Abstract
Oscillations in the activity of cyclin-dependent kinases (CDKs) promote progression through the eukaryotic cell cycle. This review examines how proteolysis regulates CDK activity—by degrading CDK activators or inhibitors—and also how proteolysis may directly trigger the transition from metaphase to anaphase. Proteolysis during the cell cycle is mediated by two distinct ubiquitin-conjugation pathways. One pathway, requiring CDC34, initiates DNA replication by degrading a CDK inhibitor. The second pathway, involving a large protein complex called the anaphase-promoting complex or cyclosome, initiates chromosome segregation and exit from mitosis by degrading anaphase inhibitors and mitotic cyclins. Proteolysis therefore drives cell cycle progression not only by regulating CDK activity, but by directly influencing chromosome and spindle dynamics.
References
146
Referenced
997
10.1038/2191077a0
-
Sachsenmaier W., Remy U., Plattner-Schobel R., Exp. Cell Res. 73, 41 (1972);
(
10.1016/0014-4827(72)90099-7
) / Exp. Cell Res. by Sachsenmaier W. (1972) -
Kauffman S., Wille J. J., J. Theor. Biol. 55, 47 (1975).
(
10.1016/S0022-5193(75)80108-1
) / J. Theor. Biol. by Kauffman S. (1975) -
Evans T., Rosenthal E. T., Youngblom J., Distel D., Hunt T., Cell 33, 389 (1983);
(
10.1016/0092-8674(83)90420-8
) / Cell by Evans T. (1983) - Swenson K. I., Farrell K. M., Ruderman J. V., ibid. 47, 861 (1986); / ibid. by Swenson K. I. (1986)
- Minshull J., Blow J. J., Hunt T., ibid. 56, 947 (1989). / ibid. by Minshull J. (1989)
10.1038/339275a0
- Murray A. W., Solomon M. J., Kirschner M. W., ibid. 339, 280 (1989). / ibid. by Murray A. W. (1989)
-
Peters J.-M., Trends Biochem. Sci. 19, 377 (1994);
(
10.1016/0968-0004(94)90115-5
) / Trends Biochem. Sci. by Peters J.-M. (1994) 10.1016/0955-0674(95)80031-X
- Hochstrasser M. personal communication.
10.1038/366313a0
10.1126/science.270.5243.1828
-
Zhu Y., Carroll M., Papa F. R., Hochstrasser M., D'Andrea A. D., Proc. Natl. Acad. Sci. U.S.A. 93, 3275 (1996).
(
10.1073/pnas.93.8.3275
) / Proc. Natl. Acad. Sci. U.S.A. by Zhu Y. (1996) 10.1016/S0021-9258(20)82050-X
- Hershko A., Heller H., Eytan E., Reiss Y., ibid. 261, 11992 (1986). / ibid. by Hershko A. (1986)
-
Bartel B., Wunning I., Varshavsky A., EMBO J. 9, 3179 (1990).
(
10.1002/j.1460-2075.1990.tb07516.x
) / EMBO J. by Bartel B. (1990) 10.1128/mcb.13.2.775-784.1993
-
Scheffner M., Nuber U., Huibregtse J. M., Nature 373, 81 (1995).
(
10.1038/373081a0
) / Nature by Scheffner M. (1995) - Chau V. Varshavsky A. personal communication.
10.1126/science.2842867
-
Deshaies R. J., Chau V., Kirschner M., EMBO J. 14, 303 (1995).
(
10.1002/j.1460-2075.1995.tb07004.x
) / EMBO J. by Deshaies R. J. (1995) 10.1128/MCB.15.2.731
-
Kornitzer D., Raboy B., Kulka R. G., Fink G. R., EMBO J. 13, 6021 (1994).
(
10.1002/j.1460-2075.1994.tb06948.x
) / EMBO J. by Kornitzer D. (1994) 10.1016/0092-8674(94)90193-7
10.1126/science.8421781
- Nugroho T. T., Mendenhall M. D., Mol. Cell. Biol. 14, 3320 (1994). / Mol. Cell. Biol. by Nugroho T. T. (1994)
- Mendenhall M. personal communication;
- Schwob E. personal communication;
- Verma R. Deshaies R. J. unpublished data
-
Hereford L. M., Hartwell L. H., J. Mol. Biol. 84, 445 (1974).
(
10.1016/0022-2836(74)90451-3
) / J. Mol. Biol. by Hereford L. M. (1974) -
Mathias N., et al., Mol. Cell. Biol. 16, 6634 (1996).
(
10.1128/MCB.16.12.6634
) / Mol. Cell. Biol. by Mathias N. (1996) 10.1016/S0092-8674(00)80098-7
10.1038/371297a0
- Sondek J., Bohm A., Lambright D. G., Hamm H. E., Sigler P. B., ibid. 379, 369 (1996). / ibid. by Sondek J. (1996)
- Feldman R. Verma R. Deshaies R. J. unpublished data.
10.1016/S0092-8674(00)80118-X
-
Huibregtse J. M., Scheffner M., Beaudenon S., Howley P. M., Proc. Natl. Acad. Sci. U.S.A. 92, 2563 (1995).
(
10.1073/pnas.92.7.2563
) / Proc. Natl. Acad. Sci. U.S.A. by Huibregtse J. M. (1995) -
Barral Y., Jentsch S., Mann C., Genes Dev. 9, 399 (1995).
(
10.1101/gad.9.4.399
) / Genes Dev. by Barral Y. (1995) 10.1016/S0092-8674(00)80099-9
10.1002/j.1460-2075.1996.tb00730.x
-
Tyers M., Tokiwa G., Nash R., Futcher B., EMBO J. 11, 1773 (1992).
(
10.1002/j.1460-2075.1992.tb05229.x
) / EMBO J. by Tyers M. (1992) 10.1101/gad.10.16.1979
10.1002/j.1460-2075.1996.tb00793.x
-
Donovan J. D., Toyn J. H., Johnson A. L., Johnston L. H., Genes Dev. 8, 1640 (1994).
(
10.1101/gad.8.14.1640
) / Genes Dev. by Donovan J. D. (1994) 10.1126/science.271.5255.1597
- Verma R. Deshaies R. J. unpublished data.
10.1126/science.272.5261.560
10.1073/pnas.93.15.7772
10.1016/S0968-0004(96)10031-1
- Salama S. R., Hendricks K. B., Thorner J., Mol. Cell. Biol. 14, 7953 (1994). / Mol. Cell. Biol. by Salama S. R. (1994)
- Mathog D. personal communication.
-
Plon S. E., Leppig K. A., Do H. N., Groudine M., Proc. Natl. Acad. Sci. U.S.A. 90, 10484 (1993).
(
10.1073/pnas.90.22.10484
) / Proc. Natl. Acad. Sci. U.S.A. by Plon S. E. (1993) - Lyapina S. Deshaies R. J. unpublished data.
10.1016/S0092-8674(00)81267-2
- Zhang H., Kobayashi R., Galaktionov K., Beach D., ibid. 82, 915 (1995). / ibid. by Zhang H. (1995)
10.1126/science.7624798
- Yew R. Kirschner M. W. unpublished data.
10.1038/349132a0
-
Kobayashi H., et al., Mol. Biol. Cell 3, 1279 (1992).
(
10.1091/mbc.3.11.1279
) / Mol. Biol. Cell by Kobayashi H. (1992) 10.1016/0092-8674(94)90443-X
-
King R. W., Glotzer M., Kirschner M. W., Mol. Biol. Cell 7, 1343 (1996).
(
10.1091/mbc.7.9.1343
) / Mol. Biol. Cell by King R. W. (1996) -
Klotzbücher A., Stewart E., Harrison D., Hunt T., EMBO J. 15, 3053 (1996).
(
10.1002/j.1460-2075.1996.tb00668.x
) / EMBO J. by Klotzbücher A. (1996) -
Zachariae W., Nasmyth K., Mol. Biol. Cell 7, 791 (1996).
(
10.1091/mbc.7.5.791
) / Mol. Biol. Cell by Zachariae W. (1996) -
Ghiara J. B., et al., Cell 65, 163 (1991);
(
10.1016/0092-8674(91)90417-W
) / Cell by Ghiara J. B. (1991) -
Luca F. C., Shibuya E. K., Dohrmann C. E., Ruderman J. V., EMBO J. 10, 4311 (1991);
(
10.1002/j.1460-2075.1991.tb05009.x
) / EMBO J. by Luca F. C. (1991) -
Gallant P., Nigg E. A., J. Cell Biol. 117, 213 (1992);
(
10.1083/jcb.117.1.213
) / J. Cell Biol. by Gallant P. (1992) -
Rimmington G., Dalby B., Glover D. M., J. Cell Sci. 107, 2729 (1994).
(
10.1242/jcs.107.10.2729
) / J. Cell Sci. by Rimmington G. (1994) -
Holloway S. L., Glotzer M., King R. W., Murray A. W., Cell 73, 1393 (1993).
(
10.1016/0092-8674(93)90364-V
) / Cell by Holloway S. L. (1993) 10.1002/j.1460-2075.1993.tb05846.x
- Yamano H., Gannon J., Hunt T., ibid. 15, 5268 (1996). / ibid. by Yamano H. (1996)
- Okazaki K., Nishizawa M., Furuno N., Yasuda H., Sagata N., ibid. 11, 2447 (1992). / ibid. by Okazaki K. (1992)
- Brandeis M., Hunt T., ibid. 15, 5280 (1996). / ibid. by Brandeis M. (1996)
-
Funabiki H., et al., Nature 381, 438 (1996).
(
10.1038/381438a0
) / Nature by Funabiki H. (1996) - van der Velden H. M., Lohka M. J., Mol. Cell. Biol. 13, 1480 (1993); / Mol. Cell. Biol. by van der Velden H. M. (1993)
-
van der Velden H. M. W., Lohka M. J., Mol. Biol. Cell 5, 713 (1994);
(
10.1091/mbc.5.7.713
) / Mol. Biol. Cell by van der Velden H. M. W. (1994) -
Stewart E., Kobayashi H., Harrison D., Hunt T., EMBO J. 13, 584 (1994).
(
10.1002/j.1460-2075.1994.tb06296.x
) / EMBO J. by Stewart E. (1994) - Izumi T., Maller J. L., Mol. Cell. Biol. 11, 3860 (1991); / Mol. Cell. Biol. by Izumi T. (1991)
- Li J. K., Meyer A. N., Donoghue D. J., Mol. Biol. Cell 9, 1111 (1995). / Mol. Biol. Cell by Li J. K. (1995)
-
King R. W., et al., Cell 81, 279 (1995).
(
10.1016/0092-8674(95)90338-0
) / Cell by King R. W. (1995) -
Yu H., King R. W., Peters J.-M., Kirschner M. W., Curr. Biol. 6, 455 (1996).
(
10.1016/S0960-9822(02)00513-4
) / Curr. Biol. by Yu H. (1996) -
Aristarkhov A., et al., Proc. Natl. Acad. Sci. U.S.A. 93, 4294 (1996).
(
10.1073/pnas.93.9.4294
) / Proc. Natl. Acad. Sci. U.S.A. by Aristarkhov A. (1996) -
Seufert W., Futcher B., Jentsch S., Nature 373, 78 (1995).
(
10.1038/373078a0
) / Nature by Seufert W. (1995) -
Irniger S., Piatti S., Michaelis C., Nasmyth K., Cell 81, 269 (1995).
(
10.1016/0092-8674(95)90337-2
) / Cell by Irniger S. (1995) 10.1091/mbc.6.2.185
-
Hershko A., et al., J. Biol. Chem. 269, 4940 (1994).
(
10.1016/S0021-9258(17)37636-6
) / J. Biol. Chem. by Hershko A. (1994) 10.1126/science.274.5290.1199
-
Sikorski R. S., Boguski M. S., Goebl M., Hieter P., Cell 60, 307 (1990).
(
10.1016/0092-8674(90)90745-Z
) / Cell by Sikorski R. S. (1990) 10.1016/S0968-0004(00)89037-4
-
Hirano T., Kinoshita N., Morikawa K., Yanagida M., Cell 60, 319 (1990).
(
10.1016/0092-8674(90)90746-2
) / Cell by Hirano T. (1990) -
Lamb J. R., Michaud W. A., Sikorski R. S., Hieter P. A., EMBO J. 13, 4321 (1994).
(
10.1002/j.1460-2075.1994.tb06752.x
) / EMBO J. by Lamb J. R. (1994) -
Hirano T., Hiraoka Y., Yanagida M., J. Cell Biol. 106, 1171 (1988).
(
10.1083/jcb.106.4.1171
) / J. Cell Biol. by Hirano T. (1988) -
O'Donnell K. L., Osmani A. H., Osmani S. A., Morris N. R., J. Cell Sci. 99, 711 (1991).
(
10.1242/jcs.99.4.711
) / J. Cell Sci. by O'Donnell K. L. (1991) -
Samejima I., Yanagida M., J. Cell Biol. 127, 1655 (1994).
(
10.1083/jcb.127.6.1655
) / J. Cell Biol. by Samejima I. (1994) 10.1016/0092-8674(95)90336-4
10.1126/science.274.5290.1201
-
Osmani S. A., Engle D. B., Doonan J. H., Morris N. R., Cell 52, 241 (1988).
(
10.1016/0092-8674(88)90513-2
) / Cell by Osmani S. A. (1988) -
Engle D. B., et al., J. Biol. Chem. 265, 16132 (1990).
(
10.1016/S0021-9258(17)46198-9
) / J. Biol. Chem. by Engle D. B. (1990) 10.1126/science.2683077
10.1083/jcb.133.1.85
- Cohen-Fix O. Peters J.-M. Kirschner M. W. Koshland D. Genes Dev. in press.
10.1083/jcb.133.1.99
-
Zhang D., Nicklas R. B., Nature 382, 466 (1996).
(
10.1038/382466a0
) / Nature by Zhang D. (1996) - Félix M. A., Labbé J. C., Dorée M., Hunt T., Karsenti E., ibid. 346, 379 (1990). / ibid. by Félix M. A. (1990)
-
Mirabito P. M., Morris N. R., J. Cell Biol. 120, 959 (1993).
(
10.1083/jcb.120.4.959
) / J. Cell Biol. by Mirabito P. M. (1993) -
Lahav-Baratz S., Sudakin V., Ruderman J. V., Hershko A., Proc. Natl. Acad. Sci. U.S.A. 92, 9303 (1995).
(
10.1073/pnas.92.20.9303
) / Proc. Natl. Acad. Sci. U.S.A. by Lahav-Baratz S. (1995) 10.1126/science.271.5256.1718
- Sethi N., Monteagudo M. C., Koshland D., Hogan E., Burke D. J., Mol. Cell. Biol. 11, 5592 (1991). / Mol. Cell. Biol. by Sethi N. (1991)
-
Dawson I. A., Roth S., Akam M., Artavanis-Tsakonis S., Development 117, 359 (1993);
(
10.1242/dev.117.1.359
) / Development by Dawson I. A. (1993) -
Dawson I. A., Roth S., Artavanis-Tsakonis S., J. Cell Biol. 129, 725 (1995);
(
10.1083/jcb.129.3.725
) / J. Cell Biol. by Dawson I. A. (1995) -
Sigrist S., Jacobs H., Stratmann R., Lehner C. F., EMBO J. 14, 4827 (1995).
(
10.1002/j.1460-2075.1995.tb00164.x
) / EMBO J. by Sigrist S. (1995) -
Ohkura H., Kinoshita N., Miyatani S., Toda T., Yanagida M., Cell 57, 997 (1989);
(
10.1016/0092-8674(89)90338-3
) / Cell by Ohkura H. (1989) - Doonan J. H. Morris N. R. ibid. p. 987;
- Axton J. M., Dombradi V., Cohen P. T., Glover D. M., ibid. 63, 33 (1990); / ibid. by Axton J. M. (1990)
- Hisamoto N., Sugimoto K., Matsumoto K., Mol. Cell. Biol. 14, 3158 (1994). / Mol. Cell. Biol. by Hisamoto N. (1994)
-
Schwob E., Bohm T., Mendenhall M. D., Nasmyth K., Cell 84, U13 (1996).
(
10.1016/S0092-8674(00)80988-5
) / Cell by Schwob E. (1996) -
Wells W. A. E., Trends Cell Biol. 6, 228 (1996).
(
10.1016/0962-8924(96)10018-0
) / Trends Cell Biol. by Wells W. A. E. (1996) -
Galipeau P. C., et al., Proc. Natl. Acad. Sci. U.S.A. 93, 7081 (1996).
(
10.1073/pnas.93.14.7081
) / Proc. Natl. Acad. Sci. U.S.A. by Galipeau P. C. (1996) -
Sagata N., Trends Cell Biol. 6, 22 (1996).
(
10.1016/0962-8924(96)81034-8
) / Trends Cell Biol. by Sagata N. (1996) - Posada J., Yew N., Ahn N. G., Vande Woude G. F., Cooper J. A., Mol. Cell Biol. 13, 2546 (1993); / Mol. Cell Biol. by Posada J. (1993)
-
Kosako H., Gotoh Y., Nishida E., J. Biol. Chem. 269, 28354 (1994).
(
10.1016/S0021-9258(18)46935-9
) / J. Biol. Chem. by Kosako H. (1994) -
Minshull J., Sun H., Tonks N. K., Murray A. W., Cell 79, 475 (1994).
(
10.1016/0092-8674(94)90256-9
) / Cell by Minshull J. (1994) 10.1101/gad.7.5.833
-
Whitfield W. G., Gonzalez C., Maldonado-Codina G., Glover D. M., EMBO J. 9, 2563 (1990).
(
10.1002/j.1460-2075.1990.tb07437.x
) / EMBO J. by Whitfield W. G. (1990) -
Hunt T., Luca F. C., Ruderman J. V., J. Cell Biol. 116, 707 (1992).
(
10.1083/jcb.116.3.707
) / J. Cell Biol. by Hunt T. (1992) - Yeh E., Skibbens R. V., Cheng J. W., Salmon E. D., Bloom K., ibid. 130, 687 (1995). / ibid. by Yeh E. (1995)
- McGarry T. Kirschner M. W. unpublished data.
-
Pellman D., Bagget M., Tu H., Fink G. R., J. Cell Biol. 130, 1373 (1995);
(
10.1083/jcb.130.6.1373
) / J. Cell Biol. by Pellman D. (1995) - Juang Y.-L. Peters J.-M. McLaughlin M. E. Tai C.-Y. Pellman D. in preparation
10.1083/jcb.125.6.1303
-
Stratmann R., Lehner C. F., Cell 84, 25 (1996).
(
10.1016/S0092-8674(00)80990-3
) / Cell by Stratmann R. (1996) -
Pu R. T., Osmani S. A., EMBO J. 14, 995 (1995).
(
10.1002/j.1460-2075.1995.tb07080.x
) / EMBO J. by Pu R. T. (1995) -
Heichman K. A., Roberts J. M., Cell 85, 39 (1996).
(
10.1016/S0092-8674(00)81080-6
) / Cell by Heichman K. A. (1996) -
Osmani A. H., O'Donnell K., Pu R. T., Osmani S. A., EMBO J. 10, 2669 (1991);
(
10.1002/j.1460-2075.1991.tb07810.x
) / EMBO J. by Osmani A. H. (1991) -
James S. W., Mirabito P. M., Scacheri P. C., Morris N. R., J. Cell Sci. 108, 3485 (1995);
(
10.1242/jcs.108.11.3485
) / J. Cell Sci. by James S. W. (1995) -
Ye X. S., Fincher R. R., Tang A., O'Donnell K., Osmani S. A., EMBO J. 15, 3599 (1996).
(
10.1002/j.1460-2075.1996.tb00729.x
) / EMBO J. by Ye X. S. (1996) -
Nefsky B., Beach D., EMBO J. 15, 1301 (1996).
(
10.1002/j.1460-2075.1996.tb00472.x
) / EMBO J. by Nefsky B. (1996) - Seufert W., McGrath J. P., Jentsch S., ibid. 9, 4535 (1990). / ibid. by Seufert W. (1990)
-
Finley D., Ciechanover A., Varshavsky A., Cell 37, 43 (1984).
(
10.1016/0092-8674(84)90299-X
) / Cell by Finley D. (1984) -
al-Khodairy F., Enoch T., Hagan I. M., Carr A. M., J. Cell Sci. 108, 475 (1995).
(
10.1242/jcs.108.2.475
) / J. Cell Sci. by al-Khodairy F. (1995) -
Singer J. D., Manning B. M., Formosa T., Mol. Cell. Biol. 16, 1356 (1996).
(
10.1128/MCB.16.4.1356
) / Mol. Cell. Biol. by Singer J. D. (1996) 10.1016/0092-8674(93)90722-3
-
Dahmann C., Diffley J. F., Nasmyth K. A., Curr. Biol. 5, 1257 (1995).
(
10.1016/S0960-9822(95)00252-1
) / Curr. Biol. by Dahmann C. (1995) 10.1016/0168-9525(96)10041-X
10.1126/science.3541205
-
Starborg M., Brundell E., Gell K., Höög C., J. Biol. Chem. 269, 24133 (1994).
(
10.1016/S0021-9258(19)51058-4
) / J. Biol. Chem. by Starborg M. (1994)
Dates
Type | When |
---|---|
Created | 23 years ago (July 27, 2002, 5:45 a.m.) |
Deposited | 1 year ago (Aug. 7, 2024, 7:47 a.m.) |
Indexed | 2 weeks, 6 days ago (Aug. 5, 2025, 8:18 a.m.) |
Issued | 28 years, 8 months ago (Dec. 6, 1996) |
Published | 28 years, 8 months ago (Dec. 6, 1996) |
Published Print | 28 years, 8 months ago (Dec. 6, 1996) |
@article{King_1996, title={How Proteolysis Drives the Cell Cycle}, volume={274}, ISSN={1095-9203}, url={http://dx.doi.org/10.1126/science.274.5293.1652}, DOI={10.1126/science.274.5293.1652}, number={5293}, journal={Science}, publisher={American Association for the Advancement of Science (AAAS)}, author={King, Randall W. and Deshaies, Raymond J. and Peters, Jan-Michael and Kirschner, Marc W.}, year={1996}, month=dec, pages={1652–1659} }