Browse > Article
http://dx.doi.org/10.5483/BMBRep.2018.51.7.113

Laminopathies; Mutations on single gene and various human genetic diseases  

Kang, So-mi (Department of Molecular Biology, College of Natural Science, Pusan National University)
Yoon, Min-Ho (Department of Molecular Biology, College of Natural Science, Pusan National University)
Park, Bum-Joon (Department of Molecular Biology, College of Natural Science, Pusan National University)
Publication Information
BMB Reports / v.51, no.7, 2018 , pp. 327-337 More about this Journal
Abstract
Lamin A and its alternative splicing product Lamin C are the key intermediate filaments (IFs) of the inner nuclear membrane intermediate filament. Lamin A/C forms the inner nuclear mesh with Lamin B and works as a frame with a nuclear shape. In addition to supporting the function of nucleus, nuclear lamins perform important roles such as holding the nuclear pore complex and chromatin. However, mutations on the Lamin A or Lamin B related proteins induce various types of human genetic disorders and diseases including premature aging syndromes, muscular dystrophy, lipodystrophy and neuropathy. In this review, we briefly overview the relevance of genetic mutations of Lamin A, human disorders and laminopathies. We also discuss a mouse model for genetic diseases. Finally, we describe the current treatment for laminopathies.
Keywords
EDMD; HGPS; Lamin A; Laminopathy; Nuclear membrane;
Citations & Related Records
연도 인용수 순위
  • Reference
1 Pilat U, Dechat T, Bertrand AT et al (2013) The muscle dystrophy-causing ${\Delta}K32$ lamin A/C mutant does not impair the functions of the nucleoplasmic lamin $A/C-LAP2{\alpha}$ complex in mice. J Cell Sci 126, 1753-1762   DOI
2 Odgren PR, Pratt CH, Mackay CA et al (2010) Disheveled hair and ear (Dhe), a spontaneous mouse Lmna mutation modeling human laminopathies. PLoS One 5, e9959   DOI
3 Heng MY, Lin ST, Verret L et al (2013) Lamin B1 mediates cell-autonomous neuropathology in a leukodystrophy mouse model. J Clin Invest 123, 2719-2729   DOI
4 Mounkes LC, Kozlov SV, Rottman JN and Stewart CL (2005) Expression of an LMNA-N195K variant of A-type lamins results in cardiac conduction defects and death in mice. Hum Mol Genet 14, 2167-2180   DOI
5 Arimura T, Helbling-Leclerc A, Massart C et al (2005) Mouse model carrying H222P-Lmna mutation develops muscular dystrophy and dilated cardiomyopathy similar to human striated muscle laminopathies. Hum Mol Genet 14, 155-169   DOI
6 Dechat T, Shimi T, Adam SA et al (2007) Alterations in mitosis and cell cycle progression caused by a mutant lamin A known to accelerate human aging. Proc Natl Acad Sci U S A 104, 4955-4960   DOI
7 Lee SJ, Jung YS, Yoon MH et al (2016) Interruption of progerin-lamin A/C binding ameliorates Hutchinson-Gilford progeria syndrome phenotype. J Clin Invest 126, 3879-3893   DOI
8 Smigiel R, Jakubial A, Esteves-Vieira V et al (2010) Novel frameshifting mutations of the ZMPSTE24 gene in two siblings affected with restrictive dermopathy and review of the mutations described in the literature. Am J Med Genet 152A, 447-452   DOI
9 Yu CE, Oshima J, Fu YH et al (1996) Positional cloning of the Werner’s syndrome gene. Science 272, 258-262   DOI
10 Mok Q, Curley R, Tolmie J and Marsden R (1990) Restrictive dermopathy: a report of three cases. J Met Genet 27, 315-319   DOI
11 Hisama FM, Lessel D, Leistritz D et al (2011) Coronary artery disease in a Werner syndrome-like form of progeria characterized by low levels of progerin, a splice variant of lamin A. Am J Med Genet 155A, 3002-3006
12 Hisama FM, Kubisch C, Martin GM and Oshima J (2012) Clinical utility gene card for: Werner syndrome. Eur J Hum Genet 20, 1-3
13 Goto M, Horiuchi Y, Tanimoto K, Ishii T and Nakashima H (1978) Werner’s syndrome: analysis of 15 cases with a review of the Japanese literature. J Am Geriatr Soc 26, 341-347   DOI
14 Padiath QS, Saigoh K, Schiffmann R et al (2006) Lamin B1 duplications cause autosomal dominant leukodystrophy. Nat Genet 38, 1114-1123   DOI
15 Sullivan T, Escalante-Alcalde D, Bhatt H et al (1999) Loss of A-type lamin expression compromise nuclear envelope integrity leading to muscular dystrophy. J Cell Biol 147, 913-920   DOI
16 Garg A, Subramanyam L, Agarwal AK et al (2009) Atypical progeroid syndrome due to heterozygous missense LMNA mutations. J Clin Endocrinol Metab 94, 4971-1983   DOI
17 Shackleton S, Lloyd DJ, Jackson SN et al (2000) LMNA, encoding lamin A/C, is mutated in partial lipodystrophy. Nat Genet 24, 153-156   DOI
18 Schuster J, Sundblom J, Thuresson AC et al (2011) Genomic duplications mediate overexpression of lamin B1 in adult-onset autosomal dominant leukodystrophy with autonomic symptoms. Neurogenetics 12, 65-72   DOI
19 Eriksson M, Brown WT, Gordon LB et al (2003) Recurrent de novo point mutations in lamin A cause Hutchinson-Gilford progeria syndrome. Nature 423, 293-298   DOI
20 Capell B, Erdos M, Medigan J and Fiordalisi J (2005) Inhibiting farnesylation of progerin prevents the characteristic nuclear blebbing of Hutchinson-Gilford progeria syndrome. Pro Natl Acad Sci U S A 102, 12879-12884   DOI
21 Rodriguez JI, Perez-Alonso P, Funes R and Perez-Rodriguez J (1999) Lethal neonatal Hutchinson-Gilford progeria syndrome. Am J Med Genet 82, 242-248   DOI
22 Gillar PJ, Kaye CI and McCourt JW (1991) Progressive early dermatologic changes in Hutchinson-Gilford progeria syndrome. Pediatr Dermatol 8, 199-206   DOI
23 Chen L, Lee L, Kudlow BA et al (2003) LMNA mutations in atypical Werner’s syndrome. Lancet 362, 440-445   DOI
24 Merideth MA, Gordon LB, Clauss S et al (2008) Phenotype and course of Hutchinson-Gilford progeria syndrome. N Engl J Med 358, 592-604   DOI
25 Salamat M, Dhar PK, Neagu DL and Lyon JB (2010) Aortic calcification in a patient with Hutchinson-Gilford progeria syndrome. Pediatr Cardiol 31, 925-926   DOI
26 Scaffidi P (2006) Lamin A-dependent nuclear defects in human aging. Science 312, 1059-1063   DOI
27 Fong L, Frost D, Meta M, Qiao X and Yang S (2006) A protein farnesyltransferase inhibitor ameliorates disease in a mouse model of progeria. Science 311, 1621-1623   DOI
28 Gordon LB, Kleinman ME, Miller DT et al (2012) Clinical trial of a farnesyltransferase inhibitor in children with Hutchinson-Gilford progeria syndrome. Proc Natl Acad Sci USA 109, 16666-16671   DOI
29 Verstraeten VL, Peckham LA, Olive M et al (2011) Protein farnesylation inhibitors cause donut-shaped cell nuclei attributable to a centrosome separation defect. Proc Natl Acad Sci U S A 108, 4997-5002   DOI
30 Osorio FG, Navarro CL, Cadinanos J et al (2011) Splicing-directed therapy in a new mouse model of human accelerated aging. Sci Transl Med 3, 106ra107
31 McKenna T, Baek JH and Eriksson M (2013) Laminopathies. Genetic Disorders chapter 2, 28-64
32 Cronshaw JM, Kruchinsky AN, Zhang W, Chait BT and Matunis MJ (2002) Proteomic analysis of the mammalian nuclear pore complex. J Cell Biol 158, 915-927   DOI
33 Bonne G, Mercuri E, Muchir A et al (2000) Clinical and molecular genetic spectrum of autosomal dominant Emery-Dreifuss muscular dystrophy due to mutations of the lamin A/C gene. Ann Neurol 48, 170-180   DOI
34 Gordon LB, Kleinman ME, Massaro J et al (2016) Clinical trial of the protein farnesylation inhibitors Lonafarnib, Pravastatin, and Zoledronic Acid in children with Hutchinson-Gilford progeria syndrome. Circulation 134, 114-125   DOI
35 Aebi U, Cohn J, Buhle L and Gerace L (1986) The nuclear lamina is a meshwork of intermediate-type filaments. Nature 323, 560-564   DOI
36 Choi JC, Muchir A, Wu W and Iwata S (2012) Temsirolimus activates autophagy and ameliorates cardiomyopathy caused by lamin A/C mutation. Sci Transl Med 4, 144ra102   DOI
37 Kieran MW, Gordon L and Kleinman M (2007) New approaches to progeria. Pediatrics 120, 834-841   DOI
38 Ramos FJ, Chen SC, Garelick MG et al (2012) Rapamycin reverses elevated mTORC1 signaling in lamin A/C-deficient mice, rescue cardiac and skeletal muscle function, and extends survival. Sci Transl Med 4, 144ra103   DOI
39 Emery AE and Dreifuss FE (1966) Unusual type of benign x-linked muscular dystrophy. J Neurol Neurosurg Psychiatry 29, 338-342   DOI
40 Muchir A and Worman HJ (2007) Emery-Dreifuss muscular dystrophy. Curr Neurol Neurosci Rep 7, 78-83   DOI
41 Helbling-Leclerc A, Bonne G and Schwartz K (2002) Emery-Dreifuss muscular dystrophy. Eur J Hum Genet 10, 157-161   DOI
42 Stewart CL, Kozlov S, Fong LG and Young SG (2007) Mouse models of the laminopathies. Exp Cell Res 313, 2144-2156   DOI
43 Canki-Klain N, Recan D, Milicic D et al (2000) Clinical variability and molecular diagnosis in a four-generation family with X-linked Emery-Dreifuss muscular dystrophy. Croat Med J 41, 389-395
44 Fatkin D, MacRae C, Sasaki T et al (1999) 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 341, 1715-1724   DOI
45 Fisher D, Chaudhary N (1986) cDNA sequencing of nuclear lamins A and C reveals primary and secondary structural homology to intermediate filament proteins. Proc Ntl Acad Sci U S A 83, 6450-6454   DOI
46 Muchir A, Bonne G, van der Kooi AJ et al (2000) Identification of mutations in the gene encoding lamins A/C in autosomal dominant limb girdle muscular dystrophy with atrioventricular conduction disturbances. Hum Mol Genet 9, 1453-1459   DOI
47 Yuan WL, Huang CY, Wang JF et al (2009) R25G mutation in exon 1 of LMNA gene is associated with dilated cardiomyopathy and limb-girdle muscular dystrophy 1B. Chin Med J 122, 2840-2845
48 McPherson E, Turner L, Zador I, Reynolds K, Macgregor D and Giampietro PF (2009) Ovarian failure and dilated cardiomyopathy due to a novel lamin mutation. Am J Med Genet 149A, 567-572   DOI
49 Lin F, Worman HJ (1993) Structural organization of the human gene encoding nuclear lamin A and nuclear lamin C. J Biol Chem 268, 16321-16326
50 Barrowman J, Hamblet C, Geoge CM and Michaelis S (2008) Analysis of prelamin A biogenesis reveals the nucleus to be a CaaX processing compartment. Mol Biol Cell 19, 5398-5408   DOI
51 Barrowman J, Hamblet C, Kane MS and Michaelis S (2012) Requirements for efficient proteolytic cleavage of prelamin A by ZMPSTE24. PLoS One 7, e32120   DOI
52 Landires I, Pascale JM and Motta J (2007) The position of the mutation within the LMNA gene determines the type and extent of tissue involvement in laminopathies. Clin Genet 71, 592-593   DOI
53 Broers JLV, Ramaekers FCS, Bonne G, Yaou RB and Hutchison CJ (2006) Nuclear lamins: laminopathies and their role in premature ageing. Physiol Rev 86, 967-1008   DOI
54 Kitten GT and Nigg EA (1991) The CaaX motif is required for isoprenylation, carboxyl methylation, and nuclear membrane association of lamin B2. J Cell Biol 113, 13-23   DOI
55 Coffinier C, Jung HJ, Li Z et al (2010) Direct synthesis of lamin A, bypassing prelamin a processing, causes misshapen nuclei in fibroblasts but no detectable pathology in mice. J Biol Chem 285, 20818-20826   DOI
56 Ben Yaou R, Muchir A, Arimura T et al (2005) Genetics of laminopathies. Novartis Found Symp 264, 81-90
57 Hollstein M, Sidransky D, Vogelstein B and Harris CC (1991) p53 mutations in human cancers. Science 253, 49-53   DOI
58 Zastrow MS, Vlcek S and Wilson KL (2004) Proteins that bind A-type lamins: integrating isolated clues. J Cell Sci 117, 979-987   DOI
59 Salpingidou G, Smertenko A, Hausmanowa-Petrucewicz I, Hussey PJ and Hutchison CJ (2007) A novel role for the nuclear membrane protein emerin in association of the centrosome to the outer nuclear membrane. J Cell Biol 178, 897-904   DOI
60 Chang W, Folker ES, Worman HJ and Gundersen GG (2013) Emerin organizes actin flow for nuclear movement and centrosome orientation in migrating fibroblasts. Mol Biol Cell 24, 3869-3880   DOI
61 Constantinescu D, Gray HL, Sammak PJ, Schatten GP and Csoka AB (2006) Lamin A/C expression is a marker of mouse and human embryonic stem cell differentiation. Stem Cells 24, 177-185   DOI
62 Rober RA, Weber K and Osborn M (1989) Differential timing of nuclear lamin A/C expression in the various organs of the mouse embryo and the young animal: a developmental study. Development 105, 365-378
63 Wang Y, Herron AJ and Worman HJ (2006) Pathology 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 15, 2479-2489   DOI
64 Briand N and Collas P (2018) Laminopathy-causing lamin A mutations reconfigure lamina-associated domains and local spatial chromatin conformation. Nucleus 9, 216-226   DOI
65 Chojnowski A, Ong PF and Dreesen O (2015) Nuclear lamina remodeling and its implications for human disease. Cell Tissue Res 360, 621-631   DOI
66 Gruenbaum Y and Foisner R (2015) Lamins: Nuclear intermediate filament proteins with fundamental functions in nuclear mechanics and genome regulation. Annu Rev Biochem 84, 131-164   DOI
67 Clements L, Manilal S, Love DR and Morris GE (2000) Direct interaction between emerin and lamin A. Biochem Biophys Res Commun 267, 709-714   DOI
68 Worman HJ (2012) Nuclear lamins and laminopathies. J Pathol 226, 316-325   DOI
69 Wojtanik KM, Edgemon K, Viswanadha S et al (2009) The role of LMNA in adipose: a novel mouse model of lipodystrophy based on the Dunnigan-type familial partial lipodystrophy mutation. J Lipid Res 50, 1068-1079   DOI
70 Mounkes LC, Kozlov S, Hernandez L, Sullivan T and Stewart CL (2003) A progeroid syndrome in mice is caused by defects in A-type lamins. Nature 423, 298-301   DOI
71 Varga R, Eriksson M, Erdos MR et al (2006) Progressive vascular smooth muscle cell defects in a mouse model of Hutchinson-Gilford progeria syndrome. Proc Natl Acad Sci U S A 103, 3250-3255   DOI
72 Kubben N, Voncken JW, Konings G et al (2011) Post-natal myogenic and adipogenic developmental: defects and metabolic impairment upon loss of A-type lamins. Nucleus 2, 195-207   DOI
73 Osorio FG, Navarro CL, Cadinanos J et al (2011) Splicing-directed therapy in a new mouse model of human accelerated aging. Sci Transl Med 3, 106ra107
74 Vergnes L, Peterfy M, Bergo MO, Young SG and Reue K (2004) Lamin B1 is required for mouse development and nuclear integrity. Proc Natl Acad Sci U S A 101, 10428-10433   DOI
75 Ambrosi P, Mouly-Bandini A, Attarian S and Habib G (2009) Heart transplantation in 7 patients form a single family with limb-girdle muscular dystrophy caused by lamin A/C mutation. Int J Cardiol 137, e75-76   DOI
76 Dyck JD, David TE, Burke B, Webb GD, Henderson MA and Fowler RS (1987) Management of coronary artery disease in Hutchinson-Gilford syndrome. J Pediatr 111, 407-410   DOI
77 Pendas AM, Zhou Z, Candinanos J et al (2002) Defective prelamin A processing and muscular and adipocyte alterations in Zmpste24 metalloproteinase-deficient mice. Nat Genet 31, 94-99   DOI
78 Fong LG, Ng JK, Lammerding J et al (2006) Prelamin A and lamin A appear to be dispensable in the nuclear lamina. J Clin Invest 116, 743-752   DOI
79 Melcon G, Kozlov S, Cutler DA et al (2006) Loss of emerin at the nuclear envelope disrupts the Rb1/E2F and Myo D pathways during muscle regeneration. Hum Mol Genet 15, 637-651   DOI
80 Ozawa R, Hayashi YK, Ogawa M et al (2006) Emerin-lacking mice show minimal motor and cardiac dysfunctions with nuclear-associated vacuoles. Am J Pathol 168, 907-917   DOI