GGTase-I deficiency reduces tumor formation and improves survival in mice with K-RAS-induced lung cancer

Journal of Clinical Investigation

Volumn 117, Issue 5, 2007, Pages 1294-1304

  Sjogren, Anna Karin M ^a   Andersson, Karin M E ^a   Liu, Meng ^a,b   Cutts, Briony A ^a   Karlsson, Christin ^a   Wahlstrom, Annika M ^a   Dalin, Martin ^a   Weinbaum, Carolyn ^c   Casey, Patrick J ^c   Tarkowski, Andrej ^d   Swolin, Birgitta ^d   Young, Stephen G ^e   Bergo, Martin O ^a  

^a UNIVERSITY OF GOTHENBURG   (Sweden)

^b SHANDONG UNIVERSITY   (China)

^c DUKE UNIVERSITY MEDICAL CENTER   (United States)

^d SAHLGRENSKA UNIVERSITY HOSPITAL   (Sweden)

^e UNIVERSITY OF CALIFORNIA   (United States)

Author keywords

[No Author keywords available]

Indexed keywords

ACTIN; GERANYLGERANYLTRANSFERASE TYPE 1; GERANYLTRANSFERASE; PROTEIN CDC42; RAC1 PROTEIN; RHOA GUANINE NUCLEOTIDE BINDING PROTEIN; UNCLASSIFIED DRUG;

ANIMAL CELL; ANIMAL EXPERIMENT; ANIMAL MODEL; ANIMAL TISSUE; ARTICLE; BONE MARROW CELL; CANCER SURVIVAL; CARCINOGENESIS; CELL MIGRATION; CELL PROLIFERATION; CELL VIABILITY; CONTROLLED STUDY; CYTOSKELETON; ENZYME ACTIVITY; ENZYME DEFICIENCY; ENZYME INHIBITION; FIBROBLAST; GENE EXPRESSION; GENE INACTIVATION; HEMATOPOIETIC CELL; LUNG ALVEOLUS CELL; LUNG CANCER; MALIGNANT TRANSFORMATION; MOUSE; MYELOPOIESIS; MYELOPROLIFERATIVE DISORDER; NONHUMAN; ONCOGENE K RAS; PHENOTYPE; PRIORITY JOURNAL;

ALKYL AND ARYL TRANSFERASES; ANIMALS; GENE SILENCING; LUNG NEOPLASMS; MICE; RAS PROTEINS; SURVIVAL;

EID: 34248177249     PISSN: 00219738     EISSN: 15588238     Source Type: Journal    
DOI: 10.1172/JCI30868     Document Type: Article

References (49)

1. 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.
2. Casey, P.J., and Seabra, M.C. 1996. Protein prenyltransferases. J. Biol. Chem. 271:5289-5292.
3. Yokoyama, K., Goodwin, G.W., Ghomashchi, F., Glomset, J.A., and Gelb, M.H. 1991. A protein geranylgeranyltransferase from bovine brain: implications for protein prenylation specificity. Proc. Natl. Acad. Sci. U. S. A. 88:5302-5306.
4. Therrien, M., et al. 1995. KSR, a novel protein kinase required for RAS signal transduction. Cell. 83:879-888.
5. Ohya, Y., et al. 1991. Yeast CAL1 is a structural and functional homologue to the DPR1 (RAM) gene involved in ras processing. J. Biol. Chem. 266:12356-12360.
6. Ohya, Y., Qadota, H., Anraku, Y., Pringle, J.R., and Botstein, D. 1993. Suppression of yeast geranylgeranyl transferase I defect by alternative prenylation of two target GTPases, Rho1p and Cdc42p. Mol. Biol. Cell. 4:1017-1025.
7. Kelly, R., et al. 2000. Geranylgeranyltransferase I of Candida albicans: null mutants or enzyme inhibitors produce unexpected phenotypes. J. Bacteriol. 182:704-713.
8. Running, M.P., et al. 2004. Enlarged meristems and delayed growth in plp mutants result from lack of CaaX prenyltransferases. Proc. Natl. Acad. Sci. U. S. A. 101:7815-7820.
9. Casey, P.J., Solski, P.A., Der, C.J., and Buss, J.E. 1989. p21ras is modified by a farnesyl isoprenoid. Proc. Natl. Acad. Sci. U. S. A. 86:8323-8327.
10. Kato, K., et al. 1992. Isoprenoid addition to Ras protein is the critical modification for its membrane association and transforming activity. Proc. Natl. Acad. Sci. U. S. A. 89:6403-6407.
11. Kohl, N.E., et al. 1995. Inhibition of farnesyltransferase induces regression of mammary and salivary carcinomas in ras transgenic mice. Nat. Med. 1:792-797.
12. Basso, A.D., Kirschmeier, P., and Bishop, W.R. 2006. Lipid posttranslational modifications. Farnesyl transferase inhibitors. J. Lipid Res. 47:15-31.
13. V12 proteins to farnesyltransferase inhibitors in Rat1 cells. Proc. Natl. Acad. Sci. U. S. A. 93:4454-4458.
14. Waf1/Cip1. Nature. 394:295-299.
15. Clark, E.A., Golub, T.R., Lander, E.S., and Hynes, R.O. 2000. Genomic analysis of metastasis reveals an essential role for RhoC. Nature. 406:532-535.
16. Lim, K.H., et al. 2005. Activation of RalA is critical for Ras-induced tumorigenesis of human cells. Cancer Cell. 7:533-545.
17. Peterson, Y.K., Kelly, P., Weinbaum, C.A., and Casey, P.J. 2006. A novel protein geranylgeranyltransferase-I inhibitor with high potency, selectivity, and cellular activity. J. Biol. Chem. 281:12445-12450.
18. Sun, J., Qian, Y., Hamilton, A.D., and Sebti, S.M. 1998. Both farnesyltransferase and geranylgeranyltransferase I inhibitors are required for inhibition of oncogenic K-Ras prenylation but each alone is sufficient to suppress human tumor growth in nude mouse xenografts. Oncogene. 16:1467-1473.
19. El Oualid, F., Cohen, L.H., van der Marel, G.A., and Overhand, M. 2006. Inhibitors of protein: geranylgeranyl transferases. Curr. Med. Chem. 13:2385-2427.
20. Gelb, M.H., et al. 2006. Therapeutic intervention based on protein prenylation and associated modifications. Nat. Chem. Biol. 2:518-528.
21. Walters, C.E., et al. 2002. Inhibition of Rho GTPases with protein prenyltransferase inhibitors prevents leukocyte recruitment to the central nervous system and attenuates clinical signs of disease in an animal model of multiple sclerosis. J. Immunol. 168:4087-4094.
22. Ye, J., et al. 2003. Disruption of hepatitis C virus RNA replication through inhibition of host protein geranylgeranylation. Proc. Natl. Acad. Sci. U. S. A. 100:15865-15870.
23. Murthi, K.K., et al. 2003. Antifungal activity of a Candida albicans GGTase I inhibitor-alanine conjugate. Inhibition of Rho1p prenylation in C. albicans. Bioorg. Med. Chem. Lett. 13:1935-1937.
24. Lobell, R.B., et al. 2001. Evaluation of farnesyl: protein transferase and geranylgeranyl:protein transferase inhibitor combinations in preclinical models. Cancer Res. 61:8758-8768.
25. Li, X., et al. 2002. Inhibition of protein geranylgeranylation and RhoA/RhoA kinase pathway induces apoptosis in human endothelial cells. J. Biol. Chem. 277:15309-15316.
26. Dan, H.C., et al. 2004. Phosphatidylinositol-3-OH kinase/AKT and survivin pathways as critical targets for geranylgeranyltransferase I inhibitor-induced apoptosis. Oncogene. 23:706-715.
27. Sun, J., et al. 2003. Geranylgeranyltransferase I inhibitor GGTI-2154 induces breast carcinoma apoptosis and tumor regression in H-Ras transgenic mice. Cancer Res. 63:8922-8929.
28. Vogt, A., Sun, J., Qian, Y., Hamilton, A.D., and Sebti, S.M. 1997. The geranylgeranyltransferase-I inhibitor GGTI-298 arrests human tumor cells in G0/G1 and induces p21(WAF1/CIP1/SDI1) in a p53-independent manner. J. Biol. Chem. 272:27224-27229.
29. Zhang, F.L., Moomaw, J.F., and Casey, P.J. 1994. Properties and kinetic mechanism of recombinant mammalian protein geranylgeranyltransferase type I. J. Biol. Chem. 269:23465-23470.
30. Jackson, E.L., et al. 2001. Analysis of lung tumor initiation and progression using conditional expression of oncogenic K-ras. Genes Dev. 15:3243-3248.
31. Clausen, B.E., Burkhardt, C., Reith, W., Renkawitz, R., and Förster, I. 1999. Conditional gene targeting in macrophages and granulocytes using LysMcre mice. Transgenic Res. 8:265-277.
32. Rupec, R.A., et al. 2005. Stroma-mediated dysregulation of myelopoiesis in mice lacking I kappa B alpha. Immunity. 22:479-491.
33. Kimura, A., et al. 2004. SOCS3 is a physiological negative regulator for granulopoiesis and granulocyte colony-stimulating factor receptor signaling. J. Biol. Chem. 279:6905-6910.
34. Herbert, D.R., et al. 2004. Alternative macrophage activation is essential for survival during schistosomiasis and downmodulates T helper 1 responses and immunopathology. Immunity. 20:623-635.
35. Singh, G., Katyal, S.L., Brown, W.E., Collins, D.L., and Mason, R.J. 1988. Pulmonary lysozyme-a secretory protein of type II pneumocytes in the rat. Am. Rev. Respir. Dis. 138:1261-1267.
36. Markart, P., et al. 2004. Comparison of the microbicidal and muramidase activities of mouse lysozyme M and P. Biochem. J. 380:385-392.
37. Kim, C.F., et al. 2005. Mouse models of human non-small-cell lung cancer: raising the bar. Cold Spring Harb. Symp. Quant. Biol. 70:241-250.
38. Adamson, P., Marshall, C.J., Hall, A., and Tilbrook, P.A. 1992. Post-translational modifications of p21rho proteins. J. Biol. Chem. 267:20033-20038.
39. Whyte, D.B., et al. 1997. K- and N-Ras are geranylgeranylated in cells treated with farnesyl protein transferase inhibitors. J. Biol. Chem. 272:14459-14464.
40. Braun, B.S., et al. 2004. Somatic activation of oncogenic Kras in hematopoietic cells initiates a rapidly fatal myeloproliferative disorder. Proc. Natl. Acad. Sci. U. S. A. 101:597-602.
41. Chan, I.T., et al. 2004. Conditional expression of oncogenic K-ras from its endogenous promoter induces a myeloproliferative disease. J. Clin. Invest. 113:528-538. doi:10.1172/JCI200420476.
42. Mijimolle, N., et al. 2005. Protein farnesyltransferase in embryogenesis, adult homeostasis, and tumor development. Cancer Cell. 7:313-324.
43. Silvius, J.R., and l'Heureux, F. 1994. Fluorimetric evaluation of the affinities of isoprenylated peptides for lipid bilayers. Biochemistry. 33:3014-3022.
44. Adnane, J., Bizouarn, F.A., Qian, Y., Hamilton, A.D., and Sebti, S.M. 1998. p21(WAF1/CIP1) is upregulated by the geranylgeranyltransferase I inhibitor GGTI-298 through a transforming growth factor beta- and Sp1-responsive element: involvement of the small GTPase rhoA. Mol. Cell. Biol. 18:6962-6970.
45. Miquel, K., et al. 1997. GGTI-298 induces G0-G1 block and apoptosis whereas FTI-277 causes G2-M enrichment in A549 cells. Cancer Res. 57:1846-1850.
46. Hanks, M., Wurst, W., Anson-Cartwright, L., Auerbach, A.B., and Joyner, A.L. 1995. Rescue of the En-1 mutant phenotype by replacement of En-1 with En-2. Science. 269:679-682.
47. Thissen, J.A., and Casey, P.J. 1996. Kinetics of protein farnesyltransferase: sigmoidal vs hyperbolic behavior as a function of assay conditions. Anal. Biochem. 243:80-85.
48. Bergo, M.O., et al. 2004. Inactivation of Icmt inhibits transformation by oncogenic K-Ras and B-Raf. J. Clin. Invest. 113:539-550. doi:10.1172/JCI200418829.
49. Takeshita, S., Kaji, K., and Kudo, A. 2000. Identification and characterization of the new osteoclast progenitor with macrophage phenotypes being able to differentiate into mature osteoclasts. J. Bone Miner. Res. 15:1477-1488.