Lamin A-linked progerias: Is farnesylation the be all and end all?

Biochemical Society Transactions

Volumn 38, Issue 1, 2010, Pages 281-286

  Smallwood, Dawn T ^a   Shackleton, Sue ^a  

^a UNIVERSITY OF LEICESTER   (United Kingdom)

Author keywords

Farnesylation; Hutchinson Gilford progeria syndrome (HGPS); Lamin A; Laminopathy; Nuclear envelope; Premature aging

Indexed keywords

LAMIN A; PROTEIN FARNESYLTRANSFERASE; PROTEIN FARNESYLTRANSFERASE INHIBITOR;

ARTICLE; CARBOXY TERMINAL SEQUENCE; CELL DAMAGE; DISEASE SEVERITY; ENZYME INHIBITION; GENE MUTATION; GENE SEQUENCE; GENETIC ASSOCIATION; GENOMIC INSTABILITY; GENOTYPE PHENOTYPE CORRELATION; HUMAN; NONHUMAN; PRIORITY JOURNAL; PROGERIA; PROTEIN PROCESSING; RISK ASSESSMENT; RISK FACTOR;

AMINO ACID SEQUENCE; CHILD; CLINICAL TRIALS AS TOPIC; ENZYME INHIBITORS; FARNESYLTRANSTRANSFERASE; GENOTYPE; HUMANS; INFANT; LAMIN TYPE A; MOLECULAR SEQUENCE DATA; MUTATION; NUCLEAR ENVELOPE; PHENOTYPE; PRENYLATION; PROGERIA;

EID: 76449091104     PISSN: 03005127     EISSN: 14708752     Source Type: Journal    
DOI: 10.1042/BST0380281     Document Type: Article

References (50)

1. Hennekam, R.C. (2006) Hutchinson-Gilford progeria syndrome: review of the phenotype. Am. J. Med. Genet. A 140, 2603-2624
2. Worman, H.J. and Bonne, G. (2007) "Laminopathies": a wide spectrum of human diseases. Exp. Cell Res. 313, 2121-2133
3. Agarwal, A.K., Fryns, J.P., Auchus, R.J. and Garg, A. (2003) Zinc metalloproteinase, ZMPSTE24, is mutated in mandibuloacral dysplasia. Hum. Mol. Genet. 12, 1995-2001
4. Navarro, C.L., Cadinanos, J., De Sandre-Giovannoli, A., Bernard, R., Courrier, S., Boccaccio, I., Boyer, A., Kleijer, W.J., Wagner, A., Giuliano, F. et al. (2005) Loss of ZMPSTE24 (FACE-1) causes autosomal recessive restrictive dermopathy and accumulation of Lamin A precursors. Hum. Mol. Genet. 14, 1503-1513
5. Navarro, C.L., De Sandre-Giovannoli, A., Bernard, R., Boccaccio, I., Boyer, A., Genevieve, D., Hadj-Rabia, S., Gaudy-Marqueste, C., Smitt, H.S., Vabres, P. et al. (2004) Lamin A and ZMPSTE24 (FACE-1) defects cause nuclear disorganization and identify restrictive dermopathy as a lethal neonatal laminopathy. Hum. Mol. Genet. 13, 2493-2503
6. Prokocimer, M., Davidovich, M., Nissim-Rafinia, M., Wiesel-Motiuk, N., Bar, D., Barkan, R., Meshorer, E. and Gruenbaum, Y. (2009) Nuclear lamins: key regulators of nuclear structure and activities. J. Cell. Mol. Med., doi:10.1111/j.1582-4934.2008.00676.x
7. Dechat, T., Pfleghaar, K., Sengupta, K., Shimi, T., Shumaker, D.K., Solimando, L. and Goldman, R.D. (2008) Nuclear lamins: major factors in the structural organization and function of the nucleus and chromatin. Genes Dev. 22, 832-853
8. Davies, B.S., Fong, L.G., Yang, S.H., Coffinier, C. and Young, S.G. (2009) The posttranslational processing of prelamin A and disease. Annu. Rev. Genomics Hum. Genet. 10, 153-174
9. Navarro, C.L., Cau, P. and Lévy, N. (2006) Molecular bases of progeroid syndromes. Hum. Mol. Genet. 15, R151-R161
10. De Sandre-Giovannoli, A., Bernard, R., Cau, P., Navarro, C., Amiel, J., Boccaccio, I., Lyonnet, S., Stewart, C.L., Munnich, A., Le Merrer, M. and Lévy, N. (2003) Lamin A truncation in Hutchinson-Gilford progeria. Science 300, 2055
11. Eriksson, M., Brown, W.T., Gordon, L.B., Glynn, M.W., Singer, J., Scott, L., Erdos, M.R., Robbins, C.M., Moses, T.Y., Berglund, P. et al. (2003) Recurrent de novo point mutations in lamin A cause Hutchinson-Gilford progeria syndrome. Nature 423, 293-298
12. Moulson, C.L., Fong, L.G., Gardner, J.M., Farber, E.A., Go, G., Passariello, A., Grange, D.K., Young, S.G. and Miner, J.H. (2007) Increased progerin expression associated with unusual LMNA mutations causes severe progeroid syndromes. Hum. Mutat. 28, 882-889
13. Moulson, C.L., Go, G., Gardner, J.M., van der Wal, A.C., Smitt, J.H., van Hagen, J.M. and Miner, J.H. (2005) Homozygous and compound heterozygous mutations in ZMPSTE24 cause the laminopathy restrictive dermopathy. J. Invest. Dermatol. 125, 913-919
14. Plasilova, M., Chattopadhyay, C., Pal, P., Schaub, N.A., Buechner, S.A., Mueller, H., Miny, P., Ghosh, A. and Heinimann, K. (2004) Homozygous missense mutation in the lamin A/C gene causes autosomal recessive Hutchinson-Gilford progeria syndrome. J. Med. Genet. 41, 609-614
15. Verstraeten, V.L., Broers, J.L., van Steensel, M.A., Zinn-Justin, S., Ramaekers, F.C., Steijlen, P.M., Kamps, M., Kuijpers, H.J., Merckx, D., Smeets, H.J. et al. (2006) Compound heterozygosity for mutations in LMNA causes a progeria syndrome without prelamin A accumulation. Hum. Mol. Genet. 15, 2509-2522
16. Goldman, R.D., Shumaker, D.K., Erdos, M.R., Eriksson, M., Goldman, A.E., Gordon, L.B., Gruenbaum, Y., Khuon, S., Mendez, M., Varga, R. and Collins, F.S. (2004) Accumulation of mutant lamin A causes progressive changes in nuclear architecture in Hutchinson-Gilford progeria syndrome. Proc. Natl. Acad. Sci. U.S.A. 101, 8963-8968
17. Dahl, K.N., Scaffidi, P., Islam, M.F., Yodh, A.G., Wilson, K.L. and Misteli, T. (2006) Distinct structural and mechanical properties of the nuclear lamina in Hutchinson-Gilford progeria syndrome. Proc. Natl. Acad. Sci. U.S.A. 103, 10271-10276
18. Verstraeten, V.L., Ji, J.Y., Cummings, K.S., Lee, R.T. and Lammerding, J. (2008) Increased mechanosensitivity and nuclear stiffness in Hutchinson-Gilford progeria cells: effects of farnesyltransferase inhibitors. Aging Cell 7, 383-393
19. Scaffidi, P. and Misteli, T. (2005) Reversal of the cellular phenotype in the premature aging disease Hutchinson-Gilford progeria syndrome. Nat. Med. 11, 440-445
20. Delbarre, E., Tramier, M., Coppey-Moisan, M., Gaillard, C., Courvalin, J.C. and Buendia, B. (2006) The truncated prelamin A in Hutchinson-Gilford progeria syndrome alters segregation of A-type and B-type lamin homopolymers. Hum. Mol. Genet. 15, 1113-1122
21. Shumaker, D.K., Dechat, T., Kohlmaier, A., Adam, S.A., Bozovsky, M.R., Erdos, M.R., Eriksson, M., Goldman, A.E., Khuon, S., Collins, F.S. et al. (2006) Mutant nuclear lamin A leads to progressive alterations of epigenetic control in premature aging. Proc. Natl. Acad. Sci. U.S.A. 103, 8703-8708
22. Csoka, A.B., English, S.B., Simkevich, C.P., Ginzinger, D.G., Butte, A.J., Schatten, G.P., Rothman, F.G. and Sedivy, J.M. (2004) Genome-scale expression profiling of Hutchinson-Gilford progeria syndrome reveals widespread transcriptional misregulation leading to mesodermal/ mesenchymal defects and accelerated atherosclerosis. Aging Cell 3, 235-243
23. Busch, A., Kiel, T., Heupel, W.M., Wehnert, M. and Hubner, S. (2009) Nuclear protein import is reduced in cells expressing nuclear envelopathy-causing lamin A mutants. Exp. Cell Res. 315, 2373-2385
24. Bohr, V.A. (2008) Rising from the RecQ-age: the role of human RecQ helicases in genome maintenance. Trends Biochem. Sci. 33, 609-620
25. Liu, B., Wang, J., Chan, K.M., Tjia, W.M., Deng, W., Guan, X., Huang, J.D., Li, K.M., Chau, P.Y., Chen, D.J. et al. (2005) Genomic instability in laminopathy-based premature aging. Nat. Med. 11, 780-785
26. Liu, Y., Rusinol, A., Sinensky, M., Wang, Y. and Zou, Y. (2006) DNA damage responses in progeroid syndromes arise from defective maturation of prelamin A. J. Cell Sci. 119, 4644-4649
27. Cao, K., Capell, B.C., Erdos, M.R., Djabali, K. and Collins, F.S. (2007) A lamin A protein isoform overexpressed in Hutchinson-Gilford progeria syndrome interferes with mitosis in progeria and normal cells. Proc. Natl. Acad. Sci. U.S.A. 104, 4949-4954
28. Dechat, T., Shimi, T., Adam, S.A., Rusinol, A.E., Andres, D.A., Spielmann, H.P., Sinensky, M.S. and Goldman, R.D. (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
29. Allsopp, R.C., Vaziri, H., Patterson, C., Goldstein, S., Younglai, E.V., Futcher, A.B., Greider, C.W. and Harley, C.B. (1992) Telomere length predicts replicative capacity of human fibroblasts. Proc. Natl. Acad. Sci. U.S.A. 89, 10114-10118
30. Huang, S., Risques, R.A., Martin, G.M., Rabinovitch, P.S. and Oshima, J. (2008) Accelerated telomere shortening and replicative senescence in human fibroblasts overexpressing mutant and wild-type lamin A. Exp. Cell Res. 314, 82-91
31. Scaffidi, P. and Misteli, T. (2006) Lamin A-dependent nuclear defects in human aging. Science 312, 1059-1063
32. Toth, J.I., Yang, S.H., Qiao, X., Beigneux, A.P., Gelb, M.H., Moulson, C.L., Miner, J.H., Young, S.G. and Fong, L.G. (2005) Blocking protein farnesyltransferase improves nuclear shape in fibroblasts from humans with progeroid syndromes. Proc. Natl. Acad. Sci. U.S.A. 102, 12873-12878
33. Capell, B.C., Erdos, M.R., Madigan, J.P., Fiordalisi, J.J., Varga, R., Conneely, K.N., Gordon, L.B., Der, C.J., Cox, A.D. and Collins, F.S. (2005) Inhibiting farnesylation of progerin prevents the characteristic nuclear blebbing of Hutchinson-Gilford progeria syndrome. Proc. Natl. Acad. Sci. U.S.A. 102, 12879-12884
34. Glynn, M.W. and Glover, T.W. (2005) Incomplete processing of mutant lamin A in Hutchinson-Gilford progeria leads to nuclear abnormalities, which are reversed by farnesyltransferase inhibition. Hum. Mol. Genet. 14, 2959-2969
35. Fong, L.G., Frost, D., Meta, M., Qiao, X., Yang, S.H., Coffinier, C. and Young, S.G. (2006) A protein farnesyltransferase inhibitor ameliorates disease in a mouse model of progeria. Science 311, 1621-1623
36. Yang, S.H., Meta, M., Qiao, X., Frost, D., Bauch, J., Coffinier, C., Majumdar, S., Bergo, M.O., Young, S.G. and Fong, L.G. (2006) A farnesyltransferase inhibitor improves disease phenotypes in mice with a Hutchinson-Gilford progeria syndrome mutation. J. Clin. Invest. 116, 2115-2121
37. Yang, S.H., Andres, D.A., Spielmann, H.P., Young, S.G. and Fong, L.G. (2008) Progerin elicits disease phenotypes of progeria in mice whether or not it is farnesylated. J. Clin. Invest. 118, 3291-3300
38. Lattanzi, G., Columbaro, M., Mattioli, E., Cenni, V., Camozzi, D., Wehnert, M., Santi, S., Riccio, M., Del Coco, R., Maraldi, N.M. et al. (2007) Pre-lamin A processing is linked to heterochromatin organization. J. Cell. Biochem. 102, 1149-1159
39. Kieran, M.W., Gordon, L. and Kleinman, M. (2007) New approaches to progeria. Pediatrics 120, 834-841
40. Sagelius, H., Rosengardten, Y., Schmidt, E., Sonnabend, C., Rozell, B. and Eriksson, M. (2008) Reversible phenotype in a mouse model of Hutchinson-Gilford progeria syndrome. J. Med. Genet. 45, 794-801
41. Csoka, A.B., Cao, H., Sammak, P.J., Constantinescu, D., Schatten, G.P. and Hegele, R.A. (2004) Novel lamin A/C gene (LMNA) mutations in atypical progeroid syndromes. J. Med. Genet. 41, 304-308
42. Kirschner, J., Brune, T., Wehnert, M., Denecke, J., Wasner, C., Feuer, A., Marquardt, T., Ketelsen, U.P., Wieacker, P., Bonnemann, C.G. and Korinthenberg, R. (2005) p.S143F mutation in lamin A/C: a new phenotype combining myopathy and progeria. Ann. Neurol. 57, 148-151
43. Madej-Pilarczyk, A., Kmiec, T., Fidzianska, A., Rekawek, J., Niebroj-Dobosz, I., Turska-Kmiec, A., Nestorowicz, K., Jozwiak, S. and Hausmanowa-Petrusewicz, I. (2008) Progeria caused by a rare LMNA mutation p.S143F associated with mild myopathy and atrial fibrillation. Eur. J. Paediatr. Neurol. 12, 427-430
44. Zirn, B., Kress, W., Grimm, T., Berthold, L.D., Neubauer, B., Kuchelmeister, K., Muller, U. and Hahn, A. (2008) Association of homozygous LMNA mutation R471C with new phenotype: mandibuloacral dysplasia, progeria, and rigid spine muscular dystrophy. Am. J. Med. Genet. A 146A, 1049-1054
45. Liang, L., Zhang, H. and Gu, X. (2009) Homozygous LMNA mutation R527C in atypical Hutchinson-Gilford progeria syndrome: evidence for autosomal recessive inheritance. Acta Paediatr. 98, 1365-1368
46. Cao, H. and Hegele, R.A. (2003) LMNA is mutated in Hutchinson-Gilford progeria (MIM 176670) but not in Wiedemann-Rautenstrauch progeroid syndrome (MIM 264090). J. Hum. Genet. 48, 271-274
47. Fukuchi, K., Katsuya, T., Sugimoto, K., Kuremura, M., Kim, H.D., Li, L. and Ogihara, T. (2004) LMNA mutation in a 45 year old Japanese subject with Hutchinson-Gilford progeria syndrome. J. Med. Genet. 41, e67
48. Shalev, S.A., De Sandre-Giovannoli, A., Shani, A.A. and Lévy, N. (2007) An association of Hutchinson-Gilford progeria and malignancy. Am. J. Med. Genet. A 143A, 1821-1826
49. Shackleton, S., Smallwood, D.T., Clayton, P., Wilson, L.C., Agarwal, A.K., Garg, A. and Trembath, R.C. (2005) Compound heterozygous ZMPSTE24 mutations reduce prelamin A processing and result in a severe progeroid phenotype. J. Med. Genet. 42, e36
50. Denecke, J., Brune, T., Feldhaus, T., Robenek, H., Kranz, C., Auchus, R.J., Agarwal, A.K. and Marquardt, T. (2006) A homozygous ZMPSTE24 null mutation in combination with a heterozygous mutation in the LMNA gene causes Hutchinson-Gilford progeria syndrome (HGPS): insights into the pathophysiology of HGPS. Hum. Mutat. 27, 524-531