The Emery-Dreifuss muscular dystrophy phonotype arises from aberrant targeting and binding of emerin at the inner nuclear membrane

Journal of Cell Science

Volumn 112, Issue 15, 1999, Pages 2571-2582

  Fairley, Elizabeth A L ^a,b   Kendrick Jones, John ^a   Ellis, Juliet A ^b  

^a MRC LABORATORY OF MOLECULAR BIOLOGY   (United Kingdom)

^b ADDENBROOKE S HOSPITAL   (United Kingdom)

Author keywords

Emerin; Emery Dreifuss muscular dystrophy; Lamin binding; Nuclear targeting

Indexed keywords

ACTIN; COMPLEMENTARY DNA; EMERIN; LAMIN; MEMBRANE PROTEIN; MUTANT PROTEIN; NUCLEAR PROTEIN;

AMINO TERMINAL SEQUENCE; ANIMAL CELL; ARTICLE; CARBOXY TERMINAL SEQUENCE; CELL NUCLEUS; CELL NUCLEUS MEMBRANE; CELLULAR DISTRIBUTION; CONTROLLED STUDY; CYTOPLASM; DNA TRANSFECTION; EMERY DREIFUSS MUSCULAR DYSTROPHY; GENE CONSTRUCT; GENE DELETION; GENE EXPRESSION; IMMUNOPRECIPITATION; LIVER CELL; MEMBRANE BINDING; MOUSE; MYOBLAST; NONHUMAN; PHENOTYPE; PRIORITY JOURNAL; PROTEIN AGGREGATION; PROTEIN PROTEIN INTERACTION; PROTEIN TARGETING;

AMINO ACID SUBSTITUTION; ANIMALS; BASE SEQUENCE; CELL LINE; COS CELLS; GREEN FLUORESCENT PROTEINS; HUMANS; LUMINESCENT PROTEINS; MEMBRANE PROTEINS; MICE; MOLECULAR SEQUENCE DATA; MUSCLE, SKELETAL; MUSCULAR DYSTROPHIES; MUSCULAR DYSTROPHY, EMERY-DREIFUSS; MUTATION, MISSENSE; NUCLEAR ENVELOPE; NUCLEAR PROTEINS; PHENOTYPE; POLYMERASE CHAIN REACTION; RECOMBINANT FUSION PROTEINS; SEQUENCE DELETION; THYMOPOIETINS; TRANSFECTION; X CHROMOSOME;

ANIMALIA;

EID: 0032771080     PISSN: 00219533     EISSN: None     Source Type: Journal    
DOI: None     Document Type: Article

References (50)

1. Alsheimer, M., Fecher, E. and Benavente, R. (1998). Nuclear envelope remodelling during rat spermatogenesis: distribution and expression pattern of LAP2. J. Cell Sci. 111, 2227-2234.
2. Ansorge, W. (1985). Fast and sensitive detection of protein and DNA bands by treatment with potassium permanganate. J. Biochem. Biophys. Meth. 11, 13-20.
3. Bione S., Maestrini, E., Rivella, S., Mancini, M., Regis, S., Romeo, G. and Toniolo, D. (1994). Identification of a novel X-linked gene responsible for Emery-Dreifuss muscular dystrophy. Nature Genet. 8, 323-327.
4. Bonne, G., Di Barletta, M. R., Varnous, S., Becane, H.-M., Hammouda, E-H., Merlini, L., Muntoni, F., Greenberg, C. R., Gary, F., Urtizbera, J.-A, Doboc, D., Fardeau, M., Toniolo, D. and Schwartz, K. (1999). Mutations in the gene encoding lamin A/C cause autosomal dominant EDMD. Nature Genet. 21, 285-288.
5. Burnette, W. N. (1981). 'Western blotting' Electrophoretic transfer of proteins from SDS-PAGE gels to unmodified nitrocellulose and radiographic detection with antibodies and radioiodinated protein A. Anal. Biochem. 112, 195-303.
6. Cartegni, L., Raffaele de Barletta, M., Barresi, R., Sqarzoni, S., Sabatelli, P., Maraldi, N., Mora, M., Di Dlasi, C., Cornelio, F., Merlino, L., Villa, A., Cobianchi, F. and Toniolo, D. (1997). Heart-specific localization of emerin: new insights into Emery-Dreifuss muscular dystrophy. Hum. Mol. Genet. 6, 2257-2264.
7. Cullen, M. J. (1997). Muscle regeneration in Dystrophin-Gene, Protein and Cell Biology (ed. S. C. Brawn and J. A. Lucy), pp. 233-273. Cambridge, Cambridge University Press.
8. Dingwell, C. and Laskej, R. A. (1991). Nuclear targeting sequences - a consensus? Trends Biol. Chem. 16, 478-481.
9. Ellis, J. A., Craxton, M., Yates, J. R. W. and Kendrick-Jones, J. (1998). Aberrant intracellular targeting and cell cycle-dependent phosphorylation of emerin contribute to the EMD phenotype. J. Cell Sci. 111, 781-792.
10. Ellis, J. A., Tilley, L. D., Yates, J. R. W., Kendrick-Jones, J. and Brown C. B. (1999). Changes at P183 of emerin weaken its protein-protein interactions resulting in X-linked EDMD. Hum. Genet. 104, 262-268.
11. Emery, A. E. H. (1989). Emery-Dreifuss syndrome. J. Med. Genet. 26, 637-641.
12. rd edn (ed. D. L. Rimon, J. M. Connor and R. E. Pyeritz), pp. 2337-2354. Churchill Livingstone.
13. Foisner, R. and Gerace, L. (1993). Integral membrane proteins of the nuclear envelope interact with lamins and chromosomes, and binding is modulated by mitotic phosphorylation. Cell 73, 1267-1279.
14. Furukawa, K., Pane, N., Aebi, U. and Gerace, L. (1995). Cloning of a cDNA for lamina-associated polypeptide 2 (LAP2) and identification of regions that specify targeting to the nuclear envelope. EMBO J. 14, 1626-1636.
15. Furukawa, K., Fritze, C. E. and Gerace, L. (1998). The major nuclear envelope targeting domain of LAP2 coincides with its lamin binding region but is distinct from its chromatin interaction domain. J. Biol. Chem. 273, 4213-4219.
16. Furukawa, K. and Kondo, T. (1998). Identification of the lamina-associated-polypeptide-2-binding domain of B-type lamin. Eur. J. Biochem. 251, 729-733.
17. Gerace, L. and Foisner, R. (1994). Integral membrane proteins and dynamic organization of the nuclear envelope. Trends. Cell Biol. 4, 127-131.
18. Georgatos, S. P., Meier, J. and Simos, G. (1994). Lamins and lamin-associated proteins. Curr. Opin. Cell Biol. 6, 347-353.
19. Harris, C. A., Andryuk, P. J., Cline, S. W., Mathew, S., Siekierka, J. J. and Goldstein, G. (1995). Structure and mapping of the human thymopoietin (TMPO) gene and relationship of the human TMPO-β to rat lamina-associated polypeptide 2. Genomics 28, 198-205.
20. Laemmli, U. K. (1970). Cleavage of structural proteins during assembly of the head of bacteriophage T4. Nature 227, 680-685.
21. Lorim, D. and Lin, J. J.-C. (1989). Expression of nuclear lamin A and muscle-specific proteins in differentiating muscle cells in ovo and in vitro. J. Cell Biol. 109, 495-504.
22. Maison, C., Pyrpasopoulou, A., Theodoropoulos, P. A. and Georgatos, S. D. (1997). The inner nuclear membrane protein LAP1 forms a native complex with B-type lamins and partitions with spindle-associated mitotic vesicles. EMBO J. 16, 4839-4850.
23. Manilal, S., Nguyen thi Man, Sewry, C. A. and Morris G. E. (1996). The Emery-Dreifuss muscular dystrophy protein, emerin, is a nuclear protein. Hum. Mol. Genet. 5, 801-808.
24. Manilal, S., Sewry C. A., Nguyen thi Man, Muntoni, F. and Morris G. E. (1997). Diagnosis of Emery-Dreifuss muscular dystrophy by protein analysis of leucocytes with monocloncal antibodies. Neuromusc. Disorders 7, 63-66.
25. Manilal, S., Recan, D., Sewry, C. A., Hoeltzenbein, M., Llense, S., Leturcq, F., Deburgrave, N., Barbot, J.-C., Nguyen thi Man, Muntoni, F., Wehnert, M., Kaplan, J.-C. and Morris, G. E. (1998a). Mutations in Emery-Dreifuss muscular dystrophy and their effects on emerin protein expression. Hum. Mol. Genet. 7, 855-864.
26. Manilal, S., Nguyen thi Man and Morris G. E. (1998b). Co-localization of emerin and lamins in interphase nuclei and changes in mitosis. Biochem. Biophys. Res. Commun. 249, 643-647.
27. Manilal, S., Sewry, C. A., Pereboev, A., Nguyen thi man, Gobbi, P., Hawkes, S., Love, D. R. and Morris, G. E. (1999). Distribution of emerin and lamins in the heart and implications for EDMD. Hum. Mol. Genet. 8, 353-359.
28. Maniotis, A. J., Chen, C. S. and Ingber, D. E. (1997). Demonstration of mechanical connections between integrins, cytoskeletal filaments and nucleoplasm that stabilize nuclear structure, Proc. Natl. Acad. Sci. USA 94, 849-854.
29. Martin, L., Crimaudo, C. and Gerace, L. (1995). cDNA cloning and characterization of lamina-associated polypeptide 1C (LAP1C), an integral protein of the inner nuclear membrane. J. Biol. Chem. 270, 8822-8828.
30. McKeon, F. D., Kirschner, M. W. and Caput, D. (1986). Homologies in both primary and secondary structure between nuclear envelope and intermediate filament proteins. Nature 319, 463-468.
31. Moir, R. D., Montag-Lowy, M. and Goldman, R. D. (1994). Intrinsic properties of nuclear lamins: lamin B is associated with sites of DNA replication. J. Cell Biol. 125, 1201-1212.
32. Mora, M., Carregni, L., Di Dlasi, C., Barresi, R., Bione, S., Raffaele di Barletta, M., Morandi, L., Merlini, L., Nigro, V., Politano, L., Donati, M. A., Cornelio, F., Cobianchi, F. and Toniolo, D. (1997). X-linked Emery-Dreifuss muscular dystrophy can be diagnosed from skin biopsy or blood sample. Ann. Neurol. 42, 249-253.
33. Nagano, A., Koga, R., Ogawa, M., Kurano, Y., Kawada, J., Okada, R., Hayashi, Y. K., Tsukahara, T. and Arahata, K. (1996). Emerin deficiency at the nuclear membrane in patients with Emery-Dreifuss muscular dystrophy. Nature Genet. 2, 254-259.
34. Nikolakaki, E., Simos, G., Georgatos, S. D. and Giannakouros, T. (1996). A nuclear envelope-associated kinase phosphorylates arginine-serine motifs and modulates interactions between the lamin B receptor and other nuclear proteins. J. Biol. Chem. 271, 8365-8372.
35. Paine, P. L. (1975). Nucleocytoplasmic movement of fluorescent tracers microinjected into living salivary gland cells. J. Cell Biol. 66, 652-657.
36. Pardee, J. D. and Spudich, J. A. (1982). Purification of muscle actin. Meth. Enzymol. 85, 164-181.
37. Parfenov, V. N., Davis, D. S., Pochukalina, G. N., Sample, C. E., Bugaeva, E. A. and Muriti, K. G. (1995). Nuclear filaments and their topological changes in frog oocytes. Exp. Cell Res. 217, 385-394.
38. Roberts, R.G. (1995). Dystrophin, its gene and the dystrophinopathies. Adv. Gen, 33, 177-231.
39. Sasseville, A. M.-J. and Langelier, Y. (1998). In vitro interaction of the carboxy-terminal domain of lamin A with actin. FEBS Lett. 425, 485-489.
40. Simos, G. and Georgatos, S. D. (1992). The inner nuclear membrane protein p58 associates in vivo with a p58 kinase and nuclear lamins. EMBO. J. 11, 4027-4036.
41. Smith, S. and Blobel, G. (1993). The first membrane spanning region of the LBR is sufficient for sorting to the inner nuclear membrane. J. Cell Biol. 120, 631-637.
42. Soullam, B. and Worman, G. (1993). The amino-terminal domain of the lamin-B receptor is a nuclear-envelope targeting signal. J. Cell Biol. 120, 1093-1100.
43. Soullam, B. and Worman, G. (1995). Signals and structural features involved in integral membrane targeting to the inner nuclear membrane. J. Cell Biol. 130, 15-27.
44. Squarzoni, S., Sabatelli, P., Ognibene, A., Toniolo, D., Cartegni, L., Cobianchi, F., Petrini, S., Merlini, L. and Maraldi, N. M. (1998). Immunocytochemical detection of emerin within the nuclear matrix. Neuromusc. Disorders 8, 338-344.
45. Yang, L., Guan, T. and Gerace, L. (1997a). Integral membrane proteins of the nuclear envelope are dispersed throughout the ER during mitosis. J. Cell Biol. 137, 1199-1210.
46. Yang, L., Guan, T. and Gerace, L. (1997b). Lamin-binding fragment of LAP2 inhibits increase in nuclear volume during the cell cycle and progression into S-phase. J. Cell Biol. 139, 1077-1087.
47. Yates, J. R. W. and Wehnert, M. (1999). The Emery-Dreifuss muscular dystrophy mutation database. Neuromusc. Disorders (in press).
48. Yates, J. R. W., Bagshaw, J., Aksmanovic, V. M. A., Coomber, E., McMahon, R., Whittaker, J. L., Morrison, P. J., Kendrick-Jones, J. and Ellis, J. A. (1999). Genotype-phenotype analysis in X-linked Emery-Dreifuss muscular dystrophy and identification of a missense mutation associated with a milder phenotype. Neuromusc. Disorders 9, 159-165.
49. Ye, Q. and Worman, H. J. (1994). Primary structure analysis and DNA binding of human LBR, an integral protein of the nuclear envelope inner membrane. J. Biol. Chem. 269, 11306-11311.
50. Yorifuji, H., Tadano, Y., Tsuchiya, Y., Ogawa, M., Goto, K., Umetani, A., Asaka, Y. and Arahata, K. (1997). Emerin, deficiency of which causes EDMD, is localized at the inner nuclear membrane. Neurogenet. 1, 135-140.