Expansion of protein farnesyltransferase specificity using "tunable" active site interactions: Development of bioengineered prenylation pathways

Journal of Biological Chemistry

Volumn 287, Issue 45, 2012, Pages 38090-38100

  Hougland, James L ^a,b   Gangopadhyay, Soumyashree A ^b   Fierke, Carol A ^a  

^a UNIVERSITY OF MICHIGAN   (United States)

^b SYRACUSE UNIVERSITY   (United States)

Author keywords

[No Author keywords available]

Indexed keywords

ACTIVE SITE; ACTIVE SITE RESIDUES; IN-VITRO; PEPTIDE RECOGNITION; PRENYLATION; PROTEIN FARNESYLTRANSFERASE; SUBSTRATE SELECTIVITY;

BIOCHEMISTRY; BIOLOGY;

PROTEINS;

ALANINE; HISTIDINE; PROTEIN FARNESYLTRANSFERASE; VALINE;

AMINO ACID SEQUENCE; AMINO ACID SUBSTITUTION; ARTICLE; BIOENGINEERING; CARBOXY TERMINAL SEQUENCE; CATALYSIS; CELL FUNCTION; ENZYME ACTIVITY; ENZYME SPECIFICITY; ENZYME SUBSTRATE; IN VITRO STUDY; IN VIVO STUDY; NONHUMAN; PRIORITY JOURNAL; PROTEIN EXPRESSION; PROTEIN FUNCTION; PROTEIN INTERACTION; PROTEIN PRENYLATION; PROTEIN PROCESSING; SIGNAL TRANSDUCTION; SITE DIRECTED MUTAGENESIS; WILD TYPE;

ALKYL AND ARYL TRANSFERASES; AMINO ACID SEQUENCE; BINDING SITES; BIOCATALYSIS; CATALYTIC DOMAIN; HEK293 CELLS; HUMANS; KINETICS; MODELS, MOLECULAR; MOLECULAR SEQUENCE DATA; MUTAGENESIS, SITE-DIRECTED; PEPTIDES; PROTEIN ENGINEERING; PROTEIN PRENYLATION; PROTEIN STRUCTURE, TERTIARY; PROTEIN SUBUNITS; SEQUENCE HOMOLOGY, AMINO ACID; SIGNAL TRANSDUCTION; SUBSTRATE SPECIFICITY; TRYPTOPHAN;

EID: 84868308586     PISSN: 00219258     EISSN: 1083351X     Source Type: Journal    
DOI: 10.1074/jbc.M112.404954     Document Type: Article

References (50)

1. Walsh, C. T. (2005) Posttranslational Modification of Proteins: Expanding Naturés Inventory, Roberts and Co. Publishers, Englewood, CO
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. Benetka, W., Koranda, M., and Eisenhaber, F. (2006) Protein Prenylation. An (almost) comprehensive overview on discovery, history, enzymology, and significance in physiology and disease. Monatshefte für Chemie 137, 1241-1281 (Pubitemid 44701778)
4. Casey, P. J. (1994) Lipid modifications of G proteins. Curr. Opin. Cell Biol. 6, 219-225 (Pubitemid 24109779)
5. Marshall, C. J. (1993) Protein prenylation. A mediator of protein-protein interactions. Science 259, 1865-1866 (Pubitemid 23124458)
6. Berndt, N., Hamilton, A. D., and Sebti, S. M. (2011) Targeting protein prenylation for cancer therapy. Nat. Rev. Cancer 11, 775-791
7. Onono, F. O., Morgan, M. A., Spielmann, H. P., Andres, D. A., Subramanian, T., Ganser, A., and Reuter, C. W. (2010) A tagging-via-substrate approach to detect the farnesylated proteome using two-dimensional electrophoresis coupled with Western blotting. Mol. Cell. Proteomics 9, 742-751
8. Kho, Y., Kim, S. C., Jiang, C., Barma, D., Kwon, S. W., Cheng, J., Jaunbergs, J., Weinbaum, C., Tamanoi, F., Falck, J., and Zhao, Y. (2004) A taggingvia- substrate technology for detection and proteomics of farnesylated proteins. Proc. Natl. Acad. Sci. U.S.A. 101, 12479-12484 (Pubitemid 39122049)
9. 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 (Pubitemid 39296875)
10. Maurer-Stroh, S., and Eisenhaber, F. (2005) Refinement and prediction of protein prenylation motifs. Genome Biol. 6, R55
11. Hougland, J. L., Hicks, K. A., Hartman, H. L., Kelly, R. A., Watt, T. J., and Fierke, C. A. (2010) Identification of novel peptide substrates for protein farnesyltransferase reveals two substrate classes with distinct sequence selectivities. J. Mol. Biol. 395, 176-190
12. London, N., Lamphear, C. L., Hougland, J. L., Fierke, C. A., and Schueler- Furman, O. (2011) Identification of a novel class of farnesylation targets by structure-based modeling of binding specificity. PLoS Comput. Biol. 7, e1002170
13. Krzysiak, A. J., Aditya, A. V., Hougland, J. L., Fierke, C. A., and Gibbs, R. A. (2010) Synthesis and screening of a CaaL peptide library versus FTase reveals a surprising number of substrates. Bioorg. Med. Chem. Lett. 20, 767-770
14. Krzysiak, A. J., Scott, S. A., Hicks, K. A., Fierke, C. A., and Gibbs, R. A. (2007) Evaluation of protein farnesyltransferase substrate specificity using synthetic peptide libraries. Bioorg. Med. Chem. Lett. 17, 5548-5551 (Pubitemid 47391326)
15. Omer, C. A., Kral, A. M., Diehl, R. E., Prendergast, G. C., Powers, S., Allen, C. M., Gibbs, J. B., and Kohl, N. E. (1993) Characterization of recombinant human farnesyl-protein transferase. Cloning, expression, farnesyl diphosphate binding, and functional homology with yeast prenyl-protein transferases. Biochemistry 32, 5167-5176 (Pubitemid 23162086)
16. Reiss, Y., Seabra, M. C., Armstrong, S. A., Slaughter, C. A., Goldstein, J. L., and Brown, M. S. (1991) Nonidentical subunits of p21H-ras farnesyltransferase. Peptide binding and farnesyl pyrophosphate carrier functions. J. Biol. Chem. 266, 10672-10677 (Pubitemid 21906854)
17. Moores, S. L., Schaber, M. D., Mosser, S. D., Rands, E., O'Hara, M. B., Garsky, V. M., Marshall, M. S., Pompliano, D. L., and Gibbs, J. B. (1991) Sequence dependence of protein isoprenylation. J. Biol. Chem. 266, 14603-14610 (Pubitemid 21907546)
18. Fu, H. W., and Casey, P. J. (1999) Enzymology and biology of CaaX protein prenylation. Recent Prog. Horm. Res. 54, 315-342
19. 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
20. Hicks, K. A., Hartman, H. L., and Fierke, C. A. (2005) Upstream polybasic region in peptides enhances dual specificity for prenylation by both farnesyltransferase and geranylgeranyltransferase type I. Biochemistry 44, 15325-15333 (Pubitemid 41681466)
21. Hougland, J. L., Lamphear, C. L., Scott, S. A., Gibbs, R. A., and Fierke, C. A. (2009) Context-dependent substrate recognition by protein farnesyltransferase. Biochemistry 48, 1691-1701
22. Terry, K. L., Casey, P. J., and Beese, L. S. (2006) Conversion of protein farnesyltransferase to a geranylgeranyltransferase. Biochemistry 45, 9746-9755 (Pubitemid 44257422)
23. Nguyen, U. T., Guo, Z., Delon, C., Wu, Y., Deraeve, C., Fränzel, B., Bon, R. S., Blankenfeldt, W., Goody, R. S., Waldmann, H., Wolters, D., and Alexandrov, K. (2009) Analysis of the eukaryotic prenylome by isoprenoid affinity tagging. Nat. Chem. Biol. 5, 227-235
24. Reigard, S. A., Zahn, T. J., Haworth, K. B., Hicks, K. A., Fierke, C. A., and Gibbs, R. A. (2005) Interplay of isoprenoid and peptide substrate specificity in protein farnesyltransferase. Biochemistry 44, 11214-11223 (Pubitemid 41209057)
25. Hightower, K. E., Casey, P. J., and Fierke, C. A. (2001) Farnesylation of nonpeptidic thiol compounds by protein farnesyltransferase. Biochemistry 40, 1002-1010 (Pubitemid 32109320)
26. Goldstein, J. L., Brown, M. S., Stradley, S. J., Reiss, Y., and Gierasch, L. M. (1991) Nonfarnesylated tetrapeptide inhibitors of protein farnesyltransferase. J. Biol. Chem. 266, 15575-15578 (Pubitemid 21907690)
27. Riddles, P. W., Blakeley R. L., and Zerner, B. (1979) Ellman's reagent: 5, 5'-dithiobis(2-nitrobenzoic acid). A reexamination. Anal. Biochem. 94, 75-81 (Pubitemid 9170207)
28. Zimmerman, K. K., Scholten, J. D., Huang, C. C., Fierke, C. A., and Hupe, D. J. (1998) High level expression of rat farnesyl:protein transferase in Escherichia coli as a translationally coupled heterodimer. Protein Expr. Purif. 14, 395-402 (Pubitemid 29020374)
29. Cassidy, P. B., Dolence, J. M., and Poulter, C. D. (1995) Continuous fluorescence assay for protein prenyltransferases. Methods Enzymol. 250, 30-43
30. Fersht, A. (1999) Structure and Mechanism in Protein Science, pp. 110-111, W. H. Freeman and Co., New York
31. Zamyatnin, A. A. (1972) Protein Volume in Solution. Prog. Biophys. Mol. Biol. 24, 107-123
32. Patrick, W. M., Firth, A. E., and Blackburn, J. M. (2003) User-friendly algorithms for estimating completeness and diversity in randomized protein- encoding libraries. Protein Eng. 16, 451-457 (Pubitemid 36917359)
33. Pickett, J. S., Bowers, K. E., Hartman, H. L., Fu, H. W., Embry, A. C., Casey, P. J., and Fierke, C. A. (2003) Kinetic studies of protein farnesyltransferase mutants establish active substrate conformation. Biochemistry 42, 9741-9748 (Pubitemid 36993147)
34. Tong, H., Wiemer, A. J., Neighbors, J. D., and Hohl, R. J. (2008) Quantitative determination of farnesyl and geranylgeranyl diphosphate levels in mammalian tissue. Anal. Biochem. 378, 138-143
35. Roberts, P. J., Mitin, N., Keller, P. J., Chenette, E. J., Madigan, J. P., Currin, R. O., Cox, A. D., Wilson, O., Kirschmeier, P., and Der, C. J. (2008) Rho Family GTPase modification and dependence on CAAX motif-signaled posttranslational modification. J. Biol. Chem. 283, 25150-25163
36. Bergo, M. O., Leung, G. K., Ambroziak, P., Otto, J. C., Casey, P. J., and Young, S. G. (2000) Targeted inactivation of the isoprenylcysteine carboxyl methyltransferase gene causes mislocalization of K-Ras in mammalian cells. J. Biol. Chem. 275, 17605-17610 (Pubitemid 30430806)
37. Chen, Z., Otto, J. C., Bergo, M. O., Young, S. G., and Casey, P. J. (2000) The C-terminal polylysine region and methylation of K-Ras are critical for the interaction between K-Ras and microtubules. J. Biol. Chem. 275, 41251-41257 (Pubitemid 32054958)
38. Merzlyak, E. M., Goedhart, J., Shcherbo, D., Bulina, M. E., Shcheglov, A. S., Fradkov, A. F., Gaintzeva, A., Lukyanov, K. A., Lukyanov, S., Gadella, T. W., and Chudakov, D. M. (2007) Bright monomeric red fluorescent protein with an extended fluorescence lifetime. Nat Methods 4, 555-557 (Pubitemid 47214772)
39. Kurth, T., Ullmann, D., Jakubke, H. D., and Hedstrom, L. (1997) Converting trypsin to chymotrypsin. Structural determinants of S1' specificity. Biochemistry 36, 10098-10104 (Pubitemid 27357718)
40. Marino, F., Pelc, L. A., Vogt, A., Gandhi, P. S., and Di Cera, E. (2010) Engineering thrombin for selective specificity toward proteinCand PAR1. J. Biol. Chem. 285, 19145-19152
41. Varadarajan, N., Rodriguez, S., Hwang, B. Y., Georgiou, G., and Iverson, B. L. (2008) Highly active and selective endopeptidases with programmed substrate specificities. Nat. Chem. Biol. 4, 290-294 (Pubitemid 351550889)
42. Hedstrom, L. (1996) Trypsin. A case study in the structural determinants of enzyme specificity. Biol. Chem. 377, 465-470 (Pubitemid 26383896)
43. Wouters, M. A., Liu, K., Riek, P., and Husain, A. (2003) A despecialization step underlying evolution of a family of serine proteases. Mol. Cell 12, 343-354 (Pubitemid 37238921)
44. Erijman, A., Aizner, Y., and Shifman, J. M. (2011) Multispecific recognition. Mechanism, evolution, and design. Biochemistry 50, 602-611
45. Khersonsky, O., and Tawfik, D. S. (2010) Enzyme promiscuity. A mechanistic and evolutionary perspective. Annu. Rev. Biochem. 79, 471-505
46. Hightower, K. E., Huang, C. C., Casey, P. J., and Fierke, C. A. (1998) H-Ras peptide and protein substrates bind protein farnesyltransferase as an ionized thiolate. Biochemistry 37, 15555-15562 (Pubitemid 28516020)
47. Crowell, D. N. (2000) Functional implications of protein isoprenylation in plants. Prog Lipid Res 39, 393-408
48. Hanker, A. B., Mitin, N., Wilder, R. S., Henske, E. P., Tamanoi, F., Cox, A. D., and Der, C. J. (2010) Differential requirement of CAAX-mediated posttranslational processing for Rheb localization and signaling. Oncogene 29, 380-391
49. Allal, C., Favre, G., Couderc, B., Salicio, S., Sixou, S., Hamilton, A. D., Sebti, S. M., Lajoie-Mazenc, I., and Pradines, A. (2000) RhoA prenylation is required for promotion of cell growth and transformation and cytoskeleton organization but not for induction of serum response element transcription. J. Biol. Chem. 275, 31001-31008
50. Allal, C., Pradines, A., Hamilton, A. D., Sebti, S. M., and Favre, G. (2002) Farnesylated RhoB prevents cell cycle arrest and actin cytoskeleton disruption caused by the geranylgeranyltransferase I Inhibitor GGTI-298. Cell Cycle 1, 430-437