Lipodystrophy-linked LMNA p.R482W mutation induces clinical early atherosclerosis and in vitro endothelial dysfunction

Arteriosclerosis, Thrombosis, and Vascular Biology

Volumn 33, Issue 9, 2013, Pages 2162-2171

  Bidault, Guillaume ^a,b,g   Garcia, Marie ^a,b,g   Vantyghem, Marie Christine ^c   Ducluzeau, Pierre Henri ^d   Morichon, Romain ^e   Thiyagarajah, Kayathri ^a,b,g   Moritz, Sylviane ^b,g   Capeau, Jacqueline ^a,b,f,g   Vigouroux, Corinne ^a,b,f,g   Béréziat, Véronique ^a,b,g  

^a SORBONNE UNIVERSITÉ   (France)

^b CENTRE DE RECHERCHE SAINT ANTOINE   (France)

^c LILLE UNIVERSITY HOSPITAL   (France)

^d Centre de Recherche en Nutrition Humaine   (France)

^e Institut de Recherche en Santé   (France)

^f HÔPITAL TENON   (France)

^g IHU ICAN   (France)

Author keywords

arteriosclerosis; endothelial cells; laminin A C; oxidative stress; prelamin A; statins, HMG CoA

Indexed keywords

APOLIPOPROTEIN B; C REACTIVE PROTEIN; HEMOGLOBIN A1C; HIGH DENSITY LIPOPROTEIN CHOLESTEROL; HISTONE H2AX; INTERCELLULAR ADHESION MOLECULE 1; INTERLEUKIN 6; INTERLEUKIN 8; LAMIN A; LOW DENSITY LIPOPROTEIN CHOLESTEROL; MONOCYTE CHEMOTACTIC PROTEIN 1; NITRIC OXIDE; PRAVASTATIN; REACTIVE OXYGEN METABOLITE; TRIACYLGLYCEROL; VASCULAR CELL ADHESION MOLECULE 1;

ADULT; ANTIHYPERTENSIVE THERAPY; ARTICLE; ATHEROSCLEROSIS; BODY MASS; CARDIOVASCULAR RISK; CELL ADHESION; CELL AGING; CELL CYCLE ARREST; CELL NUCLEUS MEMBRANE; DIABETES MELLITUS; DISEASE SEVERITY; DNA DAMAGE; DNA REPAIR; DYSLIPIDEMIA; ENDOTHELIAL DYSFUNCTION; FEMALE; HEMOGLOBIN BLOOD LEVEL; HUMAN; HUMAN TISSUE; IN VITRO STUDY; LIPODYSTROPHY; MECHANOTRANSDUCTION; MUTATION; OXIDATIVE STRESS; PERIPHERAL BLOOD MONONUCLEAR CELL; PHENOTYPE; PRIORITY JOURNAL; PROTEIN EXPRESSION; PROTEIN LOCALIZATION; PROTEIN PHOSPHORYLATION; TELOMERE SHORTENING; TRIACYLGLYCEROL BLOOD LEVEL;

ARTERIOSCLEROSIS; ENDOTHELIAL CELLS; LAMININ A/C; OXIDATIVE STRESS; PRELAMIN A; STATINS, HMG-COA;

ADULT; AGE OF ONSET; ANTIOXIDANTS; ATHEROSCLEROSIS; CELL ADHESION; CELL AGING; COCULTURE TECHNIQUES; DNA DAMAGE; ENDOTHELIAL CELLS; FEMALE; FIBROBLASTS; GENETIC PREDISPOSITION TO DISEASE; HEK293 CELLS; HETEROZYGOTE; HUMANS; HYDROXYMETHYLGLUTARYL-COA REDUCTASE INHIBITORS; LAMIN TYPE A; LIPODYSTROPHY, FAMILIAL PARTIAL; MALE; MIDDLE AGED; MUTATION; NITRIC OXIDE; NUCLEAR ENVELOPE; NUCLEAR PROTEINS; OXIDATIVE STRESS; PHENOTYPE; PRENYLATION; PROTEIN PRECURSORS; PROTEIN PROCESSING, POST-TRANSLATIONAL; TRANSDUCTION, GENETIC; TRANSFECTION;

EID: 84883282498     PISSN: 10795642     EISSN: 15244636     Source Type: Journal    
DOI: 10.1161/ATVBAHA.113.301933     Document Type: Article

References (48)

1. Dechat T, Adam SA, Taimen P, Shimi T, Goldman RD. Nuclear lamins. Cold Spring Harb Perspect Biol. 2010;2:a000547.
2. Worman HJ. Nuclear lamins and laminopathies. J Pathol. 2012;226:316-325.
3. 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)
4. 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;24:153-156. (Pubitemid 30094715)
5. Garg A, Peshock RM, Fleckenstein JL. Adipose tissue distribution pattern in patients with familial partial lipodystrophy (Dunnigan variety). J Clin Endocrinol Metab. 1999;84:170-174. (Pubitemid 29036696)
6. Vigouroux C, Magré J, Vantyghem MC, Bourut C, Lascols O, Shackleton S, Lloyd DJ, Guerci B, Padova G, Valensi P, Grimaldi A, Piquemal R, Touraine P, Trembath RC, Capeau J. 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.
7. Hegele RA, Anderson CM, Wang J, Jones DC, Cao H. Association between nuclear lamin A/C R482Q mutation and partial lipodystrophy with hyperinsulinemia, dyslipidemia, hypertension, and diabetes. Genome Res. 2000;10:652-658. (Pubitemid 30333193)
8. Garg A. Gender differences in the prevalence of metabolic complications in familial partial lipodystrophy (Dunnigan variety). J Clin Endocrinol Metab. 2000;85:1776-1782. (Pubitemid 32269275)
9. Hegele RA. Premature atherosclerosis associated with monogenic insulin resistance. Circulation. 2001;103:2225-2229. (Pubitemid 32433709)
10. 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)
11. Olive M, Harten I, Mitchell R, et al. Cardiovascular pathology in Hutchinson-Gilford progeria: correlation with the vascular pathology of aging. Arterioscler Thromb Vasc Biol. 2010;30:2301-2309.
12. Gordon LB, Harten IA, Patti ME, Lichtenstein AH. Reduced adiponectin and HDL cholesterol without elevated C-reactive protein: clues to the biology of premature atherosclerosis in Hutchinson-Gilford Progeria Syndrome. J Pediatr. 2005;146:336-341. (Pubitemid 40341742)
13. Capanni C, Mattioli E, Columbaro M, Lucarelli E, Parnaik VK, Novelli G, Wehnert M, Cenni V, Maraldi NM, Squarzoni S, Lattanzi G. Altered pre-lamin A processing is a common mechanism leading to lipodystrophy. Hum Mol Genet. 2005;14:1489-1502. (Pubitemid 40823458)
14. Caron M, Auclair M, Donadille B, Béréziat V, Guerci B, Laville M, Narbonne H, Bodemer C, Lascols O, Capeau J, Vigouroux C. Human lipodystrophies linked to mutations in A-type lamins and to HIV protease inhibitor therapy are both associated with prelamin A accumulation, oxidative stress and premature cellular senescence. Cell Death Differ. 2007;14:1759-1767. (Pubitemid 47423643)
15. De Sandre-Giovannoli A, Bernard R, Cau P, Navarro C, Amiel J, Boccaccio I, Lyonnet S, Stewart CL, Munnich A, Le Merrer M, Lévy N. Lamin a truncation in Hutchinson-Gilford progeria. Science. 2003;300:2055. (Pubitemid 36760124)
16. 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)
17. McClintock D, Gordon LB, Djabali K. Hutchinson-Gilford progeria mutant lamin A primarily targets human vascular cells as detected by an anti-Lamin A G608G antibody. Proc Natl Acad Sci USA. 2006;103:2154-2159. (Pubitemid 43271639)
18. Varga R, Eriksson M, Erdos MR, et al. Progressive vascular smooth muscle cell defects in a mouse model of Hutchinson-Gilford progeria syndrome. Proc Natl Acad Sci USA. 2006;103:3250-3255. (Pubitemid 43346456)
19. Capell BC, Collins FS, Nabel EG. Mechanisms of cardiovascular disease in accelerated aging syndromes. Circ Res. 2007;101:13-26. (Pubitemid 47094620)
20. Liu Y, Rusinol A, Sinensky M, Wang Y, Zou Y. DNA damage responses in progeroid syndromes arise from defective maturation of prelamin A. J Cell Sci. 2006;119(pt 22):4644-4649. (Pubitemid 44964261)
21. Liu B, Wang J, Chan KM, et al. Genomic instability in laminopathy-based premature aging. Nat Med. 2005;11:780-785. (Pubitemid 41021211)
22. Ragnauth CD, Warren DT, Liu Y, McNair R, Tajsic T, Figg N, Shroff R, Skepper J, Shanahan CM. Prelamin A acts to accelerate smooth muscle cell senescence and is a novel biomarker of human vascular aging. Circulation. 2010;121:2200-2210.
23. Richards SA, Muter J, Ritchie P, Lattanzi G, Hutchison CJ. The accumulation of un-repairable DNA damage in laminopathy progeria fibroblasts is caused by ROS generation and is prevented by treatment with N-acetyl cysteine. Hum Mol Genet. 2011;20:3997-4004.
24. Capell BC, Erdos MR, Madigan JP, Fiordalisi JJ, Varga R, Conneely KN, Gordon LB, Der CJ, Cox AD, Collins FS. 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)
25. Fong LG, Frost D, Meta M, Qiao X, Yang SH, Coffinier C, Young SG. A protein farnesyltransferase inhibitor ameliorates disease in a mouse model of progeria. Science. 2006;311:1621-1623.
26. 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.
27. Varela I, Pereira S, Ugalde AP, Navarro CL, Suárez MF, Cau P, Cadiñanos J, Osorio FG, Foray N, Cobo J, de Carlos F, Lévy N, Freije JM, López-Otín C. Combined treatment with statins and aminobisphosphonates extends longevity in a mouse model of human premature aging. Nat Med. 2008;14:767-772.
28. Gordon LB, Kleinman ME, Miller DT, et al. Clinical trial of a farnesyltransferase inhibitor in children with Hutchinson-Gilford progeria syndrome. Proc Natl Acad Sci USA. 2012;109:16666-16671.
29. Minamino T, Miyauchi H, Yoshida T, Ishida Y, Yoshida H, Komuro I. Endothelial cell senescence in human atherosclerosis: role of telomere in endothelial dysfunction. Circulation. 2002;105:1541-1544. (Pubitemid 34297628)
30. Davignon J, Ganz P. Role of endothelial dysfunction in atherosclerosis. Circulation. 2004;109:III27-III32. (Pubitemid 38786440)
31. Liu H, Colavitti R, Rovira II, Finkel T. Redox-dependent transcriptional regulation. Circ Res. 2005;97:967-974. (Pubitemid 41668909)
32. Madamanchi NR, Vendrov A, Runge MS. Oxidative stress and vascular disease. Arterioscler Thromb Vasc Biol. 2005;25:29-38. (Pubitemid 40054251)
33. Lefèvre C, Auclair M, Boccara F, Bastard JP, Capeau J, Vigouroux C, Caron-Debarle M. Premature senescence of vascular cells is induced by HIV protease inhibitors: implication of prelamin A and reversion by statin. Arterioscler Thromb Vasc Biol. 2010;30:2611-2620.
34. Widlansky ME, Gutterman DD. Regulation of endothelial function by mitochondrial reactive oxygen species. Antioxid Redox Signal. 2011;15:1517-1530.
35. Malik Q, Herbert KE. Oxidative and non-oxidative DNA damage and cardiovascular disease. Free Radic Res. 2012;46:554-564.
36. Mattioli E, Columbaro M, Capanni C, Santi S, Maraldi NM, D'Apice MR, Novelli G, Riccio M, Squarzoni S, Foisner R, Lattanzi G. Drugs affecting prelamin A processing: effects on heterochromatin organization. Exp Cell Res. 2008;314:453-462.
37. Celeste A, Petersen S, Romanienko PJ, et al. Genomic instability in mice lacking histone H2AX. Science. 2002;296:922-927. (Pubitemid 34464900)
38. Lanigan F, Geraghty JG, Bracken AP. Transcriptional regulation of cellular senescence. Oncogene. 2011;30:2901-2911.
39. Hwang SJ, Ballantyne CM, Sharrett AR, Smith LC, Davis CE, Gotto AM Jr, Boerwinkle E. Circulating adhesion molecules VCAM-1, ICAM-1, and E-selectin in carotid atherosclerosis and incident coronary heart disease cases: the Atherosclerosis Risk In Communities (ARIC) study. Circulation. 1997;96:4219-4225. (Pubitemid 28007447)
40. Ridker PM, Rifai N, Stampfer MJ, Hennekens CH. Plasma concentration of interleukin-6 and the risk of future myocardial infarction among apparently healthy men. Circulation. 2000;101:1767-1772. (Pubitemid 30213096)
41. Luc G, Arveiler D, Evans A, Amouyel P, Ferrieres J, Bard JM, Elkhalil L, Fruchart JC, Ducimetiere P; PRIME Study Group. Circulating soluble adhesion molecules ICAM-1 and VCAM-1 and incident coronary heart disease: the PRIME Study. Atherosclerosis. 2003;170:169-176. (Pubitemid 37083576)
42. Kaptoge S, Di Angelantonio E, Pennells L, et al. C-reactive protein, fibrinogen, and cardiovascular disease prediction. N Engl J Med. 2012;367:1310-1320.
43. Liu Q, Kim DI, Syme J, LuValle P, Burke B, Roux KJ. Dynamics of lamin-A processing following precursor accumulation. PLoS One. 2010;5:e10874.
44. Oemar BS, Tschudi MR, Godoy N, Brovkovich V, Malinski T, Lüscher TF. Reduced endothelial nitric oxide synthase expression and production in human atherosclerosis. Circulation. 1998;97:2494-2498. (Pubitemid 28294493)
45. Martinet W, Knaapen MW, De Meyer GR, Herman AG, Kockx MM. Elevated levels of oxidative DNA damage and DNA repair enzymes in human atherosclerotic plaques. Circulation. 2002;106:927-932. (Pubitemid 34925325)
46. Mahmoudi M, Gorenne I, Mercer J, Figg N, Littlewood T, Bennett M. Statins use a novel Nijmegen breakage syndrome-1-dependent pathway to accelerate DNA repair in vascular smooth muscle cells. Circ Res. 2008;103:717-725.
47. Coffinier C, Hudon SE, Farber EA, Chang SY, Hrycyna CA, Young SG, Fong LG. HIV protease inhibitors block the zinc metalloproteinase ZMPSTE24 and lead to an accumulation of prelamin A in cells. Proc Natl Acad Sci USA. 2007;104:13432-13437. (Pubitemid 47293962)
48. Dahl KN, Ribeiro AJ, Lammerding J. Nuclear shape, mechanics, and mechanotransduction. Circ Res. 2008;102:1307-1318.