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The anaphase-promoting complex: a key factor in the regulation of cell cycle

Oncogene volume 24, pages 314–325 (2005)Cite this article

Abstract

Events controlling cell division are governed by the degradation of different regulatory proteins by the ubiquitin-dependent pathway. In this pathway, the attachment of a polyubiquitin chain to a substrate by an ubiquitin-ligase targets this substrate for degradation by the 26S proteasome. Two different ubiquitin ligases play an important role in the cell cycle: the SCF (Skp1/Cullin/F-box) and the anaphase-promoting complex (APC). In this review, we describe the present knowledge about the APC. We pay particular attention to the latest results concerning APC structure, APC regulation and substrate recognition, and we discuss the implication of these findings in the understanding the APC function.

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References

  • Antonio C, Ferby I, Wilhelm H, Jones M, Karsenti E, Nebreda AR and Vernos I . (2000). Cell, 102, 425–435.

  • Araki M, Wharton RP, Tang Z, Yu H and Asano M . (2003). EMBO J., 22, 6115–6126.

  • Ayad NG, Rankin S, Murakami M, Jebanathirajah J, Gygi S and Kirschner MW . (2003). Cell, 113, 101–113.

  • Bai C, Sen P, Hofmann K, Ma L, Goebl M, Harper JW and Elledge SJ . (1996). Cell, 86, 263–274.

  • Brassac T, Castro A, Lorca T, Le Peuch C, Doree M, Labbe JC and Galas S . (2000). Oncogene, 19, 3782–3790.

  • Burton JL and Solomon MJ . (2001). Genes Dev., 15, 2381–2395.

  • Carroll CW and Morgan DO . (2002). Nat. Cell Biol., 4, 880–887.

  • Castro A, Arlot-Bonnemains Y, Vigneron S, Labbe JC, Prigent C and Lorca T . (2002a). EMBO Rep., 3, 457–462.

  • Castro A, Vigneron S, Bernis C, Labbe JC and Lorca T . (2003). Mol. Cell. Biol., 23, 4126–4138.

  • Castro A, Vigneron S, Bernis C, Labbe JC, Prigent C and Lorca T . (2002b). EMBO Rep., 3, 1209–1214.

  • Charles JF, Jaspersen SL, Tinker-Kulberg RL, Hwang L, Szidon A and Morgan DO . (1998). Curr. Biol., 8, 497–507.

  • Chung E and Chen RH . (2003). Nat. Cell Biol., 5, 748–753.

  • Ciosk R, Zachariae W, Michaelis C, Shevchenko A, Mann M and Nasmyth K . (1998). Cell, 93, 1067–1076.

  • Clute P and Pines J . (1999). Nat. Cell Biol., 1, 82–87.

  • Cooper KF, Mallory MJ, Egeland DB, Jarnik M and Strich R . (2000). Proc. Natl. Acad. Sci. USA, 97, 14548–14553.

  • D'Andrea LD and Regan L . (2003). Trends Biochem. Sci., 28, 655–662.

  • Engle DB, Osmani SA, Osmani AH, Rosborough S, Xin XN and Morris NR . (1990). J. Biol. Chem., 265, 16132–16137.

  • Fang G . (2002). Mol. Biol. Cell, 13, 755–766.

  • Fang G, Yu H and Kirschner MW . (1998a). Genes Dev., 12, 1871–1883.

  • Fang G, Yu H and Kirschner MW . (1998b). Mol. Cell, 2, 163–171.

  • Funabiki H and Murray AW . (2000). Cell, 102, 411–424.

  • Furuta T, Tuck S, Kirchner J, Koch B, Auty R, Kitagawa R, Rose AM and Greenstein D . (2000). Mol. Biol. Cell, 11, 1401–1419.

  • Gabellini D, Colaluca IN, Vodermaier HC, Biamonti G, Giacca M, Falaschi A, Riva S and Peverali FA . (2003). EMBO J., 22, 3715–3724.

  • Gallant P and Nigg EA . (1992). J. Cell. Biol., 117, 213–224.

  • Geley S, Kramer E, Gieffers C, Gannon J, Peters JM and Hunt T . (2001). J. Cell Biol., 153, 137–148.

  • Glotzer M, Murray AW and Kirschner MW . (1991). Nature, 349, 132–138.

  • Gmachl M, Gieffers C, Podtelejnikov AV, Mann M and Peters JM . (2000). Proc. Natl. Acad. Sci. USA, 97, 8973–8978.

  • Golan A, Yudkovsky Y and Hershko A . (2002). J. Biol. Chem., 277, 15552–15557.

  • Gordon DM and Roof DM . (2001). Proc. Natl. Acad. Sci. USA, 98, 12515–12520.

  • Grossberger R, Gieffers C, Zachariae W, Podtelejnikov AV, Schleiffer A, Nasmyth K, Mann M and Peters JM . (1999). J. Biol. Chem., 274, 14500–14507.

  • Hall MC, Torres MP, Schroeder GK and Borchers CH . (2003). J. Biol. Chem., 278, 16698–16705.

  • Hames RS, Wattam SL, Yamano H, Bacchieri R and Fry AM . (2001). EMBO J., 20, 7117–7127.

  • Hartwell LH, Culotti J and Reid B . (1970). Proc. Natl. Acad. Sci. USA, 66, 352–359.

  • Hartwell LH and Smith D . (1985). Genetics, 110, 381–395.

  • Hershko A and Ciechanover A . (1998). Annu. Rev. Biochem., 67, 425–479.

  • Hershko A, Ganoth D, Sudakin V, Dahan A, Cohen LH, Luca FC, Ruderman JV and Eytan E . (1994). J. Biol. Chem., 269, 4940–4946.

  • Hildebrandt ER and Hoyt MA . (2001). Mol. Biol. Cell, 12, 3402–3416.

  • Hilioti Z, Chung YS, Mochizuki Y, Hardy CF and Cohen-Fix O . (2001). Curr. Biol., 11, 1347–1352.

  • Holloway SL, Glotzer M, King RW and Murray AW . (1993). Cell, 73, 1393–1402.

  • Hsu JY, Reimann JD, Sorensen CS, Lukas J and Jackson PK . (2002). Nat. Cell. Biol., 4, 358–366.

  • Hwang LH and Murray AW . (1997). Mol. Biol. Cell, 8, 1877–1887.

  • Irniger S, Piatti S, Michaelis C and Nasmyth K . (1995). Cell, 81, 269–278.

  • Jaspersen SL, Charles JF and Morgan DO . (1999). Curr. Biol., 9, 227–236.

  • Jorgensen PM, Graslund S, Betz R, Stahl S, Larsson C and Hoog C . (2001). Gene, 262, 51–59.

  • Juang YL, Huang J, Peters JM, McLaughlin ME, Tai CY and Pellman D . (1997). Science, 275, 1311–1314.

  • Kallio M, Weinstein J, Daum JR, Burke DJ and Gorbsky GJ . (1998). J. Cell Biol., 141, 1393–1406.

  • Kamura T, Koepp DM, Conrad MN, Skowyra D, Moreland RJ, Iliopoulos O, Lane WS, Kaelin Jr WG, Elledge SJ, Conaway RC, Harper JW and Conaway JW . (1999). Science, 284, 657–661.

  • Ke PY and Chang ZF . (2004). Mol. Cell. Biol., 24, 514–526.

  • King RW, Peters JM, Tugendreich S, Rolfe M, Hieter P and Kirschner MW . (1995). Cell, 81, 279–288.

  • Kominami K, Seth-Smith H and Toda T . (1998). EMBO J., 17, 5388–5399.

  • Kotani S, Tugendreich S, Fujii M, Jorgensen PM, Watanabe N, Hoog C, Hieter P and Todokoro K . (1998). Mol. Cell, 1, 371–380.

  • Kraft C, Herzog F, Gieffers C, Mechtler K, Hagting A, Pines J and Peters JM . (2003). EMBO J., 22, 6598–6609.

  • Kramer ER, Gieffers C, Holzl G, Hengstschlager M and Peters JM . (1998). Curr. Biol., 8, 1207–1210.

  • Lahav-Baratz S, Sudakin V, Ruderman JV and Hershko A . (1995). Proc. Natl. Acad. Sci. USA, 92, 9303–9307.

  • Lamb JR, Michaud WA, Sikorski RS and Hieter PA . (1994). EMBO J., 13, 4321–4328.

  • Leverson JD, Joazeiro CA, Page AM, Huang H, Hieter P and Hunter T . (2000). Mol. Biol. Cell, 11, 2315–2325.

  • Levesque AA and Compton DA . (2001). J. Cell Biol., 154, 1135–1146.

  • Littlepage LE and Ruderman JV . (2002). Genes Dev., 16, 2274–2285.

  • Lorca T, Castro A, Martinez AM, Vigneron S, Morin N, Sigrist S, Lehner C, Doree M and Labbe JC . (1998). EMBO J., 17, 3565–3575.

  • Lorca T, Devault A, Colas P, Van Loon A, Fesquet D, Lazaro JB and Doree M . (1992). FEBS Lett., 306, 90–93.

  • Luca FC, Shibuya EK, Dohrmann CE and Ruderman JV . (1991). EMBO J., 10, 4311–4320.

  • Lupas A, Baumeister W and Hofmann K . (1997). Trends Biochem. Sci., 22, 195–196.

  • Margottin-Goguet F, Hsu JY, Loktev A, Hsieh HM, Reimann JD and Jackson PK . (2003). Dev. Cell, 4, 813–826.

  • McGarry TJ and Kirschner MW . (1998). Cell, 93, 1043–1053.

  • Mechali F, Chiung-Yueh H, Castro A, Lorca T and Bonne-Andrea C . (2004). J Viriol, 78, 2615–2619.

  • Meraldi P, Honda R and Nigg EA . (2002). EMBO J., 21, 483–492.

  • Murray AW and Kirschner MW . (1989). Nature, 339, 275–280.

  • Nasmyth K . (2001). Annu. Rev. Genet., 35, 673–745.

  • Parry DH and O'Farrell PH . (2001). Curr. Biol., 11, 671–683.

  • Passmore LA, McCormack EA, Au SW, Paul A, Willison KR, Harper JW and Barford D . (2003). EMBO J., 22, 786–796.

  • Patra D and Dunphy WG . (1998). Genes Dev., 12, 2549–2559.

  • Patton EE, Willems AR, Sa D, Kuras L, Thomas D, Craig KL and Tyers M . (1998). Genes Dev., 12, 692–705.

  • Perez LH, Antonio C, Flament S, Vernos I and Nebreda AR . (2002). Nat. Cell Biol., 4, 737–742.

  • Peter M, Castro A, Lorca T, Le Peuch C, Magnaghi-Jaulin L, Doree M and Labbe JC . (2001). Nat. Cell Biol., 3, 83–87.

  • Peters JM, King RW, Hoog C and Kirschner MW . (1996). Science, 274, 1199–1201.

  • Petersen BO, Wagener C, Marinoni F, Kramer ER, Melixetian M, Denchi EL, Gieffers C, Matteucci C, Peters JM and Helin K . (2000). Genes Dev., 14, 2330–2343.

  • Pfleger CM and Kirschner MW . (2000). Genes Dev., 14, 655–665.

  • Pfleger CM, Lee E and Kirschner MW . (2001a). Genes Dev., 15, 2396–2407.

  • Pfleger CM, Salic A, Lee E and Kirschner MW . (2001b). Genes Dev., 15, 1759–1764.

  • Pintard L, Willems A and Peter M . (2004). EMBO J., 23, 1681–1687.

  • Reimann JD, Freed E, Hsu JY, Kramer ER, Peters JM and Jackson PK . (2001). Cell, 105, 645–655.

  • Rudner AD and Murray AW . (2000). J. Cell Biol., 149, 1377–1390.

  • Salah SM and Nasmyth K . (2000). Chromosoma, 109, 27–34.

  • Schwab M, Lutum AS and Seufert W . (1997). Cell, 90, 683–693.

  • Schwab M, Neutzner M, Mocker D and Seufert W . (2001). EMBO J., 20, 5165–5175.

  • Seol JH, Feldman RM, Zachariae W, Shevchenko A, Correll CC, Lyapina S, Chi Y, Galova M, Claypool J, Sandmeyer S, Nasmyth K and Deshaies RJ . (1999). Genes Dev., 13, 1614–1626.

  • Shirayama M, Toth A, Galova M and Nasmyth K . (1999). Nature, 402, 203–207.

  • Shirayama M, Zachariae W, Ciosk R and Nasmyth K . (1998). EMBO J, 17, 1336–1349.

  • Sigrist S, Jacobs H, Stratmann R and Lehner CF . (1995). EMBO J., 14, 4827–4838.

  • Sigrist SJ and Lehner CF . (1997). Cell, 90, 671–681.

  • Sikorski RS, Boguski MS, Goebl M and Hieter P . (1990). Cell, 60, 307–317.

  • Skowyra D, Koepp DM, Kamura T, Conrad MN, Conaway RC, Conaway JW, Elledge SJ and Harper JW . (1999). Science, 284, 662–665.

  • Song MS, Song SJ, Ayad NG, Chang JS, Lee JH, Hong HK, Lee H, Choi N, Kim J, Kim H, Kim JW, Choi EJ, Kirschner MW and Lim DS . (2004). Nat. Cell Biol., 2, 129–137.

  • Sorensen CS, Lukas C, Kramer ER, Peters JM, Bartek J and Lukas J . (2001). Mol. Cell. Biol., 21, 3692–3703.

  • Starborg M, Brundell E, Gell K and Hoog C . (1994). J. Biol. Chem., 269, 24133–24137.

  • Stemmann O, Zou H, Gerber SA, Gygi SP and Kirschner MW . (2001). Cell, 107, 715–726.

  • Stroschein SL, Bonni S, Wrana JL and Luo K . (2001). Genes Dev., 15, 2822–2836.

  • Sudakin V, Chan GK and Yen TJ . (2001). J Cell Biol., 154, 925–936.

  • Sudakin V, Ganoth D, Dahan A, Heller H, Hershko J, Luca FC, Ruderman JV and Hershko A . (1995). Mol. Biol. Cell, 6, 185–197.

  • Surana U, Amon A, Dowzer C, McGrew J, Byers B and Nasmyth K . (1993). EMBO J., 12, 1969–1978.

  • Taieb FE, Gross SD, Lewellyn AL and Maller JL . (2001). Curr. Biol., 11, 508–513.

  • Tang Z, Bharadwaj R, Li B and Yu H . (2001a). Dev. Cell, 1, 227–237.

  • Tang Z, Li B, Bharadwaj R, Zhu H, Ozkan E, Hakala K, Deisenhofer J and Yu H . (2001b). Mol. Biol. Cell, 12, 3839–3851.

  • Terret ME, Wassmann K, Waizenegger I, Maro B, Peters JM and Verlhac MH . (2003). Curr. Biol., 13, 1797–1802.

  • Uhlmann F, Lottspeich F and Nasmyth K . (1999). Nature, 400, 37–42.

  • Uhlmann F, Wernic D, Poupart MA, Koonin EV and Nasmyth K . (2000). Cell, 103, 375–386.

  • Visintin R, Prinz S and Amon A . (1997). Science, 278, 460–463.

  • Vodermaier HC, Gieffers C, Maurer-Stroh S, Eisenhaber F and Peters JM . (2003). Curr. Biol., 13, 1459–1468.

  • Vodermaier HC and Peters JM . (2004). Cell Cycle, 3, 265–266.

  • Wan Y and Kirschner MW . (2001). Proc. Natl. Acad. Sci. USA, 98, 13066–13071.

  • Wan Y, Liu X and Kirschner MW . (2001). Mol. Cell, 8, 1027–1039.

  • Weinstein J . (1997). J. Biol. Chem., 272, 28501–28511.

  • Wendt KS, Vodermaier HC, Jacob U, Gieffers C, Gmachl M, Peters JM, Huber R and Sondermann P . (2001). Nat. Struct. Biol., 8, 784–788.

  • Yamada H, Kumada K and Yanagida M . (1997). J. Cell. Sci., 110 (Part 15), 1793–1804.

  • Yamamoto A, Guacci V and Koshland D . (1996). J. Cell. Biol., 133, 85–97.

  • Yamano H, Gannon J, Mahbubani H and Hunt T . (2004). Mol. Cell, 13, 137–147.

  • Yamashita YM, Nakaseko Y, Samejima I, Kumada K, Yamada H, Michaelson D and Yanagida M . (1996). Nature, 384, 276–279.

  • Yanagida M . (2000). Genes Cells, 5, 1–8.

  • Yoon HJ, Feoktistova A, Wolfe BA, Jennings JL, Link AJ and Gould KL . (2002). Curr. Biol., 12, 2048–2054.

  • Yu H, Peters JM, King RW, Page AM, Hieter P and Kirschner MW . (1998). Science, 279, 1219–1222.

  • Zachariae W and Nasmyth K . (1999). Genes Dev., 13, 2039–2058.

  • Zachariae W, Schwab M, Nasmyth K and Seufert W . (1998a). Science, 282, 1721–1724.

  • Zachariae W, Shevchenko A, Andrews PD, Ciosk R, Galova M, Stark MJ, Mann M and Nasmyth K . (1998b). Science, 279, 1216–1219.

  • Zachariae W, Shin TH, Galova M, Obermaier B and Nasmyth K . (1996). Science, 274, 1201–1204.

  • Zur A and Brandeis M . (2001). EMBO J., 20, 792–801.

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Acknowledgements

We are indebted to Dr Catherine Bonne-Andrea, Dr Carsten Janke and Dr May Morris for the critical reading of this manuscript. This work was supported by the Ligue Nationale Contre le Cancer (Equipe Labellisée).

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  1. Centre de Recherche de Biochimie Macromoléculaire, CNRS FRE 2593 1919 Route de Mende, 34293, Montpellier cedex, 5, France

    Anna Castro, Cyril Bernis, Suzanne Vigneron, Jean-Claude Labbé & Thierry Lorca

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Castro, A., Bernis, C., Vigneron, S. et al. The anaphase-promoting complex: a key factor in the regulation of cell cycle. Oncogene 24, 314–325 (2005). https://doi.org/10.1038/sj.onc.1207973

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