Control of RhoA methylation by carboxylesterase I

Journal of Biological Chemistry

Volumn 288, Issue 26, 2013, Pages 19177-19183

  Cushman, Ian ^a,c   Cushman, Stephanie M ^a   Potter, Philip M ^b   Casey, Patrick J ^a,c  

^a DUKE UNIVERSITY MEDICAL CENTER   (United States)

^b ST JUDE CHILDREN S RESEARCH HOSPITAL   (United States)

^c DUKE NUS MEDICAL SCHOOL   (Singapore)

Author keywords

[No Author keywords available]

Indexed keywords

CARBOXYL TERMINUS; CARBOXYLESTERASES; CELL MORPHOLOGY; ISOPRENYLCYSTEINE CARBOXYLMETHYLTRANSFERASE; MDA-MB-231 CELLS; NORMAL CONDITION; PRENYLATION;

ALKYLATION; CELLS; CYTOLOGY; METHYLATION; MORPHOLOGY;

PROTEINS;

CARBOXYLESTERASE; CARBOXYLESTERASE I; PROTEIN S ISOPRENYLCYSTEINE O METHYLTRANSFERASE; RHOA GUANINE NUCLEOTIDE BINDING PROTEIN; UNCLASSIFIED DRUG;

ANIMAL CELL; ARTICLE; CARBOXY TERMINAL SEQUENCE; CELL STRAIN MDA MB 231; CELL STRUCTURE; CONTROLLED STUDY; EMBRYO; ENZYME ACTIVATION; ENZYME ACTIVITY; ENZYME REGULATION; GENE SILENCING; HUMAN; HUMAN CELL; MOUSE; NONHUMAN; PRIORITY JOURNAL; PROTEIN ANALYSIS; PROTEIN FAMILY; PROTEIN FUNCTION; PROTEIN METHYLATION; PROTEIN PRENYLATION; PROTEIN PROCESSING; SIGNAL TRANSDUCTION;

CARBOXYLESTERASE; CARBOXYLESTERASE 1; ISOPRENYLCYSTEINE CARBOXYLMETHYLTRANSFERASE; METHYLATION; POST-TRANSLATIONAL MODIFICATION; PRENYLATION; PROTEIN ISOPRENYLATION; PROTEIN METHYLATION; RHOA;

AMINO ACID MOTIFS; ANIMALS; CARBOXYLESTERASE; CELL LINE; CELL LINE, TUMOR; GENE EXPRESSION REGULATION, ENZYMOLOGIC; HUMANS; ISOELECTRIC FOCUSING; METHYLATION; MICE; MICROSCOPY, FLUORESCENCE; PROTEIN METHYLTRANSFERASES; PROTEIN PRENYLATION; PROTEIN PROCESSING, POST-TRANSLATIONAL; RHOA GTP-BINDING PROTEIN; RNA, SMALL INTERFERING; SIGNAL TRANSDUCTION;

EID: 84879588015     PISSN: 00219258     EISSN: 1083351X     Source Type: Journal    
DOI: 10.1074/jbc.M113.467407     Document Type: Article

References (34)

1. Glomset, J. A., and Farnsworth, C. C. (1994) Role of protein modification reactions in programming interactions between ras-related GTPases and cell membranes. Annu. Rev. Cell Biol. 10, 181-205 (Pubitemid 24372820)
2. Zhang, F. L., and Casey, P. J. (1996) Protein prenylation: molecular mechanisms and functional consequences. Annu. Rev. Biochem. 65, 241-269 (Pubitemid 26250610)
3. Casey, P. J., and Seabra, M. C. (1996) Protein prenyltransferases. J. Biol. Chem. 271, 5289-5292 (Pubitemid 26083855)
4. Ashby, M. N. (1998) CaaX converting enzymes. Curr. Opin. Lipidol. 9, 99-102
5. Young, S. G., Ambroziak, P., Kim, E., and Clarke, S. (2001) Postisoprenylation protein processing: CXXX (CaaX) endoproteases and isoprenylcysteine carboxyl methyltransferase. The Enzymes (Tamanoi, F., and Sigman, D. S., eds) 3rd Ed., vol. 21, pp. 156-213, Academic Press, San Diego, CA
6. Doll, R. J., Kirschmeier, P., and Bishop, W. R. (2004) Farnesyltransferase inhibitors as anticancer agents: critical crossroads. Curr. Opin. Drug Discov. Devel. 7, 478-486 (Pubitemid 44383554)
7. Gelb, M. H., Brunsveld, L., Hrycyna, C. A., Michaelis, S., Tamanoi, F., Van Voorhis, W. C., and Waldmann, H. (2006) Therapeutic intervention based on protein prenylation and associated modifications. Nat. Chem. Biol. 2, 518-528 (Pubitemid 44413234)
8. Winter-Vann, A. M., and Casey, P. J. (2005) Post-prenylation processing enzymes as new targets in oncogenesis. Nat. Rev. Cancer 5, 405-412 (Pubitemid 40637832)
9. Wright, L. P., and Philips, M. R. (2006) Thematic review series: lipid post-translational modifications. CAAX modification and membrane targeting of Ras. J. Lipid Res. 47, 883-891
10. Cushman, I., and Casey, P. J. (2009) Role of isoprenylcysteine carboxylmethyltransferase-catalyzed methylation in Rho function and migration. J. Biol. Chem. 284, 27964-27973
11. Winter-Vann, A. M., Baron, R. A., Wong, W., dela Cruz, J., York, J. D., Gooden, D. M., Bergo, M. O., Young, S. G., Toone, E. J., and Casey, P. J. (2005) A small-molecule inhibitor of isoprenylcysteine carboxyl methyltransferase with antitumor activity in cancer cells. Proc. Natl. Acad. Sci. U.S.A. 102, 4336-4341 (Pubitemid 40397112)
12. Baron, R. A., and Casey, P. J. (2004) Analysis of the kinetic mechanism of recombinant human isoprenylcysteine carboxylmethyltransferase (Icmt). BMC Biochem. 5, 19
13. Baron, R. A., Peterson, Y. K., Otto, J. C., Rudolph, J., and Casey, P. J. (2007) Time-dependent inhibition of isoprenylcysteine carboxyl methyltransferase by indole-based small molecules. Biochemistry 46, 554-560 (Pubitemid 46105444)
14. Otto, J. C., Kim, E., Young, S. G., and Casey, P. J. (1999) Cloning and characterization of a mammalian prenyl protein-specific protease. J. Biol. Chem. 274, 8379-8382 (Pubitemid 29164625)
15. Morton, C. L., and Potter, P. M. (2000) Comparison of Escherichia coli, Saccharomyces cerevisiae, Pichia pastoris, Spodoptera frugiperda, and COS7 cells for recombinant gene expression. Application to a rabbit liver carboxylesterase. Mol. Biotechnol. 16, 193-202 (Pubitemid 32217198)
16. Meigs, T. E., Juneja, J., Demarco, C. T., Stemmle, L. N., Kaplan, D. D., and Casey, P. J. (2005) Selective uncoupling of Gα 12 from Rho-mediated signaling. J. Biol. Chem.
17. Brüsehaber, E., Böttcher, D., and Bornscheuer, U. T. (2009) Insights into the physiological role of pig liver esterase: isoenzymes show differences in the demethylation of prenylated proteins. Bioorg. Med. Chem. 17, 7878-7883
18. Deem, A. K., Bultema, R. L., and Crowell, D. N. (2006) Prenylcysteine methylesterase in Arabidopsis thaliana. Gene 380, 159-166 (Pubitemid 44345116)
19. Huizinga, D. H., Omosegbon, O., Omery, B., and Crowell, D. N. (2008) Isoprenylcysteine methylation and demethylation regulate abscisic acid signaling in Arabidopsis. Plant Cell 20, 2714-2728 (Pubitemid 352844586)
20. Oboh, O. T., and Lamango, N. S. (2008) Liver prenylated methylated protein methyl esterase is the same enzyme as Sus scrofa carboxylesterase. J. Biochem. Mol. Toxicol. 22, 51-62 (Pubitemid 351360162)
21. Wang, M., Tan, W., Zhou, J., Leow, J., Go, M., Lee, H. S., and Casey, P. J. (2008) A small molecule inhibitor of isoprenylcysteine carboxymethyltransferase induces autophagic cell death in PC3 prostate cancer cells. J. Biol. Chem. 283, 18678-18684
22. Wahlstrom, A. M., Cutts, B. A., Liu, M., Lindskog, A., Karlsson, C., Sjogren, A. K., Andersson, K. M., Young, S. G., and Bergo, M. O. (2008) Inactivating Icmt ameliorates K-RAS-induced myeloproliferative disease. Blood 112, 1357-1365
23. Bergo, M. O., Leung, G. K., Ambroziak, P., Otto, J. C., Casey, P. J., Gomes, A. Q., Seabra, M. C., and Young, S. G. (2001) Isoprenylcysteine carboxyl methyltransferase deficiency in mice. J. Biol. Chem. 276, 5841-5845
24. Lu, Q., Harrington, E. O., Hai, C. M., Newton, J., Garber, M., Hirase, T., and Rounds, S. (2004) Isoprenylcysteine carboxyl methyltransferase modulates endothelial monolayer permeability: involvement of RhoA carboxyl methylation. Circ. Res. 94, 306-315 (Pubitemid 38240721)
25. Rounds, S., Lu, Q., Harrington, E. O., Newton, J., and Casserly, B. (2008) Pulmonary endothelial cell signaling and function. Trans. Am. Clin. Climatol. Assoc. 119, 155-167; discussion 167-159
26. Jayaram, B., Syed, I., Singh, A., Subasinghe, W., Kyathanahalli, C. N., and Kowluru, A. (2011) Isoprenylcysteine carboxyl methyltransferase facilitates glucose-induced Rac1 activation, ROS generation and insulin secretion in INS 832/13 β-cells. Islets 3, 48-57
27. Backlund, P. S., Jr. (1997) Post-translational processing of RhoA. Carboxyl methylation of the carboxyl-terminal prenylcysteine increases the half-life of Rhoa. J. Biol. Chem. 272, 33175-33180
28. Berg, T. J., Gastonguay, A. J., Lorimer, E. L., Kuhnmuench, J. R., Li, R., Fields, A. P., and Williams, C. L. (2010) Splice variants of SmgGDS control small GTPase prenylation and membrane localization. J. Biol. Chem. 285, 35255-35266
29. Holmes, R. S., Wright, M. W., Laulederkind, S. J., Cox, L. A., Hosokawa, M., Imai, T., Ishibashi, S., Lehner, R., Miyazaki, M., Perkins, E. J., Potter, P. M., Redinbo, M. R., Robert, J., Satoh, T., Yamashita, T., Yan, B., Yokoi, T., Zechner, R., and Maltais, L. J. (2010) Recommended nomenclature for five mammalian carboxylesterase gene families: human, mouse, and rat genes and proteins. Mamm. Genome 21, 427-441
30. Ross, M. K., and Crow, J. A. (2007) Human carboxylesterases and their role in xenobiotic and endobiotic metabolism. J. Biochem. Mol. Toxicol. 21, 187-196 (Pubitemid 350194379)
31. Harrington, E. O., Newton, J., Morin, N., and Rounds, S. (2004) Barrier dysfunction and RhoA activation are blunted by homocysteine and adenosine in pulmonary endothelium. Am. J. Physiol. Lung Cell Mol. Physiol. 287, L1091-1097 (Pubitemid 39507184)
32. Michaelson, D., Ali, W., Chiu, V. K., Bergo, M., Silletti, J., Wright, L., Young, S. G., and Philips, M. (2005) Postprenylation CAAX Processing Is Required for Proper Localization of Ras but Not Rho GTPases. Mol. Biol. Cell 4, 1606-1616 (Pubitemid 40471934)
33. Cushman, I., and Casey, P. J. (2011) RHO methylation matters: a role for isoprenylcysteine carboxylmethyltransferase in cell migration and adhesion. Cell Adh. Migr. 5, 11-15
34. Garcia-Mata, R., Boulter, E., and Burridge, K. (2011) The 'invisible hand': regulation of RHO GTPases by RHOGDIs. Nat. Rev. Mol. Cell Biol. 12, 493-504