Heterologous expression studies of Saccharomyces cerevisiae reveal two distinct trypanosomatid CaaX protease activities and identify their potential targets

Eukaryotic Cell

Volumn 8, Issue 12, 2009, Pages 1891-1900

  Mokry, David Z ^a   Manandhar, Surya P ^a   Chicola, Kristen A ^a   Santangelo, George M ^b   Schmidt, Walter K ^a  

^a University of Georgia ^*  (United States)

^b The University of Southern Mississippi   (United States)

Author keywords

[No Author keywords available]

Indexed keywords

GREEN FLUORESCENT PROTEIN; GUANOSINE TRIPHOSPHATASE; HEAT SHOCK PROTEIN 40; PROTEINASE; PROTEINASE INHIBITOR; PROTOZOAL PROTEIN; SACCHAROMYCES CEREVISIAE PROTEIN; YDJ1 PROTEIN, S CEREVISIAE;

ANIMAL; ARTICLE; CELL MEMBRANE; CYTOLOGY; DRUG EFFECT; ENZYME SPECIFICITY; ENZYMOLOGY; FUNGAL GENE; GENETICS; IC 50; METABOLISM; NUCLEOTIDE SEQUENCE; PHENOTYPE; PROTEIN PROCESSING; PROTEIN TRANSPORT; SACCHAROMYCES CEREVISIAE; TEMPERATURE; TRYPANOSOMA BRUCEI;

ANIMALS; CELL MEMBRANE; DNA MUTATIONAL ANALYSIS; ENDOPEPTIDASES; GENES, MATING TYPE, FUNGAL; GREEN FLUORESCENT PROTEINS; GTP PHOSPHOHYDROLASES; HSP40 HEAT-SHOCK PROTEINS; INHIBITORY CONCENTRATION 50; PHENOTYPE; PROTEASE INHIBITORS; PROTEIN PROCESSING, POST-TRANSLATIONAL; PROTEIN TRANSPORT; PROTOZOAN PROTEINS; SACCHAROMYCES CEREVISIAE; SACCHAROMYCES CEREVISIAE PROTEINS; SUBSTRATE SPECIFICITY; TEMPERATURE; TRYPANOSOMA BRUCEI BRUCEI;

EUKARYOTA; SACCHAROMYCES CEREVISIAE; TRYPANOSOMA BRUCEI; TRYPANOSOMATIDAE;

EID: 73349096578     PISSN: 15359778     EISSN: None     Source Type: Journal    
DOI: 10.1128/EC.00169-09     Document Type: Article

References (53)

1. Anderson, J. L., B. S. Henriksen, R. A. Gibbs, and C. A. Hrycyna. 2005. The isoprenoid substrate specificity of isoprenylcysteine carboxylmethyltransferase: development of novel inhibitors. J. Biol. Chem. 280:29454-29461.
2. Ashby, M., D. King, and J. Rine. 1992. Endoproteolytic processing of a farnesylated peptide in vitro. Proc. Natl. Acad. Sci. USA 89:4613-4617.
3. Boyartchuk, V. L., M. N. Ashby, and J. Rine. 1997. Modulation of Ras and a-factor function by carboxy1-terminal proteolysis. Science 275:1796-1800.
4. Bracha, K., M. Lavy, and S. Yalovsky. 2002. The Arabidopsis AtSTE24 is a CAAX protease with broad substrate specificity. J. Biol. Chem., 277:29856-29864.
5. Cadiñanos, J., W. K. Schmidt, A. Fueyo, I. Varela, C. Lopez-Otin, and J. M. Freije. 2003. Identification, functional expression and enzymic analysis of two distinct CaaX proteases from Caenorhabditis elegans. Biochem. J. 370: 1047-1054.
6. Cadiñanos, J., I. Varela, D. Mandel, W. K. Schmidt, A. Díaz-Perales, C. López-Otín, and F. JMP. 2003. AtFACE-2, a prenylated-protein protease from Arabidopsis thaliana related to Ras converting enzymes. J. Biol. Chem. 278:42091-42097.
7. Caplan, A. J., J. Tsai, P. J. Casey, and M. G. Douglas. 1992. Farnesylation of Ydj1p is required for function at elevated growth temperatures in Saccharomyces cerevisiae. J. Biol. Chem. 267:18890-18895.
8. Caplin, B. E., L. A. Hettich, and M. S. Marshall. 1994. Substrate characterization of the Saccharomyces cerevisiae protein f arnesyltransferase and type-I protein geranylgeranyltransferase. Biochim. Biophys. Acta 1205:39-48.
9. Cox, A., and C. Der. 2002. Farnesyltransferase inhibitors: promises and realities. Curr. Opin. Pharmacol. 2:388-393.
10. Dai, Q., E. Choy, V. Chiu, J. Romano, S. R. Slivka, S. A. Steltz, S. Michaelis, and M. R. Philips. 1998. Human prenylcysteine carboxyl mcthyltransferase is in the endoplasmic reticulum. J. Biol. Chem. 273:15030-15034.
11. Dolence, E. K., J. M. Dolence, and C. D. Poulter. 2000. Solid-phase synthesis of a farnesylated CaaX peptide library: inhibitors of the Ras CaaX endoprotease. J. Comb. Chem. 2:522-536.
12. Dolence, J. M., L. E. Steward, E. K. Dolence, D. H. Wong, and C. D. Poulter. 2000. Studies with recombinant Saccharomyces cerevisiae CaaX prenyl protease Rce1p. Biochemistry 39:4096-4104.
13. Eastman, R. T., F. S. Buckner, K. Yokoyama, M. H. GeIb, and W. C. Van Voorhis. 2006. Thematic review series: lipid posttranslational modifications: fighting parasitic disease by blocking protein farnesylation. J. Lipid Res. 47:233-240.
14. Elble, R. 1992. A simple and efficient procedure for transformation of yeasts. BioTechniques 13:18-20.
15. Esteva, M. I., K. Kettler, C. Maidana, L. Fichera, A. M. Ruiz, E. J. Bontempi, B. Andersson, H. M. Dahse, P. Haebel, R. Ortmann, G. Klebe, and M. Schlitzer. 2005. Benzophenone-based farnesyltransferase inhibitors with high activity against Trypanosoma cruzi. J. Med. Chem. 48:7186-7191.
16. Farh, L., D. Mitchell, and R. Deschenes. 1995. Farnesylation and proteolysis are sequential, but distinct steps in the CaaX box modification pathway. Arch, Biochem, Biophys. 318:113-121.
17. Field, M. C. 2005. Signalling the genome: the Ras-like small GTPase family of trypanosomatids. Trends Parasitol. 21:447-450.
18. 2-terminal processing of the yeast a-factor precursor. J. Cell Biol. 136: 271-285.
19. Giaever, G., A. M. Chu, L. Ni, C. Connelly, L. Riles, S. Veronneau, S. Dow, A. Lucau-Danila, K. Anderson, B. Andre, A. P. Arkin, A. Astromoff, M. El-Bakkoury, R. Bangham, R. Benito, S. Brachat, S. Campanaro, M. Curtiss, K. Davis, A. Deutschbauer, K. D. Entian, P. Flaherty, F. Foury, D. J. Garfinkel, M. Gerstein, D. Gotte, U. Guidener, J. H. Hegemann, S. Hempel, Z. Herman, D. F. Jaramillo, D. E. Kelly, S. L. Kelly, P. Kotter, D. LaBonte, D. C. Lamb, N. Lan, H. Liang, H. Liao, L. Liu, C. Luo, M. Lussier, R. Mao, P. Menard, S. L. Ooi, J. L. Revuelta, C. J. Roberts, M. Rose, P. RossMacdonald, B. Scherens, G. Schimmack, B. Shafer, D. D. Shoemaker, S. Sookhai-Mahadeo, R. K. Storms, J. N. Strathern, G. Valle, M. Voet, G. Volckaert, C. Y. Wang, T. R. Ward, J. Wilhelmy, E. A. Winzeler, Y. Yang, G. Yen, E. Youngman, K. Yu, H. Bussey, J. D. Boeke, M. Snyder, P. Philippsen, R. W. Davis, and M. Johnston. 2002. Functional profiling of. the Saccharomyces cerevisiae genome. Nature 418:387-391.
20. Gillespie, J. R., K. Yokoyama, K. Lu, R. T. Eastman, J. G. Bollinger, W. C. Van Voorhis, M. H. Gelb, and F. S. Buckner. 2007. C-terminal proteolysis of prenylated proteins in trypanosomatids and RNA interference of enzymes required for the posttranslational processing pathway of farnesylated proteins. Mol. Biochem. Parasitol. 153:115-124.
21. Hollander, I., E. Frommer, and R. Mallon. 2000. Human ras-converting enzyme (hRCE1.) endoproteolytic activity on K-ras-derived peptides. Anal. Biochem. 286:129-137.
22. Hrycyna, C. A., and S. Clarke. 1992. Maturation of isoprenylated proteins in Saccharomyces cerevisiae. J. Biol. Chem. 267:10457- 10464.
23. Hrycyna, C. A., S. K. Sapperstein, S. Clarke, and S. Michaelis. 1991. The Saccharomyces cerevisiae STE14 gene encodes a methyl transferase that mediates C-terminal. methylation of a-factor and RAS proteins. EMBO J. 10: 1699-1709.
24. Jang, G. F., K. Yokoyama, and M. H. Gelb. 1993. A prenylated proteinspecific endoprotease in rat liver microsomes that produces a carboxylterminal tripeptide. Biochemistry 32:9500-9507.
25. Kim, S., A. Lapham, C. Freedman, T. Reed, and W. Schmidt. 2005. Yeast as a tractable genetic system for functional studies of the insulin-degrading enzyme. J. Biol. Chem. 280:27481-27490.
26. Lane, K. T., and L. S. Beese. 2006. Thematic review series: lipid posttranslational. modifications: structural biology of protein farnesyltransferase and geranylgeranyltransferase type I. J. Lipid Res. 47:681-699.
27. Leung, K. F., R. Baron, B. R. Ali, A. I. Magee, and M. C. Seabra. 2007. Rab GTPases containing a CAAX. motif are processed post- geranylgeranylation by proteolysis and methylation. J. Biol. Chem. 282:1487-1497.
28. Manandhar, S. P., E. R. Hildebrandt, and W. K. Schmidt. 2007. Smallmolecule inhibitors of the Rcelp CaaX. protease. J. Biomol. Screen. 12:983-993.
29. Marizen, M. R., S. M. McCraith, S. L. Spinelu, F. M. Torres, S. Fields, E. J. Grayhack, and E. M. Phizicky. 1999. A biochemical genomics approach for identifying genes by the activity of their products. Science 286:1153-1155.
30. Michaelis, S., and I. Herskowitz. 1988. The a-factor pheromone of Saccharomyces cerevisiae is essential, for mating. Mol. Cell. Biol. 8:1309-1318.
31. Moores, S. L., M. D. Schaber, S. D. Mosser, E. Rands, M. B. O'Hara, V. M. Garsky, M. S. Marshall, D. L. Pompliano, and J. B. Gibbs. 1991. Sequence dependence of protein isoprenylation. J. Biol. Chem. 266:14603-14610.
32. Ohkanda, J., J. W. Lockman, K. Yokoyama, M. H. Gelb, S. L. Croft, H. Kendrick, M. I. Harrell, J. E. Feagin, M. A. Blaskovich, S. M. Sebti, and A. D. Hamilton. 2001. Peptidomimetic inhibitors of protein farnesyltransferase show potent antimalarial activity. Bioorg. Med. Chem. Lett. 11:761-764.
33. Oldenburg, K. R., K. T. Vo, S. Michaelis, and C. Paddon. 1997. Recombination-mediated PCR-directed plasmid construction in vivo in yeast. Nucleic Acids Res. 25:451-452.
34. Otto, J. C, E. Kim, S. G. Young, and P. J. Casey. 1999. Cloning and characterization of a mammalian prenyl protein-specific protease. J. Biol. Chem. 274:8379-8382.
35. Pei, J., and N. V. Grishin. 2001. Type II CAAX prenyl endopeptidases belong to a novel, superfamily of putative membrane-bound metalloproteases. Trends Biochem. Sci. 26:275-277.
36. Plummer, L. J., E. R. Hildebrandt, S. B. Porter, V. A. Rogers, J. McCracken, and W. K. Schmidt. 2006. Mutational analysis of the ras converting enzyme reveals a requirement for glutamate and histidine residues. J. Biol. Chem. 281:4596-4605.
37. Porter, S. B., E. R. Hildebrandt, S. R. Breevoort, D. Z. Mokry, T. M. Dore, and W. K. Schmidt. 2007. Inhibition of the CaaX proteases Rce1p and Ste24p by peptidyl (acyloxy)methyl ketones. Biochim. Biophys. Acta 1773: 853-862.
38. Romano, J. D., W. K. Schmidt, and S. Michaelis. 1998. The Saccharomyces cerevisiae prenylcysteine carboxyl methltransferase Ste14p is in the endoplasmic reticulum membrane. Mol. Biol. Cell 9:2231-2247.
39. Schlitzer, M., A. Winter-Vann, and P. J. Casey. 2001. Non-peptidic, nonprenyllc inhibitors of the prenyl protein-specific protease Reel. Bioorg. Med. Chem. Lett. 11:425-427.
40. Schmidt, W. K., A. Tam, K. Fujimura-Kamada, and S. Michaelis. 1998. Endoplasmic reticulum membrane localization of. Rce1p and Ste24p, yeast proteases involved in carboxy1-terminal CAAX. protein processing and ammoterminal a-factor cleavage. Proc. Natl. Acad. Sci. USA 95:11175- 11180.
41. Schmidt, W. K., A. Tam, and S. Michaelis. 2000. Reconstitution, of the Ste24p-dependent N-terminal proteolytic step in yeast a-factor biogenesis. J. Biol. Chem. 275:6227-6233.
42. Sikorski, R. S., and P. Hieter. 1989. A system of shuttle vectors and yeast host strains designed for efficient manipulation of DNA in Saccharomyces cerevisiae. Genetics 122:19-27.
43. Siliciano, P., and K. Tatchell. 1984. Transcription and regulatory signals at the mating type locus in yeast. Cell 37:969-978.
44. Reference deleted.
45. 2terminal. proteolysis and COOH-terminal CAAX processing. J. Cell Biol. 1142:635-649.
46. 2-termmal processing of the yeast a-factor precursor. J. Biol. Chem. 276:46798- 46806.
47. Trueblood, C. E., V. L. Boyartchuk, E. A. Picologlou, D. Rozema, C. D. Poulter, and J. Rine. 2000. The CaaX proteases, Afc1p and Rce1p, have overlapping but distinct substrate specificities. Mol. Cell. Biol. 20:4381-4392.
48. Winter-Vann, A. M., R. A. Baron, W. Wong, J. dela Cruz, J. D. York, D. M. Gooden, M. O. Bergo, S. G. Young, E. J. Toone, and P. J. Casey. 2005. A small-molecule inhibitor of isoprenylcysteine carboxy1 methyltransferase with antitumor activity in cancer cells. Proc. Natl. Acad. Sci. USA 102:4336-4341.
49. Winter-Vann, A. M., and P. J. Casey. 2005. Post-prenylation- processing enzymes as new targets in oncogenesis. Nat. Rev. Cancer 5:405-412.
50. Young, S. G., P. Ambroziak, E. Kim, and S. Clarke. 2001. Postisoprenylation protein processing: CXXX (CaaX) endoproteases and isoprenylcysteine carboxyl methyltransferase, p. 155-213. In F. Tamanoi. and D. S. Sigman (ed.), The enzymes, vol. XXI. Academic Press, Inc., New York, NY.
51. Young, S. G., M. Meta, S. H. Yang, and L. G. Fong. 2006. Prelamin A farnesylation and progeroid syndromes. J. Biol. Chem. 281:39741-39745.
52. Zhang, Y., G. Nijbroek, M. L. Sullivan, A. A. McCracken, S. C. Watkins, S. Michaelis, and J. L. Brodsky. 2001. Hsp70 molecular chaperone facilitates endoplasmic reticulum-associated protein degradation of cystic fibrosis transmembrane conductance regulator in yeast. Mol. Biol. Cell 12:1303-1314.
53. Zhu, K., A. D. Hamilton, and S. M. Sebti. 2003. Farnesyltransferase inhibitors as anticancer agents: current status. Curr. Opin. Investig. Drugs 4:1428-1435.