Expression and localization of nuclear proteins in autosomal-dominant Emery-Dreifuss muscular dystrophy with LMNA R377H mutation

BMC Cell Biology

Volumn 5, Issue , 2004, Pages

  Reichart, Beate ^a   Klafke, Ruth ^a   Dreger, Christine ^b   Krüeger, Eleonora ^a   Motsch, Isabell ^a   Ewald, Andrea ^a   Schäfer, Jochen ^c   Reichmann, Heinz ^c   Müeller, Clemens R ^a   Dabauvalle, Marie Christine ^a  

^a UNIVERSITY OF WÜRZBURG   (Germany)

^b GERMAN CANCER RESEARCH CENTER DKFZ   (Germany)

^c UNIVERSITY HOSPITAL CARL GUSTAV CARUS   (Germany)

Author keywords

[No Author keywords available]

Indexed keywords

CELL RECEPTOR; EMERIN; ENVELOPE PROTEIN; LAMIN A; LAMIN B; LAMIN C; MEMBRANE PROTEIN; MESSENGER RNA; NUCLEAR PROTEIN; RNA POLYMERASE II;

ARTICLE; AUTOSOMAL DOMINANT DISORDER; CASE REPORT; CELL LEVEL; CELL MATURATION; CELL NUCLEUS; CELL NUCLEUS MEMBRANE; CELL STRUCTURE; CELL SYNCHRONIZATION; CELL TYPE; CELLULAR DISTRIBUTION; CHROMATIN STRUCTURE; CYTOPLASM; ELECTRON MICROSCOPY; EMERY DREIFUSS MUSCULAR DYSTROPHY; ENDOPLASMIC RETICULUM; ENZYME ACTIVITY; ENZYME LOCALIZATION; GENE MUTATION; GENETIC TRANSCRIPTION; HUMAN; HUMAN CELL; HUMAN TISSUE; IMMUNOCYTOCHEMISTRY; IMMUNOFLUORESCENCE MICROSCOPY; LYMPHOBLASTOID CELL; MUSCLE CELL; MUSCLE DISEASE; MUSCLE TISSUE; MYOBLAST; PATHOLOGY; POINT MUTATION; PROTEIN EXPRESSION; PROTEIN LOCALIZATION; PROTEIN STABILITY; RNA INTERFERENCE; RNA TRANSCRIPTION; SKIN FIBROBLAST; SYMPTOMATOLOGY; TISSUE SECTION; WILD TYPE;

AMINO ACID SUBSTITUTION; CELL NUCLEUS; CHROMATIN; HUMANS; LAMIN TYPE A; MUSCULAR DYSTROPHY, EMERY-DREIFUSS; MYOBLASTS; NUCLEAR ENVELOPE; NUCLEAR PROTEINS; POINT MUTATION; RECEPTORS, CYTOPLASMIC AND NUCLEAR; RNA POLYMERASE II;

EID: 2342555610     PISSN: 14712121     EISSN: None     Source Type: Journal    
DOI: 10.1186/1471-2121-5-12     Document Type: Article

References (84)

1. Gruenbaum Y, Goldman RD, Meyuhas R, Mills E, Margalit A, Fridkin A, Dayani Y, Prokocimer M, Enosh A: The nuclear lamina and its functions in the nucleus. Int Rev Cyt 2003,226:1-62.
2. Lin F, Worman HJ. Structural organization of the human gene encoding nuclear lamin A and nuclear lamin C. J Biol Chem 1993,268:16321-16326.
3. Stuurmann N, Heins S, Aebi U: Nuclear lamins: Their structure, assembly, and interactions. J Struct Biol 1998,122:42-66.
4. Bonne G, Di Barletta MR, Varnous S, Becane HM, Hammouda EH, Merlini L, Muntoni F, Greenberg CR, Gary F, Urtizberea JA, Duboc D, Fardeau M, Toniolo D, Schwartz K: Mutations in the gene encoding lamin A/C cause autosomal dominant Emery-Dreifuss muscular dystrophy. Nature Genet 1999,21:285-288.
5. Bione S, Maestrini E, Rivella S, Mancini M, Regis S, Romeo G,Toniolo D: Identification of a novel X-linked gene responsible for Emery-Dreifuss muscular dystrophy. Nature Genet 1994,8:323-327.
6. Emery AEH: Emery-Dreifuss syndrome. J Med Genet 1989,26:637-641.
7. Muchir A, Bonne G, van der Kooi AJ, van Meegen M, Baas F, Bolhuis PA, de Visser M, Schwartz K: Identification of mutations in the gene encoding lamins A/C in autosomal dominant limb girdle muscular dystrophy with atrioventricular conduction disturbances (LGMD1B). Hum Molec Genet 2000,9:1453-1459.
8. Fatkin D, MacRae C, Sasaki T, Wolff MR, Porcu M, Frenneaux M, Atherton J, Vidaillet HJ jr, Spudisch S, De Girolami U, Seidman JG, Seidman C, Muntoni F, Muehle G, Johnson W, McDonough B: Missense mutations in the rod domain of the lamin A/C gene as causes of dilated cardiomyopathy and conduction-system disease. N Engl J Med 1999,2:1759-1762.
9. Cao H, Hegele RA: Nuclear lamin A/C R482Q mutation in Canadian kindreds with Dunnigan-type familial partial lipodystrophy. Hum Molec Genet 2000,9:109-112.
10. Shackleton S, Lloyd DJ, Jackson, SNJ, Evans R, Niermeijer MF, Singh BM, Schmidt H, Brabant G, Kumar S, Durrington PN, Gregory S, O'Rahilly S, Trembath RC: LMNA, encoding lamin A/C, is mutated in partial lipodystrophy. Nature Genet 2000,24:153-156.
11. Raffaele di Barletta M, Ricci E, Galluzzi G, Tonali P, Mora M, Morandi L, Romorini A, Voit T, Orstavik, KH, Merlini L, Trevisan C, Biancalana V, Housmanowa-Petrusewicz I, Bione S, Ricotti R, Schwartz K, Bonne G, Toniolo D: Different mutations in the LMNA gene cause autosomal dominant and autosomal recessive Emery-Dreifuss muscular dystrophy. Am J Hum Genet 2000,66:1407-1412.
12. Bouhouche A, Benomar A, Birouk N, Mularoni A, Meggouh F, Tassin J, Grid D, Vandenberghe A, Yahyaoui M, Chkili T, Brice A, LeGuern E: A locus for an axonal form of autosomal recessive Charcot-Marie-Tooth disease maps to chromosome 1q21.2-q21.3. Am J Hum Genet 1999,65:722-727.
13. De Sandre-Giovannoli A, Chaouch M, Kozlov S, Vallat JM, Tazir M, Kassouri N, Szepetowski P, Hammadouche T, Vandenberghe A, Stewart CL, Grid D, Levy N: Homozygous defects in LMNA, encoding lamin A/C nuclear-envelope proteins, cause autosomal recessive axonal neuropathy in human (Charcot-Marie-Tooth disorder type 2) and mouse. Am J Hum Genet 2002,70:726-736.
14. Novelli G, Muchir A, Sangiuolo F, Helbling-Leclerc A, D'Apice MR, Massart C, Capon F, Sbraccia P, Federici M, Lauro R, Tudisco C, Pallotta R, Scarano G, Dallapiccola B, Merlini L, Bonne G: Mandibuloacral dysplasia is caused by a mutation in LMNAencoding lamin A/C. Am J Hum Genet 2002,71:426-431.
15. Erikson M, Ted Brown W, Gordon LB, Glynn MW, Singer J, Scott L, Erdos MR, Robbins CM, Moses TY, Berglund P, Dutra A, Pak E, Durkin S, Csoka A, Boehnke M, Glower TW, Collins FS: Recurrent de novo point mutations in lamin A cause Hutchinson_gilford progeria syndrome. Nature 2003, 423:293-298.
16. De Sandre-Giovannoli A, Bernard R, Cau P, Navarro C, Amiel J, Boccaccio I, Lyonnet S, Stewrt C., Munnich A, Le Merrer M, Lévy N: Lamin A truncation in HUtchinson-Gilford Progeria. Science 2003,300:2055.
17. Hegele R A, Huff MW, Young TK: Common genomic variation in LMNA modulates indexes of obesity in Inuit. J Clin Endocr Metab 2001,86:2747-2751.
18. Genschel J, Schmidt HH: Mutations in the LMNA gene encoding lamin A/C. Hum Mut 2000,16:451-459.
19. Leiden Muscular Dystrophy pages:http://www.dmd.nl
20. Morris GE, Manilal S. Heart to Heart: From nuclear proteins to Emery-Dreifuss muscular dystrophy. Hum Mol Genet 1999,8:847-1851.
21. Clements L, Manilal S, Love DR, Morris GE: Direct interaction between emerin and lamin A. Biochem Biophys Res Commun 2000,267:709-714.
22. Fairley EA, Kendrick-Jones J, Ellis JA: The Emery-Dreifuss muscular dystrophy phenotype arises from aberrant targeting and binding of emerin at the inner nuclear membrane. J Cell Sci 1999,112:2571-2582.
23. Morris GE: The role of the nuclear envelope in Emery-dreifuss muscular dystrophy. Trends Mol Med 2001,7:572-577.
24. Manilal S, Sewry CA, Perebeov A, thi Man N, Gobbi P, Hawkes S, Love DR, Morris GE: Distribution of emerin and lamins in the heart and implications for Emery-Dreifuss muscular dystrophy. Hum Mol Genet 1999,8:353-359.
25. Tsuchiya Y, Hase A, Ogawa M, Yorifuji H, Arahata K: Distinct regions specify the nuclear membrane targeting of emerin, the responsible protein for Emery-Dreifuss muscular dystrophy. Eur J Biochem 1999,259:859-865.
26. Holt I, Östlund C, Stewart CL, Thi Man N, Worman HJ, Morris GE: Effect of pathogenic mis-sense mutations in lamin A on its interaction with emerin in vivo. J Cell Sci 2003,116: 3027-3053.
27. Vaughan OA, Alvarez-Reyes M, Bridger JM, Broers JLV, Ramaekers FCS, Wehnert M, Morris GE, Whitfield WGF, Hutchison CJ: Both emerin and lamin C depend on lamin A for localization at the nuclear envelope. J Cell Sci 2001, 114: 2577-2590.
28. Dabauvalle MC, Scheer U: Assembly of nuclear pore complexes in Xenopus egg extract. Biol Cell 1991,72:25-29.
29. Dabauvalle MC, Loos K, Merkert H, Scheer U. Spontaneous assembly of pore complex-containing membranes ("annulate lamellae") in Xenopus egg extract in the absence of chromatin. J Cell Biol 1991,112:1073-1082.
30. Spann TP, Goldman AE, Wang C Huang S, Goldman RD: Alteration of nuclear lamin organization inhibits RNA polymerase II-dependent transcription. J Cell Biol 2002,156:603-608.
31. 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 2002,25:898-901.
32. Sabatelli P, Lattanzi G, Ognibene A, Columbaro M, Capanni C, Merlini L, Maraldi N, Squarzoni S: Nuclear alteration in autosomal-dominant Emery-Dreifuss muscular dystrophy. Muscle and Nerve 2001,24:826-829
33. Alberts AW, Chen J, Kuron G., Hunt V, Huff J, Hoffman C, Rothrock J, Lopez M, Joshua H, Harris E, Patchett A, Monaghan R, Currie S, Stapley E, Albers-Schinberg G, Hensens O, Hirshfield J, Hoogsteen K, Liesch J, Springer J: A highly potent competitive inhibitor of hydroxymethylglutaryl-coenzyme A reductase and a cholesterol-lowering agent. Proc Natl Acad Sci USA 1980, 77: 3957-3961.
34. Beck LA, Hosick TJ, Sinensky M: Isoprenylation is required for the processing of the lamin A precursor. J Cell Biol 1990,110:1489-1499.
35. Fidzianska A, Hausmanowa-Petrusewicz I: Architectural abnormalities in muscle nuclei. Ultrastructural differences between X-linked and autosomal dominant forms of EDMD. J Neurol Sci 2003,210:47-51.
36. Powell L, Burke B: Internuclear exchange of an inner nuclear membrane protein (p55) in heterokaryons: in vivo evidence for the association of p55 with the nuclear lamina. J Cell Biol 1990,111:1709-1719.
37. Ellenberg J, Siggia ED, Moreira JE, Smith CL, Presley JF, Worman HJ, Lippincott-Schwartz J: Nuclear membrane dynamics and reassembly in living cells: targeting of an inner nuclear membrane protein in interphase and mitosis. J Cell Biol 1997,138:1193-1206.
38. Yang L, Guan T, Gerace L: Integral membrane proteins of the nuclear envelope are dispersed throughout the endoplasmic reticulum during mitosis. J Cell Biol 1997,137:1199-1210.
39. Foisner R, Gerace L: Integral membrane proteins of the nuclear envelope interact with lamins and chromosomes, and binding is modulated by mitotic phosphorylation. Cell 1993, 73:1267-1279.
40. Furukawa K, Fritze CE, Gerace L: 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 1998,273:4213-4219.
41. Lin F, Blake D, Callebaut I, Skerjanc IS, Holmer L, Mc Burney MW, Paulin-Levasseur M, Worman J: MAN1, an inner nuclear membrane protein that shares the LEM domain with lamina-associated polypeptide 2 and emerin. J Biol Chem 2000,275:4840-4847.
42. Holmer H, Worman HJ: Inner nuclear membrane proteins: Functions and targeting. Cell Mol Life Sci 2001,58:1741-1747.
43. Östlund C, Ellenberg J, Hallberg E, Lippincott-Scwartz J, Worman HJ: Intracellular trafficking of emerin, the Emery-Dreifuss muscular dystrophy protein. J Cell Sci 1999,112:1709-1719.
44. Colomer J, Itturiaga C, Bonne G, Schwartz K, Manilal S, Morris GE, Puche M, Fernández-Álvarez E: Autosomal dominant Emery-Dreifuss muscular Dystrophy: a new family with late diagnosis. Neuromusc Disord 2002,12:19-25.
45. Ognibene A, Sabatelli P, Petrini S, Squarzoni S, Riccio M, Santi S, Villanova M, Palmeri S, Merlini L, Maraldi MN: Nuclear changes in a case of X-linked Emery Dreifuss muscular dystrophy. Muscle Nerve 1999,22:864-869.
46. Markiewicz E, Venables R, Alvarez-Reyes M, Quinlan R, Dorobek M, Hausmanowa-Petrucewicz I, Hutchison C: Increased solubility of lamins and redistribution of lamin C in X-linked Emery-Dreifuss muscular dystrophy fibroblasts. J Struc Biol 2002,140:241-253.
47. Vigouroux C, Auclair M, Dubosclard E, Pouchelet M, Capeau J, Courvalin JC, Buendia B: Nuclear envelope disorganization in fibroblasts from lipodystrophic patients with heterozygous R482Q/W mutations in the lamin A/C gene. J Cell Sci 2001,114:4459-4468.
48. Östlund C, Bonne G, Schwartz K, Worman H: Properties of lamin A mutants found in Emery-Dreifuss muscular dystrophy, cardiomyopathiy and Dunnigan-type partial lipodystrophy. J Cell Sci 2001,114:4435-4445.
49. Moir RD, Yoon M, Khuon S, Goldman RD: Nuclear lamins A and B1: different pathways of assembly during nuclear envelope formation in living cells. J Cell Biol 2000,151:1155-1168.
50. Fidzianska A, Toniolo D, Hausmanowa-Petrusewisz I: Ultrastructural abnormality of sarcolemmal nuclei in Emery-Dreifuss muscular dystrophy (EDMD). J Neur Sci 1998,159:88-93.
51. Sullivan T, Escalante-Alcade D, Bhatt H, Anver M, Bhat N, Nagashima K, Stewart C, Burke B: Loss of A-type lamin expression compromises nuclear envelope integrity leading to muscular dystrophy. J Cell Biol 1999,147:913-919.
52. Charniot JC, Pascal C, Bouchier C, Sébillon P, Salama J, Duboscq-Bidot L, Peuchmaurd M, Desnos M, Artigou JY, Komajda M: Functional Consequences of an LMNA Mutation Associated with a new cardiac and non-cardiac phenotype. Hum Mutat 2003,21:473-481.
53. Cartegni L, di Barletta MR, Barresi R, Squarzoni S, Sabatelli P, Maraldi N, Mora M, Di Blasi C, Cornelio F, Merlini L, Villa A, Cobianchi F, Toniolo D: Heart-specific localization of emerin: new insights into Emery-Dreifuss muscular dystrophy. Hum Mol Genet 1997,6:2257-2264.
54. Squarzoni S, Sabatelli P, Ognibene A, Toniolo D, Cartegni L, Cobianchi F, Petrini S, Merlini L, Maraldi NM: Immunocytochemical detection of emerin within the nuclear matrix. Neuromusc Disord 1998,8:338-344.
55. Harborth J, Elbashir SM, Bechert K, Tuschl T, Weber K: Identification of essential genes in cultured mammalian cells using small interfering RNAs. J Cell Sci 2001,114:4557-4565.
56. Raharjo WH, Enarson P, Sullivan T, Stewart CL, Burke B: Nuclear envelope defects associated with LMNA mutations cause dilated cardiomyopathy and Emery-Dreifuss muscular dystrophy. J Cell Sci 2001,114:4447-4457.
57. Capanni C, Cenni V, Mattioli E, Sabatelli P, Ognibene A, Columbaro M, Parnaik VK, Wehnert M, Maraldi NM, Sqarzoni S, Lattanzi G: Failure of lamin A/C to functionally assemble in R482L mutated familial partial lipodystrophy fibroblasts: altered intermolecular interaction with emerin and implications for gene transcription. Exp Cell Res 2003,291:122-134.
58. Worman HJ, Courvalin JC: The inner nuclear membrane. J Membr Biol 2000,177:1-11.
59. Worman HJ, Yuan J, Blobel G, Georgatos SD: A lamin B receptor in the nuclear envelope. Proc Natl Acad Sci USA 1998,85:8531-8534.
60. Olins A, Herrmann H, Lichter P, Kratzmeier M, Doenecke D, Olins DE: Nuclear envelope and chromatin compositional differences comparing undifferentiated and retinoic acid- and phorbol ester-treated HL-60 cells. Exp Cell Res 2001,268:115-127.
61. Gajewski A, Krohne G: Subcellular distribution of the Xenopus p58/lamin B receptor in oocytes and eggs. J Cell Sci 1999,112:2583-2596.
62. Ye Q, Worman HJ: 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 1994,269:11306-11311.
63. Meier J, Georgatos S: Type B lamins remain associated with the integral nuclear envelope protein p58 during mitosis: implications for nuclear reassembly. EMBO J 1994,13:1888-1898.
64. Pyrpasopoulou A, Meir J, Maison C, Simos G, Georgatos SD: The lamin B receptor (LBR) provides essential chromatin docking sites at the nuclear envelope. EMBO J 1996,24:7108-7119.
65. Kawahire S, Takeuchi M, Gohshi T, Sasagawa S, Shimada M, Takahashi M, Abe TK, Ueda T, Kuwano R, Hikawa A, Ichimura T, Omata S, Horigome T: cDNA cloning of nuclear localization signal binding protein NBP60, a rat homologue of lamin B receptor, and identification of binding sites of human lamin B receptor for nuclear localization signals and chromatin. J Biochem 1997,121:881-889.
66. Ye Q, Worman HJ: Interaction between an integral protein of the nuclear envelope inner membrane and human chromodomain proteins homologous to Drosophila HP1. J Biol Chem 1996,271:14653-14656.
67. Ye Q, Callebaut I, Pezhman A, Courvalin JC, Worman HJ: Domain-specific interactions of human HP1-type chromodomain proteins and inner nuclear membrane protein LBR. J Biol Chem 1997,272:14983-14989.
68. Liu J, Ben-Shahar TR, Riemer D, Treinin M, Spann P, Weber K, Fire A, Gruenbaum Y: Essential roles for Caenorhabditis elegans lamin gene in nuclear organization, cell cycle progression, and spatial organization of nuclear pore complexes. Mol Biol Cell 2000,11:3937-3947.
69. Moir RD, Spann TP, Herrmann H, Goldman RD: Disruption of nuclear lamin organization blocks the elongation phase of DNA replication. J Cell Biol 2000,149:1179-1192.
70. Favreau C, Dubosclard E, Östlund C, Vigouroux C, Capeau J, Wehnert M, Higuet D, Worman HJ, Courvalin JC, Buendia B: Expression of lamin A mutated in the carboxylterminal tail generates an aberrant nuclear phenotype similar to that observed in cells from patients with Dunnigan-type partial lipodystrophy and Emery-Dreifuss muscular dystrophy. Exp Cell Res 2003,282:14-23.
71. Wilson KL. The nuclear envelope, muscular dystrophy, and gene expression. Trends Cell Biol 2000,10:125-129.
72. Wilson KL, Zastrow MS, Lee KK: Lamins and disease: insights into nuclear infrastructure. Cell 2001,104:647-650.
73. Wilczynski GM, Engel WK, Askanas V: Novel cytoplasmic immunolocalization of RNA polymerase II in inclusion-body myositis muscle. Neur Rep 2001,12:1809-1814.
74. Dahmus ME: Reversible phosphorylation of the C-terminal domain of RNA polymerase II. J Biol Chem 1996,271:19009-19012.
75. Dubowitz V: Muscle biopsy: a practical approach. 2nd ed. London: Baillière Tindall, 1985.
76. Lourim D, Kempf A, Krohne G: Characterization and quantitation of three B-type lamins in Xenopus oocytes and eggs: increase of lamin LI protein synthesis during meiotic maturation. J Cell Sci 1996,109:1775-1785.
77. Höger TH, Grund C, Franke WW, Krohne G: Immunolocalization of lamins in the thick nuclear lamina of human synovial cells. Eur J Cell Biol 1991,54:150-156.
78. O'Brien T, Hardin S, Greenleaf A, List JT: Phosphorylation of RNA polymerase II C-terminal domain and transcription elongation. Nature 1994,370:75-77.
79. Patturajan M, Schulte RJ, Sefton BM, Berezney R, Vinvent M, Bensaude O, Warren SL, Corden JL: Growth-related changes in phosphorylation of yeast RNA polymerase II. J Biol Chem 1998,273:4689-4694.
80. Christensen ME, MolooJ, Swischuk JL, Schelling ME: Characterization of the nucleolar protein, B-36, using monoclonal antibodies. Exp Cell Res 1986,166:77-93.
81. Dreger CK, König AR, Spring H, Lichter P, Hermann H: Investigation of nuclear architecture with a domain-presenting expression system. J Struct Biol 2002,140: 100-115.
82. Benavente R, Krohne G: Involvement of nuclear lamins in postmitotic reorganization of chromatin as demonstrated by microinjection of lamin antibodies. J Cell Biol 1986,103:1847-1854.
83. Thomas JO, Kornberg RD: An octamer of histones in chromatin and free in solution. Proc Natl Acad Sci USA 1975,72:2626-2630.
84. Kyhse-Anderson J: Electroblotting of multiple gels: a simple apparatus without buffertank for rapid transfer of proteins from polyacrylamid to nitrocellulose. J Biochem Biophys 1984,10:203-209.