The nuclear lamina comes of age

Nature Reviews Molecular Cell Biology

Volumn 6, Issue 1, 2005, Pages 21-31

  Gruenbaum, Yosef ^a   Margalit, Ayelet ^a   Goldman, Robert D ^b   Shumaker, Dale K ^b   Wilson, Katherine L ^c  

^a HEBREW UNIVERSITY OF JERUSALEM   (Israel)

^b NORTHWESTERN UNIVERSITY   (United States)

^c JOHNS HOPKINS UNIVERSITY SCHOOL OF MEDICINE   (United States)

Author keywords

[No Author keywords available]

Indexed keywords

ACTIN; CELL CYCLE PROTEIN; DNA BINDING PROTEIN; EMERIN; HISTONE H2A; HISTONE H2B; INTERMEDIATE FILAMENT PROTEIN; LAMIN A; LAMIN B; MEMBRANE PROTEIN; NUCLEAR PROTEIN; PROTEIN BAF; PROTEIN BARRIER TO AUTOINTEGRATION FACTOR; PROTEIN GERM CELL LESS; PROTEIN LAMINA ASSOCITAED POLYPEPTIDE 1; PROTEIN LAMINA ASSOCITAED POLYPEPTIDE 2 ALPHA; PROTEIN LBR; PROTEIN LEM DOMAIN; PROTEIN MAN1; PROTEIN MOK2; PROTEIN NESPRIN; PROTEIN NESPRIN 1 ALPHA; PROTEIN SREBP; PROTEIN SUN DOMAIN; PROTEIN UNC 83; PROTEIN UNC 84; PROTEIN ZYG 12; REGULATOR PROTEIN; RETINOBLASTOMA PROTEIN; UNCLASSIFIED DRUG; UNINDEXED DRUG;

BONE DYSPLASIA; CELL NUCLEUS; CELL NUCLEUS MEMBRANE; CELLULAR DISTRIBUTION; CENTROSOME; CHROMATIN CONDENSATION; CHROMATIN STRUCTURE; CONGESTIVE CARDIOMYOPATHY; CYTOSKELETON; EMERY DREIFUSS MUSCULAR DYSTROPHY; ENZYME BINDING; GENE CONTROL; GENE MUTATION; GENE REPRESSION; GENETIC DISORDER; HEREDITARY MOTOR SENSORY NEUROPATHY; HETEROCHROMATIN; HUMAN; LAMINOPATHY; LEUKOCYTE DISORDER; LIMB GIRDLE MUSCULAR DYSTROPHY; LIPODYSTROPHY; MOLECULAR INTERACTION; NONHUMAN; NUCLEAR LAMINA; NUCLEAR LOCALIZATION SIGNAL; NUCLEAR PORE COMPLEX; PRIORITY JOURNAL; PROGERIA; PROTEIN EXPRESSION; PROTEIN FUNCTION; PROTEIN MOTIF; PROTEIN PROTEIN INTERACTION; REVIEW; SIGNAL TRANSDUCTION; SKELETON MALFORMATION;

EID: 11244320353     PISSN: 14710072     EISSN: None     Source Type: Journal    
DOI: 10.1038/nrm1550     Document Type: Review

References (107)

1. Stuurman, N., Heins, S. & Aebi, U. Nuclear lamins: their structure, assembly, and interactions. J. Struct Biol. 122, 42-66 (1998).
2. Schirmer, E. C., Florens, L., Guan, T., Yates, J. R. & Gerace, L. Nuclear membrane proteins with potential disease links found by subtractive proteomics. Science 531, 1380-1382 (2003).
3. Weber, K., Plessmann, U. & Traub, P. Maturation of nuclear lamin A involves a specific carboxy-terminal trimming, which removes the polyisoprenylation site from the precursor; implications for the structure of the nuclear lamina. FEBS Lett. 257, 411-414 (1989).
4. Leung, G. K. et al. Biochemical studies of Zmpste24-deficient mice. J. Biol. Chem. 276, 29051-29058 (2001).
5. Herrmann, H. & Foisner, R. Intermediate filaments: novel assembly models and exciting new functions for nuclear lamins. Cell. Mol. Life Sci. 60, 1607-1612 (2003).
6. Moir, R. D., Yoon, M., Khuon, 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).
7. Karabinos, A., Schunemann, J., Meyer, M., Aebi, U. & Weber, K. The single nuclear lamin of Caenorhabditis elegans forms in vitro stable intermediate filaments and paracrystals with a reduced axial periodicity. J. Mol. Biol. 325, 241-247 (2003). The first study showing that lamin can form 10-nm filaments in vitro, similar to cytoplasmic intermediate filaments.
8. Aebi, U., Cohn, J., Buhle, L. & Gerace, L. The nuclear lamina is a meshwork of intermediate-type filaments. Nature 323, 560-564 (1986).
9. Gruenbaum, Y. et al. The nuclear lamina and its functions in the nucleus. Int. Rev. Cyt. 226, 1-62 (2003).
10. Zastrow, M. S., Vlcek, S. & Wilson, K. L. Proteins that bind A-type lamins: integrating isolated clues. J. Cell Sci. 117, 979-987 (2004).
11. Liu, J. et al. Essential roles for Caenorhabditis elegans lamin gene in nuclear organization, cell cycle progression, and spatial organization of nuclear pore complexes. Mol. Biol. Cell 11, 3937-3947 (2000).
12. Liu, J. et al. MAN1 and emerin have overlapping function(s) essential for chromosome segregation and cell division in C. elegans, Proc. Natl Acad. Sci. USA 100, 4598-4603 (2003). LEM-domain proteins have redundant functions in regulating mitosis and chromatin organization. This functional overlap might explain why loss of emerin, which is expressed in nearly all tissues, has no phenotype in C. elegans, and affects only three human tissues.
13. 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).
14. Guillemin, K., Williams, T. & Krasnow, M. A. A nuclear lamin is required for cytoplasmic organization and egg polarity in Drosophila. Nature Cell Biol. 3, 848-651 (2001).
15. Schirmer, E. C., Guan, T. & Gerace, L. Involvement of the lamin rod domain in heterotypic lamin interactions important for nuclear organization, J. Cell Biol. 153, 479-490 (2001).
16. Starr, D. A. et al. unc-83 encodes a novel component of the nuclear envelope and is essential for proper nuclear migration. Development 128, 5039-5050 (2001).
17. Starr, D. A. & Han, M. Role of ANC-1 in tethering nuclei to the actin cytoskeleton. Science 11, 406-409 (2002). Evidence that the C. elegans nesprin homologue, ANC-1, is localized in the ONM and anchors the nucleus by binding both UNC-84 (at the nuclear envelope) and actin (in the cytoplasm).
18. Lopez-Soler, R. I., Moir, R. D., Spann, T. P., Stick, R. & Goldman, R. D. A role for nudear lamins in nuclear envelope assembly. J. Cell Biol. 154, 61-70 (2001).
19. 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).
20. Spann, T. P., 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).
21. Lee, K. K. et al. Lamin-dependent localization of UNC-84, a protein required for nuclear migration in C. elegans. Mol. Biol. Cell 13, 892-901 (2002).
22. Malone, C. J. et al. The C. elegans Hook protein, ZYG-12, mediates the essential attachment between the centrosome and nucleus. Cell 115, 825-836 (2003). Evidence that ZYG-12 homodimers attach C. elegans centrosomes to the outer nuclear membrane, and to the nuclear lamina through direct or indirect binding to SUN1/matefin, an inner-nuclear-membrane protein.
23. Zhen, Y. Y., Libotte, T., Munck, M., Noegel, A. A. & Korenbaum, E. NUANCE, a giant protein connecting the nucleus and actin cytoskeleton. J. Cell Sci. 115, 3207-3222 (2002).
24. Croft, J. A. et al. Differences in the localization and morphology of chromosomes in the human nucleus. J. Cell Biol. 145, 1119-1131 (1999).
25. Nikolova, V. et al. Defects in nuclear structure and function promote dilated cardiomyopathy in lamin A/C-deficient mice. J. Clin. Invest. 113, 357-369 (2004).
26. Goldman, R. D. et al. Accumulation of mutant lamin A causes progressive changes in nuclear architecture in Hutchinson-Gilford progeria syndrome. Proc. Natl Acad. Sci. USA 101, 8963-8968 (2004). Fibroblasts from Hutchinson-Gilford progeria patients show dramatic changes in nuclear structure, loss of peripheral heterochromatin and changes in nuclear-envelope composition.
27. 14-reductase deficiency due to mutations in the Lamin B receptor gene. Am. J. Hum. Genet. 72, 1013-1017 (2003).
28. Holmer, L. & Worman, H. J. Inner nuclear membrane proteins: functions and targeting. Cell. Mol. Life Sci. 58, 1741-1747 (2001).
29. Hoffmann, K. et al. Mutations in the gene encoding the lamin B receptor produce an altered nuclear morphology in granulocytes (Pelger-Huet anomaly). Nature Genet. 31, 410-414 (2002). Evidence that LBR influences chromatin organization and nuclear shape during white-blood-cell differentiation.
30. Lin, F. et al. MAN1, an inner nuclear membrane protein that shares the LEM domain with lamina-associated polypeptide 2 and emerin. J. Biol. Chem. 275, 4840-4847 (2000).
31. Lee, K. K. & Wilson, K. L. The Nuclear Envelope (eds Evans. D. E., Hutchinson, C. & Bryant, J.) 331-341 (BIOS Scientific Publishers, Abingdon, UK, 2004).
32. Shumaker, D. K., Lee, K. K., Tanhehco, Y. C., Craigie, R. & Wilson, K. L. LAP2 binds to BAF-DNA complexes: requirement for the LEM domain and modulation by variable regions. EMBO J. 20, 1754-1764 (2001).
33. Lee, K. K. et al. Distinct functional domains in emerin bind lamin A and DNA-bridging protein BAF. J. Cell Sci. 114, 4567-4573 (2001).
34. Dechat, T. et al. Lamina-associated polypeptide 2α binds intranuclear A-type lamins. J. Cell Sci. 19, 3473-3484 (2000).
35. Goldberg, M. et al. Interactions among Drosophila nuclear envelope proteins lamin, otefin, and YA. Mol. Cell. Biol. 18, 4315-4323 (1998).
36. Wagner, N., Schmitt, J. & Krohne, G. Two novel LEM-domain proteins are splice products of the annotated Drosophila melanogaster gene CG9424 (Bocksbeutel). Euro. J. Cell Biol. 82, 605-616 (2004).
37. Furukawa, K. LAP2 binding protein 1 (L2BP1/BAF) is a candidate mediator of LAP2- chromatin interaction. J. Cell Sci. 112, 2485-2492 (1999).
38. Segura-Totten, M. & Wilson, K. L. BAF: roles in chromatin, nuclear structure and retrovirus integration. Trends Cell Biol. 14, 261-266 (2004).
39. Zheng, R. et al. Barrier-to-autointegration factor (BAF) bridges DNA in a discrete, higher-order nucleoprotein complex. Proc. Natl Acad Sci. USA 97, 8997-9002 (2000).
40. Wang, X. et al. Barrier to autointegration factor interacts with the cone-rod homeobox and represses its transactivation function. J. Biol. Chem. 277, 43288-43300 (2002).
41. Furukawa, K. et al. Barrier-to-autointegration factor plays crucial roles in cell cycle progression and nuclear organization in Drosophila. J. Cell Sci. 116, 3811-3823 (2003).
42. Vlcek, S., Korbei, B. & Foisner, R. Distinct functions of LAP2α's unique C-terminus in cell proliferation and nuclear assembly. J. Biol. Chem. 277, 18898-18907 (2002).
43. Johnson, et al. A-type lamins regulate retinoblastoma protein function by promoting subnuclear localization and preventing proteasomal degradation. Proc. Natl Acad. Sci. USA 101, 9677-9682 (2004).
44. Haraguchi, T. et al. BAF is required for emerin assembly into the reforming nuclear envelope. J. Cell Sci. 114, 4575-4585 (2001).
45. Cohen, M., Lee, K., Wilson, K. W. & Gruenbaum Y. Transcriptional repression, apoptosis, human disease and the functional evolution of the nuclear lamina. Trends Biochem. Sci 26, 41-47 (2001).
46. Nili, E. et al. Nuclear membrane protein, LAP2ß, mediates transcriptional repression alone and together with its binding partner GCL (germ cell-less). J. Cell Sci. 114, 3297-3307 (2001).
47. Jongens, T. A., Ackerman, L. D., Swedlow, J. R., Jan, L. Y. & Jan, Y. N. Germ cell-less encodes a cell type-specific nuclear pore-associated protein and functions early in the germ-cell specification pathway of Drosophila. Genes Dev. 8, 2123-2136 (1994).
48. de la Luna, S., Allen, K. E., Mason, S. L. & La Thangue, N. B. Integration of a growth-suppressing BTB/POZ domain protein with the DP component of the E2F transcription factor. EMBO J. 18, 212-228 (1999).
49. Martins, S., Eikvar, S., Furukawa, K. & Collas, P. HA95 and LAP2β mediate a novel chromatin-nuclear envelope interaction implicated in initiation of DNA replication. J. Cell Biol. 160, 177-188. (2003).
50. Holaska, J. M., Lee, K. K., Kowalski, A. K. & Wilson, K. L. Transcriptional repressor germ cell-less (GCL) and barrier-to-autointegration factor (BAF) compete for binding to emerin in vitro. J. Biol. Chem. 278, 6969-6975 (2003).
51. Bengtsson, L. & Wilson, K. L. Multiple and surprising new functions for emerin, a nuclear membrane protein. Curr. Opin. Cell Biol. 16, 73-79 (2004).
52. Haraguchi, T. et al. Emerin binding to Btf, a death-promoting transcriptional repressor, is disrupted by a missense mutation that causes Emery-Dreifuss muscular dystrophy. Eur. J. Biochem. 271, 1035-1045 (2004).
53. Pederson, T. & Aebi, U. Actin in the nucleus: what form and what for? J. Struct. Biol. 140, 3-9 (2002).
54. Pestic-Dragovich, L. et al. A myosin I isoform in the nucleus. Science 290, 337-342 (2000).
55. Bettinger, B. T., Gilbert, D. M. & Amberg, D. C. Actin up in the nucleus. Nature Rev. Mol. Cell Biol. 5, 410-415 (2004).
56. Sasseville, A. M. & Langelier, Y. In vitro interaction of the carboxy-terminal domain of lamin A with actin. FEBS Lett. 425, 485-489 (1998).
57. 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).
58. Lattanzi, G. et al. Association of emerin with nuclear and cytoplasmic actin is regulated in differentiating myoblasts. Biochem. Biophys. Res. Commun. 303, 764-770 (2003).
59. Mattioli, E. et al. Nuclear AKAPs in muscle differentiation: redistribution of PKA in myotubes and regulation of AKAP149 expression by MAPK/ERK pathway. FEBS Lett. (in the press).
60. Holaska, J. M., Kowalski, A. K. & Wilson, K. L. Emerin caps the pointed end of actin filaments: evidence for an actin cortical network at the nuclear inner membrane. PLoS Biol. 2, E231 (2004). Evidence that emerin caps the pointed end of F-actin and thereby indirectly enhances actin polymerization rates in vitm. Emerin also affinity-purifies nuclear-enriched αII-spectrin from HeLa-cell nuclear lysates, indicating that emerin anchors a spectrin- and actin-containing cortical network at the NE.
61. Luque, C. M. et al. An alternative domain containing a leucine-rich sequence regulates nuclear cytoplasmic localization of protein 4.1R. J. Biol. Chem. 278, 2686-2691 (2003).
62. Sridharan, D., Brown, M., Lambert, W. C., McMahon, L. W. & Lambert, M. W. Nonerythroid all spectrin is required for recruitment of FANCA and XPF to nuclear foci induced by DNA interstrand cross-links. J. Cell Sci. 116, 823-835 (2003).
63. Krauss, S. W., Chen, C., Penman, S. & Heald, R. Nuclear actin and protein 4.1: essential interactions during nuclear assembly in vitro. Proc. Natl Acad. Sci. USA 100, 10752-10757 (2003).
64. Lammerding, J. et al. Lamin A/C deficiency causes defective nuclear mechanics and mechanotransduction. J. Clin. Invest. 113, 370-378 (2004). Evidence that Imna-null mouse embryo fibroblasts have deformed nuclei, impaired viability under mechanical stress, defective mechanotransduction and attenuated gene-expression responses to mechanical stress via the NFκB signalling pathway.
65. Dahl, K. N., Kahn, S. M., Wilson, K. L. & Discher, D. E. The nuclear envelope lamina network has elasticity and a compressibility limit suggestive of a molecular shock absorber. J. Cell Sci. 15, 4779-4786 (2004).
66. Osada, S., Ohmori, S. Y. & Taira, M. XMAN1, an inner nuclear membrane protein, antagonizes BMP signaling by interacting with Smad1 in Xenopus embryos. Development 130, 1783-1794 (2003). Evidence that X. laevis Man1 is a neuralizing factor that blocks Bmp signalling by direct binding to Smad proteins. Similar results were reported by Raju et al. (2003).
67. ten Dijke, P. & Hill, C. S. New insights into TGF-β-Smad signalling. Trends Biochem. Sci. 29, 265-273 (2004).
68. Nakayama, T., Cui, Y. & Christian, J. L. Regulation of BMP/Dpp signaling during embryonic development. Cell. Mol. Life Sci. 57, 943-956 (2000).
69. Lee, H., Habas, R. & Abate-Shen, C. Msx1 cooperates with histone H1b for inhibition of transcription and myogenesis. Science 304, 1675-1678 (2004).
70. Fainsod, A., Steinbeisser, H. & De Robertis, E. M. On the function of BMP-4 in patterning the marginal zone of the Xenopus embryo. EMBO J. 13, 5015-5025 (1994).
71. Malone, C. J., Fixsen, W. D., Horvitz, H. R. & Han, M. UNC-84 localizes to the nuclear envelope and is required for nuclear migration and anchoring during C. elegans development. Development 126, 3171-3181 (1999).
72. Hedgecock, E. M. & Thomson, J. N. A gene required for nuclear and mitochondrial attachment in the nematode Caenorhabditis elegans. Cell 30, 321-330 (1982).
73. Hodzic, D. M., Yeater, D. B., Bengtsson, L., Otto, H. & Stahl, P. D. Sun2 is a novel mammalian inner nuclear membrane protein. J. Biol. Chem. 279, 25805-25812 (2004).
74. Fridkin, A. et al. Matefin, a C. elegans germ-line specific SUN-domain nuclear membrane protein, is essential for early embryonic and germ cell development. Proc. Natl Acad. Sci. USA 101, 6987-6992 (2004).
75. Zhang, Q., Ragnauth, C., Greener, J. M., Shanahan, C. M. & Roberts, R. G. The nesprins are giant actin-binding proteins, orthologous to Drosophila muscle protein MSP-300. Genomics 80, 473-481 (2002).
76. Padmakumar, V. C. et al. Enaptin, a giant actin-binding protein, is an element of the nuclear membrane and the actin cytoskeleton. Exp. Cell Res. 295, 330-339 (2004).
77. Starr, D. A. & Han, M. ANChors away: an actin based mechanism of nuclear positioning. J. Cell Sci. 116, 211-216 (2003).
78. Mislow, M. K. J. et al. Nesprin-1α self-associates and binds directly to emerin and lamin A in vitro. FEBS Lett. 525, 135-140 (2002).
79. Muchir, A. et al. Nuclear envelope alterations in fibroblasts from LGMD1B patients carrying nonsense Y259X heterozygous or homozygous mutation in lamin A/C gene. Exp. Cell Res. 291, 352-362 (2003). Homozygous-null Imna fibroblasts were derived from a 30-week-old human fetus that was born prematurely to consanguineous parents. The infant had severe muscle defects and fibrosis, joint contractures and missing diaphragm muscles, and died after birth. The fibroblast nuclei were highly lobulated; lamin B and LAP2β were not detected at the NE; and emerin and nesprin-1α both mislocalized to the ER.
80. Paddock, S. W. & Albrecht-Buehler, G. Rigidity of the nucleus during nuclear rotation in 3T3 cells. Exp. Cell Res. 175, 409-413 (1988).
81. Gonczy, P., Pichler, S., Kirkham, M. & Hyman, A. A. Cytoplasmic dynein is required for distinct aspects of MTOC positioning, including centrosome separation, in the one cell stage Caenorhabditis elegans embryo. J. Cell Biol. 147, 135-150 (1999).
82. Yoder, J. H. & Han, M. Cytoplasmic dynein light intermediate chain is required for discrete aspects of mitosis in Caenorhabditis elegans. Mol. Biol. Cell 12, 2921-2933 (2001).
83. Walenta, J. H., Didier, A. J., Liu, X. & Kramer, H. The Golgi-associated hook3 protein is a member of a novel family of microtubule-binding proteins. J. Cell Biol. 152, 923-934 (2001).
84. Worman, H. J. & Courvalin, J. C. How do mutations in lamins A and C cause disease? J. Clin. Invest. 113, 349-351 (2004).
85. Mounkes, L., Kozlov, S., Burke, B. & Stewart, C. L. The laminopathies: nuclear structure meets disease. Curr. Opin. Genet. Dev. 213, 223-230 (2003).
86. Navarro, C. et al. Lamin A and ZMPSTE24 (FACE-1) defects cause nuclear disorganisation and identify restrictive dermopathy as a lethal neonatal laminopathy. Hum. Mol. Genet. 13, 2493-2503 (2004).
87. Vigouroux, C. et al. Nuclear envelope disorganization in fibroblasts from lipodystrophic patients with heterozygous R482Q/W mutations in the lamin A/C gene. J. Cell Sci. 114, 4459-4468 (2001).
88. Markiewicz, E. et al. Increased solubility of lamins and redistribution of lamin C in X-linked Emery-Dreifuss muscular dystrophy fibroblasts. J. Struct. Biol. 140, 241-253 (2002).
89. -/- cells is caused by defective nucleo-cytoskeletal integrity: implications for the development of laminopathies. Hum. Mol. Genet. 13, 2567-2580 (2004).
90. Morris, G. E. in The Nuclear Envelope (eds Evans, D. E., Hutchinson, C. & Bryant, J.) (BIOS Scientific Publishers, Abingdon, UK, 2004).
91. Allsopp, R. C. et al. Telomere length predicts replicative capacity of human fibroblasts. Proc. Natl Acad. Sci. USA 89, 10114-10118 (1992).
92. Sarkar, P. K. & Shinton, R. A. Hutchinson-Gilford progeria syndrome. Postgrad. Med. J. 77, 312-317 (2001).
93. Mukherjee, A. B. & Costello, C. Aneuploidy analysis in fibroblasts of human premature aging syndromes by FISH during in vitro cellular aging. Mech. Ageing Dev. 103, 209-222 (1998).
94. Morris, G. E. The role of the nuclear envelope in Emery-Dreifuss muscular dystrophy. Trends. mol. Med. 7, 572-577 (2001).
95. Chen, L. et al. LMNA mutations in atypical Werner's syndrome. Lancet 362, 440-445 (2003).
96. Brodsky, G. L. et al. Lamin A/C gene mutation associated with dilated cardiomyopathy with variable skeletal muscle involvement. Circulation 101, 473-476 (2000).
97. 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).
98. 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).
99. Nedivi, E., Fieldust, S., Theill, L. E. & Hevron, D. A set of genes expressed in response to light in the adult cerebral cortex and regulated during development. Proc. Natl Acad. Sci. USA 93, 2048-2053 (1996).
100. Apel, E. D., Lewis, R. M., Grady, R. M. & Sanesi, J. R. Syne-1, a dystrophin-and Klarsicht-related protein associated with synaptic nuclei at the neuromuscular junction. J. Biol. Chem. 275, 31986-31995 (2000).
101. Mislow, J. M., Kim, M. S., Davis, D. B. & McNally, E. M. Myne-1, a spectrin repeat transmembrane protein of the myocyte inner nuclear membrane, interacts with lamin A/C. J. Cell Sci. 115, 61-70 (2002).
102. Rosenberg-Hasson, Y., Renert-Pasca, M. & Volk, T. A Drosophila dystrophin-related protein, MSP-300, is required for embryonic muscle morphogenesis. Mech. Dev. 60, 83-94 (1996).
103. Patterson, K. et al. The functions of Klarsicht and nuclear lamin in developmentally regulated nuclear migrations of photoreceptor cells in the Drosophila eye. Mol. Biol. Cell 15, 600-610 (2004).
104. Gough, L. L., Fan, J., Chu, S., Winnick, S. & Beck, K. A. Golgi localization of syne-1. Mol. Biol. Cell 14, 2410-2424 (2003).
105. Vlcek, S., Dechat, T. & Foisner, R. Nuclear envelope and nuclear matrix: interactions and dynamics. Cell. Mol. Life Sci. 58, 1758-1765 (2001).
106. Tsukahara, T., Tsujino, S. & Arahata, K. cDNA microarray analysis of gene expression in fibroblasts of patients with X-linked Emery-Dreifuss muscular dystrophy. Muscle Nerve 25, 898-901 (2002).
107. Shimi, T. et al. Dynamic interaction between BAF and emerin revealed by FRAP, FLIP, and FRET analyses in living HeLa cells. J. Struct. Biol. 147, 31-41 (2004).