Prelamin a acts to accelerate smooth muscle cell senescence and is a novel biomarker of human vascular aging

Circulation

Volumn 121, Issue 20, 2010, Pages 2200-2210

  Ragnauth, Cassandra D ^a,d   Warren, Derek T ^a   Liu, Yiwen ^a   McNair, Rosamund ^c   Tajsic, Tamara ^a   Figg, Nichola ^c   Shroff, Rukshana ^b   Skepper, Jeremy ^d   Shanahan, Catherine M ^a  

^a KING'S COLLEGE LONDON   (United Kingdom)

^b GREAT ORMOND STREET HOSPITAL   (United Kingdom)

^c ADDENBROOKE S HOSPITAL   (United Kingdom)

^d UNIVERSITY OF CAMBRIDGE   (United Kingdom)

Author keywords

Aging; Arteriosclerosis; Muscle; Nuclear lamina; Progeria; Smooth

Indexed keywords

BIOLOGICAL MARKER; FACE1 METALLOPROTEINASE; FARNESYLATION INHIBITOR; HYDROXYMETHYLGLUTARYL COENZYME A REDUCTASE INHIBITOR; LAMIN A; METALLOPROTEINASE; NUCLEAR PROTEIN; PRELAMIN A; SMALL INTERFERING RNA; UNCLASSIFIED DRUG;

AGED; AGING; ARTICLE; ATHEROSCLEROSIS; CELL DEGENERATION; CONTROLLED STUDY; DNA DAMAGE; HUMAN; HUMAN CELL; MITOSIS; OXIDATIVE STRESS; PRIORITY JOURNAL; PROTEIN LOCALIZATION; SENESCENCE; SMOOTH MUSCLE FIBER; VASCULAR SMOOTH MUSCLE;

AGING; ATHEROSCLEROSIS; BIOLOGICAL MARKERS; BLOOD VESSELS; CELL AGING; CELL DIVISION; CELL NUCLEUS; CELLS, CULTURED; DNA DAMAGE; DOWN-REGULATION; HUMANS; LAMIN TYPE A; MEMBRANE PROTEINS; METALLOENDOPEPTIDASES; MITOSIS; MUSCLE, SMOOTH, VASCULAR; MYOCYTES, SMOOTH MUSCLE; NUCLEAR PROTEINS; OXIDATIVE STRESS; PROTEIN PRECURSORS; RNA, MESSENGER; TIME FACTORS; UP-REGULATION;

EID: 77953023624     PISSN: 00097322     EISSN: 15244539     Source Type: Journal    
DOI: 10.1161/CIRCULATIONAHA.109.902056     Document Type: Article

References (43)

1. Gruenbaum Y, Margalit A, Goldman RD, Shumaker DK, Wilson KL. The nuclear lamina comes of age. Nat Rev Mol Cell Biol. 2005;6:21-31.
2. Sinensky M, Fantle K, Trujillo M, McLain T, Kupfer A, Dalton M. The processing pathway of prelamin A. J Cell Sci. 1994;107(pt 1):61-67.
3. De Sandre-Giovannoli A, Bernard R, Cau P, Navarro C, Amiel J, Boccaccio I, Lyonnet S, Stewart CL, Munnich A, Le Merrer M, Levy N. Lamin A truncation in Hutchinson-Gilford progeria. Science. 2003; 300:2055.
4. Dechat T, Pfleghaar K, Sengupta K, Shimi T, Shumaker DK, Solimando L, Goldman RD. Nuclear lamins: major factors in the structural organization and function of the nucleus and chromatin. Genes Dev. 2008;22: 832-853.
5. Denecke J, Brune T, Feldhaus T, Robenek H, Kranz C, Auchus RJ, Agarwal AK, Marquardt T. A homozygous ZMPSTE24 null mutation in combination with a heterozygous mutation in the LMNA gene causes Hutchinson-Gilford progeria syndrome (HGPS): insights into the patho-physiology of HGPS. Hum Mutat. 2006;27:524-531.
6. Shackleton S, Smallwood DT, Clayton P, Wilson LC, Agarwal AK, Garg A, Trembath RC. Compound heterozygous ZMPSTE24 mutations reduce prelamin A processing and result in a severe progeroid phenotype. J Med Genet. 2005;42:e36.
7. Goldman RD, Shumaker DK, Erdos MR, Eriksson M, Goldman AE, Gordon LB, Gruenbaum Y, Khuon S, Mendez M, Varga R, Collins FS. Accumulation of mutant lamin A causes progressive changes in nuclear architecture in Hutchinson-Gilford progeria syndrome. Proc Natl Acad Sci USA. 2004;101:8963-8968.
8. Bridger JM, Kill IR. Aging of Hutchinson-Gilford progeria syndrome fibroblasts is characterised by hyperproliferation and increased apoptosis. Exp Gerontol. 2004;39:717-724.
9. Scaffidi P, Misteli T. Lamin A-dependent nuclear defects in human aging. Science. 2006;312:1059-1063.
10. 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 Z. Genomic instability in laminopathy-based premature aging. Nat Med. 2005;11:780-785.
11. Merideth MA, Gordon LB, Clauss S, Sachdev V, Smith AC, Perry MB, Brewer CC, Zalewski C, Kim HJ, Solomon B, Brooks BP, Gerber LH, Turner ML, Domingo DL, Hart TC, Graf J, Reynolds JC, Gropman A, Yanovski JA, Gerhard-Herman M, Collins FS, Nabel EG, Cannon RO III, Gahl WA, Introne WJ. Phenotype and course of Hutchinson-Gilford progeria syndrome. N Engl J Med. 2008;358:592-604.
12. Kudlow BA, Kennedy BK, Monnat RJ Jr. Werner and Hutchinson-Gilford progeria syndromes: mechanistic basis of human progeroid diseases. Nat Rev Mol Cell Biol. 2007;8:394-404.
13. Scaffidi P, Misteli T. Lamin A-dependent misregulation of adult stem cells associated with accelerated ageing. Nat Cell Biol. 2008;10:452-459.
14. 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.
15. Varga R, Eriksson M, Erdos MR, Olive M, Harten I, Kolodgie F, Capell BC, Cheng J, Faddah D, Perkins S, Avallone H, San H, Qu X, Ganesh S, Gordon LB, Virmani R, Wight TN, Nabel EG, Collins FS. Progressive vascular smooth muscle cell defects in a mouse model of Hutchinson-Gilford progeria syndrome. Proc Natl Acad Sci USA. 2006;103: 3250-3255.
16. Stehbens WE, Delahunt B, Shozawa T, Gilbert-Barness E. Smooth muscle cell depletion and collagen types in progeric arteries. Cardiovasc Pathol. 2001;10:133-136.
17. Stehbens WE, Wakefield SJ, Gilbert-Barness E, Olson RE, Ackerman J. Histological and ultrastructural features of atherosclerosis in progeria. Cardiovasc Pathol. 1999;8:29-39.
18. Davies JD, Carpenter KL, Challis IR, Figg NL, McNair R, Proudfoot D, Weissberg PL, Shanahan CM. Adipocytic differentiation and liver x receptor pathways regulate the accumulation of triacylglycerols in human vascular smooth muscle cells. J Biol Chem. 2005;280:3911-3919.
19. Shanahan CM, Cary NR, Salisbury JR, Proudfoot D, Weissberg PL, Edmonds ME. Medial localization of mineralization-regulating proteins in association with Monckeberg's sclerosis: evidence for smooth muscle cell-mediated vascular calcification. Circulation. 1999;100:2168-2176.
20. McClintock D, Ratner D, Lokuge M, Owens DM, Gordon LB, Collins FS, Djabali K. The mutant form of lamin A that causes Hutchinson-Gilford progeria is a biomarker of cellular aging in human skin. PLoS ONE. 2007;2:e1269.
21. Matthews C, Gorenne I, Scott S, Figg N, Kirkpatrick P, Ritchie A, Goddard M, Bennett M. Vascular smooth muscle cells undergo telomere-based senescence in human atherosclerosis: effects of telomerase and oxidative stress. Circ Res. 2006;99:156-164.
22. Olive PL, Banath JP. Induction and rejoining of radiation-induced DNA single-strand breaks: "tail moment" as a function of position in the cell cycle. Mutat Res. 1993;294:275-283.
23. Toth JI, Yang SH, Qiao X, Beigneux AP, Gelb MH, Moulson CL, Miner JH, Young SG, Fong LG. Blocking protein farnesyltransferase improves nuclear shape in fibroblasts from humans with progeroid syndromes. Proc Natl Acad Sci USA. 2005;102:12873-12878.
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.
25. Tintut Y, Alfonso Z, Saini T, Radcliff K, Watson K, Bostrom K, Demer LL. Multilineage potential of cells from the artery wall. Circulation. 2003;108:2505-2510.
26. Mounkes LC, Kozlov S, Hernandez L, Sullivan T, Stewart CL. A progeroid syndrome in mice is caused by defects in A-type lamins. Nature. 2003;423:298-301.
27. Tyson KL, Reynolds JL, McNair R, Zhang Q, Weissberg PL, Shanahan CM. Osteo/chondrocytic transcription factors and their target genes exhibit distinct patterns of expression in human arterial calcification. Arterioscler Thromb Vasc Biol. 2003;23:489-494.
28. Zaidi SK, Javed A, Pratap J, Schroeder TM, J JW, Lian JB, van Wijnen AJ, Stein GS, Stein JL. Alterations in intranuclear localization of Runx2 affect biological activity. J Cell Physiol. 2006;209:935-942.
29. Lloyd DJ, Trembath RC, Shackleton S. A novel interaction between lamin A and SREBP1: implications for partial lipodystrophy and other laminopathies. Hum Mol Genet. 2002;11:769-777.
30. Dechat T, Shimi T, Adam SA, Rusinol AE, Andres DA, Spielmann HP, Sinensky MS, Goldman RD. Alterations in mitosis and cell cycle progression caused by a mutant lamin A known to accelerate human aging. Proc Natl Acad Sci USA. 2007;104:4955-4960.
31. Cao K, Capell BC, Erdos MR, Djabali K, Collins FS. A lamin A protein isoform overexpressed in Hutchinson-Gilford progeria syndrome interferes with mitosis in progeria and normal cells. Proc Natl Acad Sci USA. 2007;104:4949-4954.
32. Fong LG, Ng JK, Meta M, Cote N, Yang SH, Stewart CL, Sullivan T, Burghardt A, Majumdar S, Reue K, Bergo MO, Young SG. Heterozygosity for LMNA deficiency eliminates the progeria-like phenotypes in Zmpste24-deficient mice. Proc Natl Acad Sci USA. 2004;101:18111-18116.
33. Martinet W, De Bie M, Schrijvers DM, De Meyer GR, Herman AG, Kockx MM. 7-Ketocholesterol induces protein ubiquitination, myelin figure formation, and light chain 3 processing in vascular smooth muscle cells. Arterioscler Thromb Vasc Biol. 2004;24:2296-2301.
34. Vakifahmetoglu H, Olsson M, Zhivotovsky B. Death through a tragedy: mitotic catastrophe. Cell Death Differ. 2008;15:1153-1162.
35. Minamino T, Komuro I. Vascular cell senescence: contribution to atherosclerosis. Circ Res. 2007;100:15-26.
36. Matturri L, Cazzullo A, Turconi P, Lavezzi AM. Cytogenetic aspects of cell proliferation in atherosclerotic plaques. Cardiologia. 1997;42:833-836.
37. Jones MR, Ravid K. Vascular smooth muscle polyploidization as a biomarker for aging and its impact on differential gene expression. J Biol Chem. 2004;279:5306-5313.
38. 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.
39. Yang SH, Qiao X, Fong LG, Young SG. Treatment with a farnesyl-transferase inhibitor improves survival in mice with a Hutchinson-Gilford progeria syndrome mutation. Biochim Biophys Acta. 2008; 1781:36-39.
40. Yang SH, Meta M, Qiao X, Frost D, Bauch J, Coffinier C, Majumdar S, Bergo MO, Young SG, Fong LG. A farnesyltransferase inhibitor improves disease phenotypes in mice with a Hutchinson-Gilford progeria syndrome mutation. J Clin Invest. 2006;116:2115-2121.
41. 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.
42. Capell BC, Olive M, Erdos MR, Cao K, Faddah DA, Tavarez UL, Conneely KN, Qu X, San H, Ganesh SK, Chen X, Avallone H, Kolodgie FD, Virmani R, Nabel EG, Collins FS. 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.
43. Varela I, Pereira S, Ugalde AP, Navarro CL, Suarez MF, Cau P, Cadinanos J, Osorio FG, Foray N, Cobo J, de Carlos F, Levy N, Freije JM, Lopez-Otin C. Combined treatment with statins and aminobisphos-phonates extends longevity in a mouse model of human premature aging. Nat Med. 2008;14:767-772.