Chromosomal passengers: the four-dimensional regulation of mitotic events

Adams RR, Wheatley SP, Gouldsworthy AM, Kandels-Lewis SE, Carmena M, Smythe C, Gerloff DL, Earnshaw WC (2000) INCENP binds the aurora-related kinase AIRK2 and is required to target it to chromosomes, the central spindle and the cleavage furrow. Curr Biol 10:1075–1078 Adams RR, Carmena M, Earnshaw WC (2001a) Chromosomal passengers and the (aurora) ABCs of mitosis. Trends Cell Biol 11:49–54 Adams RR, Maiato H, Earnshaw WC, Carmena M (2001b) Essential roles of Drosophila inner centromere protein (INCENP) and Aurora-B in histone H3 phosphorylation, metaphase chromosome alignment, kinetochore disjunction, and chromosome segregation. J Cell Biol 153:865–880 Ainsztein AM, Kandels-Lewis SE, Mackay AM, Earnshaw WC (1998) INCENP centromere and spindle targeting: identification of essential conserved motifs and involvement of heterochromatin protein HP1. J Cell Biol 143:1763–1774 Ambrosini G, Adida C, Altieri DC (1997) A novel anti-apoptosis gene, survivin, expressed in cancer and lymphoma. Nat Med 3:917–921 Andreassen PR, Palmer DK, Wener MH, Margolis RL (1991) Telophase disk: a new mammalian mitotic organelle that bisects telophase cells with a possible function in cytokinesis. J Cell Sci 99:523–534 Andrews PD, Knatko E, Moore WJ, Swedlow JR (2003) Mitotic mechanics: the auroras come into view. Curr Opin Cell Biol 15:672–683 Andrews PD, Ovechkina Y, Morrice N, Wagenbach M, Duncan K, Wordeman L, Swedlow JR (2004) Aurora B regulates MCAK at the mitotic centromere. Dev Cell 6:253–268 Banks DP, Plescia J, Altieri DC, Chen J, Rosenberg SH, Zhang H, Ng SC (2000) Survivin does not inhibit caspase-3 activity. Blood 96:4002–4003 Beltrami E, Plescia J, Wilkinson JC, Duckett CS, Altieri DC (2004) Acute ablation of survivin uncovers p53-dependent mitotic checkpoint functions and control of mitochondrial apoptosis. J Biol Chem 279:2077–2084 Bernard M, Sanseau P, Henry C, Couturier A, Prigent C (1998) Cloning of STK13, a third human protein kinase related to Drosophila aurora and budding yeast Ipl1 that maps on chromosome 19q13.3-ter. Genomics 53:406–409 Bernat RL (1991) The human centromere proteins CENP-s A, B, and C: an in vivo analysis of centromere structure and function. Johns Hopkins University Press, Baltimore Biggins S, Murray AW (2001) The budding yeast protein kinase Ipl1/aurora allows the absence of tension to activate the spindle checkpoint. Genes Dev 15:3118–3129 Bishop JD, Schumacher JM (2002) Phosphorylation of the carboxyl terminus of inner centromere protein (INCENP) by the Aurora B kinase stimulates Aurora B kinase activity. J Biol Chem 277:27577–27580 Bolton MA, Lan W, Powers SE, McCleland ML, Kuang J, Stukenberg, PT (2002) Aurora B kinase exists in a complex with survivin and INCENP and its kinase activity is stimulated by survivin binding and phosphorylation. Mol Biol Cell 13:3064–3077 Carmena M, Earnshaw WC (2003) The cellular geography of aurora kinases. Nat Rev Mol Cell Biol 4:842–854 Carvalho A, Carmena M, Sambade C, Earnshaw WC, Wheatley SP (2003) Survivin is required for stable checkpoint activation in taxol-treated HeLa cells. J Cell Sci 116:2987–2998 Chantalat L, Skoufias DA, Kleman JP, Jung B, Dideberg O, Margolis RL (2000) Crystal structure of human survivin reveals a bow tie-shaped dimer with two unusual alpha-helical extensions. Mol Cell 6:183–189 Cheeseman IM, Anderson S, Jwa M, Green EM, Kang J-s, Yates JR, Chan CSM, Drubin DG, Barnes G (2002) Phospho-regulation of kinetochore-microtubule attachments by the aurora kinase Ipl1p. Cell 111:163–172 Cimini D, Howell B, Maddox P, Khodjakov A, Degrassi F, Salmon ED (2001) Merotelic kinetochore orientation is a major mechanism of aneuploidy in mitotic mammalian tissue cells. J Cell Biol 153:517–527 Cimini D, Moree B, Canman JC, Salmon ED (2003) Merotelic kinetochore orientation occurs frequently during early mitosis in mammalian tissue cells and error correction is achieved by two different mechanisms. J Cell Sci 116:4213–4225 Cooke CA, Heck MMS, Earnshaw WC (1987) The INCENP antigens: movement from the inner centromere to the midbody during mitosis. J Cell Biol 105:2053–2067 Cutts SM, Fowler KJ, Kile BT, Hii LLP, O’Dowd RA, Hudson DF, Saffery R, Kalitsis P, Earle E, Choo KHA (1999) Defective chromosome segregation, microtubule bundling and nuclear bridging in inner centromere protein gene (Incenp)-disrupted mice. Hum Mol Genet 8:1145–1155 Daub H, Gevaert K, Vandekerckhove J, Sobel A, Hall A (2001) Rac/Cdc42 and p65PAK regulate the microtubule-destabilizing protein stathmin through phosphorylation at serine 16. J Biol Chem 276:1677–1680 Di Fiore B, Ciciarello M, Lavia P (2004) Mitotic functions of the Ran GTPase network: the importance of being in the right place at the right time. Cell Cycle 3:305–313 Ditchfield C, Johnson VL, Tighe A, Ellston R, Haworth C, Johnson T, Mortlock A, Keen N, Taylor SS (2003) Aurora B couples chromosome alignment with anaphase by targeting bubR1, Mad2 and CENP-E to kinetochores. J Cell Biol 161:267–280 Earnshaw WC, Cooke CA (1991) Analysis of the distribution of the INCENPs throughout mitosis reveals the existence of a pathway of structural changes in the chromosomes during metaphase and early events in cleavage furrow formation. J Cell Sci 98:443–461 Eckley DM, Ainsztein AM, Mackay A, Goldberg IG, Earnshaw WC (1997a) Chromosomal proteins and cytokinesis: patterns of cleavage furrow formation and inner-centromere protein positioning in mitotic heterokaryons and mid-anaphase cells. J Cell Biol 136:1169–1183 Eckley DM, Ainsztein AM, Mackay AM, Goldberg IG, Earnshaw WC (1997b) Chromosomal proteins and cytokinesis: patterns of cleavage furrow formation and inner centromere protein positioning in mitotic heterokaryons and mid-anaphase cells. J Cell Biol 136:1169–1183 Fukata M, Watanabe T, Noritake J, Nakagawa M, Yamaga M, Kuroda S, Matsuura Y, Iwamatsu A, Perez F, Kaibuchi K (2002) Rac1 and Cdc42 capture microtubules through IQGAP1 and CLIP-170. Cell 109:873–885 Gassmann R, Carvalho A, Henzing AJ, Ruchaud S, Hudson DF, Honda R, Nigg EA, Gerloff DL, Earnshaw WC (2004) Borealin: a novel chromosomal passenger required for stability of the bipolar mitotic spindle. J Cell Biol 166:179–191 Giet R, Prigent C (1999) Aurora/Ipl1p-related kinases, a new oncogenic family of mitotic serine–threonine kinases. J Cell Sci 112:3591–3601 Giet R, Glover DM (2001) Drosophila aurora B kinase is required for histone H3 phosphorylation and condensin recruitment during chromosome condensation and to organize the central spindle during cytokinesis. J Cell Biol 152:669–682 Glover DM, Leibowitz MH, McLean DA, Parry H (1995) Mutations in aurora prevent centrosome separation leading to the formation of monopolar spindles. Cell 81:95–105 Gorbsky GJ (2004) Mitosis: MCAK under the Aura of Aurora B. Curr Biol 14:R346-R348 Gorbsky GJ, Ricketts WA (1993) Differential expression of a phosphoepitope at the kinetochores of moving chromosomes. J Cell Biol 122:1311–1321 Goto H, Yasui Y, Kawajiri A, Nigg EA, Terada Y, Tatsuka M, Nagata K, Inagaki M (2003) Aurora-B regulates the cleavage furrow-specific vimentin phosphorylation in the cytokinetic process. J Biol Chem 278:8526–8530 Gurley LR, Walters RA, Tobey RA (1974) Cell cycle-specific changes in histone phosphorylation associated with cell proliferation and chromosome condensation. J Cell Biol 60:356–364 Hagstrom KA, Holmes VF, Cozzarelli NR, Meyer BJ (2002) C. elegans condensin promotes mitotic chromosome architecture, centromere organization, and sister chromatid segregation during mitosis and meiosis. Genes Dev 16:729–742 Hauf S, Cole RW, LaTerra S, Zimmer C, Schnapp G, Walter R, Heckel A, Van Meel J, Rieder CL, Peters JM (2003) The small molecule Hesperadin reveals a role for Aurora B in correcting kinetochore-microtubule attachment and in maintaining the spindle assembly checkpoint. J Cell Biol 161:281–294 Honda R, Korner R, Nigg EA (2003) Exploring the functional interactions between Aurora B, INCENP, and survivin in mitosis. Mol Biol Cell 14:3325–3341 Hsu JY, Sun ZW, Li X, Reuben M, Tatchell K, Bishop DK, Grushcow JM, Brame CJ, Caldwell JA, Hunt DF, Lin R, Smith MM, Allis CD (2000) Mitotic phosphorylation of histone H3 is governed by Ipl1/aurora kinase and Glc7/PP1 phosphatase in budding yeast and nematodes. Cell 102:279–291 Hu HM, Chuang CK, Lee MJ, Tseng TC, Tang TK (2000) Genomic organization, expression, and chromosome localization of a third aurora-related kinase gene, Aie1. DNA Cell Biol 19:679–688 Hudson DF, Vagnarelli P, Gassmann R, Earnshaw WC (2003) Condensin is required for nonhistone protein assembly and structural integrity of vertebrate mitotic chromosomes. Dev Cell 5:323–336 Jantsch-Plunger V, Gonczy P, Romano A, Schnabel H, Hamill D, Schnabel R, Hyman AA, Glotzer M (2000) CYK-4: a Rho family GTPase activating protein (GAP) required for central spindle formation and cytokinesis. J Cell Biol 149:1391–1404 Kaitna S, Mendoza M, Jantsch-Plunger V, Glotzer M (2000) Incenp and an aurora-like kinase form a complex that is essential for chromosome segregation and for efficient completion of cytokinesis. Curr Biol 10:1172–1181 Kaitna S, Pasierbek P, Jantsch M, Loidl J, Glotzer M (2002) The Aurora B kinase AIR-2 regulates kinetochores during mitosis and is required for separation of homologous chromosomes during meiosis. Curr Biol 12:798–812 Kawajiri A, Yasui Y, Goto H, Tatsuka M, Takahashi M, Nagata K, Inagaki M (2003) Functional significance of the specific sites phosphorylated in desmin at cleavage furrow: Aurora-B may phosphorylate and regulate type III intermediate filaments during cytokinesis coordinatedly with Rho-kinase. Mol Biol Cell 14:1489–1500 Ke YW, Dou Z, Zhang J, Yao XB (2003) Function and regulation of Aurora/Ipl1p kinase family in cell division. Cell Res 13:69–81 Kim JH, Kang JS, Chan CS (1999) Sli15 associates with the ipl1 protein kinase to promote proper chromosome segregation in Saccharomyces cerevisiae. J Cell Biol 145:1381–1394 Kimura M, Matsuda Y, Yoshioka T, Sumi N, Okano Y (1998) Identification and characterization of STK12/Aik2: a human gene related to aurora of Drosophila and yeast IPL1. Cytogenet Cell Genet 82:147–152 Kline-Smith SL, Khodjakov A, Hergert P, Walczak CE (2004) Depletion of centromeric MCAK leads to chromosome congression and segregation defects due to improper kinetochore attachments. Mol Biol Cell 15:1146–1159 Kobayashi K, Hatano M, Otaki M, Ogasawara T, Tokuhisa T (1999) Expression of a murine homologue of the inhibitor of apoptosis protein is related to cell proliferation. Proc Natl Acad Sci USA 96:1457–1462 Kunitoku N, Sasayama T, Marumoto T, Zhang D, Honda S, Kobayashi O, Hatakeyama K, Ushio Y, Saya H, Hirota T (2003) CENP-A phosphorylation by Aurora-A in prophase is required for enrichment of Aurora-B at inner centromeres and for kinetochore function. Dev Cell 5:853–864 Lampson MA, Renduchitala K, Khodjakov A, Kapoor TM (2004) Correcting improper chromosome-spindle attachments during cell division. Nat Cell Biol 6:232–237 Lan W, Zhang X, Kline-Smith SL, Rosasco SE, Barrett-Wilt GA, Shabanowitz J, Hunt DF, Walczak CE, Stukenberg PT (2004) Aurora B phosphorylates centromeric MCAK and regulates its localization and microtubule depolymerization activity. Curr Biol 14:273–286 Lens SMA, Wolthuis RMF, Klompmaker R, Kauw J, Agami R, Brummelkamp T, Kops G, Medema RH (2003) Survivin is required for a sustained spindle checkpoint arrest in response to lack of tension. EMBO J 22:2934–2947 Li F, Altieri DC (1999) Transcriptional analysis of human survivin gene expression. Biochem J 344(Pt 2):305–311 Li F, Ambrosini G, Chu EY, Plescia J, Tognin S, Marchisio PC, Altieri DC (1998) Control of apoptosis and mitotic spindle checkpoint by survivin. Nature 396:580–584 Losada A, Hirano M, Hirano T (2002) Cohesin release is required for sister chromatid resolution, but not for condensin-mediated compaction, at the onset of mitosis. Genes Dev 16:3004–3016 MacCallum DE, Losada A, Kobayashi R, Hirano T (2002) ISWI remodeling complexes in Xenopus egg extracts: identification as major chromosomal components that are regulated by INCENP-aurora B. Mol Biol Cell 13:25–39 Mackay AM, Eckley DM, Chue C, Earnshaw WC (1993) Molecular analysis of the INCENPs (inner centromere proteins): separate domains are required for association with microtubules during interphase and with the central spindle during anaphase. J Cell Biol 123:373–385 Mackay AM, Ainsztein AM, Eckley DM, Earnshaw WC (1998) A dominant mutant of inner centromere protein (INCENP), a chromosomal protein, disrupts prometaphase congression and cytokinesis. J Cell Biol 140:991–1002 Maney T, Hunter AW, Wagenbach M, Wordeman L (1998) Mitotic centromere-associated kinesin is important for anaphase chromosome segregation. J Cell Biol 142:787–801 Martineau-Thuillier S, Andreassen PR, Margolis RL (1998) Colocalization of TD-60 and INCENP throughout G2 and mitosis: evidence for their possible interaction in signalling cytokinesis. Chromosoma 107:461–470 Marusawa H, Matsuzawa S, Welsh K, Zou H, Armstrong R, Tamm I, Reed JC (2003) HBXIP functions as a cofactor of survivin in apoptosis suppression. EMBO J 22:2729–2740 Meraldi P, Honda R, Nigg EA (2004) Aurora kinases link chromosome segregation and cell division to cancer susceptibility. Curr Opin Genet Dev 14:29–36 Minoshima Y, Kawashima T, Hirose K, Tonozuka Y, Kawajiri A, Bao YC, Deng X, Tatsuka M, Narumiya S, May WS, Nosaka T, Semba K, Inoue T, Satoh T, Inagaki M, Kitamura T (2003) Phosphorylation by Aurora B converts MgcRacGAP to a RhoGAP during cytokinesis. Dev Cell 4:549–560 Mishima M, Kaitna S, Glotzer M (2002) Central spindle assembly and cytokinesis require a kinesin-like protein/RhoGAP complex with microtubule bundling activity. Dev Cell 2:41–54 Mollinari C, Reynaud C, Martineau-Thuillier S, Monier S, Kieffer S, Garin J, Andreassen PR, Boulet A, Goud B, Kleman JP, Margolis RL (2003) The mammalian passenger protein TD-60 is an RCC1 family member with an essential role in prometaphase to metaphase progression. Dev Cell 5:295–307 Morishita J, Matsusaka T, Goshima G, Nakamura T, Tatebe H, Yanagida M (2001) Bir1/Cut17 moving from chromosome to spindle upon the loss of cohesion is required for condensation, spindle elongation and repair. Genes Cells 6:743–763 Morrison C, Henzing AJ, Jensen ON, Osheroff N, Dodson H, Kandels-Lewis SE, Adams RR, Earnshaw WC (2002) Proteomic analysis of human metaphase chromosomes reveals topoisomerase II alpha as an Aurora B substrate. Nucleic Acids Res 30:5318–5327 Muchmore SW, Chen J, Jakob C, Zakula D, Matayoshi ED, Wu W, Zhang H, Li F, Ng SC, Altieri DC (2000) Crystal structure and mutagenic analysis of the inhibitor-of-apoptosis protein survivin. Mol Cell 6:173–182 Murata-Hori M, Wang YL (2002) Both midzone and astral microtubules are involved in the delivery of cytokinesis signals: insights from the mobility of aurora B. J Cell Biol 159:45–53 Murata-Hori M, Fumoto K, Fukuta Y, Iwasaki T, Kikuchi A, Tatsuka M, Hosoya H (2000) Myosin II regulatory light chain as a novel substrate for AIM-1, an aurora/Ipl1p-related kinase from rat. J Biochem (Tokyo) 128:903–907 Murnion ME, Adams RR, Callister DM, Allis CD, Earnshaw WC, Swedlow JR (2001) Chromatin-associated protein phosphatase 1 regulates aurora-B and histone H3 phosphorylation. J Biol Chem 276:26656–26665 Nigg EA (2001) Mitotic kinases as regulators of cell division and its checkpoints. Nat Rev Mol Cell Biol 2:21–32 O’Connor DS, Grossman D, Plescia J, Li F, Zhang H, Villa A, Tognin S, Marchisio PC, Altieri DC (2000) Regulation of apoptosis at cell division by p34cdc2 phosphorylation of survivin. Proc Natl Acad Sci USA 97:13103–13107 Oegema K, Desai A, Rybina S, Kirkham M, Hyman AA (2001) Functional analysis of kinetochore assembly in Caenorhabditis elegans. J Cell Biol 153:1209–1226 Ohi R, Coughlin ML, Lane WS, Mitchison TJ (2003) An inner centromere protein that stimulates the microtubule depolymerizing activity of a KinI kinesin. Dev Cell 5:309–321 Parra MT, Viera A, Gomez R, Page J, Carmena M, Earnshaw WC, Rufas JS, Suja JA (2003) Dynamic relocalization of the chromosomal passenger complex proteins inner centromere protein (INCENP) and aurora-B kinase during male mouse meiosis. J Cell Sci 116:961–974 Pereira G, Schiebel E (2003) Separase regulates INCENP-Aurora B anaphase spindle function through Cdc14. Science 302:2120–2124 Rogers E, Bishop JD, Waddle JA, Schumacher JM, Lin R (2002) The aurora kinase AIR-2 functions in the release of chromosome cohesion in Caenorhabditis elegans meiosis. J Cell Biol 157:219–229 Romano A, Guse A, Krascenicova I, Schnabel H, Schnabel R, Glotzer M (2003) CSC-1: a subunit of the Aurora B kinase complex that binds to the survivin-like protein BIR-1 and the incenp-like protein ICP-1. J Cell Biol 161:229–236 Sampath SC, Ohi R, Leismann O, Salic A, Pozniakovski A, Funabiki H (2004) The chromosomal passenger complex is required for chromatin-induced microtubule stabilization and spindle assembly. Cell (in press) Savoian M, Earnshaw WC, Khodjakov A, Rieder CL (1999) Cleavage furrows formed between centrosomes in fused PtK1 cells that lack an intervening spindle and chromosomes contain microtubule bundles, INCENP and CHO1 but not CENP-E. Mol Biol Cell 10:297–311 Schumacher JM, Golden A, Donovan PJ (1998) AIR-2: an Aurora/Ipl1-related protein kinase associated with chromosomes and midbody microtubules is required for polar body extrusion and cytokinesis in Caenorhabditis elegans embryos. J Cell Biol 143:1635–1646 Severson AF, Hamill DR, Carter JC, Schumacher J, Bowerman B (2000) The aurora-related kinase AIR-2 recruits ZEN-4/CeMKLP1 to the mitotic spindle at metaphase and is required for cytokinesis. Curr Biol 10:1162–1171 Skoufias DA, Mollinari C, Lacroix FB, Margolis RL (2000) Human survivin is a kinetochore-associated passenger protein. J Cell Biol 151:1575–1582 Song Z, Liu S, He H, Hoti N, Wang Y, Feng S, Wu M (2004) A single amino acid change (Asp 53→ Ala53) converts survivin from anti-apoptotic to pro-apoptotic. Mol Biol Cell 15:1287–1296 Tamm I, Wang Y, Sausville E, Scudiero DA, Vigna N, Oltersdorf T, Reed JC (1998) IAP-family protein survivin inhibits caspase activity and apoptosis induced by Fas (CD95), Bax, caspases, and anticancer drugs. Cancer Res 58:5315–5320 Tanaka TU, Rachidi N, Janke C, Pereira G, Galova M, Schiebel E, Stark MJ, Nasmyth K (2002) Evidence that the Ipl1-Sli15 (Aurora kinase-INCENP) complex promotes chromosome bi-orientation by altering kinetochore-spindle pole connections. Cell 108:317–329 Tatsuka M, Katayama H, Ota T, Tanaka T, Odashima S, Suzuki F, Terada Y (1998) Multinuclearity and increased ploidy caused by overexpression of the Aurora- and Ipl1-like midbody-associated protein mitotic kinase in human cancer cells. Cancer Res 58:4811–4816 Temme A, Rieger M, Reber F, Lindemann D, Weigle B, Diestelkoetter-Bachert P, Ehninger G, Tatsuka M, Terada Y, Rieber EP (2003) Localization, dynamics, and function of survivin revealed by expression of functional survivinDsRed fusion proteins in the living cell. Mol Biol Cell 14:78–92 Terada Y, Tatsuka M, Suzuki F, Yasuda Y, Fujita S, Otsu M (1998) AIM-1: a mammalian midbody-associated protein required for cytokinesis. EMBO J 17:667–676 Tseng TC, Chen SH, Hsu YP, Tang TK (1998) Protein kinase profile of sperm and eggs: cloning and characterization of two novel testis-specific protein kinases (AIE1, AIE2) related to yeast and fly chromosome segregation regulators. DNA Cell Biol 17:823–833 Uren AG, Wong L, Pakusch M, Fowler KJ, Burrows FJ, Vaux DL, Choo KHA (2000) Survivin and the inner centromere protein INCENP show similar cell-cycle localization and gene knockout phenotype. Curr Biol 10:1319–1328 Verdecia MA, Huang H, Dutil E, Kaiser DA, Hunter T, Noel JP (2000) Structure of the human anti-apoptotic protein survivin reveals a dimeric arrangement. Nat Struct Biol 7:602–608 Wheatley SP, Wang Y (1996) Midzone microtubule bundles are continuously required for cytokinesis in cultured epithelial cells. J Cell Biol 135:981–989 Wheatley SP, Carvalho A, Vagnarelli P, Earnshaw WC (2001a) INCENP is required for proper targeting of survivin to the centromeres and the anaphase spindle during mitosis. Curr Biol 11:886–890 Wheatley SP, Kandels-Lewis SE, Adams RR, Ainsztein AM, Earnshaw WC (2001b) INCENP binds directly to tubulin and requires dynamic microtubules to target to the cleavage furrow. Exp Cell Res 262:122–127 Wheatley SP, Henzing AJ, Dodson H, Khaled W, Earnshaw WC (2004) Aurora-B phosphorylation in vitro identifies a residue of survivin that is essential for its localization and binding to inner centromere protein (INCENP) in vivo. J Biol Chem 279:5655–5660 Yasui Y, Urano T, Kawajiri A, Nagata K, Tatsuka M, Saya H, Furukawa K, Takahashi T, Izawa I, Inagaki M (2004) Autophosphorylation of a newly identified site of Aurora-B is indispensable for cytokinesis. J Biol Chem 279:12997–13003 Zeitlin SG, Shelby RD, Sullivan KF (2001) CENP-A is phosphorylated by Aurora B kinase and plays an unexpected role in completion of cytokinesis. J Cell Biol 155:1147–1157