Characterization of mammalian synemin, an intermediate filament protein present in all four classes of muscle cells and some neuroglial cells: Co-localization and interaction with type III intermediate filament proteins and keratins

Cell and Tissue Research

Volumn 313, Issue 2, 2003, Pages 195-207

  Hirako, Yoshiaki ^a,e   Yamakawa, Hisashi ^b   Tsujimura, Yuki ^a   Nishizawa, Yuji ^c   Okumura, Masayo ^a   Usukura, Jiro ^c   Matsumoto, Hiroyuki ^d   Jackson, Kenneth W ^d   Owaribe, Katsushi ^a   Ohara, Osamu ^b  

^a NAGOYA UNIVERSITY   (Japan)

^b KAZUSA DNA RESEARCH INSTITUTE   (Japan)

^c NAGOYA UNIVERSITY SCHOOL OF MEDICINE   (Japan)

^d UNIVERSITY OF OKLAHOMA COLLEGE OF MEDICINE   (United States)

^e UNIVERSITY OF WÜRZBURG   (Germany)

Author keywords

Electron microscopy; Immunohistochemistry; Intermediate filament; Mammalian synemin; Mammalian tissues; Purification

Indexed keywords

COMPLEMENTARY DNA; CYTOKERATIN 14; DESMIN; GLIAL FIBRILLARY ACIDIC PROTEIN; INTERMEDIATE FILAMENT PROTEIN; KERATIN; KERATIN 5; KERATIN 6; NEBULIN; SYNEMIN; UNCLASSIFIED DRUG; VIMENTIN;

AMINO ACID SEQUENCE; ANIMAL CELL; ARTICLE; ASTROCYTE; CYTOSKELETON; HEART MUSCLE; HUMAN; IMMUNOBLOTTING; INTERMEDIATE FILAMENT; MOLECULAR CLONING; MUSCLE CELL; NONHUMAN; NUCLEOTIDE SEQUENCE; OPTIC NERVE; PRIORITY JOURNAL; PROTEIN ASSEMBLY; PROTEIN FUNCTION; PROTEIN LOCALIZATION; PROTEIN PROTEIN INTERACTION; SCHWANN CELL; SKELETAL MUSCLE; SMOOTH MUSCLE;

ANIMALS; ANTIBODIES, MONOCLONAL; ANTIGENS; DESMIN; GENE EXPRESSION REGULATION; HUMANS; IMMUNOHISTOCHEMISTRY; INTERMEDIATE FILAMENT PROTEINS; KERATINS; MUSCLE PROTEINS; MUSCLE, SKELETAL; MUSCLE, SMOOTH; MUSCLES; MYOCARDIUM; NEUROGLIA; RABBITS; TISSUE DISTRIBUTION;

ANIMALIA; MAMMALIA;

EID: 10744230626     PISSN: 0302766X     EISSN: None     Source Type: Journal    
DOI: 10.1007/s00441-003-0732-2     Document Type: Article

References (44)

1. Bellin RM, Sernett SW, Becker B, Ip W, Huiatt TW, Robson RM (1999) Molecular characteristics and interactions of the intermediate filament protein synemin. Interactions with alpha-actinin may anchor synemin-containing heterofilaments. J Biol Chem 274:29493-29499
2. Bellin RM, Huiatt TW, Critchley DR, Robson RM (2001) Synemin may function to directly link muscle cell intermediate filaments to both myofibrillar Z-lines and costameres. J Biol Chem 276:32330-32337
3. Bilak SR, Sernett SW, Bilak MM, Bellin RM, Stromer MH, Huiatt TW, Robson RM (1998) Properties of the novel intermediate filament protein synemin and its identification in mammalian muscle. Arch Biochem Biophys 355:63-76
4. Calvo JL, Carbonell AL, Boya J (1990) Coexpression of vimentin and glial fibrillary acidic protein in astrocytes of the adult rat optic nerve. Brain Res 532:355-357
5. Church GM, Gilbert W (1984) Genomic sequencing. Proc Natl Acad Sci U S A 81:1991-1995
6. Giudice GJ, Emery DJ, Diaz LA (1992) Cloning and primary structural analysis of the bullous pemphigoid autoantigen BP180. J Invest Dermatol 99:243-250
7. Granger BL, Lazarides E (1978) The existence of an insoluble Z disc scaffold in chicken skeletal muscle. Cell 15:1253-1268
8. Granger BL, Lazarides E (1980) Synemin: a new high molecular weight protein associated with desmin and vimentin filaments in muscle. Cell 22:727-738
9. Granzier HL, Wang K (1993) Gel electrophoresis of giant proteins: solubilization and silver-staining of titin and nebulin from single muscle fiber segments. Electrophoresis 14:56-64
10. Hatzfeld M, Maier G, Franke WW (1987) Cytokeratin domains involved in heterotypic complex formation determined by in-vitro binding assays. J Mol Biol 197:237-255
11. Hemken PM, Bellin RM, Sernett SW, Becker B, Huiatt TW, Robson RM (1997) Molecular characteristics of the novel intermediate filament protein paranemin. Sequence reveals EAP-300 and IFAPa-400 are highly homologous to paranemin. J Biol Chem 272:32489-32499
12. Hemmati-Brivanlou A, Mann RW, Harland RM (1992) A protein expressed in the growth cones of embryonic vertebrate neurons defines a new class of intermediate filament protein. Neuron 9:417-428
13. Herrmann H, Aebi U (2000) Intermediate filaments and their associates: multi-talented structural elements specifying cytoarchitecture and cytodynamics. Curr Opin Cell Biol 12:79-90
14. Hesse M, Magin TM, Weber K (2001) Genes for intermediate filament proteins and the draft sequence of the human genome: novel keratin genes and a surprisingly high number of pseudogenes related to keratin genes 8 and 18. J Cell Sci 114:2569-2575
15. Hieda Y, Nishizawa Y, Uematsu J, Owaribe K (1992) Identification of a new hemidesmosomal protein, HD1: a major, high molecular mass component of isolated hemidesmosomes. J Cell Biol 116:1497-1506
16. Hirako Y, Usukura J, Nishizawa Y, Owaribe K (1996) Demonstration of the molecular shape of BP180, a 180-kDa bullous pemphigoid antigen and its potential for trimer formation. J Biol Chem 271:13739-13745
17. Hirako Y, Tsujimura Y, Nishizawa Y, Owaribe K (1998) Novel muscle proteins associating with desmin. Cell Struct Funct 23:78 (Abstr)
18. Hisanaga S, Hirokawa N (1988) Structure of the peripheral domains of neurofilaments revealed by low angle rotary shadowing. J Mol Biol 202:297-305
19. Hori K, Hashimoto K, Eto H, Dekio S (1985) Keratin type intermediate filaments in sweat gland myoepithelial cells. J Invest Dermatol 85:453-459
20. Keller TC (1995) Structure and function of titin and nebulin. Curr Opin Cell Biol 7:32-38
21. Labeit S, Kolmerer B (1995) The complete primary structure of human nebulin and its correlation to muscle structure. J Mol Biol 248:308-315
22. Lendahl U, Zimmerman LB, McKay RD (1990) CNS stem cells express a new class of intermediate filament protein. Cell 60:585-595
23. Leung CL, Liem RK, Parry DA, Green KJ (2001) The plakin family. J Cell Sci 114:3409-3410
24. Marvin MJ, Dahlstrand J, Lendahl U, McKay RD (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
25. Mirsky R, Jessen KR (1986) The biology of non-myelin-forming Schwann cells. Ann N Y Acad Sci 486:132-146
26. Mizuno Y, Thompson TG, Guyon JR, Lidov HG, Brosius M, Imamura M, Ozawa E, Watkins SC, Kunkel LM (2001) Desmuslin, an intermediate filament protein that interacts with alpha-dystrobrevin and desmin. Proc Natl Acad Sci U S A 98:6156-6161
27. Moncman CL, Wang K (1996) Assembly of nebulin into the sarcomeres of avian skeletal muscle. Cell Motil Cytoskeleton 34:167-184
28. Nagase T, Ishikawa K, Nakajima D, Ohira M, Seki N, Miyajima N, Tanaka A, Kotani H, Nomura N, Ohara O (1997) Prediction of the coding sequences of unidentified human genes. VII. The complete sequences of 100 new cDNA clones from brain which can code for large proteins in vitro. DNA Res 4:141-150
29. Newey SE, Howman EV, Ponting CP, Benson MA, Nawrotzki R, Loh NY, Davies KE, Blake DJ (2001) Syncoilin, a novel member of the intermediate filament superfamily that interacts with alpha-dystrobrevin in skeletal muscle. J Biol Chem 276:6645-6655
30. Nishizawa Y, Uematsu J, Owaribe K (1993) HD4, a 180 kDa bullous pemphigoid antigen, is a major transmembrane glycoprotein of the hemidesmosome. J Biochem (Tokyo) 113:493-501
31. Nishizawa Y, Komori N, Usukura J, Jackson KW, Tobin SL, Matsumoto H (1999) Initiating ocular proteomics for cataloging bovine retinal proteins: microanalytical techniques permit the identification of proteins derived from a novel photoreceptor preparation. Exp Eye Res 69:195-212
32. Ohara O, Ohara R, Yamakawa H, Nakajima D, Nakayama M (1998) Characterization of a new beta-spectrin gene which is predominantly expressed in brain. Mol Brain Res 57:181-192
33. Owaribe K, Nishizawa Y, Franke WW (1991) Isolation and characterization of hemidesmosomes from bovine corneal epithelial cells. Exp Cell Res 192:622-630
34. Paramio JM, Casanova ML, Alonso A, Jorcano JL (1997) Keratin intermediate filament dynamics in cell heterokaryons reveals diverse behaviour of different keratins. J Cell Sci 110:1099-1111
35. Poon E, Howman EV, Newey SE, Davies KE (2002) Association of syncoilin and desmin: linking intermediate filament proteins to the dystrophin-associated protein complex. J Biol Chem 277:3433-3439
36. Purkis PE, Steel JB, Mackenzie IC, Nathrath WB, Leigh IM, Lane EB (1990) Antibody markers of basal cells in complex epithelia. J Cell Sci 97:39-50
37. Renner W, Franke WW, Schmid E, Geisler N, Weber K, Mandelkow E (1981) Reconstitution of intermediate-sized filaments from denatured monomeric vimentin. J Mol Biol 149:285-306
38. Schmid E, Schiller DL, Grund C, Stadler J, Franke WW (1983) Tissue type-specific expression of intermediate filament proteins in a cultured epithelial cell line from bovine mammary gland. J Cell Biol 96:37-50
39. Schweitzer SC, Klymkowsky MW, Bellin RM, Robson RM, Capetanaki Y, Evans RM (2001) Paranemin and the organization of desmin filament networks. J Cell Sci 114:1079-1089
40. Sejersen T, Lendahl U (1993) Transient expression of the intermediate filament nestin during skeletal muscle development. J Cell Sci 106:1291-1300
41. Steinert PM, Chou YH, Prahlad V, Parry DA, Marekov LN, Wu KC, Jang SI, Goldman RD (1999) A high molecular weight intermediate filament-associated protein in BHK-21 cells is nestin, a type VI intermediate filament protein. Limited coassembly in vitro to form heteropolymers with type III vimentin and type IV alpha-internexin. J Biol Chem 274:9881-9890
42. Sugita H, Nonaka I, Itoh Y, Asakura A, Hu DH, Kimura S, Maruyama K (1987) Is nebulin the product of Duchenne muscular dystrophy gene? Proc Jpn Acad 63:107-110
43. Sultana S, Sernett SW, Bellin RM, Robson RM, Skalli O (2000) Intermediate filament protein synemin is transiently expressed in a subset of astrocytes during development. Glia 30:143-153
44. Titeux M, Brocheriou V, Xue Z, Gao J, Pellissier JF, Guicheney P, Paulin D, Li Z (2001) Human synemin gene generates splice variants encoding two distinct intermediate filament proteins. Eur J Biochem 268:6435-6449