Nuclear lamins and laminopathies

Journal of Pathology

Volumn 226, Issue 2, 2012, Pages 316-325

  Worman, Howard J ^a  

^a Columbia University ^*  (United States)

Author keywords

cardiomyopathy; lamin; laminopathy; nuclear envelope; progeria

Indexed keywords

BISPHOSPHONIC ACID DERIVATIVE; EMERIN; HYDROXYMETHYLGLUTARYL COENZYME A REDUCTASE INHIBITOR; LAMIN; LAMIN A; LAMIN B; LAMIN C; PROTEIN FARNESYLTRANSFERASE INHIBITOR; RAPAMYCIN; WNT PROTEIN;

CELL NUCLEUS MEMBRANE; CLINICAL TRIAL (TOPIC); CONGESTIVE CARDIOMYOPATHY; EMERY DREIFUSS MUSCULAR DYSTROPHY; GENE MUTATION; GENETIC DISORDER; HUMAN; LAMINOPATHY; LIMB GIRDLE MUSCULAR DYSTROPHY; NONHUMAN; PATHOPHYSIOLOGY; PRIORITY JOURNAL; PROGERIA; REVIEW; SIGNAL TRANSDUCTION;

ANIMALS; CARDIOMYOPATHIES; DISEASE MODELS, ANIMAL; GENE THERAPY; HUMANS; LAMINS; METABOLIC DISEASES; MICE; MUTATION; NUCLEAR LAMINA; PHENOTYPE; PROGERIA;

EID: 82755161872     PISSN: 00223417     EISSN: 10969896     Source Type: Journal    
DOI: 10.1002/path.2999     Document Type: Review

References (108)

1. Melcer S, Gruenbaum Y, Krohne G,. Invertebrate lamins. Exp Cell Res 2007; 313: 2157-2166. (Pubitemid 46844822)
2. Hutchison CJ, Worman HJ,. A-type lamins: guardians of the soma? Nat Cell Biol 2004; 6: 1062-1067. (Pubitemid 39468007)
3. Frangioni J, Neel, B,. Use of a general purpose mammalian expression vector for studying intracellular protein targeting: identification of critical residues in the nuclear lamin A/C nuclear localisation sequence. J Cell Sci 1993; 105: 481-488. (Pubitemid 23234166)
4. Dhe-Paganon S, Werner ED, Chi YI, et al., Structure of the globular tail of nuclear lamin. J Biol Chem 2002; 277: 17381-17384. (Pubitemid 34967536)
5. Krimm I, Östlund C, Gilquin B, et al., The Ig-like structure of the C-terminal domain of lamin A/C, mutated in muscular dystrophies, cardiomyopathy, and partial lipodystrophy. Structure 2002; 10: 811-823. (Pubitemid 34628710)
6. Rusiñol AE, Sinensky MS,. Farnesylated lamins, progeroid syndromes and farnesyl transferase inhibitors. J Cell Sci 2006; 119: 3265-3272. (Pubitemid 44405212)
7. Nigg EA,. Assembly and cell cycle dynamics of the nuclear lamina. Semin Cell Biol 1992; 3: 245-253.
8. Lin F, Worman HJ,. Structural organization of the human gene (LMNB1) encoding nuclear lamin B1. Genomics 1995; 27: 230-236.
9. Biamonti G, Giacca M, Perini G, et al., The 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.
10. Furukawa K, Hotta Y,. cDNA 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. (Pubitemid 23042386)
11. 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. (Pubitemid 23229934)
12. Stewart C, Burke B,. Teratocarcinoma stem cells and early mouse embryos contain only a single major lamin polypeptide closely resembling lamin B. Cell 1987; 51: 383-392.
13. Guilly MN, Bensussan A, Bourge JF, et al., A human T lymphoblastic cell line lacks lamins A and C. EMBO J 1987; 6: 3795-3799.
14. 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.
15. Röber RA, Weber K, Osborn M,. Differential timing of nuclear lamin A/C expression in the various organs of the mouse embryo and the young animal: a developmental study. Development 1989; 105: 365-378. (Pubitemid 19053283)
16. Furukawa K, Inagaki H, Hotta Y,. Identification and cloning of an mRNA coding for a germ cell-specific A-type lamin in mice. Exp Cell Res 1994; 212: 426-430.
17. Machiels BM, Zorenc AH, Endert JM, et al., An alternative splicing product of the lamin A/C gene lacks exon 10. J Biol Chem 1996; 271: 9249-9253. (Pubitemid 26137326)
18. Fisher DZ, Chaudhary N, Blobel G,. cDNA sequencing of nuclear lamins A and C reveals primary and secondary structural homology to intermediate filament proteins. Proc Natl Acad Sci USA 1986; 83: 6450-6454. (Pubitemid 17174752)
19. McKeon FD, Kirschner MW, Caput D,. Homologies in both primary and secondary structure between nuclear envelope and intermediate filament proteins. Nature 1986; 319: 463-468. (Pubitemid 16212925)
20. Davies BS, Fong LG, Yang SH, et al., The posttranslational processing of prelamin A and disease. Annu Rev Genomics Hum Genet 2009; 10: 153-174.
21. Dechat T, Pfleghaar K, Sengupta K, et al., Nuclear lamins: major factors in the structural organization and function of the nucleus and chromatin. Genes Dev 2008; 22: 832-853. (Pubitemid 351482836)
22. Reddy KL, Zullo JM, Bertolino E, et al., Transcriptional repression mediated by repositioning of genes to the nuclear lamina. Nature 2008; 452: 243-247. (Pubitemid 351380248)
23. Spann TP, Moir RD, Goldman AE, et al., Disruption of nuclear lamin organization alters the distribution of replication factors and inhibits DNA synthesis. J Cell Biol 1997; 136: 1201-1212. (Pubitemid 27421909)
24. Ellis DJ, Jenkins H, Whitfield WG, et al., GST-lamin fusion proteins act as dominant negative mutants in Xenopus egg extract and reveal the function of the lamina in DNA replication. J Cell Sci 1997; 110: 2507-2518. (Pubitemid 27483028)
25. Moir RD, Spann TP, Herrmann H, et al., Disruption of nuclear lamin organization blocks the elongation phase of DNA replication. J Cell Biol 2000; 149: 1179-1192.
26. Tsai MY, Wang S, Heidinger JM, et al., A mitotic lamin B matrix induced by RanGTP required for spindle assembly. Science 2006; 311: 1887-1893.
27. Vergnes L, Péterfy M, Bergo MO, et al., Lamin B1 is required for mouse development and nuclear integrity. Proc Natl Acad Sci USA 2004; 101: 10428-10433. (Pubitemid 38924942)
28. Coffinier C, Chang SY, Nobumori C, et al., Abnormal development of the cerebral cortex and cerebellum in the setting of lamin B2 deficiency. Proc Natl Acad Sci USA 2010; 107: 5076-5081.
29. Yang SH, Chang SY, Yin L, et al., An absence of both lamin B1 and lamin B2 in keratinocytes has no effect on cell proliferation or the development of skin and hair. Hum Mol Genet 2011; 20: 3537-3544.
30. Sullivan T, Escalante-Alcalde D, Bhatt H, et al., Loss of A-type lamin expression compromises nuclear envelope integrity leading to muscular dystrophy. J Cell Biol 1999; 147: 913-920.
31. Bonne G, Di Barletta MR, Varnous S, et al., Mutations in the gene encoding lamin A/C cause autosomal dominant Emery-Dreifuss muscular dystrophy. Nat Genet 1999; 21: 285-288. (Pubitemid 29124935)
32. Muchir A, Worman HJ,. Emery-Dreifuss muscular dystrophy. Curr Neurol Neurosci Rep 2007; 7: 78-83. (Pubitemid 46188779)
33. Fatkin D, MacRae C, Sasaki T, et al., 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; 341: 1715-1724.
34. Muchir A, Bonne G, van der Kooi AJ, et al., Identification 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. (Pubitemid 30312494)
35. Lu JT, Muchir A, Nagy PL, et al., LMNA cardiomyopathy: cell biology and genetics meet clinical medicine. Dis Model Mech 2011; 4: 562-568.
36. Quijano-Roy S, Mbieleu B, Bönnemann CG, et al., De novo LMNA mutations cause a new form of congenital muscular dystrophy. Ann Neurol 2008; 64: 177-186.
37. Renou L, Stora S, Yaou RB, et al., Heart-hand syndrome of Slovenian type: a new kind of laminopathy. J Med Genet 2008; 45: 666-671.
38. Bione S, Maestrini E, Rivella S, et al., Identification of a novel X-linked gene responsible for Emery-Dreifuss muscular dystrophy. Nat Genet 1994; 8: 323-327. (Pubitemid 24375595)
39. Nagano A, Koga R, Ogawa M, et al., Emerin deficiency at the nuclear membrane in patients with Emery-Dreifuss muscular dystrophy. Nat Genet 1996; 12: 254-259. (Pubitemid 26080083)
40. Manilal S, Nguyen TM, Sewry CA, et al., The Emery-Dreifuss muscular dystrophy protein, emerin, is a nuclear membrane protein. Hum Mol Genet 1996; 5: 801-808. (Pubitemid 26171704)
41. Clements L, Manilal S, Love DR, et al., Direct interaction between emerin and lamin A. Biochem Biophys Res Commun 2000; 267: 709-714. (Pubitemid 30099388)
42. Cao H, Hegele RA,. Nuclear lamin A/C R482Q mutation in canadian kindreds with Dunnigan-type familial partial lipodystrophy. Hum Mol Genet 2000; 9: 109-112. (Pubitemid 30145295)
43. Shackleton S, Lloyd DJ, Jackson SN, et al., LMNA, encoding lamin A/C, is mutated in partial lipodystrophy. Nat Genet 2000; 24: 153-156. (Pubitemid 30094715)
44. Speckman RA, Garg A, Du F, et al., Mutational 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. (Pubitemid 30468776)
45. Vigouroux C, Magré J, Vantyghem MC, et al., Lamin A/C gene: sex-determined expression of mutations in Dunnigan-type familial partial lipodystrophy and absence of coding mutations in congenital and acquired generalized lipoatrophy. Diabetes 2000; 49: 1958-1962.
46. Lüdtke A, Genschel J, Brabant G, et al., Hepatic steatosis in Dunnigan-type familial partial lipodystrophy. Am J Gastroenterol 2005; 100: 2218-2224.
47. Novelli G, Muchir A, Sangiuolo F, et al., Mandibuloacral dysplasia is caused by a mutation in LMNA-encoding lamin A/C. Am J Hum Genet 2002; 71: 426-431. (Pubitemid 34800259)
48. Caux F, Dubosclard E, Lascols O, et al., A 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 Endocrinol Metab 2003; 88: 1006-1013. (Pubitemid 36337748)
49. Decaudain A, Vantyghem MC, Guerci B, et al., New metabolic phenotypes in laminopathies: LMNA mutations in patients with severe metabolic syndrome. J Clin Endocrinol Metab 2007; 92: 4835-4844. (Pubitemid 350223467)
50. Dutour A, Roll P, Gaborit B, et al., High prevalence of laminopathies among patients with metabolic syndrome. Hum Mol Genet 2011; 20: 3779-3786.
51. De Sandre-Giovannoli A, Chaouch M, Kozlov S, et al., 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. (Pubitemid 34177926)
52. Tazir M, Azzedine H, Assami S, et al., Phenotypic variability in autosomal recessive axonal Charcot-Marie-Tooth disease due to the R298C mutation in lamin A/C. Brain 2004; 127: 154-163. (Pubitemid 38055354)
53. Walter MC, Witt TN, Weigel BS, et al., Deletion of the LMNA initiator codon leading to a neurogenic variant of autosomal dominant Emery-Dreifuss muscular dystrophy. Neuromuscul Disord 2005; 15: 40-44. (Pubitemid 41556631)
54. Agarwal AK, Kazachkova I, Ten S, et al., Severe mandibuloacral dysplasia-associated lipodystrophy and progeria in a young girl with a novel homozygous Arg527Cys LMNA mutation. J Clin Endocrinol Metab 2008; 93: 4617-4623.
55. Merideth MA, Gordon LB, Clauss S, et al., Phenotype and course of Hutchinson-Gilford progeria syndrome. N Engl J Med 2008; 358: 592-604. (Pubitemid 351214286)
56. Eriksson M, Brown WT, Gordon LB, et al., Recurrent de novo point mutations in lamin A cause Hutchinson-Gilford progeria syndrome. Nature 2003; 423: 293-298. (Pubitemid 40852699)
57. De Sandre-Giovannoli A, Bernard R, Cau P, et al., Lamin A truncation in Hutchinson-Gilford progeria. Science 2003; 300: 2055. (Pubitemid 36760124)
58. Navarro CL, Cadiñanos J, De Sandre-Giovannoli A, et al., Loss of ZMPSTE24 (FACE-1) causes autosomal recessive restrictive dermopathy and accumulation of lamin A precursors. Hum Mol Genet 2005; 14: 1503-1513. (Pubitemid 40823459)
59. Moulson CL, Go G, Gardner JM, et al., Homozygous and compound heterozygous mutations in ZMPSTE24 cause the laminopathy restrictive dermopathy. J Invest Dermatol 2005; 125: 913-919.
60. Chen L, Lee L, Kudlow BA, et al., LMNA mutations in atypical Werner's syndrome. Lancet 2003; 362: 440-445. (Pubitemid 36999707)
61. Verstraeten VL, Broers JL, van Steensel MA, et al., Compound heterozygosity for mutations in LMNA causes a progeria syndrome without prelamin A accumulation. Hum Mol Genet 2006; 15: 2509-2522. (Pubitemid 44288703)
62. Garg A, Subramanyam L, Agarwal AK, et al., Atypical progeroid syndrome due to heterozygous missense LMNA mutations. J Clin Endocrinol Metab 2009; 94: 4971-4983.
63. Padiath QS, Saigoh K, Schiffmann R, et al., Lamin B1 duplications cause autosomal dominant leukodystrophy. Nat Genet 2006; 38: 1114-1123. (Pubitemid 44470356)
64. Hegele RA, Cao H, Liu DM, et al., Sequencing of the reannotated LMNB2 gene reveals novel mutations in patients with acquired partial lipodystrophy. Am J Hum Genet 2006; 79: 383-389. (Pubitemid 44141838)
65. Dauer WT, Worman HJ,. The nuclear envelope as a signaling node in development and disease. Dev Cell 2009; 17: 626-638.
66. Worman HJ, Östlund C, Wang Y,. Diseases of the nuclear envelope. Cold Spring Harb Perspect Biol 2010; 2: a000760.
67. Young SG, Fong, LG, Michaelis S,. Prelamin 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. (Pubitemid 43107466)
68. Worman HJ, Bonne G,. 'Laminopathies': a wide spectrum of human diseases. Exp Cell Res 2007; 313: 2121-2133. (Pubitemid 46850729)
69. Worman HJ, Fong LG, Muchir A, et al., Laminopathies and the long strange trip from basic cell biology to therapy. J Clin Invest 2009; 119: 1825-1836.
70. Lammerding J, Schulze PC, Takahashi T, et al., Lamin A/C deficiency causes defective nuclear mechanics and mechanotransduction. J Clin Invest 2004; 113: 370-378. (Pubitemid 38544181)
71. Ji JY, Lee RT, Vergnes L, et al., Cell nuclei spin in the absence of lamin b1. J Biol Chem 2007; 282: 20015-20026. (Pubitemid 47100106)
72. Lee JS, Hale CM, Panorchan P, et al., Nuclear lamin A/C deficiency induces defects in cell mechanics, polarization, and migration. Biophys J 2007; 93: 2542-2552. (Pubitemid 47511153)
73. Verstraeten VL, Ji JY, Cummings KS, et al., Increased mechanosensitivity and nuclear stiffness in Hutchinson-Gilford progeria cells: effects of farnesyltransferase inhibitors. Aging Cell 2008; 7: 383-393. (Pubitemid 351663907)
74. Hale CM, Shrestha AL, Khatau SB, et al., Dysfunctional connections between the nucleus and the actin and microtubule networks in laminopathic models. Biophys J 2008; 95: 5462-5475.
75. Folker ES, Östlund C, Luxton GW, et al., Lamin A variants that cause striated muscle disease are defective in anchoring transmembrane actin-associated nuclear lines for nuclear movement. Proc Natl Acad Sci USA 2011; 108: 131-136.
76. Bergo MO, Gavino B, Ross J, et al., Zmpste24 deficiency in mice causes spontaneous bone fractures, muscle weakness, and a prelamin A processing defect. Proc Natl Acad Sci USA 2002; 99: 13049-13054.
77. Pendás AM, Zhou Z, Cadiñanos J, et al., Defective prelamin A processing and muscular and adipocyte alterations in Zmpste24 metalloproteinase-deficient mice. Nat Genet 2002; 31: 94-99.
78. Fong LG, Ng JK, Meta M, et al., Heterozygosity for Lmna deficiency eliminates the progeria-like phenotypes in Zmpste24-deficient mice. Proc Natl Acad Sci USA 2004; 101: 18111-18116. (Pubitemid 40054082)
79. Fong LG, Frost D, Meta M, et al., A protein farnesyltransferase inhibitor ameliorates disease in a mouse model of progeria. Science 2006; 311: 1621-1623.
80. Varela I, Pereira S, Ugalde AP, et al., Combined treatment with statins and aminobisphosphonates extends longevity in a mouse model of human premature aging. Nat Med 2008; 14: 767-772.
81. Yang SH, Meta M, Qiao X, et al., A farnesyltransferase inhibitor improves disease phenotypes in mice with a Hutchinson-Gilford progeria syndrome mutation. J Clin Invest 2006; 116: 2115-2121. (Pubitemid 44162320)
82. Yang SH, Qiao X, Fong LG, et al., Treatment with a farnesyltransferase inhibitor improves survival in mice with a Hutchinson-Gilford progeria syndrome mutation. Biochim Biophys Acta 2008; 1781: 36-39.
83. Capell BC, Olive M, Erdos MR, et al., A farnesyltransferase inhibitor prevents both the onset and late progression of cardiovascular disease in a progeria mouse model. Proc Natl Acad Sci USA 2008; 105: 15902-15907.
84. Yang SH, Andres DA, Spielmann HP, et al., Progerin elicits disease phenotypes of progeria in mice whether or not it is farnesylated. J Clin Invest 2008; 118: 3291-3300.
85. Yang SH, Chang SY, Ren S, et al., Absence of progeria-like disease phenotypes in knock-in mice expressing a non-farnesylated version of progerin. Hum Mol Genet 2011; 20: 436-444.
86. Yang SH, Bergo MO, Toth JI, et al., Blocking protein farnesyltransferase improves nuclear blebbing in mouse fibroblasts with a targeted Hutchinson-Gilford progeria syndrome mutation. Proc Natl Acad Sci USA 2005; 102: 10291-10296. (Pubitemid 41023365)
87. Toth JI, Yang SH, Qiao X, et al., Blocking protein farnesyltransferase improves nuclear shape in fibroblasts from humans with progeroid syndromes. Proc Natl Acad Sci USA 2005; 102: 12873-12878. (Pubitemid 41279458)
88. Capell BC, Erdos MR, Madigan JP, et al., Inhibiting farnesylation of progerin prevents the characteristic nuclear blebbing of Hutchinson-Gilford progeria syndrome. Proc Natl Acad Sci USA 2005; 102: 12879-12884. (Pubitemid 41282816)
89. Mallampalli MP, Huyer G, Bendale P, et al., Inhibiting farnesylation reverses the nuclear morphology defect in a HeLa cell model for Hutchinson-Gilford progeria syndrome. Proc Natl Acad Sci USA 2005; 102: 14416-14421. (Pubitemid 41429712)
90. Glynn MW, Glover TW,. Incomplete 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. (Pubitemid 41535461)
91. Gordon LB, Harling-Berg CJ, Rothman FG,. Highlights of the 2007 Progeria Research Foundation scientific workshop: progress in translational science. J Gerontol A Biol Sci Med Sci 2008; 63: 777-787.
92. Wang Y, Panteleyev AA, Owens DM, et al., Epidermal expression of the truncated prelamin A causing Hutchinson-Gilford progeria syndrome: effects on keratinocytes, hair and skin. Hum Mol Genet 2008; 17: 2357-2369.
93. Liu B, Wang J, Chan KM, et al., Genomic instability in laminopathy-based premature aging. Nat Med 2005; 11: 780-785. (Pubitemid 41021211)
94. Liu Y, Wang Y, Rusinol AE, et al., Involvement of xeroderma pigmentosum group A (XPA) in progeria arising from defective maturation of prelamin A. FASEB J 2008; 22: 603-611. (Pubitemid 351225596)
95. Constantinescu D, Csoka AB, Navara CS, et al., Defective DSB repair correlates with abnormal nuclear morphology and is improved with FTI treatment in Hutchinson-Gilford progeria syndrome fibroblasts. Exp Cell Res 2010; 316: 2747-2759.
96. Liu GH, Barkho BZ, Ruiz S, et al., Recapitulation of premature ageing with iPSCs from Hutchinson-Gilford progeria syndrome. Nature 2011; 472: 221-225.
97. Kudlow BA, Stanfel MN, Burtner CR, et al., Suppression of proliferative defects associated with processing-defective lamin A mutants by hTERT or inactivation of p53. Mol Biol Cell 2008; 19: 5238-5248.
98. Benson EK, Lee SW, Aaronson SA,. Role of progerin-induced telomere dysfunction in HGPS premature cellular senescence. J Cell Sci 2010; 123: 2605-2612.
99. Cao K, Blair CD, Faddah DA, et al., Progerin and telomere dysfunction collaborate to trigger cellular senescence in normal human fibroblasts. J Clin Invest 2011; 121: 2833-2844.
100. Scaffidi P, Misteli T,. Lamin A-dependent misregulation of adult stem cells associated with accelerated ageing. Nat Cell Biol 2008; 10: 452-459.
101. Hernandez L, Roux KJ, Wong ES, et al., Functional coupling between the extracellular matrix and nuclear lamina by Wnt signaling in progeria. Dev Cell 2010; 19: 413-425.
102. Espada J, Varela I, Flores I, et al., Nuclear envelope defects cause stem cell dysfunction in premature-aging mice. J Cell Biol 2008; 181: 9-13.
103. Cao K, Graziotto JJ, Blair CD, et al., Rapamycin reverses cellular phenotypes and enhances mutant protein clearance in Hutchinson-Gilford progeria syndrome cells. Sci Transl Med 2011; 3: 89ra58.
104. Muchir A, Pavlidis P, Decostre V, et al., Activation of MAPK pathways links LMNA mutations to cardiomyopathy in Emery-Dreifuss muscular dystrophy. J Clin Invest 2007; 117: 1282-1293. (Pubitemid 46718416)
105. Muchir A, Pavlidis P, Bonne G, et al., Activation of MAPK in hearts of EMD null mice: similarities between mouse models of X-linked and autosomal dominant Emery-Dreifuss muscular dystrophy. Hum Mol Genet 2007; 16: 1884-1895. (Pubitemid 47244536)
106. Muchir A, Shan J, Bonne G, et al., Inhibition of extracellular signal-regulated kinase signaling to prevent cardiomyopathy caused by mutation in the gene encoding A-type lamins. Hum Mol Genet 2009; 18: 241-247.
107. Wu W, Shan J, Bonne G, et al., Pharmacological inhibition of c-Jun N-terminal kinase signaling prevents cardiomyopathy caused by mutation in LMNA gene. Biochim Biophys Acta 2010; 1802: 632-638.
108. Wu W, Muchir A, Shan J, et al., Mitogen-activated protein kinase inhibitors improve heart function and prevent fibrosis in cardiomyopathy caused by mutation in lamin A/C gene. Circulation 2011; 123: 53-61.