The LMNA mutation p.Arg321Ter associated with dilated cardiomyopathy leads to reduced expression and a skewed ratio of lamin A and lamin C proteins

Experimental Cell Research

Volumn 319, Issue 19, 2013, Pages 3010-3019

  Al Saaidi, Rasha ^a   Rasmussen, Torsten B ^a   Palmfeldt, Johan ^a   Nissen, Peter H ^a   Beqqali, Abdelaziz ^b   Hansen, Jakob ^c   Pinto, Yigal M ^b   Boesen, Thomas ^c   Mogensen, Jens ^d   Bross, Peter ^a  

^a AARHUS UNIVERSITY HOSPITAL   (Denmark)

^b ACADEMIC MEDICAL CENTER   (Netherlands)

^c AARHUS UNIVERSITY   (Denmark)

^d ODENSE UNIVERSITY HOSPITAL   (Denmark)

Author keywords

Dilated cardiomyopathy; Haploinsufficiency; Laminopathies; LMNA; Nonsense mediated mRNA decay; Premature termination codon mutation

Indexed keywords

LAMIN A; LAMIN C;

ALLELE; ALTERNATIVE RNA SPLICING; ARTICLE; CASE REPORT; CELL STRUCTURE; CODON; CONGESTIVE CARDIOMYOPATHY; CONTROLLED STUDY; FIBROBLAST; GENE EXPRESSION; HUMAN; HUMAN CELL; LIQUID CHROMATOGRAPHY; NONSENSE MUTATION; PRIORITY JOURNAL; TANDEM MASS SPECTROMETRY;

EID: 84886589170     PISSN: 00144827     EISSN: 10902422     Source Type: Journal    
DOI: 10.1016/j.yexcr.2013.08.024     Document Type: Article

References (26)

1. van Berlo J.H., de Voogt W.G., van der Kooi A.J., van Tintelen J.P., Bonne G., Yaou R.B., Duboc D., Rossenbacker T., Heidbuchel H., de Visser M., et al. Meta-analysis of clinical characteristics of 299 carriers of LMNA gene mutations: do lamin A/C mutations portend a high risk of sudden death?. J. Mol. Med. 2005, 83:79-83.
2. van der Kooi A.J., Bonne G., Eymard B., Duboc D., Talim B., Van der Valk M., Reiss P., Richard P., Demay L., Merlini L., Schwartz K., Busch H.F., de Visser M. Lamin a/c mutations with lipodystrophy, cardiac abnormalities, and muscular dystrophy. Neurology 2002, 59:620-623.
3. Fatkin D., MacRae C., Sasaki T., Wolff M.R., Porcu M., Frenneaux M., Atherton J., Vidaillet H.J., Spudich S., De Girolami U., Seidman J.G., 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, 341:1715-1724.
4. Lin F., Worman H.J. Structural organization of the human gene encoding nuclear lamin A and nuclear lamin C. J. Biol. Chem. 1993, 268:16321-16326.
5. Beck L.A., Hosick T.J., Sinensky M. Isoprenylation is required for the processing of the lamin A precursor. J. Cell Biol. 1990, 110:1489-1499.
6. Geiger S.K., Bär H., Ehlermann P., Wälde S., Rutschow D., Zeller R., Ivandic B.T., Zentgraf H., Katus H.A., Herrmann H., Weichenhan D.J. Incomplete nonsense-mediated decay of mutant lamin A/C mRNA provokes dilated cardiomyopathy and ventricular tachycardia. Mol. Med. (Berlin) 2008, 86(3):281-289.
7. Becane H.M., Bonne G., Varnous S., Muchir A., Ortega V., Hammouda E.H., Urtizberea J.A., Lavergne T., Fardeau M., Eymard B., Weber S., Schwartz K., Duboc D. High incidence of sudden death with conduction system and myocardial disease due to lamins A and C gene mutation. Pacing Clin. Electrophysiol. 2000, 23(11 Pt 1):1661-1666.
8. Nagy E., Maquat L.E. A rule for termination-codon position within intron-containing genes: When nonsense affects RNA abundance. Trends Biochem. Sci. 1998, 23:198-199.
9. Muchir A., van Engelen B.G., Lammens M., Mislow J.M., McNally E., Schwartz K., Bonne G. Nuclear 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.
10. Pan H., Richards A.A., Zhu X., Joglar J.A., Yin H.L., Garg V. A novel mutation in LAMIN A/C is associated with isolated early-onset atrial fibrillation and progressive atrioventricular block followed by cardiomyopathy and sudden cardiac death. Heart Rhythm 2009, 6:707-710.
11. den Dunnen J.T., Antonarakis S.E. Nomenclature for the description of human sequence variations. Hum. Genet. 2001, 109:121-124.
12. Rasmussen, Hansen, Nissen, Palmfeldt, Dalager, Jensen, Kim, Heickendorff, Mølgaard, Jensen, Sørensen, Baandrup, Bross and Mogensen, Protein expression studies of desmoplakin mutations in cardiomyopathy patients reveal different molecular disease mechanisms, Clin. Genet. 84 (1) (2012) 20-30,. http://dx.doi.org/10.1111/cge.12056.
13. Cox J., Mann M. MaxQuant enables high peptide identification rates, individualized p.p.b.- range mass accuracies and proteome - wide protein quantification. Nat. Biotechnol. 2008, 26(12):1367.
14. Carter M.S., Doskow J., Morris P., Li S., Nhim R.P., Sandstedt S., Wilkinson M.F. A regulatory mechanism that detects premature nonsense codons in T-cell receptor transcripts in vivo is reversed by protein synthesis inhibitors in vitro. J. Biol. Chem. 1995, 270:28995-29003.
15. 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.
16. Fidzianska A., Bilinska Z.T., Tesson F., Wagner T., Walski M., Grzybowski J. Obliteration of cardiomyocyte nuclear architecture in a patient with LMNA gene mutation. J. Neurol. Sci. 2008, 271:91-96.
17. Reichart B., Klafke R., Dreger C., Kruger E., Motsch I., Ewald A., Schafer J., Reichmann H., Muller C.R., Dabauvalle M.C. Expression and localization of nuclear proteins in autosomal-dominant Emery-Dreifuss muscular dystrophy with LMNA R377H mutation. BMC Cell Biol. 2004, 5:12.
18. Navarro C.L., De Sandre-Giovannoli A., Bernard R., Boccaccio I., Boyer A., et al. Lamin A and ZMPSTE24 (FACE-1) defects cause nuclear disorganization and identify restrictive dermopathy as a lethal neonatal laminopathy. Hum. Mol. Genet. 2004, 13:2493-2503.
19. Motsch I., Kaluarachchi M., Emerson L.J. Lamins A and C are differentially dysfunctional in autosomal dominant Emery-Dreifuss muscular dystrophy. Eur. J. Cell Biol. 2005, 84(9):765-781.
20. Sylvius Nicolas, Hathaway Andrea, Boudreau Emilie Specific contribution of lamin A and lamin C in the development of laminopathies. Exp. Cell Res. 2008, 314(13):2362-2375.
21. Jung H.J., Coffinier C., Choe Y., Beigneux A.P., Davies B.S.J., Yang S.H., Barnes R.H., Hong J., Sun T., Pleasure S.J., Young S.G., Fong L.G. Regulation of prelamin A but not lamin C by miR-9, a brain-specific microRNA. Proc. Natl. Acad. Sci. USA 2012, 109:E423-E431.
22. Reunert J., Wentzell R., Walter M., Jakubiczka S., Zenker M., Brune T., Rust S., Marquardt T. Neonatal progeria: increased ratio of progerin to lamin A leads to progeria of the newborn. Eur. J. Hum. Genet. 2012, 20:933-937.
23. Cattin M.E., Bertrand A.T., Schlossarek S., Le Bihan M.C., Skov Jensen S., Neuber C., Crocini C., Maron S., Lainé J., Mougenot N., Varnous S., Fromes Y., Hansen A., Eschenhagen T., Decostre V., Carrier L., Bonne G. Heterozygous LmnadelK32 mice develop dilated cardiomyopathy through a combined pathomechanism of haploinsufficiency and peptide toxicity. Hum. Mol. Genet. 2013, 22(15):3152-3164.
24. Oh Y.S., Kim D.G., Kim G., Choi E.C., Kennedy B.K., Suh Y., Park B.J., Kim S. Downregulation of lamin A by tumor suppressor AIMP3/p18 leads to a progeroid phenotype in mice. Aging Cell 2010, 9:810-822.
25. Sakaki M., Koike H., Takahashi N., Sasagawa N., Tomioka S., et al. Interaction between emerin and nuclear lamins. J. Biochem. (Tokyo) 2001, 129:321-327.
26. Liang Y., Chiu P.H., Yip K.Y., Chan S.Y. Subcellular localization of SUN2 is regulated by Lamin A and Rab5. PloS One 2011, 6(5):e20507.