Increasing the length of progerin's isoprenyl anchor does not worsen bone disease or survival in mice with Hutchinson-Gilford progeria syndrome

Journal of Lipid Research

Volumn 50, Issue 1, 2009, Pages 126-134

  Davies, Brandon S J ^a   Yang, Shao H ^a   Farber, Emily ^a   Lee, Roger ^a   Buck, Suzanne B ^b   Andres, Douglas A ^c   Spielmann, H Peter ^c   Agnew, Brian J ^b   Tamanoi, Fuyuhiko ^a   Fong, Loren G ^a   Young, Stephen G ^a  

^a UNIVERSITY OF CALIFORNIA   (United States)

^b MOLECULAR PROBES INC   (United States)

^c UNIVERSITY OF KENTUCKY   (United States)

Author keywords

Farnesylation; Geranylgeranylation; Lamin A; Lamin C; Posttranslational modifications; Progeria; Protein prenylation

Indexed keywords

FARNESYL DIPHOSPHATE; GERANYLGERANYL PYROPHOSPHATE; LAMIN A; LAMIN C; LIPID; NUCLEAR PROTEIN; PROGERIN; UNCLASSIFIED DRUG; PRELAMIN A; PROTEIN PRECURSOR;

ANIMAL CELL; ANIMAL EXPERIMENT; ANIMAL MODEL; ARTICLE; BONE DISEASE; CELL LABELING; CELL MEMBRANE; CELL METABOLISM; CELL NUCLEUS; CONTROLLED STUDY; DISEASE SEVERITY; EMBRYO; FEMALE; MALE; MOUSE; NONHUMAN; PATHOGENESIS; PHENOTYPE; PRIORITY JOURNAL; PROGERIA; PROTEIN EXPRESSION; PROTEIN SYNTHESIS; PROTEIN TARGETING; STEADY STATE; SURVIVAL RATE; ANIMAL; BIOLOGICAL MODEL; CHEMISTRY; GENETICS; GENOTYPE; METABOLISM; MOLECULAR GENETICS; NUCLEOTIDE SEQUENCE; PATHOLOGY; PHYSIOLOGY; SYNDROME; TISSUE DISTRIBUTION; TRANSGENIC MOUSE;

ANIMALS; BASE SEQUENCE; BONE DISEASES; GENOTYPE; LAMIN TYPE A; LIPIDS; MICE; MICE, TRANSGENIC; MODELS, BIOLOGICAL; MODELS, GENETIC; MOLECULAR SEQUENCE DATA; NUCLEAR PROTEINS; PROGERIA; PROTEIN PRECURSORS; SYNDROME; TISSUE DISTRIBUTION;

EID: 63449124344     PISSN: 00222275     EISSN: 15397262     Source Type: Journal    
DOI: 10.1194/jlr.M800424-JLR200     Document Type: Article

References (37)

1. Debusk, F. L. 1972. The Hutchinson-Gilford progeria syndrome. J. Pediatr. 80: 697-724.
2. Merideth, M. A., L. B. Gordon, S. Clauss, V. Sachdev, A. C. Smith, M. B. Perry, C. C. Brewer, C. Zalewski, H. J. Kim, B. Solomon, et al. 2008. Phenotype and course of Hutchinson-Gilford progeria syndrome. N. Engl. J. Med. 358: 592-604.
3. Eriksson, M., W. T. Brown, L. B. Gordon, M. W. Glynn, J. Singer, L. Scott, M. R. Erdos, C. M. Robbins, T. Y. Moses, P. Berglund, et al. 2003. Recurrent de novo point mutations in lamin A cause Hutchinson-Gilford progeria syndrome. Nature. 423: 293-298.
4. Lin, F., and H. J. Worman. 1993. Structural organization of the human gene encoding nuclear lamin A and nuclear lamin C. J. Biol. Chem. 268: 16321-16326.
5. Yang, S. H., M. O. Bergo, J. I. Toth, X. Qiao, Y. Hu, S. Sandoval, M. Meta, P. Bendale, M. H. Gelb, S. G. Young, 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.
6. Goldman, R. D., D. K. Shumaker, M. R. Erdos, M. Eriksson, A. E. Goldman, L. B. Gordon, Y. Gruenbaum, S. Khuon, M. Mendez, R. Varga, et al. 2004. Accumulation of mutant lamin A causes progressive changes in nuclear architecture in Hutchinson-Gilford progeria syndrome. Proc. Natl. Acad. Sci. USA. 101: 8963-8968.
7. Yang, S. H., M. Meta, X. Qiao, D. Frost, J. Bauch, C. Coffinier, S. Majumdar, M. O. Bergo, S. G. Young, and L. G. Fong. 2006. Treatment with a protein farnesyltransferase inhibitor improves disease phenotypes in mice with a targeted Hutchinson-Gilford progeria syndrome mutation. J. Clin. Invest. 116: 2115-2121.
8. Young, S. G., L. G. Fong, and S. Michaelis. 2005. Prelamin A, Zmpste24, misshapen cell nuclei, and progeria - New evidence suggesting that protein farnesylation could be important for disease pathogenesis. J. Lipid Res. 46: 2531-2558.
9. Dechat, T., T. Shimi, S. A. Adam, A. E. Rusinol, D. A. Andres, H. P. Spielmann, M. S. Sinensky, and R. D. Goldman. 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.
10. Fong, L., D. Frost, M. Meta, X. Qiao, S. Yang, C. Coffinier, and S. Young. 2006. A protein farnesyltransferase inhibitor ameliorates disease in a mouse model of progeria. Science. 311: 1621-1623.
11. Yang, S. H., X. Qiao, L. G. Fong, and S. G. Young. 2008. Treatment with a farnesyltransferase inhibitor improves survival in mice with a Hutchinson-Gilford progeria syndrome mutation. Biochim. Biophys. Acta. 1781: 36-39.
12. Silvius, J. R., and F. l'Heureux. 1994. Fluorimetric evaluation of the affinities of isoprenylated peptides for lipid bilayers. Biochemistry. 33: 3014-3022.
13. Zhang, F. L., and P. J. Casey. 1996. Protein prenylation: molecular mechanisms and functional consequences. Annu. Rev. Biochem. 65: 241-269.
14. Bergo, M. O., B. Gavino, J. Ross, W. K. Schmidt, C. Hong, L. V. Kendall, A. Mohr, M. Meta, H. Genant, Y. Jiang, 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.
15. Fong, L. G., J. K. Ng, M. Meta, N. Cote, S. H. Yang, C. L. Stewart, T. Sullivan, A. Burghardt, S. Majumdar, K. Reue, et al. 2004. Heterozygosity for Lmna deficiency eliminates the progeria-like phenotypes in Zmpste24-deficient mice. Proc. Natl. Acad. Sci. USA. 101: 18111-18116.
16. Toth, J. I., S. H. Yang, X. Qiao, A. P. Beigneux, M. H. Gelb, C. L. Moulson, J. H. Miner, S. G. Young, and L. G. Fong. 2005. Blocking protein farnesyltransferase improves nuclear shape in fibroblasts from humans with progeroid syndromes. Proc. Natl. Acad. Sci. USA. 102: 12873-12878.
17. Fong, L. G., J. K. Ng, J. Lammerding, T. A. Vickers, M. Meta, N. Cote, B. Gavino, X. Qiao, S. Y. Chang, S. R. Young, et al. 2006. Prelamin A and lamin A appear to be dispensable in the nuclear lamina. J. Clin. Invest. 116: 743-752.
18. Yang, S. H., X. Qiao, E. Farber, S. Y. Chang, L. G. Fong, and S. G. Young. 2008. Eliminating the synthesis of mature lamin A reduces disease phenotypes in mice carrying a Hutchinson-Gilford progeria syndrome allele. J. Biol. Chem. 283: 7094-7099.
19. Troutman, J. M., M. J. Roberts, D. A. Andres, and H. P. Spielmann. 2005. Tools to analyze protein farnesylation in cells. Bioconjug. Chem. 16: 1209-1217.
20. Coffinier, C., S. E. Hudon, R. Lee, E. A. Farber, C. Nobumori, J. H. Miner, D. A. Andres, H. P. Spielmann, C. A. Hrycyna, L. G. Fong, et al. 2008. A potent HIV protease inhibitor, darunavir, does not inhibit ZMPSTE24 or lead to an accumulation of farnesyl-prelamin A in cells. J. Biol. Chem. 283: 9797-9804.
21. Dalton, M., and M. Sinensky. 1995. Expression systems for nuclear lamin proteins: farnesylation in assembly of nuclear lamina. In Methods Enzymol. J. C. Patrick and E. B. Janice, editors. Academic Press. 134-148.
22. Clarke, S., J. P. Vogel, R. J. Deschenes, and J. Stock. 1988. Posttranslational modification of the Ha-ras oncogene protein: evidence for a third class of protein carboxyl methyltransferases. Proc. Natl. Acad. Sci. USA. 85: 4643-4647.
23. Farnsworth, C. C., S. L. Wolda, M. H. Gelb, and J. A. Glomset. 1989. Human lamin B contains a farnesylated cysteine residue. J. Biol. Chem. 264: 20422-20429.
24. Yamane, H. K., C. C. Farnsworth, H. Xie, W. Howald, B. K-K. Fung, S. Clarke, M. H. Gelb, and J. A. Glomset. 1990. Brain G protein γ subunits contain an all-trans-geranylgeranyl-cysteine methyl ester at their carboxyl termini. Proc. Natl. Acad. Sci. USA. 87: 5868-5872.
25. Meta, M., S. H. Yang, M. O. Bergo, L. G. Fong, and S. G. Young. 2006. Protein farnesyltransferase inhibitors and progeria. Trends Mol. Med. 12: 480-487.
26. Moulson, C. L., L. G. Fong, J. M. Gardner, E. A. Farber, G. Go, A. Passariello, D. K. Grange, S. G. Young, and J. H. Miner. 2007. Increased progerin expression associated with unusual LMNA mutations causes severe progeroid syndromes. Hum. Mutat. 28: 882-889.
27. Seabra, M. C., Y. K. Ho, and J. S. Anant. 1995. Deficient geranylgeranylation of Ram/Rab27 in choroideremia. J. Biol. Chem. 270: 24420-24427.
28. Storch, S., S. Pohl, A. Quitsch, K. Falley, and T. Braulke. 2007. C-terminal prenylation of the CLN3 membrane glycoprotein is required for efficient endosomal sorting to lysosomes. Traffic. 8: 431-444.
29. Smithies, O., and N. Maeda. 1995. Gene targeting approaches to complex genetic diseases: atherosclerosis and essential hypertension. Proc. Natl. Acad. Sci. USA. 92: 5266-5272.
30. Fujino, M., and C. Kitada. 1980. Biological activity of synthetic analogs of tremeogen A-10. Naturwissenschaften. 67: 406-408.
31. Cox, A. D., M. M. Hisaka, J. E. Buss, and C. J. Der. 1992. Specific isoprenoid modification is required for function of normal, but not oncogenic, Ras protein. Mol. Cell. Biol. 12: 2606-2615.
32. Matsuda, T., Y. Hashimoto, H. Ueda, T. Asano, Y. Matsuura, T. Doi, T. Takao, Y. Shimonishi, and Y. Fukada. 1998. Specific isoprenyl group linked to transducin gamma-subunit is a determinant of its unique signaling properties among G-proteins. Biochemistry. 37: 9843-9850.
33. Kolb, H., M. Finn, and K. Sharpless. 2001. Click Chemistry: diverse chemical function from a few good reactions. Angew. Chem. 40: 2004-2021.
34. Tornoe, C. W., C. Christensen, and M. Meldal. 2002. Peptidotriazoles on solid phase: [1,2,3]-triazoles by regiospecific copper(i)-catalyzed 1,3-dipolar cycloadditions of terminal alkynes to azides. J. Org. Chem. 67: 3057-3064.
35. Varela, I., S. Pereira, A. P. Ugalde, C. L. Navarro, M. F. Suarez, P. Cau, J. Cadinanos, F. G. Osorio, N. Foray, J. Cobo, et al. 2008. Combined treatment with statins and aminobisphosphonates extends longevity in a mouse model of human premature aging. Nat. Med. 14: 767-772.
36. Whyte, D. B., P. Kirschmeier, T. N. Hockenberry, I. Nunez-Oliva, L. James, J. J. Catino, W. R. Bishop, and J-K. Pai. 1997. K- and N-Ras are geranylgeranylated in cells treated with farnesyl protein transferase inhibitors. J. Biol. Chem. 272: 14459-14464.
37. Delbarre, E., M. Tramier, M. Coppey-Moisan, C. Gaillard, J. C. Courvalin, and B. Buendia. 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.