"Laminopathies": a wide spectrum of human diseases.
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Journal: 2007/August - Experimental Cell Research
ISSN: 0014-4827
Abstract:
Mutations in genes encoding the intermediate filament nuclear lamins and associated proteins cause a wide spectrum of diseases sometimes called "laminopathies." Diseases caused by mutations in LMNA encoding A-type lamins include autosomal dominant Emery-Dreifuss muscular dystrophy and related myopathies, Dunnigan-type familial partial lipodystrophy, Charcot-Marie-Tooth disease type 2B1 and developmental and accelerated aging disorders. Duplication in LMNB1 encoding lamin B1 causes autosomal dominant leukodystrophy and mutations in LMNB2 encoding lamin B2 are associated with acquired partial lipodystrophy. Disorders caused by mutations in genes encoding lamin-associated integral inner nuclear membrane proteins include X-linked Emery-Dreifuss muscular dystrophy, sclerosing bone dysplasias, HEM/Greenberg skeletal dysplasia and Pelger-Huet anomaly. While mutations and clinical phenotypes of "laminopathies" have been carefully described, data explaining pathogenic mechanisms are only emerging. Future investigations will likely identify new "laminopathies" and a combination of basic and clinical research will lead to a better understanding of pathophysiology and the development of therapies.
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Exp Cell Res 313(10): 2121-2133
PMID: 17467691

“Laminopathies:” a wide spectrum of human diseases

Department of Medicine and Department of Anatomy and Cell Biology, College of Physicians and Surgeons, Columbia University, New York, NY 10032, USA
Institut National de la Santé et de la Recherche Médicale, U582, Institut de Myologie, Paris F-75013, France
Université Pierre et Marie Curie-Paris 6, Faculté de médecine, Paris F-75013, France
AP-HP, Groupe Hospitalier Pitié-Salpêtrière, U.F. Myogénétique et Cardiogénétique, service de Biochimie B, Paris F-75013, France
Corresponding author. Department of Medicine, College of Physicians and Surgeons, Columbia University, 630 West 168 Street, P&S 10-509, New York, NY 10032, USA; Phone: 212-305-8156; Fax: 212-305-6443; ude.aibmuloc@41wjh
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Abstract

Mutations in genes encoding the intermediate filament nuclear lamins and associated proteins cause a wide spectrum of diseases sometimes called “laminopathies.” Diseases caused by mutations in LMNA encoding A-type lamins include autosomal dominant Emery-Dreifuss muscular dystrophy and related myopathies, Dunnigan-type familial partial lipodystrophy, Charcot-Marie-Tooth disease type 2B1 and developmental and accelerated aging disorders. Duplication in LMNB1 encoding lamin B1 causes autosomal dominant leukodystrophy and mutations in LMNB2 encoding lamin B2 are associated with acquired partial lipodystrophy. Disorders caused by mutations in genes encoding lamin-associated integral inner nuclear membrane proteins include X-linked Emery-Dreifuss muscular dystrophy, sclerosing bone dysplasias, HEM/Greenberg skeletal dysplasia and Pelger-Huet anomaly. While mutations and clinical phenotypes of “laminopathies” have been carefully described, data explaining pathogenic mechanisms are only emerging. Future investigations will likely identify new “laminopathies” and a combination of basic and clinical research will lead to a better understanding of pathophysiology and the development of therapies.

Keywords: lamin, nuclear envelope, intermediate filaments, muscular dystrophy, lipodystrophy, progeria
Abstract

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References

  • 1. McKeon FD, Kirschner MW, Caput DHomologies in both primary and secondary structure between nuclear envelope and intermediate filament proteins. Nature. 1986;319:463–468.[PubMed][Google Scholar]
  • 2. Aebi U, Cohn J, Buhle L, Gerace LThe nuclear lamina is a meshwork of intermediate-type filaments. Nature. 1986;323:560–564.[PubMed][Google Scholar]
  • 3. Goldman AE, Maul G, Steinert PM, Yang HY, Goldman RDKeratin-like proteins that coisolate with intermediate filaments of BHK-21 cells are nuclear lamins. Proc Natl Acad Sci U S A. 1986;83:3839–3843.[Google Scholar]
  • 4. Fisher DZ, Chaudhary N, Blobel GcDNA sequencing of nuclear lamins A and C reveals primary and secondary structural homology to intermediate filament proteins. Proc Natl Acad Sci U S A. 1986;83:6450–6454.[Google Scholar]
  • 5. Worman HJ, Courvalin JCThe inner nuclear membrane. J Membr Biol. 2000;177:1–11.[PubMed][Google Scholar]
  • 6. Zastrow MS, Vlcek S, Wilson KLProteins that bind A-type lamins: integrating isolated clues. J Cell Sci. 2004;117:979–987.[PubMed][Google Scholar]
  • 7. Gerace L, Blobel GThe nuclear envelope lamina is reversibly depolymerized during mitosis. Cell. 1980;19:277–287.[PubMed][Google Scholar]
  • 8. Krohne G, Benavente R. The nuclear lamins. A multigene family of proteins in evolution and differentiation. Exp Cell Res. 1986;162:1–10.[PubMed]
  • 9. Wydner KL, McNeil JA, Lin F, Worman HJ, Lawrence JBChromosomal assignment of human nuclear envelope protein genes LMNA, LMNB1, and LBR by fluorescence in situ hybridization. Genomics. 1996;15:474–478.[PubMed][Google Scholar]
  • 10. Lin F, Worman HJStructural organization of the human gene encoding nuclear lamin A and nuclear lamin C. J Biol Chem. 1993;268:16321–16326.[PubMed][Google Scholar]
  • 11. Young SG, Fong LG, Michaelis SPrelamin A, Zmpste24, misshapen cell nuclei, and progeria--new evidence suggesting that protein farnesylation could be important for disease pathogenesis. J Lipid Res. 2005;46:2531–2558.[PubMed][Google Scholar]
  • 12. Rusinol AE, Sinensky MSFarnesylated lamins, progeroid syndromes and farnesyl transferase inhibitors. J Cell Sci. 2006;119:3265–3272.[PubMed][Google Scholar]
  • 13. Stewart C, Burke BTeratocarcinoma stem cells and early mouse embryos contain only a single major lamin polypeptide closely resembling lamin B. Cell. 1987;51:383–392.[PubMed][Google Scholar]
  • 14. Guilly MN, Bensussan A, Bourge JF, Bornens M, Courvalin JCA human T lymphoblastic cell line lacks lamins A and C. EMBO J. 1987;6:3795–3799.[Google Scholar]
  • 15. Worman HJ, Lazaridis I, Georgatos SD. Nuclear lamina heterogeneity in mammalian cells. Differential expression of the major lamins and variations in lamin B phosphorylation. J Biol Chem. 1988;263:12135–12141.[PubMed]
  • 16. Rober RA, Weber K, Osborn MDifferential timing of nuclear lamin A/C expression in the various organs of the mouse embryo and the young animal: a developmental study. Development. 1989;105:365–378.[PubMed][Google Scholar]
  • 17. Cance WG, Chaudhary N, Worman HJ, Blobel G, Cordon-Cardo CExpression of the nuclear lamins in normal and neoplastic human tissues. J Exp Clin Cancer Res. 1992;11:233–246.[PubMed][Google Scholar]
  • 18. Furukawa K, Inagaki H, Hotta YIdentification and cloning of an mRNA coding for a germ cell-specific A-type lamin in mice. Exp Cell Res. 1994;212:426–430.[PubMed][Google Scholar]
  • 19. Lin F, Worman HJStructural organization of the human gene (LMNB1) encoding nuclear lamin B1. Genomics. 1995;27:230–236.[PubMed][Google Scholar]
  • 20. Höger TH, Zatloukal K, Waizenegger I, Krohne GCharacterization of a second highly conserved B-type lamin present in cells previously thought to contain only a single B-type lamin. Chromosoma. 1990;99:379–390.[PubMed][Google Scholar]
  • 21. Biamonti G, Giacca M, Perini G, Contreas G, Zentilin L, Weighardt F, Guerra M, Della Valle G, Saccone S, Riva S, Falaschi AThe gene for a novel human lamin maps at a highly transcribed locus of chromosome 19 which replicates at the onset of S-phase. Mol Cell Biol. 1992;12:3499–3506.[Google Scholar]
  • 22. Furukawa K, Hotta YcDNA cloning of a germ cell specific lamin B3 from mouse spermatocytes and analysis of its function by ectopic expression in somatic cells. EMBO J. 1993;12:97–106.[Google Scholar]
  • 23. Tsai MY, Wang S, Heidinger JM, Shumaker DK, Adam SA, Goldman RD, Zheng YA mitotic lamin B matrix induced by RanGTP required for spindle assembly. Science. 2006;311:1887–1893.[PubMed][Google Scholar]
  • 24. Schirmer EC, Florens L, Guan T, Yates JR, 3rd, Gerace LNuclear membrane proteins with potential disease links found by subtractive proteomics. Science. 2003;301:1380–1382.[PubMed][Google Scholar]
  • 25. Soullam B, Worman HJThe amino-terminal domain of the lamin B receptor is a nuclear envelope targeting signal. J Cell Biol. 1993;120:1093–1100.[Google Scholar]
  • 26. Soullam B, Worman HJSignals and structural features involved in integral membrane protein targeting to the inner nuclear membrane. J Cell Biol. 1995;130:15–27.[Google Scholar]
  • 27. Ellenberg J, Siggia ED, Moreira JE, Smith CL, Presley JF, Worman HJ, Lippincott-Schwartz JNuclear 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.[Google Scholar]
  • 28. Ohba T, Schirmer EC, Nishimoto T, Gerace LEnergy- and temperature-dependent transport of integral proteins to the inner nuclear membrane via the nuclear pore. J Cell Biol. 2004;167:1051–1062.[Google Scholar]
  • 29. King MC, Lusk CP, Blobel GKaryopherin-mediated import of integral inner nuclear membrane proteins. Nature. 2006;442:1003–1007.[PubMed][Google Scholar]
  • 30. Yang L, Guan T, Gerace LIntegral membrane proteins of the nuclear envelope are dispersed throughout the endoplasmic reticulum during mitosis. J Cell Biol. 1997;137:1199–1210.[Google Scholar]
  • 31. Bione S, Maestrini E, Rivella S, Mancini M, Regis S, Romeo G, Toniolo DIdentification of a novel X-linked gene responsible for Emery-Dreifuss muscular dystrophy. Nat Genet. 1994;8:323–327.[PubMed][Google Scholar]
  • 32. Nagano A, Koga R, Ogawa M, Kurano Y, Kawada J, Okada R, Hayashi YK, Tsukahara T, Arahata KEmerin deficiency at the nuclear membrane in patients with Emery-Dreifuss muscular dystrophy. Nat Genet. 1996;12:254–259.[PubMed][Google Scholar]
  • 33. Manilal S, Nguyen TM, Sewry CA, Morris GEThe Emery-Dreifuss muscular dystrophy protein, emerin, is a nuclear membrane protein. Hum Mol Genet. 1996;5:801–808.[PubMed][Google Scholar]
  • 34. 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 KMutations in the gene encoding lamin A/C cause autosomal dominant Emery-Dreifuss muscular dystrophy. Nat Genet. 1999;21:285–288.[PubMed][Google Scholar]
  • 35. 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 DDifferent mutations in the LMNA gene cause autosomal dominant and autosomal recessive Emery-Dreifuss muscular dystrophy. Am J Hum Genet. 2000;66:1407–1412.[Google Scholar]
  • 36. Emery AEEmery-Dreifuss muscular dystrophy - a 40 year retrospective. Neuromuscul Disord. 2000;10:228–232.[PubMed][Google Scholar]
  • 37. Fatkin D, MacRae C, Sasaki T, Wolff MR, Porcu M, Frenneaux M, Atherton J, Vidaillet HJ, Jr, Spudich S, De Girolami U, Seidman JG, Seidman C, Muntoni F, Muehle G, Johnson W, McDonough BMissense 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;341:1715–1724.[PubMed][Google Scholar]
  • 38. Muchir A, Bonne G, van der Kooi AJ, van Meegen M, Baas F, Bolhuis PA, de Visser M, Schwartz KIdentification of mutations in the gene encoding lamins A/C in autosomal dominant limb girdle muscular dystrophy with atrioventricular conduction disturbances (LGMD1B) Hum Mol Genet. 2000;9:1453–1459.[PubMed][Google Scholar]
  • 39. Bonne G, Mercuri E, Muchir A, Urtizberea A, Becane HM, Recan D, Merlini L, Wehnert M, Boor R, Reuner U, Vorgerd M, Wicklein EM, Eymard B, Duboc D, Penisson-Besnier I, Cuisset JM, Ferrer X, Desguerre I, Lacombe D, Bushby K, Pollitt C, Toniolo D, Fardeau M, Schwartz K, Muntoni FClinical and molecular genetic spectrum of autosomal dominant Emery-Dreifuss muscular dystrophy due to mutations of the lamin A/C gene. Ann Neurol. 2000;48:170–180.[PubMed][Google Scholar]
  • 40. Brodsky GL, Muntoni F, Miocic S, Sinagra G, Sewry C, Mestroni LLamin A/C gene mutation associated with dilated cardiomyopathy with variable skeletal muscle involvement. Circulation. 2000;101:473–476.[PubMed][Google Scholar]
  • 41. Cao H, Hegele RANuclear lamin A/C R482Q mutation in canadian kindreds with Dunnigan-type familial partial lipodystrophy. Hum Mol Genet. 2000;9:109–112.[PubMed][Google Scholar]
  • 42. Shackleton S, Lloyd DJ, Jackson SN, 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. Nat Genet. 2000;24:153–166.[PubMed]
  • 43. Speckman RA, Garg A, Du F, Bennett L, Veile R, Arioglu E, Taylor SI, Lovett M, Bowcock AMMutational and haplotype analyses of families with familial partial lipodystrophy (Dunnigan variety) reveal recurrent missense mutations in the globular C-terminal domain of lamin A/C. Am J Hum Genet. 2000;66:1192–1198.[Google Scholar]
  • 44. Caux F, Dubosclard E, Lascols O, Buendia B, Chazouilleres O, Cohen A, Courvalin JC, Laroche L, Capeau J, Vigouroux C, Christin-Maitre SA new clinical condition linked to a novel mutation in lamins A and C with generalized lipoatrophy, insulin-resistant diabetes, disseminated leukomelanodermic papules, liver steatosis, and cardiomyopathy. J Clin Endocr Metab. 2003;88:1006–1013.[PubMed][Google Scholar]
  • 45. Young J, Morbois-Trabut L, Couzinet B, Lascols O, Dion E, Bereziat V, Feve B, Richard I, Capeau J, Chanson P, Vigouroux CType A insulin resistance syndrome revealing a novel lamin A mutation. Diabetes. 2005;54:1873–1878.[PubMed][Google Scholar]
  • 46. Garg A, Speckman RA, Bowcock AMMultisystem dystrophy syndrome due to novel missense mutations in the amino-terminal head and alpha-helical rod domains of the lamin A/C gene. Am J Med. 2002;112:549–555.[PubMed][Google Scholar]
  • 47. van der Kooi AJ, Bonne G, Eymard B, Duboc D, Talim B, Van der Valk M, Reiss P, Richard P, Demay L, Merlini L, Schwartz K, Busch HF, de Visser MLamin A/C mutations with lipodystrophy, cardiac abnormalities, and muscular dystrophy. Neurology. 2002;59:620–623.[PubMed][Google Scholar]
  • 48. 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 GMandibuloacral dysplasia is caused by a mutation in LMNA-encoding lamin A/C. Am J Hum Genet. 2002;71:426–431.[Google Scholar]
  • 49. Simha V, Agarwal AK, Oral EA, Fryns JP, Garg AGenetic and phenotypic heterogeneity in patients with mandibuloacral dysplasia-associated lipodystrophy. J Clin Endocr Metab. 2003;88:2821–2824.[PubMed][Google Scholar]
  • 50. Agarwal AK, Fryns JP, Auchus RJ, Garg AZinc metalloproteinase, ZMPSTE24, is mutated in mandibuloacral dysplasia. Hum Molec Genet. 2003;12:1995–2001.[PubMed][Google Scholar]
  • 51. 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 NHomozygous 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.[Google Scholar]
  • 52. Goizet C, Yaou RB, Demay L, Richard P, Bouillot S, Rouanet M, Hermosilla E, Le Masson G, Lagueny A, Bonne G, Ferrer XA new mutation of the lamin A/C gene leading to autosomal dominant axonal neuropathy, muscular dystrophy, cardiac disease, and leuconychia. J Med Genet. 2004;41:e29.[Google Scholar]
  • 53. Benedetti S, Bertini E, Iannaccone S, Angelini C, Trisciani M, Toniolo D, Sferrazza B, Carrera P, Comi G, Ferrari M, Quattrini A, Previtali SCDominant LMNA mutations can cause combined muscular dystrophy and peripheral neuropathy. J Neurol Neurosurg Psychiatry. 2005;76:1019–1021.[Google Scholar]
  • 54. Walter MC, Witt TN, Weigel BS, Reilich P, Richard P, Pongratz D, Bonne G, Wehnert MS, Lochmuller HDeletion of the LMNA initiator codon leading to a neurogenic variant of autosomal dominant Emery-Dreifuss muscular dystrophy. Neuromuscul Disord. 2005;15:40–44.[PubMed][Google Scholar]
  • 55. Eriksson M, Brown WT, Gordon LB, Glynn MW, Singer J, Scott L, Erdos MR, Robbins CM, Moses TY, Berglund P, Dutra A, Pak E, Durkin S, Csoka AB, Boehnke M, Glover TW, Collins FSRecurrent de novo point mutations in lamin A cause Hutchinson-Gilford progeria syndrome. Nature. 2003;423:293–298.[PubMed][Google Scholar]
  • 56. De Sandre-Giovannoli A, Bernard R, Cau P, Navarro C, Amiel J, Boccaccio I, Lyonnet S, Stewart CL, Munnich A, Le Merrer M, Levy NLamin A truncation in Hutchinson-Gilford progeria. Science. 2003;300:2055.[PubMed][Google Scholar]
  • 57. DeBusk FLThe Hutchinson-Gilford progeria syndrome. J Pediatr. 1972;80:697–724.[PubMed][Google Scholar]
  • 58. Navarro CL, De Sandre-Giovannoli A, Bernard R, Boccaccio I, Boyer A, Genevieve D, Hadj-Rabia S, Gaudy-Marqueste C, Smitt HS, Vabres P, Faivre L, Verloes A, Van Essen T, Flori E, Hennekam R, Beemer FA, Laurent N, Le Merrer M, Cau P, Levy NLamin A and ZMPSTE24 (FACE-1) defects cause nuclear disorganization and identify restrictive dermopathy as a lethal neonatal laminopathy. Hum Molec Genet. 2004;13:2493–2503.[PubMed][Google Scholar]
  • 59. Chen L, Lee L, Kudlow BA, Dos Santos HG, Sletvold O, Shafeghati Y, Botha EG, Garg E, Hanson NB, Martin GM, Mian IS, Kennedy BK, Oshima J. LMNA mutations in atypical Werner's syndrome. Lancet. 2003;362:440–445.[PubMed]
  • 60. Bonne G, Levy N. LMNA mutations in atypical Werner's syndrome. Lancet. 2003;362:1585–1586.[PubMed]
  • 61. Pendas AM, Zhou Z, Cadinanos J, Freije JM, Wang J, Hultenby K, Astudillo A, Wernerson A, Rodriguez F, Tryggvason K, Lopez-Otin CDefective prelamin A processing and muscular and adipocyte alterations in Zmpste24 metalloproteinase-deficient mice. Nat Genet. 2002;31:94–99.[PubMed][Google Scholar]
  • 62. Bergo MO, Gavino B, Ross J, Schmidt WK, Hong C, Kendall LV, Mohr A, Meta M, Genant H, Jiang Y, Wisner ER, Van Bruggen N, Carano RA, Michaelis S, Griffey SM, Young SG. Zmpste24 deficiency in mice causes spontaneous bone fractures, muscle weakness, and a prelamin A processing defect. Proc Natl Acad Sci U S A. 2002;99:13049–13054.
  • 63. Fong LG, Ng JK, Meta M, Cote N, Yang SH, Stewart CL, Sullivan T, Burghardt A, Majumdar S, Reue K, Bergo MO, Young SGHeterozygosity for Lmna deficiency eliminates the progeria-like phenotypes in Zmpste24-deficient mice. Proc Natl Acad Sci U S A. 2004;101:18111–18116.[Google Scholar]
  • 64. Gruber J, Lampe T, Osborn M, Weber KRNAi of FACE1 protease results in growth inhibition of human cells expressing lamin A: implications for Hutchinson-Gilford progeria syndrome. J Cell Sci. 2005;118:689–696.[PubMed][Google Scholar]
  • 65. Scaffidi P, Misteli TReversal of the cellular phenotype in the premature aging disease Hutchinson-Gilford progeria syndrome. Nat Med. 2005;11:440–445.[Google Scholar]
  • 66. Yang SH, Bergo MO, Toth JI, Qiao X, Hu Y, Sandoval S, Meta M, Bendale P, Gelb MH, Young SG, Fong LGBlocking protein farnesyltransferase improves nuclear blebbing in mouse fibroblasts with a targeted Hutchinson-Gilford progeria syndrome mutation. Proc Natl Acad Sci U S A. 2005;102:10291–10296.[Google Scholar]
  • 67. Toth JI, Yang SH, Qiao X, Beigneux AP, Gelb MH, Moulson CL, Miner JH, Young SG, Fong LGBlocking protein farnesyltransferase improves nuclear shape in fibroblasts from humans with progeroid syndromes. Proc Natl Acad Sci U S A. 2005;102:12873–12878.[Google Scholar]
  • 68. Capell BC, Erdos MR, Madigan JP, Fiordalisi JJ, Varga R, Conneely KN, Gordon LB, Der CJ, Cox AD, Collins FSInhibiting farnesylation of progerin prevents the characteristic nuclear blebbing of Hutchinson-Gilford progeria syndrome. Proc Natl Acad Sci U S A. 2005;102:12879–12884.[Google Scholar]
  • 69. Mallampalli MP, Huyer G, Bendale P, Gelb MH, Michaelis SInhibiting farnesylation reverses the nuclear morphology defect in a HeLa cell model for Hutchinson-Gilford progeria syndrome. Proc Natl Acad Sci U S A. 2005;102:14416–14421.[Google Scholar]
  • 70. Glynn MW, Glover TWIncomplete processing of mutant lamin A in Hutchinson-Gilford progeria leads to nuclear abnormalities, which are reversed by farnesyltransferase inhibition. Hum Mol Genet. 2005;14:2959–2969.[PubMed][Google Scholar]
  • 71. Fong LG, Frost D, Meta M, Qiao X, Yang SH, Coffinier C, Young SGA protein farnesyltransferase inhibitor ameliorates disease in a mouse model of progeria. Science. 2006;311:1621–1623.[PubMed][Google Scholar]
  • 72. Yang SH, Meta M, Qiao X, Frost D, Bauch J, Coffinier C, Majumdar S, Bergo MO, Young SG, Fong LGA farnesyltransferase inhibitor improves disease phenotypes in mice with a Hutchinson-Gilford progeria syndrome mutation. J Clin Invest. 2006;116:2115–2121.[Google Scholar]
  • 73. Liu B, Wang J, Chan KM, Tjia WM, Deng W, Guan X, Huang JD, Li KM, Chau PY, Chen DJ, Pei D, Pendas AM, Cadinanos J, Lopez-Otin C, Tse HF, Hutchison C, Chen J, Cao Y, Cheah KS, Tryggvason K, Zhou ZGenomic instability in laminopathy-based premature aging. Nat Med. 2005;11:780–785.[PubMed][Google Scholar]
  • 74. Liu Y, Rusinol A, Sinensky M, Wang Y, Zou YDNA damage responses in progeroid syndromes arise from defective maturation of prelamin A. J Cell Sci. 2006;119:4644–4649.[Google Scholar]
  • 75. Varela I, Cadinanos J, Pendas AM, Gutierrez-Fernandez A, Folgueras AR, Sanchez LM, Zhou Z, Rodriguez FJ, Stewart CL, Vega JA, Tryggvason K, Freije JM, Lopez-Otin CAccelerated ageing in mice deficient in Zmpste24 protease is linked to p53 signalling activation. Nature. 2005;437:564–568.[PubMed][Google Scholar]
  • 76. Delbarre E, Tramier M, Coppey-Moisan M, Gaillard C, Courvalin JC, Buendia BThe truncated prelamin A in Hutchinson-Gilford progeria syndrome alters segregation of A-type and B-type lamin homopolymers. Hum Mol Genet. 2006;15:1113–1122.[PubMed][Google Scholar]
  • 77. Paradisi M, McClintock D, Boguslavsky RL, Pedicelli C, Worman HJ, Djabali KDermal fibroblasts in Hutchinson-Gilford progeria syndrome with the lamin A G608G mutation have dysmorphic nuclei and are hypersensitive to heat stress. BMC Cell Biol. 2005;6:27.[Google Scholar]
  • 78. Dahl KN, Scaffidi P, Islam MF, Yodh AG, Wilson KL, Misteli TDistinct structural and mechanical properties of the nuclear lamina in Hutchinson-Gilford progeria syndrome. Proc Natl Acad Sci U S A. 2006;103:10271–10276.[Google Scholar]
  • 79. Dhe-Paganon S, Werner ED, Chi YI, Shoelson SEStructure of the globular tail of nuclear lamin. J Biol Chem. 2002;277:17381–17384.[PubMed][Google Scholar]
  • 80. Krimm I, Östlund C, Gilquin B, Couprie J, Hossenlopp P, Mornon JP, Bonne G, Courvalin JC, Worman HJ, Zinn-Justin SThe Ig-like structure of the C-terminal domain of lamin A/C, mutated in muscular dystrophies. Structure. 2002;10:811–823.[PubMed][Google Scholar]
  • 81. Lloyd DJ, Trembath RC, Shackleton SA novel interaction between lamin A and SREBP1: implications for partial lipodystrophy and other laminopathies. Hum Mol Genet. 2002;11:769–777.[PubMed][Google Scholar]
  • 82. Bonne G, Yaou RB, Beroud C, Boriani G, Brown S, de Visser M, Duboc D, Ellis J, Hausmanowa-Petrusewicz I, Lattanzi G, Merlini L, Morris G, Muntoni F, Opolski G, Pinto YM, Sangiuolo F, Toniolo D, Trembath R, van Berlo JH, van der Kooi AJ, Wehnert M108th ENMC International Workshop, 3rd Workshop of the MYO-CLUSTER project: EUROMEN, 7th International Emery-Dreifuss Muscular Dystrophy (EDMD) Workshop, 13–15 September 2002, Naarden, The Netherlands. Neuromuscul Disord. 2003;13:508–515.[PubMed][Google Scholar]
  • 83. Vytopil M, Benedetti S, Ricci E, Galluzzi G, Dello Russo A, Merlini L, Boriani G, Gallina M, Morandi L, Politano L, Moggio M, Chiveri L, Hausmanova-Petrusewicz I, Ricotti R, Vohanka S, Toman J, Toniolo DMutation analysis of the lamin A/C gene (LMNA) among patients with different cardiomuscular phenotypes. J Med Genet. 2003;40:e132.[Google Scholar]
  • 84. Sullivan T, Escalante-Alcalde D, Bhatt H, Anver M, Bhat N, Nagashima K, Stewart CL, Burke BLoss of A-type lamin expression compromises nuclear envelope integrity leading to muscular dystrophy. J Cell Biol. 1999;147:913–920.[Google Scholar]
  • 85. Nikolova V, Leimena C, McMahon AC, Tan JC, Chandar S, Jogia D, Kesteven SH, Michalicek J, Otway R, Verheyen F, Rainer S, Stewart CL, Martin D, Feneley MP, Fatkin DDefects in nuclear structure and function promote dilated cardiomyopathy in lamin A/C-deficient mice. J Clin Invest. 2004;113:357–369.[Google Scholar]
  • 86. Arimura T, Helbling-Leclerc A, Massart C, Varnous S, Niel F, Lacene E, Fromes Y, Toussaint M, Mura AM, Keller DI, Amthor H, Isnard R, Malissen M, Schwartz K, Bonne GMouse model carrying H222P-Lmna mutation develops muscular dystrophy and dilated cardiomyopathy similar to human striated muscle laminopathies. Hum Mol Genet. 2005;14:155–169.[PubMed][Google Scholar]
  • 87. Mounkes LC, Kozlov SV, Rottman JN, Stewart CLExpression of an LMNA-N195K variant of A-type lamins results in cardiac conduction defects and death in mice. Hum Mol Genet. 2005;14:2167–2180.[PubMed][Google Scholar]
  • 88. Cutler DA, Sullivan T, Marcus-Samuels B, Stewart CL, Reitman MLCharacterization of adiposity and metabolism in Lmna-deficient mice. Biochem Biophys Res Commun. 2002;291:522–527.[PubMed][Google Scholar]
  • 89. Östlund C, Bonne G, Schwartz K, Worman HJProperties of lamin A mutants found in Emery-Dreifuss muscular dystrophy, cardiomyopathy and Dunnigan-type partial lipodystrophy. J Cell Sci. 2001;114:4435–4445.[PubMed][Google Scholar]
  • 90. Raharjo WH, Enarson P, Sullivan T, Stewart CL, Burke BNuclear envelope defects associated with LMNA mutations cause dilated cardiomyopathy and Emery-Dreifuss muscular dystrophy. J Cell Sci. 2001;114:4447–4457.[PubMed][Google Scholar]
  • 91. Muchir A, Medioni J, Laluc M, Massart C, Arimura T, van der Kooi AJ, Desguerre I, Mayer M, Ferrer X, Briault S, Hirano M, Worman HJ, Mallet A, Wehnert M, Schwartz K, Bonne GNuclear envelope alterations in fibroblasts from patients with muscular dystrophy, cardiomyopathy, and partial lipodystrophy carrying lamin A/C gene mutations. Muscle Nerve. 2004;30:444–450.[PubMed][Google Scholar]
  • 92. Wang Y, Herron AJ, Worman HJPathology and nuclear abnormalities in hearts of transgenic mice expressing M371K lamin A encoded by an LMNA mutation causing Emery-Dreifuss muscular dystrophy. Hum Mol Genet. 2006;15:2479–2489.[PubMed][Google Scholar]
  • 93. Vigouroux C, Auclair M, Dubosclard E, Pouchelet M, Capeau J, Courvalin JC, Buendia BNuclear 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.[PubMed][Google Scholar]
  • 94. Favreau C, Dubosclard E, Östlund C, Vigouroux C, Capeau J, Wehnert M, Higuet D, Worman HJ, Courvalin JC, Buendia BExpression of lamin A mutated in the carboxyl-terminal 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.[PubMed][Google Scholar]
  • 95. Bechert K, Lagos-Quintana M, Harborth J, Weber K, Osborn MEffects of expressing lamin A mutant protein causing Emery-Dreifuss muscular dystrophy and familial partial lipodystrophy in HeLa cells. Exp Cell Res. 2003;286:75–86.[PubMed][Google Scholar]
  • 96. Goldman RD, Shumaker DK, Erdos MR, Eriksson M, Goldman AE, Gordon LB, Gruenbaum Y, Khuon S, Mendez M, Varga R, Collins FSAccumulation of mutant lamin A causes progressive changes in nuclear architecture in Hutchinson-Gilford progeria syndrome. Proc Natl Acad Sci U S A. 2004;101:8963–8968.[Google Scholar]
  • 97. Lammerding J, Schulze PC, Takahashi T, Kozlov S, Sullivan T, Kamm RD, Stewart CL, Lee RTLamin A/C deficiency causes defective nuclear mechanics and mechanotransduction. J Clin Invest. 2004;113:370–378.[Google Scholar]
  • 98. Broers JL, Peeters EA, Kuijpers HJ, Endert J, Bouten CV, Oomens CW, Baaijens FP, Ramaekers FCDecreased mechanical stiffness in LMNA-/- cells is caused by defective nucleo-cytoskeletal integrity: implications for the development of laminopathies. Hum Mol Genet. 2004;13:2567–2580.[PubMed][Google Scholar]
  • 99. Favreau C, Higuet D, Courvalin JC, Buendia BExpression of a mutant lamin A that causes Emery-Dreifuss muscular dystrophy inhibits in vitro differentiation of C2C12 myoblasts. Mol Cell Biol. 2004;24:1481–1492.[Google Scholar]
  • 100. Markiewicz E, Ledran M, Hutchison CJRemodelling of the nuclear lamina and nucleoskeleton is required for skeletal muscle differentiation in vitro. J Cell Sci. 2005;118:409–420.[PubMed][Google Scholar]
  • 101. Boguslavsky RL, Stewart CL, Worman HJNuclear lamin A inhibits adipocyte differentiation: implications for Dunnigan-type familial partial lipodystrophy. Hum Mol Genet. 2006;15:653–663.[PubMed][Google Scholar]
  • 102. Capanni C, Mattioli E, Columbaro M, Lucarelli E, Parnaik VK, Novelli G, Wehnert M, Cenni V, Maraldi NM, Squarzoni S, Lattanzi GAltered pre-lamin A processing is a common mechanism leading to lipodystrophy. Hum Mol Genet. 2005;14:1489–1502.[PubMed][Google Scholar]
  • 103. Schwankhaus JD, Katz DA, Eldridge R, Schlesinger S, McFarland HClinical and pathological features of an autosomal dominant, adult-onset leukodystrophy simulating chronic progressive multiple sclerosis. Arch Neurol. 1994;51:757–766.[PubMed][Google Scholar]
  • 104. Coffeen CM, McKenna CE, Koeppen AH, Plaster NM, Maragakis N, Mihalopoulos J, Schwankhaus JD, Flanigan KM, Gregg RG, Ptacek LJ, Fu YHGenetic localization of an autosomal dominant leukodystrophy mimicking chronic progressive multiple sclerosis to chromosome 5q31. Hum Molec Genet. 2000;9:787–793.[PubMed][Google Scholar]
  • 105. Padiath QS, Saigoh K, Schiffmann R, Asahara H, Yamada T, Koeppen A, Hogan K, Ptacek LJ, Fu YHLamin B1 duplications cause autosomal dominant leukodystrophy. Nat Genet. 2006;38:1114–1123.[PubMed][Google Scholar]
  • 106. Barraquer-Ferre LLipodystrophie progressive: syndrome de Barraquer-Simons. Presse Med. 1935;86:1672–1674.[PubMed][Google Scholar]
  • 107. Hegele RA, Cao H, Liu DM, Costain GA, Charlton-Menys V, Rodger NW, Durrington PNSequencing of the reannotated LMNB2 gene reveals novel mutations in patients with acquired partial lipodystrophy. Am J Hum Genet. 2006;79:383–389.[Google Scholar]
  • 108. Vergnes L, Peterfy M, Bergo MO, Young SG, Reue KLamin B1 is required for mouse development and nuclear integrity. Proc Natl Acad Sci U S A. 2004;101:10428–10433.[Google Scholar]
  • 109. Lammerding J, Fong LG, Ji JY, Reue K, Stewart CL, Young SG, Lee RTLamins A and C but not lamin B1 regulate nuclear mechanics. J Biol Chem. 2006;281:25768–25780.[PubMed][Google Scholar]
  • 110. Boriani G, Gallina M, Merlini L, Bonne G, Toniolo D, Amati S, Biffi M, Martignani C, Frabetti L, Bonvicini M, Rapezzi C, Branzi AClinical relevance of atrial fibrillation/flutter, stroke, pacemaker implant, and heart failure in Emery-Dreifuss muscular dystrophy: a long-term longitudinal study. Stroke. 2003;34:901–908.[PubMed][Google Scholar]
  • 111. Meune C, Van Berlo JH, Anselme F, Bonne G, Pinto YM, Duboc DPrimary prevention of sudden death in patients with lamin A/C gene mutations. N Engl J Med. 2006;354:209–210.[PubMed][Google Scholar]
  • 112. Clements L, Manilal S, Love DR, Morris GEDirect interaction between emerin and lamin A. Biochem Biophys Res Commun. 2000;267:709–714.[PubMed][Google Scholar]
  • 113. Sakaki M, Koike H, Takahashi N, Sasagawa N, Tomioka S, Arahata K, Ishiura SInteraction between emerin and nuclear lamins. J Biochem. 2001;129:321–327.[PubMed][Google Scholar]
  • 114. Fairley EA, Riddell A, Ellis JA, Kendrick-Jones JThe cell cycle dependent mislocalisation of emerin may contribute to the Emery-Dreifuss muscular dystrophy phenotype. J Cell Sci. 2002;115:341–354.[PubMed][Google Scholar]
  • 115. Muchir A, van Engelen BG, Lammens M, Mislow JM, McNally E, Schwartz K, Bonne GNuclear envelope alterations in fibroblasts from LGMD1B patients carrying nonsense Y259X heterozygous or homozygous mutation in lamin A/C gene. Exp Cell Res. 2003;291:352–362.[PubMed][Google Scholar]
  • 116. Muchir A, Massart C, van Engelen BG, Lammens M, Bonne G, Worman HJProteasome-mediated degradation of integral inner nuclear membrane protein emerin in fibroblasts lacking A-type lamins. Biochem Biophys Res Commun. 2006;351:1011–1017.[Google Scholar]
  • 117. Holaska JM, Rais-Bahrami S, Wilson KLLmo7 is an emerin-binding protein that regulates the transcription of emerin and many other muscle-relevant genes. Hum Mol Genet. 2006;15:3459–3472.[PubMed][Google Scholar]
  • 118. Muntoni F, Bonne G, Goldfarb LG, Mercuri E, Piercy RJ, Burke M, Yaou RB, Richard P, Recan D, Shatunov A, Sewry CA, Brown SCDisease severity in dominant Emery Dreifuss is increased by mutations in both emerin and desmin proteins. Brain. 2006;129:1260–1268.[PubMed][Google Scholar]
  • 119. Melcon G, Kozlov S, Cutler DA, Sullivan T, Hernandez L, Zhao P, Mitchell S, Nader G, Bakay M, Rottman JN, Hoffman EP, Stewart CLLoss of emerin at the nuclear envelope disrupts the Rb1/E2F and MyoD pathways during muscle regeneration. Hum Mol Genet. 2006;15:637–651.[PubMed][Google Scholar]
  • 120. Ozawa R, Hayashi YK, Ogawa M, Kurokawa R, Matsumoto H, Noguchi S, Nonaka I, Nishino IEmerin-lacking mice show minimal motor and cardiac dysfunctions with nuclear-associated vacuoles. Am J Pathol. 2006;168:907–917.[Google Scholar]
  • 121. Lammerding J, Hsiao J, Schulze PC, Kozlov S, Stewart CL, Lee RTAbnormal nuclear shape and impaired mechanotransduction in emerin-deficient cells. J Cell Biol. 2005;170:781–791.[Google Scholar]
  • 122. Bakay M, Wang Z, Melcon G, Schiltz L, Xuan J, Zhao P, Sartorelli V, Seo J, Pegoraro E, Angelini C, Shneiderman B, Escolar D, Chen YW, Winokur ST, Pachman LM, Fan C, Mandler R, Nevo Y, Gordon E, Zhu Y, Dong Y, Wang Y, Hoffman EPNuclear envelope dystrophies show a transcriptional fingerprint suggesting disruption of Rb-MyoD pathways in muscle regeneration. Brain. 2006;129:996–1013.[PubMed][Google Scholar]
  • 123. Worman HJ, Evans CD, Blobel GThe lamin B receptor of the nuclear envelope inner membrane: a polytopic protein with eight potential transmembrane domains. J Cell Biol. 1990;111:1535–1542.[Google Scholar]
  • 124. Ye Q, Worman HJPrimary structure analysis and lamin B and DNA binding of human LBR, an integral protein of the nuclear envelope inner membrane. J Biol Chem. 1994;269:11306–113011.[PubMed][Google Scholar]
  • 125. Worman HJ, Yuan J, Blobel G, Georgatos SDA lamin B receptor in the nuclear envelope. Proc Natl Acad Sci U S A. 1988;85:8531–8534.[Google Scholar]
  • 126. Ye Q, Worman HJInteraction 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.[PubMed][Google Scholar]
  • 127. Holmer L, Pezhman A, Worman HJThe human lamin B receptor/sterol reductase multigene family. Genomics. 1998;54:469–476.[PubMed][Google Scholar]
  • 128. Hoffmann K, Dreger CK, Olins AL, Olins DE, Shultz LD, Lucke B, Karl H, Kaps R, Muller D, Vaya A, Aznar J, Ware RE, Sotelo-Cruz N, Lindner TH, Herrmann H, Reis A, Sperling KMutations in the gene encoding the lamin B receptor produce an altered nuclear morphology in granulocytes (Pelger-Huet anomaly) Nat Genet. 2002;31:410–414.[PubMed][Google Scholar]
  • 129. Waterham HR, Koster J, Mooyer P, Noort GG, Kelley RI, Wilcox WR, Wanders RJ, Hennekam RC, Oosterwijk JCAutosomal recessive HEM/Greenberg skeletal dysplasia is caused by 3 beta-hydroxysterol delta 14-reductase deficiency due to mutations in the lamin B receptor gene. Am J Hum Genet. 2003;72:1013–1017.[Google Scholar]
  • 130. Shultz LD, Lyons BL, Burzenski LM, Gott B, Samuels R, Schweitzer PA, Dreger C, Herrmann H, Kalscheuer V, Olins AL, Olins DE, Sperling K, Hoffmann KMutations at the mouse ichthyosis locus are within the lamin B receptor gene: a single gene model for human Pelger-Huet anomaly. Hum Mol Genet. 2003;12:61–69.[PubMed][Google Scholar]
  • 131. Lin F, Blake DL, Callebaut I, Skerjanc IS, Holmer L, McBurney MW, Paulin-Levasseur M, Worman HJMAN1, an inner nuclear membrane protein that shares the LEM domain with lamina-associated polypeptide 2 and emerin. J Biol Chem. 2000;275:4840–4847.[PubMed][Google Scholar]
  • 132. Mansharamani M, Wilson KLDirect binding of nuclear membrane protein MAN1 to emerin in vitro and two modes of binding to barrier-to-autointegration factor. J Biol Chem. 2005;280:13863–13870.[PubMed][Google Scholar]
  • 133. Osada S, Ohmori SY, Taira MXMAN1, an inner nuclear membrane protein, antagonizes BMP signaling by interacting with Smad1 in Xenopus embryos. Development. 2003;130:1783–1794.[PubMed][Google Scholar]
  • 134. Raju GP, Dimova N, Klein PS, Huang HCSANE, a novel LEM domain protein, regulates bone morphogenetic protein signaling through interaction with Smad1. J Biol Chem. 2003;278:428–437.[PubMed][Google Scholar]
  • 135. Hellemans J, Preobrazhenska O, Willaert A, Debeer P, Verdonk PC, Costa T, Janssens K, Menten B, Van Roy N, Vermeulen SJ, Savarirayan R, Van Hul W, Vanhoenacker F, Huylebroeck D, De Paepe A, Naeyaert JM, Vandesompele J, Speleman F, Verschueren K, Coucke PJ, Mortier GRLoss-of-function mutations in LEMD3 result in osteopoikilosis, Buschke-Ollendorff syndrome and melorheostosis. Nat Genet. 2004;36:1213–1218.[PubMed][Google Scholar]
  • 136. Lin F, Morrison JM, Wu W, Worman HJMAN1, an integral protein of the inner nuclear membrane, binds Smad2 and Smad3 and antagonizes transforming growth factor-beta signaling. Hum Mol Genet. 2005;14:437–445.[PubMed][Google Scholar]
  • 137. Pan D, Estevez-Salmeron LD, Stroschein SL, Zhu X, He J, Zhou S, Luo KThe integral inner nuclear membrane protein MAN1 physically interacts with the R-Smad proteins to repress signaling by the transforming growth factor-{beta} superfamily of cytokines. J Biol Chem. 2005;280:15992–16001.[PubMed][Google Scholar]
  • 138. Hellemans J, Debeer P, Wright M, Janecke A, Kjaer KW, Verdonk PC, Savarirayan R, Basel L, Moss C, Roth J, David A, De Paepe A, Coucke PGermline LEMD3 mutations are rare in sporadic patients with isolated melorheostosis. Hum Mutat. 2006;27:290.[PubMed][Google Scholar]
  • 139. Mumm S, Wenkert D, Zhang X, McAlister WH, Mier RJ, Whyte MPDeactivating germline mutations in LEMD3 cause osteopoikilosis and Buschke-Ollendorff syndrome, but not sporadic melorheostosis. J Bone Miner Res. 2007;22:243–250.[PubMed][Google Scholar]
  • 140. Caputo S, Couprie J, Duband-Goulet I, Konde E, Lin F, Braud S, Gondry M, Gilquin B, Worman HJ, Zinn-Justin SThe carboxyl-terminal nucleoplasmic region of MAN1 exhibits a DNA binding winged helix domain. J Biol Chem. 2006;281:18208–18215.[PubMed][Google Scholar]
  • 141. Ishimura A, Ng JK, Taira M, Young SG, Osada SMan1, an inner nuclear membrane protein, regulates vascular remodeling by modulating transforming growth factor beta signaling. Development. 2006;133:3919–3928.[PubMed][Google Scholar]
  • 142. Taylor MR, Slavov D, Gajewski A, Vlcek S, Ku L, Fain PR, Carniel E, Di Lenarda A, Sinagra G, Boucek MM, Cavanaugh J, Graw SL, Ruegg P, Feiger J, Zhu X, Ferguson DA, Bristow MR, Gotzmann J, Foisner R, Mestroni LFamilial Cardiomyopathy Registry Research Group, Thymopoietin (lamina-associated polypeptide 2) gene mutation associated with dilated cardiomyopathy. Hum Mutat. 2005;26:566–574.[PubMed][Google Scholar]
  • 143. Gros-Louis F, Dupre N, Dion P, Fox MA, Laurent S, Verreault S, Sanes JR, Bouchard JP, Rouleau GAMutations in SYNE1 lead to a newly discovered form of autosomal recessive cerebellar ataxia. Nat Genet. 2007;39:80–85.[PubMed][Google Scholar]
  • 144. Worman HJ, Gundersen GGHere come the SUNs: a nucleocytoskeletal missing link. Trends Cell Biol. 2006;16:67–69.[PubMed][Google Scholar]
  • 145. Cronshaw JM, Matunis MJThe nuclear pore complex protein ALADIN is mislocalized in triple A syndrome. Proc Natl Acad Sci U S A. 2003;100:5823–5827.[Google Scholar]
  • 146. Ozelius LJ, Hewett JW, Page CE, Bressman SB, Kramer PL, Shalish C, de Leon D, Brin MF, Raymond D, Corey DP, Fahn S, Risch NJ, Buckler AJ, Gusella JF, Breakefield XOThe early-onset torsion dystonia gene (DYT1) encodes an ATP-binding protein. Nat Genet. 1997;17:40–48.[PubMed][Google Scholar]
  • 147. Goodchild RE, Dauer WTMislocalization to the nuclear envelope: an effect of the dystonia-causing torsinA mutation. Proc Natl Acad Sci U S A. 2004;101:847–852.[Google Scholar]
  • 148. Naismith TV, Heuser JE, Breakefield XO, Hanson PITorsinA in the nuclear envelope. Proc Natl Acad Sci U S A. 2004;101:7612–7617.[Google Scholar]
  • 149. Gonzalez-Alegre P, Paulson HLAberrant cellular behavior of mutant torsinA implicates nuclear envelope dysfunction in DYT1 dystonia. J Neurosci. 2004;24:2593–2601.[Google Scholar]
  • 150. Goodchild RE, Dauer WTThe AAA+ protein torsinA interacts with a conserved domain present in LAP1 and a novel ER protein. J Cell Biol. 2005;168:855–862.[Google Scholar]
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