APC-mediated proteolysis of Ase1 and the morphogenesis of the mitotic spindle

Science

Volumn 275, Issue 5304, 1997, Pages 1311-1314

  Juang, Yue Li ^a   Huang, James ^a   Peters, Jan Michael ^b,c   McLaughlin, Margaret E ^a   Tai, Chin Yin ^a   Pellman, David ^a  

^a BOSTON CHILDREN S HOSPITAL   (United States)

^b HARVARD MEDICAL SCHOOL   (United States)

^c RESEARCH INSTITUTE OF MOLECULAR PATHOLOGY   (Austria)

Author keywords

[No Author keywords available]

Indexed keywords

CELL CYCLE PROTEIN; CYCLINE; MUTANT PROTEIN;

ANAPHASE; ARTICLE; CELL CYCLE G1 PHASE; MITOSIS SPINDLE; PRIORITY JOURNAL; PROTEIN DEGRADATION; PROTEIN STABILITY; SACCHAROMYCES CEREVISIAE; SISTER CHROMATID; TELOPHASE;

ANAPHASE; BASE SEQUENCE; CELL CYCLE PROTEINS; G1 PHASE; MICROTUBULE-ASSOCIATED PROTEINS; MITOSIS; MITOTIC SPINDLE APPARATUS; MOLECULAR SEQUENCE DATA; MORPHOGENESIS; MUTAGENESIS, SITE-DIRECTED; SACCHAROMYCES CEREVISIAE; TELOPHASE;

SACCHAROMYCES CEREVISIAE;

EID: 0031055137     PISSN: 00368075     EISSN: None     Source Type: Journal    
DOI: 10.1126/science.275.5304.1311     Document Type: Article

References (41)

1. A. Ciechanover, Cell 79, 13 (1994).
2. M. Glotzer, A. W. Murray, M. W. Kirschner, Nature 349, 132 (1991).
3. A. Hershko, D. Ganoth, J. Pehrson, R. E. Palazzo, L. H. Cohen, J. Biol. Chem 266, 16376 (1991).
4. A. Hershko et al., ibid. 269, 4940 (1994); V. Sudakin et al., Mol. Biol. Cell 6, 185 (1995).
5. A. Hershko et al., ibid. 269, 4940 (1994); V. Sudakin et al., Mol. Biol. Cell 6, 185 (1995).
6. S. Irniger, S. Piatti, C. Michaelis, K. Nasmyth, Cell 81, 269 (1995).
7. R. W. King et al., ibid., p. 279.
8. S. Tugendreich, J. Tomkiel, W. Earnshaw, P. Hieter, ibid., p. 261.
9. F. C. Luca, E. K. Shibuya, C. E. Dohrmann, J. V. Ruderman, EMBO J. 10, 4311 (1991).
10. R. S. Sikorski et al., Cold Spring Harbor Symp. Quant. Biol. 56, 663 (1991).
11. S. L. Holloway, M. Glotzer, R. W. King, A. W. Murray, Cell 73, 1393 (1993).
12. H. Funabiki et al., Nature 381, 438 (1996); O. Cohen-Fix, J.-M. Peters, M. W. Kirschner, D. Koshland, Genes Dev. 24, 3081 (1996).
13. H. Funabiki et al., Nature 381, 438 (1996); O. Cohen-Fix, J.-M. Peters, M. W. Kirschner, D. Koshland, Genes Dev. 24, 3081 (1996).
14. K. A. Heichman and J. M. Roberts, Cell 85, 39 (1996).
15. D. Pellman, M. Bagget, H. Tu, G. R. Fink, J. Cell Biol. 130, 1373 (1995). Additionally, Ase1 binds taxol-stabilized microtubules in vitro (S. Schuyler and D. Pellman, unpublished results). ASE1 is nonessential, but in the strain background used in this study, the ase1Δ mutation causes a temperature-sensitive growth defect.
16. D. Pellman, M. Bagget, H. Tu, G. R. Fink, J. Cell Biol. 130, 1373 (1995). Additionally, Ase1 binds taxol-stabilized microtubules in vitro (S. Schuyler and D. Pellman, unpublished results). ASE1 is nonessential, but in the strain background used in this study, the ase1Δ mutation causes a temperature-sensitive growth defect.
17. 2-specific expression of CLB2 [D. Lydall, G. Ammerer, K. Nasmyth, Genes Dev. 5, 2405 (1991); M. Maher, F. Cong, D. Kindelberger, K. Nasmyth, S. Dalton, Mol. Cell. Biol. 15, 3129 (1995)].
18. 2-specific expression of CLB2 [D. Lydall, G. Ammerer, K. Nasmyth, Genes Dev. 5, 2405 (1991); M. Maher, F. Cong, D. Kindelberger, K. Nasmyth, S. Dalton, Mol. Cell. Biol. 15, 3129 (1995)].
19. 2-specific expression of CLB2 [D. Lydall, G. Ammerer, K. Nasmyth, Genes Dev. 5, 2405 (1991); M. Maher, F. Cong, D. Kindelberger, K. Nasmyth, S. Dalton, Mol. Cell. Biol. 15, 3129 (1995)].
20. 2-specific expression of CLB2 [D. Lydall, G. Ammerer, K. Nasmyth, Genes Dev. 5, 2405 (1991); M. Maher, F. Cong, D. Kindelberger, K. Nasmyth, S. Dalton, Mol. Cell. Biol. 15, 3129 (1995)].
21. W. Zachariae, T. H. Shin, M. Galova, B. Obermaier, K. Nasmyth, Science 274, 1201 (1996).
22. 2 with the microtubule depolymerizing agent, nocodozole, suggesting that the stability of Ase1 during mitosis is not due to co-assembly with microtubules (M. McLaughlin and D. Pellman, unpublished results).
23. J.-M. Peters, R. W. King, C. Höög, M. W. Kirschner, Science 274, 1199 (1996).
24. R. W. King, M. Glotzer, M. W. Kirschner, Mol. Cell. Biol. 7, 1343 (1996). Although most mitotic cyclins contain a leucine at the fourth position of the destruction box, cyclin B3 from both avian and amphibian cells contains a phenylalanine in this position [P. Gallant and E. A. Nigg, EMBO J. 13, 595 (1994); T. McGarry, personal communication].
25. R. W. King, M. Glotzer, M. W. Kirschner, Mol. Cell. Biol. 7, 1343 (1996). Although most mitotic cyclins contain a leucine at the fourth position of the destruction box, cyclin B3 from both avian and amphibian cells contains a phenylalanine in this position [P. Gallant and E. A. Nigg, EMBO J. 13, 595 (1994); T. McGarry, personal communication].
26. R. W. King, M. Glotzer, M. W. Kirschner, Mol. Cell. Biol. 7, 1343 (1996). Although most mitotic cyclins contain a leucine at the fourth position of the destruction box, cyclin B3 from both avian and amphibian cells contains a phenylalanine in this position [P. Gallant and E. A. Nigg, EMBO J. 13, 595 (1994); T. McGarry, personal communication].
27. Y.-L. Juang and D. Pellman, unpublished results.
28. The rate of spindle disassembly was not different between cells containing GAL1::ASE1 and the control vector (19).
29. DNA content was determined by flow cytometry (19).
30. R. Li and A. W. Murray, Cell 66, 519 (1991); M. A. Hoyt, L. Totis, B. T. Roberts, ibid., p. 507; F. Spencer and P. Hieter, Proc. Natl. Acad. Sci. U.S.A. 89, 8908 (1992); M. W. Neff and D. J. Burke, Mol. Cell. Biol. 12, 3857 (1992).
31. R. Li and A. W. Murray, Cell 66, 519 (1991); M. A. Hoyt, L. Totis, B. T. Roberts, ibid., p. 507; F. Spencer and P. Hieter, Proc. Natl. Acad. Sci. U.S.A. 89, 8908 (1992); M. W. Neff and D. J. Burke, Mol. Cell. Biol. 12, 3857 (1992).
32. R. Li and A. W. Murray, Cell 66, 519 (1991); M. A. Hoyt, L. Totis, B. T. Roberts, ibid., p. 507; F. Spencer and P. Hieter, Proc. Natl. Acad. Sci. U.S.A. 89, 8908 (1992); M. W. Neff and D. J. Burke, Mol. Cell. Biol. 12, 3857 (1992).
33. R. Li and A. W. Murray, Cell 66, 519 (1991); M. A. Hoyt, L. Totis, B. T. Roberts, ibid., p. 507; F. Spencer and P. Hieter, Proc. Natl. Acad. Sci. U.S.A. 89, 8908 (1992); M. W. Neff and D. J. Burke, Mol. Cell. Biol. 12, 3857 (1992).
34. A. Amon, S. Irniger, K. Nasmyth, Cell 77, 1037 (1994).
35. K. D. Brown, R. M. Coulson, T. J. Yen, D. W. Cleveland, J. Cell Biol. 125, 1303 (1994); H. Liao, R. J. Winkfein, G. Mack, J. B. Rattner, T. J. Yen, ibid. 130, 507 (1995).
36. K. D. Brown, R. M. Coulson, T. J. Yen, D. W. Cleveland, J. Cell Biol. 125, 1303 (1994); H. Liao, R. J. Winkfein, G. Mack, J. B. Rattner, T. J. Yen, ibid. 130, 507 (1995).
37. 35S-labeling and measurement of protein stability was done as described [D. Kornitzer, B. Raboy, R. G. Kulka, G. R. Fink, EMBO J. 13, 6021 (1994)]. Ase1 levels were quantitated with a phosphorimager and normalized to the zero time point. Experiments using Ase1 polyclonal antibodies demonstrated that the myc epitope did not alter the half-life of Ase1 or Ase1-db (19).
38. Methods are as described (13). Cultures for pulse-chase analysis and flow cytometry were split before labeling, and the sample for flow cytometry was grown in parallel in identical medium containing unlabeled methionine.
39. The half-life of Ase1 in cycling cells at 36°C is somewhat shorter than at 30°C (compare Fig. 1 B with Fig. 2A).
40. The Ase1-db mutant was constructed by site-directed mutagenesis using an oligonucleotide of sequence 5′-CATGCAGTAAAACCAGCTCAGCTGGCTCCTATCCCGCTGGCTAAAGTCGACACTAAG-3′.
41. We thank A. Amon, A. Murray, K. Nasmyth, and W. Zachariae for strains and plasmids; O. Cohen-Fix, D. Koshland, T. McGarry, K. Nasmyth, and W. Zachariae for communicating results before publication; A. Amon, O. Cohen-Fix, A. D'Andrea, G. Fink, M. Kirschner, D. Kornitzer, R. Li, and A. Murray for helpful discussions or reading of the manuscript; M. Young for statistical analysis; and D. Kornitzer for guidance with the pulse-chase experiments. D.P. is supported by a Damon Runyon Scholar Award, a Claudia Adams Barr Award, and funds to the Dana-Farber Cancer Institute in memory of Patrick McDonough.