain of brain spectrin β subunit. Eur. J. Biochem. 205, 85-91.
37. Starr, R., Xiao, J., and Monteiro, M. J. (1995) Production of monoclonal antibodies against neurofilament-associated proteins: Demonstration of association with neurofilaments by a coimmunoprecipitation method. J. Neurochem. 64, 1860-1867.
38. Bellin, R. M., Huiatt, T. W., Critchley, D. R., and Robson, R. M. (2001) Synemin may function to directly link muscle cell intermediate filaments to both myofibrillar Z-lines and costameres. J. Biol. Chem. 276, 32330-32337.
39. Bhosle, R. C., Michele, D. E., Campbell, K. P., Li, Z., and Robson, R. M. (2006) Interactions of intermediate filament protein synemin with dystrophin and utrophin. Biochem. Biophys. Res. Commun. 346, 768-777.
40. Sun, N., Critchley, D. R., Paulin, D., Li, Z., and Robson, R. M. (2008) Human α-synemin interacts directly with vinculin and metavinculin. Biochem. J. 409, 657-667.
41. Russell, M. A., Lund, L. M., Haber, R., McKeegan, K., Cianciola, N., and Bond, M. (2006) The intermediate filament protein, synemin, is an AKAP in the heart. Arch. Biochem. Biophys. 456, 204-215.
42. Strelkov, S. V., Herrmann, H., Geisler, N., Wedig, T., Zimbelmann, R., Aebi, U., and Burkhard, P. (2002) Conserved segments 1A and 2B of the intermediate filament dimer: Their atomic structures and role in filament assembly. EMBO J. 21, 1255-1266.
43. Crewther, W. G., Dowling, L. M., Steinert, P. M., and Parry, D. A. D. (1983) Structure of intermediate filament. Int. J. Biol. Macromol. 5, 267-274.
44. Mehrani, T., Wu, K. C., Morasso, M. I., Bryan, J. T., Marekov, L. N., Parry, D. A., and Steinert, P. M. (2001) 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, 2088-2097.
45. Marchuk, D., McCrohon, S., and Fuchs, E. (1984) Remarkable conservation of structure among intermediate filament genes. Cell 39, 491-498.
46. Lersch, R., and Fuchs, E. (1988) Sequence and expression of a type II keratin, K5, in human epidermal cells. Mol. Cell. Biol. 8, 486-493.
47. Ferrari, S., Battini, R., Kaczmarek, L., Rittling, S., Calabretta, B., de Riel, J. K., Philiponis, V., Wei, J. F., and Baserga, R. (1986) Coding sequence and growth regulation of the human vimentin gene. Mol. Cell. Biol. 6, 3614-3620.
48. Li, Z. L., Lilienbaum, A., Butler-Browne, G., and Paulin, D. (1989) Human desmin-coding gene: Complete nucleotide sequence, characterization and regulation of expression during myogenesis and development. Gene 78, 243-254.
49. Landon, F., Lemonnier, M., Benarous, R., Hue, C., Fiszman, M., Gros, F., and Portier, M. M. (1989) Multiple mRNAs encode peripherin, a neuronal intermediate filament protein. EMBO J. 8, 1719-1726.
50. Kumanishi, T., Usui, H., Ichikawa, T., Nishiyama, A., Katagiri, T., Abe, S., Yoshida, Y., Washiyama, K., Kuwano, R., Sakimura, K., et al. (1992) Human glial fibrillary acidic protein (GFAP): Molecular cloning of the complete cDNA sequence and chromosomal localization (chromosome 17) of the GFAP gene. Acta Neuropathol. 83, 569-578.
51. Julien, J. P., Grosveld, F., Yazdanbaksh, K., Flavell, D., Meijer, D., and Mushynski, W. (1987) The structure of a human neurofilament gene (NF-L): A unique exon-intron organization in the intermediate filament gene family. Biochim. Biophys. Acta 909, 10-20.
52. Fliegner, K. H., Ching, G. Y., and Liem, R. K. (1990) The predicted amino acid sequence of α-internexin is that of a novel neuronal intermediate filament protein. EMBO J. 9, 749-755.