Modulation of ras and a-factor function by carboxyl-terminal proteolysis

Science

Volumn 275, Issue 5307, 1997, Pages 1796-1800

  Boyartchuk, Victor L ^a   Ashby, Matthew N ^b   Rine, Jasper ^a  

^a UNIVERSITY OF CALIFORNIA   (United States)

^b Acacia Biosciences Inc   (United States)

Author keywords

[No Author keywords available]

Indexed keywords

MATING HORMONE ALPHA FACTOR; RAS PROTEIN;

ARTICLE; CARBOXY TERMINAL SEQUENCE; NONHUMAN; PRENYLATION; PRIORITY JOURNAL; PROTEIN DEGRADATION; PROTEIN PROCESSING; SACCHAROMYCES CEREVISIAE;

CELL MEMBRANE; ENDOPEPTIDASES; FUNGAL PROTEINS; GENES, FUNGAL; GENES, RAS; LIPOPROTEINS; MEMBRANE PROTEINS; METALLOENDOPEPTIDASES; MUTATION; PROTEIN ISOPRENYLATION; PROTEIN PRECURSORS; PROTEIN PROCESSING, POST-TRANSLATIONAL; RAS PROTEINS; SACCHAROMYCES CEREVISIAE; SACCHAROMYCES CEREVISIAE PROTEINS; SEQUENCE DELETION; SIGNAL TRANSDUCTION; SUBSTRATE SPECIFICITY; ZINC;

SACCHAROMYCES CEREVISIAE;

EID: 0030909336     PISSN: 00368075     EISSN: None     Source Type: Journal    
DOI: 10.1126/science.275.5307.1796     Document Type: Article

References (53)

1. W. R. Schafer and J. Rine, Annu. Rev. Genet. 26, 209 (1992); S. Clarke, Annu. Rev. Biochem. 61, 355 (1992).
2. W. R. Schafer and J. Rine, Annu. Rev. Genet. 26, 209 (1992); S. Clarke, Annu. Rev. Biochem. 61, 355 (1992).
3. F. R. Khosravi et al., Proc. Natl. Acad. Sci. U.S.A. 88, 6264 (1991); B. T. Kinsella and W. A. Maltese, J. Biol. Chem. 267, 3940 (1992); M. C. Seabra, J. L. Goldstein, T. C. Sudhof, M. S. Brown, ibid., p. 14497.
4. F. R. Khosravi et al., Proc. Natl. Acad. Sci. U.S.A. 88, 6264 (1991); B. T. Kinsella and W. A. Maltese, J. Biol. Chem. 267, 3940 (1992); M. C. Seabra, J. L. Goldstein, T. C. Sudhof, M. S. Brown, ibid., p. 14497.
5. F. R. Khosravi et al., Proc. Natl. Acad. Sci. U.S.A. 88, 6264 (1991); B. T. Kinsella and W. A. Maltese, J. Biol. Chem. 267, 3940 (1992); M. C. Seabra, J. L. Goldstein, T. C. Sudhof, M. S. Brown, ibid., p. 14497.
6. A. A. Finegold etal., Proc. Natl. Acad. Sci. U.S.A. 88, 4448 (1991); B. T. Kinsella, R. A. Erdman, W. A. Maltese, ibid., p. 8934.
7. A. A. Finegold etal., Proc. Natl. Acad. Sci. U.S.A. 88, 4448 (1991); B. T. Kinsella, R. A. Erdman, W. A. Maltese, ibid., p. 8934.
8. P. J. Casey, Curr. Opin. Cell. Biol. 6, 219 (1994); J. E. Rothman and F. T. Wieland, Science 272, 227 (1996).
9. P. J. Casey, Curr. Opin. Cell. Biol. 6, 219 (1994); J. E. Rothman and F. T. Wieland, Science 272, 227 (1996).
10. J. F. Hancock, K. Cadwallader, C. J. Marshall, EMBO J. 10, 641 (1991); K. Kato et al., Proc. Natl. Acad. Sci. U.S.A. 89, 6403 (1992); A. D. Cox, M. M. Hisaka, J. E. Buss, C. J. Der, Mol. Cell. Biol. 12, 2606 (1992).
11. J. F. Hancock, K. Cadwallader, C. J. Marshall, EMBO J. 10, 641 (1991); K. Kato et al., Proc. Natl. Acad. Sci. U.S.A. 89, 6403 (1992); A. D. Cox, M. M. Hisaka, J. E. Buss, C. J. Der, Mol. Cell. Biol. 12, 2606 (1992).
12. J. F. Hancock, K. Cadwallader, C. J. Marshall, EMBO J. 10, 641 (1991); K. Kato et al., Proc. Natl. Acad. Sci. U.S.A. 89, 6403 (1992); A. D. Cox, M. M. Hisaka, J. E. Buss, C. J. Der, Mol. Cell. Biol. 12, 2606 (1992).
13. F. Tamanoi, Trends Biochem. Sci. 18, 349 (1993); N. E. Kohl et al., J. Cell Biochem. Suppl. 22, 145 (1995).
14. F. Tamanoi, Trends Biochem. Sci. 18, 349 (1993); N. E. Kohl et al., J. Cell Biochem. Suppl. 22, 145 (1995).
15. W. R. Schafer et al., Science 249, 1133 (1990).
16. L. Gutierrez, A. I. Magee, C. J. Marshall, J. F. Hancock, EMBO J. 8, 1093 (1989); R. S. Marr, L. C. Blair, J. Thorner, J. Biol. Chem. 265, 20057 (1990); A. Fujiyama and F. Tamanoi, ibid., p. 3362; S. D. Perez, B. A. Gilbert, E. W. Tan, R. R. Rando, Biochem. J. 284, 835 (1992); R. C. Stephenson and S. Clarke, J. Biol. Chem. 267, 13314 (1992).
17. L. Gutierrez, A. I. Magee, C. J. Marshall, J. F. Hancock, EMBO J. 8, 1093 (1989); R. S. Marr, L. C. Blair, J. Thorner, J. Biol. Chem. 265, 20057 (1990); A. Fujiyama and F. Tamanoi, ibid., p. 3362; S. D. Perez, B. A. Gilbert, E. W. Tan, R. R. Rando, Biochem. J. 284, 835 (1992); R. C. Stephenson and S. Clarke, J. Biol. Chem. 267, 13314 (1992).
18. L. Gutierrez, A. I. Magee, C. J. Marshall, J. F. Hancock, EMBO J. 8, 1093 (1989); R. S. Marr, L. C. Blair, J. Thorner, J. Biol. Chem. 265, 20057 (1990); A. Fujiyama and F. Tamanoi, ibid., p. 3362; S. D. Perez, B. A. Gilbert, E. W. Tan, R. R. Rando, Biochem. J. 284, 835 (1992); R. C. Stephenson and S. Clarke, J. Biol. Chem. 267, 13314 (1992).
19. L. Gutierrez, A. I. Magee, C. J. Marshall, J. F. Hancock, EMBO J. 8, 1093 (1989); R. S. Marr, L. C. Blair, J. Thorner, J. Biol. Chem. 265, 20057 (1990); A. Fujiyama and F. Tamanoi, ibid., p. 3362; S. D. Perez, B. A. Gilbert, E. W. Tan, R. R. Rando, Biochem. J. 284, 835 (1992); R. C. Stephenson and S. Clarke, J. Biol. Chem. 267, 13314 (1992).
20. L. Gutierrez, A. I. Magee, C. J. Marshall, J. F. Hancock, EMBO J. 8, 1093 (1989); R. S. Marr, L. C. Blair, J. Thorner, J. Biol. Chem. 265, 20057 (1990); A. Fujiyama and F. Tamanoi, ibid., p. 3362; S. D. Perez, B. A. Gilbert, E. W. Tan, R. R. Rando, Biochem. J. 284, 835 (1992); R. C. Stephenson and S. Clarke, J. Biol. Chem. 267, 13314 (1992).
21. M. N. Ashby, D. S. King, J. Rine, Proc. Natl. Acad. Sci. U.S.A. 89, 4613 (1992); Y. T. Ma and R. R. Rando, ibid., p. 6275; C. A. Hrycyna and S. Clarke, J. Biol. Chem. 267, 10457 (1992); G. F. Jang, K. Yokoyama, M. H. Gelb, Biochemistry 32, 9500 (1993).
22. M. N. Ashby, D. S. King, J. Rine, Proc. Natl. Acad. Sci. U.S.A. 89, 4613 (1992); Y. T. Ma and R. R. Rando, ibid., p. 6275; C. A. Hrycyna and S. Clarke, J. Biol. Chem. 267, 10457 (1992); G. F. Jang, K. Yokoyama, M. H. Gelb, Biochemistry 32, 9500 (1993).
23. M. N. Ashby, D. S. King, J. Rine, Proc. Natl. Acad. Sci. U.S.A. 89, 4613 (1992); Y. T. Ma and R. R. Rando, ibid., p. 6275; C. A. Hrycyna and S. Clarke, J. Biol. Chem. 267, 10457 (1992); G. F. Jang, K. Yokoyama, M. H. Gelb, Biochemistry 32, 9500 (1993).
24. M. N. Ashby, D. S. King, J. Rine, Proc. Natl. Acad. Sci. U.S.A. 89, 4613 (1992); Y. T. Ma and R. R. Rando, ibid., p. 6275; C. A. Hrycyna and S. Clarke, J. Biol. Chem. 267, 10457 (1992); G. F. Jang, K. Yokoyama, M. H. Gelb, Biochemistry 32, 9500 (1993).
25. A. Fujiyama, K. Matsumoto, F. Tamanoi, EMBO J. 6, 223 (1987); C. A. Hrycyna, S. K. Sapperstein, S. Clarke, S. Michaelis, ibid. 10, 1699 (1991).
26. A. Fujiyama, K. Matsumoto, F. Tamanoi, EMBO J. 6, 223 (1987); C. A. Hrycyna, S. K. Sapperstein, S. Clarke, S. Michaelis, ibid. 10, 1699 (1991).
27. A. Bender and G. F. Sprague, Cell 47, 929 (1986).
28. ts), JRY5319 (JRY5318 afc1Δ::HIS3), JRY5320 (JRY5318 rce1Δ::TRP1), and JRY5321 (JRY5318 afc1Δ::HIS3 rce1Δ::TRP1). All strains were generated by standard genetic and molecular methods (76).
29. val19 (pJR1040) genes were contained in the 1.9-kb Cla I-Hind III fragment inserted into pRS316 vector. The GFP-RAS2 fusion plasmid was created by subcloning the Bam HI-Sal I fragment containing the open reading frame of RAS2 fused in frame to GFP under control of the glyceraldehyde-3-phosphate dehydrogenase (GPD) promoter {pJW192 [J. L. Whistler, thesis, University of California at Berkeley (1996)]}, into Bam HI-and Sal I-cut YEplac195 vector [R. D. Gietz and A. Sugino, Gene 74, 527 (1988)]. The Rce1p-GFP fusions were constructed by engineering Xba I restriction sites flanking the RCE1 open reading frame by polymerase chain reaction (PCR) amplification with synthetic oligonucleotides (5′-ACGTAAAAATCTAGAAAGGGTTAT-3′ and 5′-AACAGCAATGTCTAGATTCTCAAC-3′). The PCR product was subcloned into an Xba I site of the constructs containing ∼1-kb promoter fragments in front of the GFP open reading fame [GAL1-pACA51, ERG12-pACA5, and MEV1-pACA1 (Acacia Biosciences)].
30. val19 (pJR1040) genes were contained in the 1.9-kb Cla I-Hind III fragment inserted into pRS316 vector. The GFP-RAS2 fusion plasmid was created by subcloning the Bam HI-Sal I fragment containing the open reading frame of RAS2 fused in frame to GFP under control of the glyceraldehyde-3-phosphate dehydrogenase (GPD) promoter {pJW192 [J. L. Whistler, thesis, University of California at Berkeley (1996)]}, into Bam HI-and Sal I-cut YEplac195 vector [R. D. Gietz and A. Sugino, Gene 74, 527 (1988)]. The Rce1p-GFP fusions were constructed by engineering Xba I restriction sites flanking the RCE1 open reading frame by polymerase chain reaction (PCR) amplification with synthetic oligonucleotides (5′-ACGTAAAAATCTAGAAAGGGTTAT-3′ and 5′-AACAGCAATGTCTAGATTCTCAAC-3′). The PCR product was subcloned into an Xba I site of the constructs containing ∼1-kb promoter fragments in front of the GFP open reading fame [GAL1-pACA51, ERG12-pACA5, and MEV1-pACA1 (Acacia Biosciences)].
31. L. J. Heilmeyer et al., Proc. Natl. Acad. Sci. U.S.A. 89, 9554 (1992).
32. E. C. Gaynor, H. S. Te, T. R. Graham, M. Aebi, S. D. Emr, J. Cell Biol. 127, 653 (1994).
33. A null allele of afc1 was constructed by replacing the 218-base pair (bp) Bgl II fragment of AFC1 (GenBank accession Z49617) with a 1764-bp Bam HI fragment containing the yeast HIS3 gene. A deletion of the entire RCE1 gene (GenBank accession Z49260) was created by PCR amplification of the TRP1 coding sequence with synthetic oligonucleotides (5′-CCTTTGATGATTTTATTACCTTTATTTTAAGTTACTAAAATATCGAGATTGTACTGAGAGTGCACC- 3′ and 5′-AAACAGTTGTCATGGAGCCTTCCTGTAATTGCTCATAAGCATGGTGTGCGGTATTTCACACCGC- 3′). The PCR product was used directly in one-step gene replacement to create rce1Δ::TRP1 [R. Rothstein, Methods Enzymol. 194, 281 (1991)].
34. 14C]SAM (M, Met) in 100 mM tris-HCl (pH 7.4), 1 mM PMSF reaction buffer for 1 hour at 370°C. After addition of 50 μl of 1 M NaOH-1% SDS, the amount of newly formed hydrolyzed methyl esters was measured by scintillation counting.
35. V. L. Boyartchuck, M. N. Ashby, J. Rine, data not shown.
36. T. Kataoka et al., Cell 40, 19 (1985).
37. D. Broek et al., ibid. 41, 763 (1985).
38. H. Mitsuzawa, I. Uno, T. Oshima, T. Ishikawa, Genetics 123, 739 (1989).
39. J. E. Buss, P. A. Solski, J. P. Schaeffer, M. J. MacDonald, C. J. Der, Science 243, 1600 (1989); W. R. Schafer et al., ibid. 245, 379 (1989).
40. J. E. Buss, P. A. Solski, J. P. Schaeffer, M. J. MacDonald, C. J. Der, Science 243, 1600 (1989); W. R. Schafer et al., ibid. 245, 379 (1989).
41. J. Inglese, W. J. Koch, M. G. Caron, R. J. Lefkowitz, Nature 359, 147 (1992); C. A. Parish and R. R. Rando, Biochemistry 35, 8473 (1996).
42. J. Inglese, W. J. Koch, M. G. Caron, R. J. Lefkowitz, Nature 359, 147 (1992); C. A. Parish and R. R. Rando, Biochemistry 35, 8473 (1996).
43. C. W. Cody, D. C. Prasher, W. M. Westler, F. G. Prendergast, W. W. Ward, Biochemistry 32, 1212 (1993).
44. B. He et al., Proc. Natl. Acad. Sci. U.S.A. 88, 11373 (1991); L. E. Goodman et al., ibid. 87, 9665 (1990).
45. B. He et al., Proc. Natl. Acad. Sci. U.S.A. 88, 11373 (1991); L. E. Goodman et al., ibid. 87, 9665 (1990).
46. M. N. Ashby, P. R. Errada, V. L. Boyartchuk, J. Rine, Yeast 9, 907 (1993); S. Sapperstein, C. Berkower, S. Michaelis, Mol. Cell. Biol. 14, 1438 (1994).
47. M. N. Ashby, P. R. Errada, V. L. Boyartchuk, J. Rine, Yeast 9, 907 (1993); S. Sapperstein, C. Berkower, S. Michaelis, Mol. Cell. Biol. 14, 1438 (1994).
48. R. C. Stephenson and S. Clarke, J. Biol. Chem. 267, 13314 (1992); J. A. Thissen and P. J. Casey, ibid. 268, 13780 (1993).
49. R. C. Stephenson and S. Clarke, J. Biol. Chem. 267, 13314 (1992); J. A. Thissen and P. J. Casey, ibid. 268, 13780 (1993).
50. K. Kuchler and J. Thorner, Curr. Opin. Cell Biol. 2, 617 (1990).
51. N. E. Kohl et al., Nature Med. 1, 792 (1995).
52. G. F. Sprague Jr., Methods Enzymol. 194, 77 (1991).
53. We thank G. Sprague Jr. for providing the GAL-STE3 construct, H. Mitsuzawa for the ras2-23 strain, J. W. Whistler for the GFP-Ras2p fusion, P. K. Herman for strains, D. King for peptide synthesis, R. Schekman and J. Thorner for critical reading of the manuscript, and all members of the Rine laboratory for support. Supported in part by NIH grant GM35827 (J.R.), California Tobacco Related Disease Research Program fellowship 4FT-0083, Acacia Biosciences, Incorporated (M.N.A.), E. B. Babckock Scholarship, and H. and E. K. Davis Memorial Fellowship (V.L.B.).