Lamins: Building blocks or regulators of gene expression?

Nature Reviews Molecular Cell Biology

Volumn 3, Issue 11, 2002, Pages 848-858

  Hutchison, Christopher J ^a  

^a DURHAM UNIVERSITY   (United Kingdom)

Author keywords

[No Author keywords available]

Indexed keywords

GENE PRODUCT; INTERMEDIATE FILAMENT PROTEIN; LAMIN; LAMIN DERIVATIVE; PROTEIN LMNA; PROTEIN STA; UNCLASSIFIED DRUG;

AUTOSOMAL DOMINANT DISORDER; AUTOSOMAL RECESSIVE DISORDER; CELL FUNCTION; CELL NUCLEUS; CELL SHAPE; CELL STRUCTURE; CYTOSKELETON; DNA REPLICATION; EMERY DREIFUSS MUSCULAR DYSTROPHY; GENE EXPRESSION REGULATION; GENETIC DISORDER; HEART DILATATION; HEREDITARY MOTOR SENSORY NEUROPATHY; HUMAN; LIMB GIRDLE MUSCULAR DYSTROPHY; LIPODYSTROPHY; MOLECULAR EVOLUTION; NONHUMAN; PATHOGENESIS; PRIORITY JOURNAL; PROTEIN DOMAIN; PROTEIN FUNCTION; REVIEW; TRANSCRIPTION REGULATION;

ANIMALS; CARDIOMYOPATHY, DILATED; CELL NUCLEUS; CHARCOT-MARIE-TOOTH DISEASE; DNA REPLICATION; EVOLUTION; GENE EXPRESSION REGULATION; HUMANS; LAMINS; LIPODYSTROPHY; MUSCULAR DYSTROPHY, EMERY-DREIFUSS; NUCLEAR ENVELOPE; NUCLEAR LAMINA; NUCLEAR PORE; TRANSCRIPTION, GENETIC;

EID: 0036843975     PISSN: 14710072     EISSN: None     Source Type: Journal    
DOI: 10.1038/nrm950     Document Type: Review

References (121)

1. Aebi, U., Cohn, J., Buhle, L. & Gerace, L. The nuclear lamina is a meshwork of intermediate filament type filaments. Nature 323, 560-564 (1986). The first demonstration that the nuclear lamina is composed of Intermediate-type filaments with a two-dimensional organization over the inner nuclear membrane.
2. Zhang, C., Jenkins, H. E., Goldberg, M., Allen, T & Hutchison, C. J. Nuclear lamina and nuclear matrix organisation in sperm pronuclei assembled in Xenopus egg extract. J. Cell Sci. 109, 2275-2286 (1996).
3. Belmont, A. S., Zhai, Y. & Thilenius, A. Lamin B distribution and association with peripheral chromatin revealed by optical sectioning and electron tomography. J. Cell Biol. 51, 383-392.(1993).
4. Hutchison, C. J., Alvarez-Reyes, M. & Vaughan, O. A, Lamins in disease: Why do ubiquitously expressed nuclear envelope proteins give rise to tissue specific disease phenotypes? J. Cell Sci. 114, 9-19 (2001). A review highlighting the way in which mutations in LMNA that cause human disease might be expected to alter LMNA assembly properties.
5. Quinlan, R., Hutchison, C. & Lane, B. Intermediate filament proteins. Protein Profiles 2, 801-952 (1995).
6. Wilson, K. L., Zastro, M. S, & Lee, K. K. Lamins and disease: Insights into nuclear infrastructure, Cell 104, 647-650 (2001).
7. Erber, A., Riemer, D., Ledger, N. & Weber, K. Molecular phylogeny of metazoan intermediate filament proteins, J. Mol. Evol. 47, 751-762 (1998).
8. Fuchs, E. & Weber, K. Intermediate filaments: Structure dynamics, function and disease. Annu. Rev. Biochem. 63, 345-382 (1994).
9. Hemmann, H. & Aebi, U. Intermediate filaments and their associates: Multi-talented structural elements specifying cytoarchitecture and cytodynamics. Curr. Opin. Cell Biol. 12, 79-90 (2000).
10. Karabinos, A., Schünemann, J., Parry, D.A. & Weber, K. Tissue-specific co-expression and in vitro heteropolymer formation of the two small Brachiostoma intermediate filament proteins A3 and B2. J. Mol. Biol. 316, 127-137 (2002).
11. Dönng, V. & Stick, R. Gene structure of nuclear lamin LIII of Xenopus laevis; a model for the evolution of IF proteins from lamin-like ancestor. EMBO J. 9, 4073-4081 (1990). An initial attempt to explain the phylogeny of intermediate filament proteins through exon shuffling
12. Röber, R.-A., Weber, K. & Osborn, M, Differential timing of nuclear lamin A/C expression in the various organs of the mouse embryo and the young animal: A developmental study. Development 105, 365-378 (1989). Elegant and comprehensive study detailing lamin expression patterns during mouse development
13. Stick, R. & Hausen, P. Changes in the nuclear lamina composition during early development of Xenopus laevis. Cell 41, 191-200 (1985). The first study on lamin expression patterns during development.
14. Lenher, C. F., Stick, R., Eppenberger, H. M. & Nigg, E.A. Differential expression of nuclear lamin proteins during chicken development. J. Cell Biol. 105, 577-587 (1987).
15. Stewart, C. & Burke, B. Teratocarcinoma stem cells and early mouse embryos contain only a single major lamin polypeptide closely resembling lamin B. Cell 51, 383-392 (1987).
16. Stick, R. cDNA cloning of the developmentally regulated lamin Liii of Xenopus laevis.EMBO J. 7, 3189-3197 (1988).
17. Hofemeister, H., Kuhn, C., Franke, W. W., Weber, K. & Stick, R, Conservation of the gene structure and membrane-targeting signals of germ cell-specific lamin Liii in amphibians and fish. Eur. J. Cell Biol. 81, 51-60 (2002).
18. Lenz-Böhme, B. etal. Insertional mutation of the Drosophila nuclear lamin Dm0 gene results in defective nuclear envelopes, clustering of nuclear pore complexes, and accumulation of annulate lamellae. J. Cell Biol. 137, 1001-1016(1997). The first in vivo evidence for the function of lamin polypeptides.
19. Lui, J. et al. Essential roles of Caenorhabditis elegans lamin gene in nuclear organisation, cell cycle progression, and spatial organization of nuclear pore complexes. Mol. Biol. Cell 11, 3937-3947 (2000). An important paper highlighting the role of lamins in organization of the nuclear envelope and revealing new functions in germline development.
20. Fisher, D., Chaudhary N. & Blobel, G. cDNA sequencing of nuclear lamins A and C reveals primary and secondary structure homology to intermediate filament proteins. Proc. Natl. Acad. Sci. USA 83, 6450-6454 (1986).
21. McKeon, F., Kirschner, M. & Caput, D. Homologies in both primary and secondary structure between nuclear envelope and intermediate filament proteins. Nature 319, 407-414 (1986). The first cloning of a lamin and direct demonstration that lamins are members of the IF superfamily.
22. Frangioni, J. & Neel, B. Use of a general purpose mammalian expression vector for studying intrace intracellular protein targeting: Identification of critical residues in the nuclear lamin A/C nuclear localisation sequence. J. Cell Sci. 105, 481-488 (1993).
23. Holt, I., Clements, L., Manilal, S., Brown, S. C. & Morris, G. E. The R428Q lamin A/C mutation that causes lipodystrophy does not prevent nuclear targeting of lamin A in adipocytes or its interaction with emerin, Eur. J. Hum. Genet. 9, 204-208 (2001).
24. Krohne, G., Walsenegger, I. & Hoger, T. The conserved carboxy-terminal cysteine of nuclear lamins is essential for lamin association with the nuclear envelope. J. Cell Biol. 109, 2003-2011 (1989).
25. Vorburger, K., Kitten, G. T. & Nigg, E. A. Modification of nuclear lamln proteins by a mevalonic acid derivative occurs in reticulocyte lysates and requires the cysteine residue of the C-terminal CxxM motif. EMBO J. 8, 4007-4013 (1989).
26. Riemer, D., Karabinos, A. & Weber, K. Analysis of eight cDNAs and six genes for intermediate filament protein in the cephalochordate Brachiostoma reveals differences in the multigene families of lower chordates and the vertebrates. Gene 211, 361-373 (1998).
27. Furukawa, K. & Hotta, Y. cDNA cloning of a germ cell specific lamin B, from mouse spermatocytes and analysis of its function by ectopic expression in somatic cells, EMBO. J. 12, 97-106 (1993).
28. Schirmer, E. Guam, T. & Gerace, L. Involvement of the lamin rod domain in heterotypic lamin interactions important for nuclear organization. J. Cell Biol. 153, 479-489 (2001). Spectacular use of dominant-negative mutants to investigate lamina function in organization of the nuclear envelope.
29. Sullivan, T. et al. Loss of A-type lamin expression compromises nuclear envelope integrity leading to muscular dystrophy. J. Cell Biol. 147, 913-920 (1999). The first mouse model of a iamin lamin disease.
30. Vigoroux, C. et al. Nuclear disorganization in fibroblasts from lipodystrophic patients with heterozygous R482Q/W mutations in the lamin A/C gene. J. Cell Sci. 114, 4459-4468 (2001)
31. de Noronha, C. M. L. et al. Dynamic disruption of nuclear envelope architecture and integrity induced by HIV-1 Vpr. Science 294, 1105-1108 (2001).
32. Hutchison, C. J. The use of cell-free extracts of xenopus eggs for studying DNA replication in vitro. The Cell Cycle: A Practical Approach (Oxford Univ. Press, Oxford, 1994)
33. Meier, J., Campbell, K. H. S., Ford, C. C., Stick, R. & Hutchison, C. J, The role oflamin Uii Lili in nuclear assembly and DNA replication, in cell-free extracts of Xenopus eggs. J. Cell Sci. 98, 271-279 (1991).
34. Newport, J., Wilson, K. L & Dunphy, W. Alamin independent pathway for nuclear envelope assembly. J. Cell Biol. 111, 2247-2259 (1990). References 33 and 34 were two initial reports on the role of lamins in DNA replication.
35. Spann, T. P., Moir, R. D., Goldman, A. E., Stick, R. & Goldman, R. D. Disruption of nuclear lamin organization alters the distribution of replication factors and inhibits DNA synthesis. J. Cell Biol. 136, 1201-1212 (1997).
36. Ellis, D. J., Jenkins, H. E., Whitfield, W. G. & Hutchison, C. J. GST-lamin fusion proteins act as dominant negative mutants in Xenopus egg extracts and reveal the function of the lamina in DNA replication. J. Cell Sci. 110, 2507-2518 (1997).
37. Gant, T. M., Harris, C. A. & Wilson, K. L. Roles of LAP2 proteins in nuclear assembly and DNA replication; truncated LAP2β proteins alter lamina assembly, envelope formation, nuclear size and DNA replication efficiency in Xenopus laevis egg extracts. J. Call Biol, 144, 1083-1096 (1999).
38. Broers, J. L. et al. A- and B-type lamins are differentially expressed in normal human tissue. Histochem. Cell Biol. 107, 505-517 (1997).
39. Moir, R. D., Yoon, M., Khoun, S. & Goldman, R. D. Nuclear lamins A and B1: Different pathways of assembly during nuclear envelope formation in living cells. J. Cell Biol. 151, 1155-1168 (2000).
40. Smythe, C., Jenkins H. E. & Hutchison, C. J. Incorporation of the nuclear pore basket protein NUP153 into nuclear pore structures is dependent upon lamina assembly. EMBO J. 19, 3918-3931 (2000).The first attempt at a molecular characterization of interactions between lamins and the nuclear pore complex.
41. Pante, N., Bastos, R., McMorrow, I., Burke. B. & Aebi,U. Interactions and three-dimensional Iocalizaton of a group of nuclear pore complex proteins. J. Cell Biol. 273, 1729-1732 (1994).
42. Walther, T. C. etal. The nucleoporin Nup153 is required for nuclear pore basket formation, nuclear pore complex anchoring and import of a subset of nuclear proteins. EMBO J. 20, 5703-5714 (2001). A comprehensive investigation of the function of Nup153 and its possible role in anchoring the NPC in the nuclear envelope.
43. Harris. C. A. et al. Structure and mapping of the human thymopoietin (TMPO) gene and relationship of human TMPO to rat lamin-associated polypeptide 2. Genomics 28, 198-205 (1994).
44. Senior, A.& Gereice, L. Integral membrane proteins specific to the inner nuclear membrane and associated with the lamina. J. Cell Biol. 107, 2029-2036 (1988). One of two papers that were the first to describe integral membrane proteins that bind to lamins.
45. Manilal, S., Nguyen, M., Sewry, C. A. & Morris, G. E. The Emery-Dreifuss muscular dystrophy protein, emerin, is a nuclear membrane protein, Hum. Mol. Genet. 5, 801-808 (1996).
46. Nagano, A. et al. Emedn deficiency at the nuclear membrane in patients with Emery-Draifuss muscular dystrophy. Nature Genet. 12, 254-259 (1996).
47. Powell, L, & Burke, B. Internuclear exchange of an inner nuclear membrane protein (p55) in heterokaryons. In vivo evidence for the interaction of p55 with the nuclear lamina. J. Cell Biol. 111, 2225-2234 (1990).
48. Vaughan, O. A. et al. Lamins A and C form a structural complex that anchors emerin at the NE, J. Cell Sci. 114, 2577-2590 (2001).
49. Lee, K. L. et al. Lamin-dependent localization of UNC-84, a protein required for nuclear migration in C. elegans. Mol. Biol. Cell 13, 892-901 (2002).
50. Gruenbaum, Y., Lee, K. K., Liu, J., Cohen, M. & Wilson, K. L. The expression, lamin-dependent localization and RNAi depletion phenotype for emerin in C. elegans. J. Cell Sci. 115, 923-929 (2002).
51. Ye, Q. & Worman, H. J. Primary structure analysis and lamin B and DNA binding of human LBR, an integral membrane protein of the nuclear envelope inner membrane. J. Biol. Chem. 269, 11306-11311 (1994). One of two important early papers on integral membrane proteins that associate with lamlns.
52. Zhang, Q. et al. Nesprins: A novel family of spectrin-repeat-containing proteins that localize to the nuclear membrane in multiple tissues. J. Cell Sci. 114, 4485-4498 (2001).
53. Dyer, J. A., Lane, E. B. & Hutchison, C. J. Investigations of the pathway of incorporation and function of lamin A in the nuclear lamina. Microsc. Res. Technol. 45, 1-12 (1999).
54. Dechat, T. et al. Intranuclear lamina-associated polypeptide 2 binds A-type lamins. J. Cell Sci. 113, 3473-3484 (2000).
55. Izumi, M., Vaughan, O. A., Hutchison, C. J. & Gilbert, D. Head and/or CaaX domain deletions of lamin proteins disrupt pre-formed lamin A/C but not lamin B structure in mammalian cells. Mol. Cell. Biol. 11, 4323-4337 (2000).
56. Horton, H., McMorrow, I. & Burke, B. Independent expression and assembly properties of heterologous lamins A and C in murine embryonal carcinomas. Eur. J. Cell Biol. 57, 172-183 (1992).
57. Pugh, G. E., Coates, P. J., Lane, E. B., Raymond, Y. & Quinlan, R. A. Distinct nuclear pathways for lamins A and C lead to their increase during quiescence in Swiss 3T3 cells. J. Cell Sci. 110, 2483,-2493 (1997).
58. Raharjo, W. H., Enarson, P., Sullivan, T., Stewart, C. L. & Burke, B. Nuclear envelope defects associated with LMNA mutations cause dilated cardiomyopathy and Emery-Dreifuss muscular dystrophy. J. Cell Sci. 114, 4447-4457 (2001).
59. Jackson, D.A. & Cook, P.R. Visualisation of a filamentous nucleoskeleton with a 23 nm axial repeat. EMBO J. 7, 3667-3677 (1988).
60. Goldman, A. E., Moir, R. D., Montag-Lowy, M., Stewart, M. & Goldman, R. D. Pathway of incorporation of microinjected lamin A into the nuclear envelope. J. Cell Biol. 119, 725-735 (1992). The first indication that lamins can be found in the interior of the nucleus as well as at the nuclear envelope.
61. Bridger, J. M., Kill, I. R., O'Farrell, M. & Hutchison, C. J. Internal lamin structures in G1 nuclei of human dermal fibroblasts. J. Cell Sci. 104, 297-306 (1993).
62. Jagatheesan, G. etal. Co-localization of intranuclear lamin foci with RNA splicing factors. J. Cell Sci. 112, 4651-4661 (1999). An interesting report on the association of lamin A with nuclear bodies.
63. Goldberg, M. W., Jenkins, H. E.. Allen, T., Whitfield, W. G. & Hutchison, C. J. Xenopus lamin B3 has a direct role in the assembly of a replication competent nucleus: Evidence from cell-free egg extracts. J. Cell Sci. 108, 3451-3461 (1995).
64. Moir, R. D., Montag-Lowy, M. & Goldman, R. D. Dynamic properties of nuclear lamins: Lamin B is associated with sites of DNA replication. J. Cell Biol. 125, 1201-1212 (1994). Initial evidence for the association of a lamin with a nuclear body.
65. Moir, R. D., Spann, T. P., Herrmann, H. & Goldberg, R. D. Disruption of nuclear lamin organization blocks the elongation phase of DNA replication. J. Cell Biol. 149, 1179-1192 (2000).
66. Harborth, J., Bbashir, S.M., Bechert, K.,Tuschl, T. & Weber, K. Identification of essential genes in cultured mammalian cells using small interfering RNAs. J. Cell Sci. 114, 4557-4565 (2001). The use of small interfering RNA (siRNA) to identify essential genes (including B-type lamins) in HeLa cells.
67. Nigg, E. A. The nuclear envelope. Curr. Opin. Cell Biol. 1, 435-440 (1989).
68. Benevente, R., Krohne, G. & Franke, W. Cell type specific expression of nuclear lamina proteins during development of Xenopus laevis. Cell 41, 177-190 (1985).
69. Spann, T. R, Goldman, A. E., Wang, C., Huang, S. & Goldman, R. D. Alteration of nuclear lamin organization inhibits RNA polymerase II-dependent transcription. J. Cell Biol. 156, 603-608 (2002). The first direct demonstration of a role for lamins in transcription.
70. Imai, S. et al. Dissociation of Oct-1 from the nuclear peripheral structures induces the cellular ageing-associated collagenase gene expression. Mol. Biol. Cell 8, 2407-2419 (1997). The first evidence of a role for nuclear envelope proteins in gene silencing.
71. Nili, E. et al. Nuclear membrane protein LAP2β mediates transcriptional repression alone and together with its binding partner GCL (germ cell-less). J. Cell Sci. 114, 3297-3307 (2001). Convincing evidence for the role of a complex of nuclear envelope proteins in transcriptional repression.
72. Ozaki,T. et al. Complex formation between lamin A and the retinoblastoma gene product: Identification of the domain on lamin A required for its interaction. Oncogene 9, 2649-2653 (1994).
73. Muralikishna, B., Dhawan, J., Rangaraj, N. & Parnaik, V. K. Distinct changes in intranuclear lamin A/C organization during myoblast differentiation. J. Cell Sci. 114, 4001-4011 (2001).
74. Lourim, D.& Lin, J.J.-C. Expression of nuclear lamin A and muscle specific proteins in differentiating muscle cells in ovo and in vitro. J. Cell Biol. 109, 495-504 (1989).
75. Sewry, C. A. et al. Skeletal muscle pathology in autosomal dominant Emery-Dreifuss muscular dystrophy with lamin A/C mutations. Neuropathol. Appl. Neurobiol. 27, 281-290 (2001).
76. Fidzianska, A. Toniolo, D. & Hausmaowa-Petrusewicz, I Ultrastructural abnormality of sarcolemmal nuclei in Emery-Dreifuss muscular dystrophy (EDMD). J. Neurol. Sci. 159, 88-93 (1998).
77. Cohen, M., Lee, K. K., Wilson, K. L. & Gruenbaum, Y. Transcriptional repression, apoptosis, human disease and the functional evolution of the nuclear lamina. Trends Biochem. Sci. 26, 41-48 (2001). An important review indicating that mutations in LMNA might promote disease phenotypes through altered gene regulation.
78. Bonne, G. et al. Mutations in the gene encoding lamin A/C cause autosomal dominant Emery-Dreifuss muscular dystrophy. Nature Genet. 21, 285-288 (1999). The first report of mutations in LMNA causing an hereditary disease.
79. Bione, S. et al. Identification of a novel X-linked gene responsible for Emery-Dreifuss muscular dystrophy. Nature Genet. 8, 323-327 (1994).
80. Bonne, G. et al. Clinical and molecular genetic spectrum of autosomal dominant Emery-Dreifuss muscular dystrophy due to mutations of the lamin A/C gene. Ann. Neurol. 48, 170-180 (2000).
81. Cutler, D. A., Sullivan, T., Marcus-Samuels, B., Stewart, C. L. & Reitman, M. L. Characterization of adiposity and metabolism in Lmna-deficient mice. Biochem. Biophys. Res. Commun. 291, 522-527 (2002).
82. Ellis, J. A., Craxton, M., Yates, J. R. & Kendrick-Jones, J. Aberrant intranuclear targeting and cell cycle-dependent phosphorylation of emerin contribute to Emery-Dreifuss muscular dystrophy phenotype. J. Cell Sci. 111, 781-792 (1998).
83. Fairley, E. A., Kendrick-Jones, J. & Ellis, J. A. The Emery-Dreifuss muscular dystrophy phenotype arises from aberrant targeting and binding of emerin at the inner nuclear membrane. J. Cell Sci. 112, 2571-2582 (1999).
84. Ostlund, C., Ellenberg, J., Hallberg, E., Lippincott-Schwartz, J. & Worman, H. J. Intranuclear trafficking of emerin, the Emery-Drelfuss muscular dystrophy protein. J. Cell Sci. 112, 1709-1719 (1999)
85. Ostlund, C., Bonne, G., Schwartz, K. & Worman, H. J. Properties of lamin A mutants found in Emery-Dreifuss muscular dystrophy, cardiomyopathy and Dunnigan-type partial lipodystrophy. J. Cell Sci. 114, 4435-4445 (2001).
86. Cao, H. & Hegele, R. A. Nuclear lamin A/C R428Q mutation in Canadian kindreds with Dunnigan-type familial partial lipodystrophy. Hum. Mol. Genet. 9, 109-112 (2000).
87. Shackleton, S. et al. LMNA encoding lamin A/C is mutated in partial lipodystrophy. Nature Genet. 24, 153-156 (2000).
88. Speckman, R. A. et al. Mutational and haplotype analyses of familial partial lipodystrophy (Dunnigan variety) reveal recurrent missense mutations in the globular C-terminal domain of lamin A/C. Am. J. Hum. Genet. 66, 1192-1198 (2000).
89. Dhe-Paganon, S., Werner, E, D., Chi, Y.-I. & Shoelson, S. E. Structure of the globular tail of nuclear lamin. J. Biol. Chem. 277, 17381-17384 (2002).
90. Krimm, L et al. The lg-like structure of the C-terminal domain of lamin A/C, mutated in muscular dystrophies, cardiomyopathies and partial lipodystrophy. Structure 10, 811-823 (2002) References 89 and 90 provide the first structural details of part of the lamln A protein, indicating Important differences In the roles of residues mutated in EDMD and those mutated in FPLD.
91. De Sandra-Giovannoli, A. et al Homozygous defects in LMNA, encoding lamin A/C nuclear envelope proteins, cause autosomal recessive axonal neuropathy in human (Charcot-Marie-Tooth disorder type2) and mouse. Am. J. Hum. Genet. 70, 726-736 (2002).
92. Pendas, A. M. et al. Defective prelamin A processing and muscular dystrophy and adipocyte alterations in Zmpste 24 metalloproteinase-deficient mice. Nature Genet. 31, 94 -99 (2002).
93. Novelli, G. et al. MandibuloacraJ dysplasia is caused by mutations in LMNA-encoding lamin A/C. Am. J. Hum. Genet. 71, 426-431 (2002).
94. Garg, A., Speckman, R. A. & Bowcock, A. M. Multisystem dystrophy syndrome due to novel missense mutations in the amino-terminal head and α-helical rod domains of the lamin A/C gene. Am. J. Med. 112, 549-555 (2002).
95. Diffley, J. F. & Stillman, B. Transcriptional silencing and lamins. Nature 342, 24-25 (1989).
96. Bartnick, E. & Weber, K. Widespread occurrence of intermediate filaments in invertebrates: Common principles and aspects of diversification. Eur. J. Cell Biol. 50, 17-33 (1989).
97. Colucci E. et al. Mice lacking vimentin develop and reproduce without an obvious phenotype. Cell 79, 679-694 (1994).
98. Georgatos, S. D., Maroulako, L & Blobel, G. Lamin A, B and lamin B receptor analogues in yeast. J. Cell Biol 108, 2069-2082 (1989).
99. Erber, A. et al. Characterization of the Hydra lamin and its gene: A molecular phylogeny of metazoan lamins. J. Mol. Evol. 49, 260-271 (1999).
100. Erber, A., Riemer, D., Bovenschulte, M. & Weber, K. Molecular phylogeny of metazoan intermediate filament proteins. J. Mol. Evol. 47, 751-762 (1998).
101. Enoch, T., Peter, M., Nurse, R & Nigg, E. A. p34cdc2 acts as a lamin kinase in fission yeast. J. Cell Biol. 112, 797-807 (1990).
102. Dodemont, H., Reimer, D. & Weber., K. Structure of an invertebrate gene encoding cytoplasmic intermediate filament proteins: Implications for the origin and the diversification of IF proteins. EMBO J. 9, 4083-4094 (1990).
103. Riemer, D., Dodemont, H. & Weber, K., Analysis of the cDNA and gene encoding a cytoplasmic intermediate filament (IF) protein from the cephalochordate Branchiostoma lanceolatum; implications for the evolution of the IF protein family. Eur. J. Cell Biol. 68, 128-135 (1992).
104. Szaro, B. G., Pant, H. C., Way, J. & Battey, J. Squid low molecular weight neurofilament proteins are a novel class of neurofilament protein. J. Biol. Chem. 266, 15035-15041 (1991).
105. Tomarev, S. I., Zinovieva, R. D. & Piatgorsky, J. Primary structure and lens-specific expression of genes for an intermediate filament protein and β-tubulin in cephalopods. Biochim. Biophys. Acta 1216, 245254 (1993).
106. Dodemont, H., Reimer, D., Ledger, N. & Weber, K. Eight genes and alternative RNA processing pathways generate an unexpectedly large diversity of cytoplasmic intermediate filament proteins in the nematode Caenorhabditis etegans. EMBO J. 13, 2625-2638 (1994).
107. Hatzfeld, M. & Franke, W. W. Pair formation and promiscuity of cytokeratins: Formation in vitro of heterotypic complexes and intermediate-sized filaments by homologous and heterologous recombinations of purified polypeptides. J. Cell Biol. 101, 1826-1841 (1985).
108. Hatzfeld, M. & Weber, K. 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. Ceil Biol. 110, 1199-1210 (1990).
109. Hesse, M., Magin, T. M. & Weber, K. 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 (2001).
110. Lee, M. K., Xu, Z., Wong, P. C. & Cleveland, D. W. Neurofilaments are obligate heteropolymers in vivo. J. Cell Biol. 122, 1337-1350 (1993).
111. Newey, S. E. et al. Syncoilin, a novel member of the intermediate filament superfamily that interacts with α-dystrobrevin in skeletal muscle. J. Biol. Chem. 276, 6645-6655 (2001).
112. Broers, J. L. et al. A- and B-type lamins are differentially expressed in normal human tissue. Histochem. Cell Biol. 107, 505-517 (1997).
113. Furukawa, K., Inagaki, L. & Hotta, Y. Identification and cloning of an mRNA coding for a germ cell-specific A-type lamin in mice. Eyp. Cell Res. 212, 426-430 (1994).
114. Riemer, D. et al. Expression of Drosophila lamin C is developmentally regulated: Analogies with vertebrate A-type lamins. J. Cell Sci. 108, 3189-3198 (1995).
115. Wydner, K. L., McNeil, J. A., Lin, F. Womian, H. J. & Lawrence, J. B. Chrormosomal assignment of human nuclear envelope protein genes LMNA, LMNB1 and LBR by fluorescence in situ hybridization. Gecomics 32, 474,-478 (1996).
116. Genschel, J. et al. A new frameshift mutation at codon 466 (1397 delA) within the LMNA gene. Hum. Mutat. 16, 278-288 (2000).
117. Raffaele di Barletta, M. et al. Different mutations in the LMNA gene causes autosomal dominant and autosomal recessive Emery-Dreifuss muscular dystrophy. Am. J. Hum. Genet. 66, 1407-1412 (2000).
118. Ki, C. S. et al. Identification of lamin A/C (LMNA) gene mutations in Korean patients with autosomal dominant Emery-Dreifuss muscular dystrophy and limb girdle muscular dystrophy 1 B. J. Hum. Genet. 47, 225-228 (2002).
119. Kitaguchi, T. et al. A mis-sense mutation in exon 8 of lamin A/C gene in a Japanese case of autosomal dominant limb girdle muscular dystrophy with cardiac conduction block. Neuromuscul. Disord. 11, 542-546 (2001).
120. Murchir, A. et al. Identification of mutations in the gene encoding lamins A/C in autoscmal autosomal dominant limb girdle muscular dystrophy with aventricular aventdcular conduction disturbances (LGMD1B). Hum. Mol. Genet. 9, 1453-1459 (2000).
121. Brodsky, G. L. et al. Lamin A/C gene mutation associated with dilated cardiomyopathy with variable skeletal muscle involvement. Circulation 101, 473-476 (2000)