An accumulation of non-farnesylated prelamin A causes cardiomyopathy but not progeria

Human Molecular Genetics

Volumn 19, Issue 13, 2010, Pages 2682-2694

  Davies, Brandon S J ^a   Barnes II, Richard H ^a   Tu, Yiping ^a   Ren, Shuxun ^a   Andres, Douglas A ^b   Peter Spielmann, H ^b   Lammerding, Jan ^c   Wang, Yibin ^a   Young, Stephen G ^a   Fong, Loren G ^a  

^a UNIVERSITY OF CALIFORNIA   (United States)

^b UNIVERSITY OF KENTUCKY   (United States)

^c BRIGHAM AND WOMEN S HOSPITAL   (United States)

Author keywords

[No Author keywords available]

Indexed keywords

LAMIN; LAMIN C; PRELAMIN A; UNCLASSIFIED DRUG; LAMIN A; NUCLEAR PROTEIN; PROTEIN PRECURSOR;

ANIMAL CELL; ANIMAL EXPERIMENT; ANIMAL MODEL; ANIMAL TISSUE; ARTICLE; CARDIOMYOPATHY; CELL NUCLEUS; CONTROLLED STUDY; CYTOPLASM; FEMALE; MALE; MOUSE; MUTANT; NONHUMAN; PRIORITY JOURNAL; PROGERIA; PROTEIN LOCALIZATION; PROTEIN PROCESSING; RISK FACTOR; WILD TYPE; ANIMAL; FIBROBLAST; GENE TARGETING; GENETICS; METABOLISM; MOUSE STRAIN; PATHOLOGY; PROTEIN PRENYLATION;

MUS;

ANIMALS; CARDIOMYOPATHIES; FIBROBLASTS; GENE KNOCK-IN TECHNIQUES; LAMIN TYPE A; MICE; MICE, INBRED STRAINS; MODELS, ANIMAL; NUCLEAR PROTEINS; PROGERIA; PROTEIN PRECURSORS; PROTEIN PRENYLATION;

EID: 77954159278     PISSN: 09646906     EISSN: 14602083     Source Type: Journal    
DOI: 10.1093/hmg/ddq158     Document Type: Article

References (46)

1. Casey, P.J. (1992) Biochemistry of protein prenylation. J. Lipid Res., 33, 1731-1740.
2. Casey, P.J. and Seabra, M.C. (1996) Protein prenyltransferases. J. Biol. Chem., 271, 5289-5292.
3. Clarke, S. (1992) Protein isoprenylation and methylation at carboxyl-terminal cysteine residues. Annu. Rev. Biochem., 61, 355-386.
4. 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.
5. Sinensky, M., Fantle, K., Trujillo, M., McLain, T., Kupfer, A. and Dalton, M. (1994) The processing pathway of prelamin A. J. Cell Sci., 107,61-67.
6. Bergo, M.O., Gavino, B., Ross, J., Schmidt, W.K., Hong, C., Kendall, L.V., Mohr, A., Meta, M., Genant, H., Jiang, Y. et al. (2002) Zmpste24 deficiency in mice causes spontaneous bone fractures, muscle weakness, and a prelamin A processing defect. Proc. Natl Acad. Sci. USA, 99, 13049-13054.
7. Corrigan, D.P., Kuszczak, D., Rusinol, A.E., Thewke, D.P., Hrycyna, C.A., Michaelis, S. and Sinensky, M.S. (2005) Prelamin A endoproteolytic processing in vitro by recombinant Zmpste24. Biochem. J., 387, 129-138.
8. Fong, L.G., Ng, J.K., Meta, M., CotÇ, N., Yang, S.H., Stewart, C.L., Sullivan, T., Burghardt, A., Majumdar, S., Reue, K. et al. (2004) Heterozygosity for Lmna deficiency eliminates the progeria-like phenotypes in Zmpste24-deficient mice. Proc. Natl Acad. Sci. USA, 101, 18111-18116.
9. Pendas, A.M., Zhou, Z., Cadinanos, J., Freije, J.M.P., Wang, J., Hultenby, K., Astudillo, A., Wernerson, A., Rodriguez, F., Tryggvason, K. et al. (2002) Defective prelamin A processing and muscular and adipocyte alterations in Zmpste24 metalloproteinase-deficient mice. Nat. Genet., 31, 94-99.
10. 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.
11. 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. USA, 104, 4955-4960.
12. 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.
13. De Sandre-Giovannoli, A., Bernard, R., Cau, P., Navarro, C., Amiel, J., Boccaccio, I., Lyonnet, S., Stewart, C.L., Munnich, A., Le Merrer, M. et al. (2003) Lamin A truncation in Hutchinson-Gilford progeria. Science, 300, 2055.
14. 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. USA, 102, 12879-12884.
15. 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.
16. Mallampalli, M.P., Huyer, G., Bendale, P., Gelb, M.H. and Michaelis, S. (2005) Inhibiting farnesylation reverses the nuclear morphology defect in a HeLa cell model for Hutchinson-Gilford progeria syndrome. Proc. Natl Acad. Sci. USA, 102, 14416-14421.
17. 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. USA, 102, 12873-12878.
18. Yang, S.H., Bergo, M.O., Toth, J.I., Qiao, X., Hu, Y., Sandoval, S., Meta, M., Bendale, P., Gelb, M.H., Young, S.G. et al. (2005) Blocking protein farnesyltransferase improves nuclear blebbing in mouse fibroblasts with a targeted Hutchinson-Gilford progeria syndrome mutation. Proc. Natl Acad. Sci. USA, 102, 10291-10296.
19. 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.
20. Yang, S.H., Chang, S.Y., Andres, D.A., Spielmann, H.P., Young, S.G. and Fong, L.G. (2010) Assessing the efficacy of protein farnesyltransferase inhibitors in mouse models of progeria. J. Lipid Res., 51, 400-405.
21. Yang, S.H., Qiao, X., Fong, L.G. and Young, S.G. (2008) Treatment with a farnesyltransferase inhibitor improves survival in mice with a Hutchinson-Gilford progeria syndrome mutation. Biochim. Biophys. Acta, 1781, 36-39.
22. Kieran, M.W., Gordon, L. and Kleinman, M. (2007) New approaches to progeria. Pediatrics, 120, 834-841.
23. Verstraeten, V.L.R.M., Broers, J.L.V., van Steensel, M.A.M., Zinn-Justin, S., Ramaekers, F.C.S., Steijlen, P.M., Kamps, M., Kuijpers, H.J.H., Merckx, D., Smeets, H.J.M. et al. (2006) Compound heterozygosity for mutations in LMNA causes a progeria syndrome without prelamin A accumulation. Hum. Mol. Genet., 15, 2509-2522.
24. Troutman, J.M., Roberts, M.J., Andres, D.A. and Spielmann, H.P. (2005) Tools to analyze protein farnesylation in cells. Bioconjug. Chem., 16, 1209-1217.
25. Lowes, B.D., Minobe, W., Abraham, W.T., Rizeq, M.N., Bohlmeyer, T.J., Quaife, R.A., Roden, R.L., Dutcher, D.L., Robertson, A.D., Voelkel, N.F. et al. (1997) Changes in gene expression in the intact human heart. Downregulation of alpha-myosin heavy chain in hypertrophied, failing ventricular myocardium. J. Clin. Invest., 100, 2315-2324.
26. Arimura, T., Helbling-Leclerc, A., Massart, C., Varnous, S., Niel, F., Lacene, E., Fromes, Y., Toussaint, M., Mura, A.M., Keller, D.I. et al. (2005) Mouse model carrying H222P-Lmna mutation develops muscular dystrophy and dilated cardiomyopathy similar to human striated muscle laminopathies. Hum. Mol. Genet., 14, 155-169.
27. DeBusk, F.L. (1972) The Hutchinson-Gilford progeria syndrome. Report of 4 cases and review of the literature. J. Pediatr., 80, 697-724.
28. Fernandez-Palazzi, F., McLaren, A.T. and Slowie, D.F. (1992) Report on a case of Hutchinson-Gilford progeria, with special reference to orthopedic problems. Eur. J. Pediatr. Surg., 2, 378-382.
29. Bonne, G., Barletta, M.R.D., Varnous, S., Becane, H.-M., Hammouda, E.-H., Merlini, L., Muntoni, F., Greenberg, C.R., Gary, F., Urtizberea, J.-A. et al. (1999) Mutations in the gene encoding lamin A/C cause autosomal dominant Emery-Dreifuss muscular dystrophy. Nat. Genet., 21, 285-288.
30. Muchir, A., Bonne, G., van der Kooi, A.J., van Meegen, M., Baas, F., Bolhuis, P.A., de Visser, M. and Schwartz, K. (2000) Identification of mutations in the gene encoding lamins A/C in autosomal dominant limb girdle muscular dystrophy with atrioventricular conduction disturbances (LGMD1B). Hum. Mol. Genet., 9, 1453-1459.
31. Vytopil, M., Benedetti, S., Ricci, E., Galluzzi, G., Dello Russo, A., Merlini, L., Boriani, G., Gallina, M., Morandi, L., Politano, L. et al. (2003) Mutation analysis of the lamin A/C gene (LMNA) among patients with different cardiomuscular phenotypes. J. Med. Genet., 40, e132-e132.
32. Mounkes, L.C., Kozlov, S.V., Rottman, J.N. and Stewart, C.L. (2005) Expression of an LMNA-N195K variant of A-type lamins results in cardiac conduction defects and death in mice. Hum. Mol. Genet., 14, 2167-2180.
33. Muchir, A., Pavlidis, P., Decostre, V., Herron, A.J., Arimura, T., Bonne, G. and Worman, H.J. (2007) Activation of MAPK pathways links LMNA mutations to cardiomyopathy in Emery-Dreifuss muscular dystrophy. J. Clin. Invest., 117, 1282-1293.
34. Lee, R., Chang, S.Y., Trinh, H., Tu, Y., White, A.C., Davies, B.S., Bergo, M.O., Fong, L.G., Lowry, W.E. and Young, S.G. (2010) Genetic studies on the functional relevance of the protein prenyltransferases in skin keratinocytes. Hum. Mol. Genet., 19, 1603-1617.
35. Maurer-Stroh, S., Koranda, M., Benetka, W., Schneider, G., Sirota, F.L. and Eisenhaber, F. (2007) Towards complete sets of farnesylated and geranylgeranylated proteins. PLoS Comput. Biol., 3, e66.
36. Reid, T.S., Terry, K.L., Casey, P.J. and Beese, L.S. (2004) Crystallographic analysis of CaaX prenyltransferases complexed with substrates defines rules of protein substrate selectivity. J. Mol. Biol., 343, 417-433.
37. Mijimolle, N., Velasco, J., Dubus, P., Guerra, C., Weinbaum, C.A., Casey, P.J., Campuzano, V. and Barbacid, M. (2005) Protein farnesyltransferase in embryogenesis, adult homeostasis, and tumor development. Cancer Cell, 7, 313-324.
38. Fong, L.G., Ng, J.K., Lammerding, J., Vickers, T.A., Meta, M., CotÇ, N., Gavino, B., Qiao, X., Chang, S.Y., Young, S.R. et al. (2006) Prelamin A and lamin A appear to be dispensable in the nuclear lamina. J. Clin. Invest., 116, 632-634.
39. Sullivan, T., Escalante-Alcalde, D., Bhatt, H., Anver, M., Bhat, N., Nagashima, K., Stewart, C.L. and Burke, B. (1999) Loss of A-type lamin expression compromises nuclear envelope integrity leading to muscular dystrophy. J. Cell Biol., 147, 913-920.
40. Beck, L.A., Hosick, T.J. and Sinensky, M. (1988) Incorporation of a product of mevalonic acid metabolism into proteins of Chinese hamster ovary cell nuclei. J. Cell Biol., 107, 1307-1316.
41. Lutz, R.J., Trujillo, M.A., Denham, K.S., Wenger, L. and Sinensky, M. (1992) Nucleoplasmic localization of prelamin A: implications for prenylation-dependent lamin A assembly into the nuclear lamina. Proc. Natl Acad. Sci. USA, 89, 3000-3004.
42. Hennekes, H. and Nigg, E.A. (1994) 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., 107, 1019-1029.
43. 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.
44. Leung, G.K., Schmidt, W.K., Bergo, M.O., Gavino, B., Wong, D.H., Tam, A., Ashby, M.N., Michaelis, S. and Young, S.G. (2001) Biochemical studies of Zmpste24-deficient mice. J. Biol. Chem., 276, 29051-29058.
45. Dalton, M. and Sinensky, M. (1995) Expression systems for nuclear lamin proteins: farnesylation in assembly of nuclear lamina. In Patrick, J.C. and Janice, E.B. (eds), Methods in Enzymology. Academic Press, San Diego, CA, USA, Vol. 250, pp. 134-148.
46. Lammerding, J., Fong, L.G., Ji, J.Y., Reue, K., Stewart, C.L., Young, S.G. and Lee, R.T. (2006) Lamins A and C but not lamin B1 regulate nuclear mechanics. J. Biol. Chem., 281, 25768-25780.