Farnesyltransferase inhibitor treatment restores chromosome territory positions and active chromosome dynamics in Hutchinson-Gilford progeria syndrome cells

Genome Biology

Volumn 12, Issue 8, 2011, Pages

  Mehta, Ishita S ^a,b   Eskiw, Christopher H ^a   Arican, Halime D ^a   Kill, Ian R ^a   Bridger, Joanna M ^a  

^a BRUNEL UNIVERSITY   (United Kingdom)

^b TATA INSTITUTE OF FUNDAMENTAL RESEARCH   (India)

Author keywords

[No Author keywords available]

Indexed keywords

DIACETYL OXIME; ENZYME INHIBITOR; GERANYLGERANYLTRANSFERASE INHIBITOR; GGTI 2147; LAMIN A; MYOSIN I; MYOSIN I BETA; N [[5 [(2 AMINO 3 MERCAPTOPROPYL)AMINO][1,1' BIPHENYL] 2 YL]CARBONYL]METHIONINE METHYL ESTER; PROTEIN FARNESYLTRANSFERASE INHIBITOR; UNCLASSIFIED DRUG; FARNESYL TRANS TRANSFERASE;

AGING; ARTICLE; CELL NUCLEUS; CELL POPULATION; CELL PROLIFERATION; CELLULAR DISTRIBUTION; CHROMOSOME 10; CHROMOSOME 18; CHROMOSOME POSITIONING; CONTROLLED STUDY; FIBROBLAST; FLUORESCENCE IN SITU HYBRIDIZATION; GENE MUTATION; HUMAN; HUMAN CELL; IMMUNOFLUORESCENCE TEST; INTERPHASE; MITOSIS; POLYMERIZATION; PROGERIA; SIGNAL TRANSDUCTION; X CHROMOSOME; CELL CULTURE; CYTOLOGY; DRUG ANTAGONISM; DRUG EFFECT; GENE EXPRESSION REGULATION; GENETICS; HUMAN CHROMOSOME; METABOLISM; MUTATION; PATHOLOGY; PREMATURE AGING; PREMATURE MORTALITY;

AGING, PREMATURE; CELL PROLIFERATION; CELLS, CULTURED; CHROMOSOMES, HUMAN; ENZYME INHIBITORS; FARNESYLTRANSTRANSFERASE; FIBROBLASTS; GENE EXPRESSION REGULATION; HUMANS; LAMIN TYPE A; MITOSIS; MORTALITY, PREMATURE; MUTATION; PROGERIA;

EID: 80051590194     PISSN: 14747596     EISSN: 1474760X     Source Type: Journal    
DOI: 10.1186/gb-2011-12-8-r74     Document Type: Article

References (64)

1. Capell BC, Collins FS. Human laminopathies: nuclei gone genetically awry. Nat Rev Genet 2006, 7:940-952. 10.1038/nrg1906, 17139325.
2. Baker PB, Baba N, Boesel CP. Cardiovascular abnormalities in progeria. Case report and review of the literature. Arch Pathol Lab Med 1981, 105:384-386.
3. Worman HJ, Ostlund C, Wang Y. Diseases of the nuclear envelope. Cold Spring Harb Perspect Biol 2010, 2:a000760. 10.1101/cshperspect.a000760, 2828284, 20182615.
4. DeBusk FL. The Hutchinson-Gilford progeria syndrome. Report of 4 cases and review of the literature. J Pediatr 1972, 80:697-724. 10.1016/S0022-3476(72)80229-4, 4552697.
5. Sarkar PK, Shinton RA. Hutchinson-Guilford progeria syndrome. Postgrad Med J 2001, 77:312-317. 10.1136/pmj.77.907.312, 1742040, 11320273.
6. 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. 10.1126/science.1084125, 12702809.
7. Barboro P, D'Arrigo C, Diaspro A, Mormino M, Alberti I, Parodi S, Patrone E, Balbi C. Unraveling the organization of the internal nuclear matrix: RNA-dependent anchoring of NuMA to a lamin scaffold. Exp Cell Res 2002, 279:202-218. 10.1006/excr.2002.5605, 12243746.
8. Bridger JM, Kill IR, O'Farrell M, Hutchison CJ. Internal lamin structures within G1 nuclei of human dermal fibroblasts. J Cell Sci 1993, 104:297-306.
9. Elcock LS, Bridger JM. Exploring the effects of a dysfunctional nuclear matrix. Biochem Soc Trans 2008, 36:1378-1383. 10.1042/BST0361378, 19021559.
10. Hozak P, Sasseville AM, Raymond Y, Cook PR. Lamin proteins form an internal nucleoskeleton as well as a peripheral lamina in human cells. J Cell Sci 1995, 108:635-644.
11. Foster HA, Bridger JM. The genome and the nucleus: a marriage made by evolution. Genome organisation and nuclear architecture. Chromosoma 2005, 114:212-229. 10.1007/s00412-005-0016-6, 16133352.
12. 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. 10.1038/nrm1550, 15688064.
13. Eriksson M, Brown WT, Gordon LB, Glynn MW, Singer J, Scott L, Erdos MR, Robbins CM, Moses TY, Berglund P, Dutra A, Pak E, Durkin S, Csoka AB, Boehnke M, Glover TW, Collins FS. Recurrent de novo point mutations in lamin A cause Hutchinson-Gilford progeria syndrome. Nature 2003, 423:293-298. 10.1038/nature01629, 12714972.
14. Hutchison CJ, Worman HJ. A-type lamins: guardians of the soma?. Nat Cell Biol 2004, 6:1062-1067. 10.1038/ncb1104-1062, 15517000.
15. Beck LA, Hosick TJ, Sinensky M. Isoprenylation is required for the processing of the lamin A precursor. J Cell Biol 1990, 110:1489-1499. 10.1083/jcb.110.5.1489, 2200179, 2335559.
16. Hennekes H, Nigg EA. The role of isoprenylation in membrane attachment of nuclear lamins. A single point mutation prevents proteolytic cleavage of the lamin A precursor and confers membrane binding properties. J Cell Sci 1994, 107:1019-1029.
17. Sinensky M, Fantle K, Trujillo M, McLain T, Kupfer A, Dalton M. The processing pathway of prelamin A. J Cell Sci 1994, 107:61-67.
18. Weber K, Plessmann U, Traub P. Maturation of nuclear lamin A involves a specific carboxy-terminal trimming, which removes the polyisoprenylation site from the precursor; implications for the structure of the nuclear lamina. FEBS Lett 1989, 257:411-414. 10.1016/0014-5793(89)81584-4, 2583287.
19. Fong LG, Ng JK, Meta M, Coté 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. 10.1073/pnas.0408558102, 536056, 15608054.
20. 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. 10.1073/pnas.0402943101, 428455, 15184648.
21. Scaffidi P, Misteli T. Reversal of the cellular phenotype in the premature aging disease Hutchinson-Gilford progeria syndrome. Nat Med 2005, 11:440-445. 10.1038/nm1204, 1351119, 15750600.
22. Adjei AA. Farnesyltransferase inhibitors. Cancer Chemother Biol Response Modif 2005, 22:123-133.
23. Yang SH, Chang SY, Ren S, Wang Y, Andres DA, Spielmann HP, Fong LG, Young SG. Absence of progeria-like disease phenotypes in knock-in mice expressing a non-farnesylated version of progerin. Hum Mol Genet 2011, 20:436-444. 10.1093/hmg/ddq490, 21088111.
24. 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. 10.1093/hmg/ddi326, 16126733.
25. Mallampalli MP, Huyer G, Bendale P, Gelb MH, Michaelis S. 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. 10.1073/pnas.0503712102, 1242289, 16186497.
26. 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. 10.1073/pnas.0505767102, 1193538, 16129834.
27. Yang SH, Bergo MO, Toth JI, Qiao X, Hu Y, Sandoval S, Meta M, Bendale P, Gelb MH, Young SG, Fong LG. 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. 10.1073/pnas.0504641102, 1174929, 16014412.
28. Taimen P, Pfleghaar K, Shimi T, Möller D, Ben-Harush K, Erdos MR, Adam SA, Herrmann H, Medalia O, Collins FS, Goldman AE, Goldman RD. A progeria mutation reveals functions for lamin A in nuclear assembly, architecture, and chromosome organization. Proc Natl Acad Sci USA 2009, 106:20788-20793. 10.1073/pnas.0911895106, 2779830, 19926845.
29. Mehta IS, Bridger JM, Kill IR. Progeria: the nucleolus and farnesyltransferase inhibitors. Biochem Soc Trans 2010, 38:287-291. 10.1042/BST0380287, 20074076.
30. Verstraeten VL, Ji JY, Cummings KS, Lee RT, Lammerding J. Increased mechanosensitivity and nuclear stiffness in Hutchinson-Gilford progeria cells: effects of farnesyltransferase inhibitors. Aging Cell 2008, 7:383-393. 10.1111/j.1474-9726.2008.00382.x, 2651412, 18331619.
31. Constantinescu D, Csoka AB, Navara CS, Schatten GP. 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. 10.1016/j.yexcr.2010.05.015, 20599958.
32. 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. 10.1126/science.1124875, 16484451.
33. Meta M, Yang SH, Bergo MO, Fong LG, Young SG. Protein farnesyltransferase inhibitors and progeria. Trends Mol Med 2006, 12:480-487. 10.1016/j.molmed.2006.08.006, 16942914.
34. 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. 10.1172/JCI28968, 1513052, 16862216.
35. 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. 10.1073/pnas.0807840105, 2562418, 18838683.
36. Meshorer E, Gruenbaum Y. Rejuvenating premature aging. Nat Med 2008, 14:713-715. 10.1038/nm0708-713, 18607367.
37. 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. 10.1038/nm1786, 18587406.
38. Boyle S, Gilchrist S, Bridger JM, Mahy NL, Ellis JA, Bickmore WA. The spatial organization of human chromosomes within the nuclei of normal and emerin-mutant cells. Hum Mol Genet 2001, 10:211-219. 10.1093/hmg/10.3.211, 11159939.
39. Croft JA, Bridger JM, Boyle S, Perry P, Teague P, Bickmore WA. Differences in the localization and morphology of chromosomes in the human nucleus. J Cell Biol 1999, 145:1119-1131. 10.1083/jcb.145.6.1119, 2133153, 10366586.
40. Bridger JM, Boyle S, Kill IR, Bickmore WA. Re-modelling of nuclear architecture in quiescent and senescent human fibroblasts. Curr Biol 2000, 10:149-152. 10.1016/S0960-9822(00)00312-2, 10679329.
41. Meaburn KJ, Cabuy E, Bonne G, Levy N, Morris GE, Novelli G, Kill IR, Bridger JM. Primary laminopathy fibroblasts display altered genome organization and apoptosis. Aging Cell 2007, 6:139-153. 10.1111/j.1474-9726.2007.00270.x, 17274801.
42. Mehta IS, Amira M, Harvey AJ, Bridger JM. Rapid chromosome territory relocation by nuclear motor activity in response to serum removal in primary human fibroblasts. Genome Biol 2010, 11:R5. 10.1186/gb-2010-11-1-r5, 2847717, 20070886.
43. Mehta IS, Figgitt M, Clements CS, Kill IR, Bridger JM. Alterations to nuclear architecture and genome behavior in senescent cells. Ann N Y Acad Sci 2007, 1100:250-263. 10.1196/annals.1395.027, 17460187.
44. Mewborn SK, Puckelwartz MJ, Abuisneineh F, Fahrenbach JP, Zhang Y, MacLeod H, Dellefave L, Pytel P, Selig S, Labno CM, Reddy K, Singh H, McNally E. Altered chromosomal positioning, compaction, and gene expression with a lamin A/C gene mutation. PLoS One 2010, 5:e14342. 10.1371/journal.pone.0014342, 3001866, 21179469.
45. Columbaro M, Capanni C, Mattioli E, Novelli G, Parnaik VK, Squarzoni S, Maraldi NM, Lattanzi G. Rescue of heterochromatin organization in Hutchinson-Gilford progeria by drug treatment. Cell Mol Life Sci 2005, 62:2669-2678. 10.1007/s00018-005-5318-6, 2773834, 16261260.
46. Shumaker DK, Dechat T, Kohlmaier A, Adam SA, Bozovsky MR, Erdos MR, Eriksson M, Goldman AE, Khuon S, Collins FS, Jenuwein T, Goldman RD. Mutant nuclear lamin A leads to progressive alterations of epigenetic control in premature aging. Proc Natl Acad Sci USA 2006, 103:8703-8708. 10.1073/pnas.0602569103, 1472659, 16738054.
47. Chuang CH, Carpenter AE, Fuchsova B, Johnson T, de Lanerolle P, Belmont AS. Long-range directional movement of an interphase chromosome site. Curr Biol 2006, 16:825-831. 10.1016/j.cub.2006.03.059, 16631592.
48. Hofmann WA, Johnson T, Klapczynski M, Fan JL, de Lanerolle P. From transcription to transport: emerging roles for nuclear myosin I. Biochem Cell Biol 2006, 84:418-426. 10.1139/o06-069, 16936815.
49. Bridger JM, Mehta IS. Nuclear molecular motors for active, directed chromatin movement in interphase nuclei. Advances in Nuclear Architecture Springer 2011, Adams N, Freemont P.
50. Mehta IS, Elcock LS, Amira M, Kill IR, Bridger JM. Nuclear motors and nuclear structures containing A-type lamins and emerin: is there a functional link?. Biochem Soc Trans 2008, 36:1384-1388. 10.1042/BST0361384, 19021560.
51. Wilson KL, Holaska JM, Montes de Oca R, Tifft K, Zastrow M, Segura-Totten M, Mansharamani M, Bengtsson L. Nuclear membrane protein emerin: roles in gene regulation, actin dynamics and human disease. Novartis Found Symp 2005, 264:51-58. discussion 58-62, 227-230.
52. Kill IR. Localisation of the Ki-67 antigen within the nucleolus. Evidence for a fibrillarin-deficient region of the dense fibrillar component. J Cell Sci 1996, 109:1253-1263.
53. Kill IR, Faragher RG, Lawrence K, Shall S. The expression of proliferation-dependent antigens during the lifespan of normal and progeroid human fibroblasts in culture. J Cell Sci 1994, 107:571-579.
54. Shimi T, Pfleghaar K, Kojima S, Pack CG, Solovei I, Goldman AE, Adam SA, Shumaker DK, Kinjo M, Cremer T, Goldman RD. The A- and B-type nuclear lamin networks: microdomains involved in chromatin organization and transcription. Genes Dev 2008, 22:3409-3421. 10.1101/gad.1735208, 2607069, 19141474.
55. Kind J, van Steensel B. Genome-nuclear lamina interactions and gene regulation. Curr Opin Cell Biol 2010, 22:320-325. 10.1016/j.ceb.2010.04.002, 20444586.
56. Percipalle P, Farrants AK. Chromatin remodelling and transcription: be-WICHed by nuclear myosin 1. Curr Opin Cell Biol 2006, 18:267-274. 10.1016/j.ceb.2006.03.001, 16574391.
57. Kuroda M, Tanabe H, Yoshida K, Oikawa K, Saito A, Kiyuna T, Mizusawa H, Mukai K. Alteration of chromosome positioning during adipocyte differentiation. J Cell Sci 2004, 117:5897-5903. 10.1242/jcs.01508, 15537832.
58. Szczerbal I, Foster HA, Bridger JM. The spatial repositioning of adipogenesis genes is correlated with their expression status in a porcine mesenchymal stem cell adipogenesis model system. Chromosoma 2009, 118:647-663. 10.1007/s00412-009-0225-5, 19585140.
59. Szczerbal I, Bridger JM. Association of adipogenic genes with SC-35 domains during porcine adipogenesis. Chromosome Res 2010, 18:887-895. 10.1007/s10577-010-9176-1, 21127962.
60. Takizawa T, Gudla PR, Guo L, Lockett S, Misteli T. Allele-specific nuclear positioning of the monoallelically expressed astrocyte marker GFAP. Genes Dev 2008, 22:489-498. 10.1101/gad.1634608, 2238670, 18281462.
61. Wilson KL. Cytoskeletal and nuclear ("nucleoskeletal") intermediate filaments and disease. Mol Biol Cell 2011, 22:725. 10.1091/mbc.E10-12-0960, 3057697, 21406588.
62. Bridger JM, Kill IR, O'Farrell M, Hutchison CJ. Internal lamin structures within G1 nuclei of human dermal fibroblasts. J Cell Sci 1993, 104:297-304.
63. Bridger JM, Kill IR. Aging of Hutchinson-Gilford progeria syndrome fibroblasts is characterised by hyperproliferation and increased apoptosis. Exp Gerontol 2004, 39:717-724. 10.1016/j.exger.2004.02.002, 15130666.
64. Telenius H, Pelmear AH, Tunnacliffe A, Carter NP, Behmel A, Ferguson-Smith MA, Nordenskjöld M, Pfragner R, Ponder BA. Cytogenetic analysis by chromosome painting using DOP-PCR amplified flow-sorted chromosomes. Genes Chromosomes Cancer 1992, 4:257-263. 10.1002/gcc.2870040311, 1382568.