Mitosis in vertebrates: the G2/M and M/A transitions and their associated checkpoints

Abrieu A, Kahana JA, Wood KW, Cleveland DW (2000) CENP-E as an essential component of the mitotic checkpoint in vitro. Cell 102:817–826

Adams RH, Poras A, Alonso G, Jones M, Vintersten K, Panelli S, Valladares A, Perez L, Klein R, Nebreda AR (2000) Essential role of p38-MAP kinase in placental but not embryonic cardiovascular development. Mol Cell 6:109–116

Andreassen PR, Margolis RL (1994) Microtubule dependency of p34cdc2 inactivation and mitotic exit in mammalian cells. J Cell Biol 127:789–802

Baek K-H, Shin H-J, Jeong S-J et al (2005) Caspases-dependent cleavage of mitotic checkpoint proteins in response to microtubule inhibitor. Oncol Res 15:161–168

Baumann C, Korner R, Hofmann K, Nigg EA (2007) PICH, a centromere-associated SNF2 family ATPase, is regulated by PlK1 and required for the spindle checkpoint. Cell 128:101–114

Bayart E, Grigorieve O, Leibovitch S, Onclercq-Delic R, Amor-Gueret M (2004) A major role for mitotic cdc2 kinase inactivation in the establishment of the mitotic DNA damage checkpoint. Cancer Res 64:8954–8959

Beltrami E, Plescia J, Wilkinson JC, Duckett CS, Altiedri DC (2004) Acute ablation of survivin uncovers p-53 dependent mitotic checkpoint functions and control of mitochondrial apoptosis. J Biol Chem 279:2077–2084

Bower JJ, Zhou Y, Zhou T et al. (2010) Revised genetic requirements for the decatenation G(2) checkpoint: the role of AMT. Cell Cycle 9:1617–1628

Brito DA, Rieder CL (2006) Mitotic checkpoint slippage in humans occurs via cyclin B destruction in the presence of an active checkpoint. Curr Biol 26:1194–2000

Brito DA, Rieder CL (2009) The ability to survive mitosis in the presence of microtubule poisons differs significantly between human nontransformed (RPE-1) and cancer (U2OS, HeLa) cells. Cell Motil Cytoskeleton 66:437–447

Brito DA, Yang Z, Rieder CL (2008) Microtubules do not promote mitotic slippage when the spindle assembly checkpoint cannot be satisfied. J Cell Biol 182:623–629

Bulavin DV, Amundson SA, Fornace AJ (2002) p38 and Chk1 kinases: different conductors for the G(2)/M checkpoint symphony. Curr Opin Genet Dev 12:92–97

Bullough WS, Johnson M (1951) The energy relations of mitotic activity in adult mouse epidermis. Proc Royal Soc Lond B 138:562–575

Burgess A, Labbe J-C, Vigneron S et al (2008) Chfr intracts and colocalizes with TCTP to the mitotic spindle. Oncogene 27:5554–5566

Cameron IL, Cleffmann G (1964) Initiation of mitosis in relation to the cell cycle following feeding of starved chickens. J Cell Biol 21:169–174

Carrassa L, Sanchez Y, Erba E et al (2009) U2OS cells lackig Chk1 undergo aberrant mitosis and fail to activate the spindle checkpoint. J Cell Mol Med 13:1565–1576

Chin CF, Yeong FM (2010) Safeguarding entry into mitosis: the antephase checkpoint. Mol Cell Biol 30:22–32

Cimini D (2007) Detection and correction of merotelic kinetochore orientation by Aurora B and its partners. Cell Cycle 6:1558–1564

Cimini D, Cameron LA, Salmon ED (2004) Anaphase spindle mechanics prevent mis-segregation of merotelically oriented chromosomes. Curr Biol 14:2149–2155

Connor F, Bertwistle D, Mee PJ et al (1997) Tumorigenesis and DNA repair defect in mice with a truncating BRCA2 mutation. Nat Genet 17:423–430

Crosio C, Fimia GM, Loury R et al (2002) Mitotic phosphorylation of histone H3: spatio-temporal regulation by mammalian Aurora kinases. Mol Cell Biol 22:874–885

Cross SM, Sanchez CA, Morgan CA et al (1995) A p53-dependent mouse spindle checkpoint. Science 267:1353–1356

Daniels MJ, Wang Y, Lee M, Venkitaraman AR (2004) Abnormal cytokinesis in cells deficient in the breast cancer susceptibility protein BRAC2. Science 306:876–879

Demming PB, Cistulli CA, Zhao H et al (2001) The human decatenation checkpoint. Proc Natl Acad Sci USA 98:12044–12049

Dobles M, Liberal V, Scott ML, Benezera R, Sorger PK (2000) Chromosome missegration and apoptosis in mice lacking the mitotic checkpoint protein Mad2. Cell 101:635–645

Donehower LA, Harvery M, Slagle BL et al (1992) Mice deficient for p53 are developmentally normal but susceptible to spontaneous tumors. Nature 356:215–221

Dotiwala F, Harrison JC, Jain S, Sugawara N, Haber JE (2010) Mad2 prolongs DNA damage checkpoint arrest caused by a double-strand break via a centromere-dependent mechanism. Curr Biol 20:328–332

Eberle AB, HEssle V, Helbig R et al (2010) Splice-site mutations cause Rrp6-mediated nuclear retention of the unspliced RNAs and transcriptional down-regulation of the splicing-defective genes. PLoS ONE 5:e11540

Ehrhardt AG, Sluder G (2005) Spindle pole fragmentation due to proteasome inhibition. J Cell Physiol 204:808–818

Escote X, Zapater M, Clotet J, Posas F (2004) Hog mediates cell-cycle arrest in G1 phase by the dual targeting of Sic1. Nat Cell Biol 6:997–1002

Futamura M, Arakawa H, Matsuda K et al (2000) Potential role of BRCA2 in mitotic checkpoint after phosphorylation by hBUBR1. Cancer Res 60:1531–1535

Gascoigne KE, Taylor SS (2008) Cancer cells display profound intra- and interline variation following prolonged exposure to antimitotic drugs. Cancer Cell 14:111–122

Gelfant S (1977) A new concept of tissue and tumor cell proliferation. Cancer Res 37:3845–3862

Giunta S, Belotserkovskaya R, Jackson SP (2010) DNA damage signaling in response to double-strand breaks during mitosis. J Cell Biol 190:197–207

Gordon RE, Lane BP (1980) Wound repair in rat tracheal epithelium: division of G1 and G2-arrested cells following injury. Lab Invest 42:616–621

Green HN, Bullough WS (1950) Mitotic activity in the shock state. Br J Exp Pathol 31:175–182

Haller K, Kibler KV, Kasai T et al (2006) The N-terminus of rodent and human Mad1 confers species-specific stringency to the spindle assembly checkpoint. Oncogene 25:2137–2147

Hartwell LH, Weinert TA (1989) Checkpoints: controls that ensure the order of cell cycle events. Science 246:629–634

Hauf S, Cole RW, LaaTerra S et al (2003) The small molecule Hesperadin reveals a role for Aurora B in correcting kinetochore-microtubule attachment and in maintaining the spindle checkpoint. J Cell Biol 161:281–294

Hendzel MJ, Wei Y, Mancini MA et al (1997) Mitosis-specific phosphorylation of histone-H3 initiates primarily within pericentromeric heterochromatin during G2 and spreads in an orderly fashion coincident with chromosome condensation. Chromosoma 106:348–360

Hiraoka Y, Minden JS, Swedlow JR, Sedat JW, Agard DA (1989) Focal points for chromosome condensation and decondensaton revealed by three-dimensional in vivo time-lapse microscopy. Nature 342:293–296

Howard A, Pelc SR (1953) Synthesis of desoxyribonucleic acid in normal and irradiated cells and its relation to chromosome breakage. Heredity 6(Suppl):261–273

Hsu S-L, Yu C-T, Ying S-C et al (2006) Caspase 3, periodically expressed and activated at G2/M transition, is required for nocodazole-induced mitotic checkpoint. Apoptosis 11:765–771

Hubner NC, Wang LH, Kaulich M, Descombes P, Poser I, Nigg EA (2010) Re-examination of siRNA specificity questions role of PICH and Tao1 in spindle checkpoint and identifies Mad2 as a sensitive target for small RNAs. Chromosoma 119:149–165

Ikui AE, Yang CP, Matsumoto T, Horwitz SB (2005) Low concentrations of taxol cause mitotic delay followed by premature dissociation of p55CDC from Mad2 and BubR1 and abrogation of the spindle checkpoint, leading to aneuploidy. Cell Cycle 4:1385–1388

Jirmanova L, Bulavin DV, Fornace AJ (2005) Inhibition of the ATR/Chk1 pathway induces a p38-dependent S-phase delay in mouse embryonic stem cells. Cell Cycle 4:1428–1434

Jordan MA, Thrower DA, Wilson L (1992) Effects of vinblastine, podophyllotoxin and nocodazole on mitotic spindles: implications for the role of microtubule dynamics in mitosis. J Cell Sci 102:401–416

Kaneko H, Watanabe H, Hosokawa Y et al (1984) The presence of G1 and G2 populations in normal epithelium of rat urinary bladder. Basic Appl Histochem 28:41–57

Kapoor TM, Mayer TU, Coughlin ML, Mitchison TJ (2000) Probing spindle assembly mechanisms with monastrol, a small molecule inhibitor of the mitotic kinesin, Eg5. J Cell Biol 150:975–988

Karlsson-Rosenthal C, Millar JB (2006) Chk25: mechanisms of checkpoint inhibition and recovery. Tr Cell Biol 16:285–292

Kasai T, Iwanaga Y, Iha H, Jeang K-T (2002) Prevalent loss of mitotic spindle checkpoint in adult T-cell leukemia confers resistance to microtubule inhibitors. J Biol Chem 277:5187–5193

Kazerouninia A, Ngo B, Martinson HG (2010) Poly (A) signal-dependent degradation of unprocessed nascent transcripts accompanies poly(A) signal-dependent transcriptional pausing in vitro. RNA 16:197–210

Khodjakov A, Rieder CL (2009) The nature of cell-cycle checkpoints: facts and fallacies. J Biol 8:88.1–88.5

Kienitz A, Vogel C, Morales I, Muller R, Bastians H (2005) Partial downregulation of Mad1 causes spindle checkpoint inactivation and aneuploidy, but does not confer resistance towards taxol. Oncogene 24:4301–4310

Kim M, Murphy K, Liu F et al (2005) Caspase-mediated specific cleavage of BubR1 is a determinant of mitotic progression. Mol Cell Biol 25:9232–9248

Kim M, Liao J, Dowling ML et al (2008) TRAIL inactivates the mitotic checkpoint and potentiates death induced by microtubule-targeting agents in human cancer cells. Cancer Res 68:3440–3449

King JM, Nicklas RB (2000) Tension on chromosomes increases the number of kinetochore microtubules but only within limits. J Cell Sci 113:3815–3823

Kops GJ (2008) The kinetochore and spindle checkpoint in mammals. Front Biosci 13:3606–3620

Kruman II, Ilyasova EN, Rudchenko SA, Khurkhulu ZS (1988) The intestinal epithelial cells of ground squirrel (Citellus undulatus) accumulate at G2 phase of the cell cycle throughout a bout of hibernation. Comp Biochem Physiol A Comp Physiol 90:233–236

Kunitoku N, Sasayama T, Marumoto T et al (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

Lafarga V, Cuadrado A, Lopez de Silanes I, Bengoechea R, Fernandez-Capetillo O, Nebreda AR (2009) P38 mitogen-activated protein kinase- and HuR-dependent stabilization of p21(Clip1) mRNA mediates the G(1)/S checkpoint. Mol Cell Biol 29:4341–4351

Lajtha LG, Oliber R, Ellis F (1954) Incorporation of 32P and adenine 14C into DNA by human bone marrow cells in vitro. Br J Cancer 8:367–379

Lajtha LG, Oliver R, Gurney CW (1962) Kinetic model of a bone-marrow stem-cell population. Br J Haematol 8:442–460

Lampson MA, Renduchitala K, Khodjakov A, Kapoor TM (2004) Correcting improper chromosome-spindle attachments during cell division. Nat Cell Biol 6:232–237

Lanni JS, Jacks T (1998) Characterization of the p53-dependent postmitotic checkpoint following spindle disruption. Mol Cell Biol 18:1055–1064

Laoukili J, Kooistra MR, Bras A et al (2005) FoxM1 is required for execution of the mitotic programme and chromosome stability. Nat Cell Biol 2:126–136

Lee K, Kenny AE, Rieder CL (2010a) P38 mitogen-activated protein kinase activity is required during mitosis for timely satisfaction of the mitotic checkpoint but not for the fidelity of chromosome segregation. Mol Biol Cell 21:2150–2160

Lee J, Kim JA, Margolis RL, Fotedar R (2010b) Substrate degradation by the anaphase promoting complex occurs during mitotic slippage. Cell Cycle 9:1792–1801

Li X, Nicklas RB (1995) Mitotic forces control a cell-cycle checkpoint. Nature 373:630–632

Lilly MA, Duronio RJ (2005) New insights into cell cycle control from the Drosophila endocycle. Oncogene 24:2765–2775

Loncarek J, Kisurina-Evgenieva O, Vinogradova T et al (2007) The centromere geometry essential for keeping mitosis error free is controlled by spindle forces. Nature 450:745–750

Manchado E, Eguren M, Malumbres M (2010) The anaphase-promoting complex/cyclosomes (APC/C): cell-cycle dependent and independent functions. Biochem Soc Trans 38:65–71

Maresca TJ, Salmon ED (2010) Welcome to a new kind of tension: translating kinetochore mechanics into a wait-anaphase signal. J Cell Sci 123:825–835

Matsusaka T, Pines J (2004) Chfr acts with the p38 stress kinase to block entry into mitosis in mammalian cells. J Cell Biol 166:507–516

Mazia D (1961) Mitosis and the physiology of cell division. In: Brachet J, Mirsky AE (eds) The cell, vol 3. Academic, New York, pp 77–412

McEwen BF, Dong Y (2009) Releasing the spindle assembly checkpoint without tension. J Cell Biol 184:355–366

McEwen BF, Heagle AB, Cassels GO, Buttle KF, Rieder CL (1997) Kinetochore fiber maturation in PtK1 cells and its implications for the mechanism of chromosome congression and anaphase onset. J Cell Biol 137:1567–1580

Meraldi P, Draviam VM, Sorger PK (2004) Timing and checkpoints in the regulation of mitotic progression. Dev Cell 7:45–60

Mikhailov A, Cole RW, Rieder CL (2002) DNA damage during mitosis in human cells delays the metaphase/anaphase transition via the spindle-assembly checkpoint. Curr Biol 12:1797–1806

Mikhailov A, Shinohara M, Rieder CL (2005) The p38-mediated stress-activated checkpoint: a rapid response system for delaying progression through antephase and entry into mitosis. Cell Cycle 4:57–62

Mikhailov A, Patel D, McCance DJ, Rieder CL (2007) The G2 p38-mediated stress-activated checkpoint pathway becomes attenuated in transformed cells. Curr Biol 17:2162–2168

Mikhaiov A, Shinohara M, Rieder CL (2004) Topoisomerase II and histone deacetylase inhibitors delay the G2/M transition by triggering the p38 MAPK checkpoint pathway. J Cell Biol 166:517–526

Murray AW (1992) Creative blocks: cell-cycle checkpoints and feedback controls. Nature 359:599–604

Nicklas RB, Arana P (1992) Evolution and the meaning of metaphase. J Cell Sci 102:681–690

Nicklas RB, Waters JC, Salmon ED, Ward SC (2001) Checkpoint signals in grasshopper meiosis are sensitive to microtubule attachment, but tension is still essential. J Cell Sci 114:4173–4183

O’Connell CB, Loncarek J, Hergert P, Kouridis A, Conklin DS, Khodkajov A (2008) The spindle assembly checkpoint is satisfied in the absence of interkinetochore tension during mitosis with unreplicated genomes. J Cell Biol 183:29–36

Oh YM, Kwon YE, Kim JM et al (2009) Chfr is linked to tumor metastasis through the downregulation of HDAC1. Nat Cell Biol 11:295–302

Orth JD, Tang Y, Shi J et al (2008) Quantitative live imaging of cancer and normal cells treated with kinesin-5 inhibitors indicates significant differences in phenotypic responses and cell fate. Mol Cancer Ther 7:3480–3489

Park I, Avraham HK (2006) Cell cycle-dependent DNA damage signaling induced by ICRF-193 involves ATM, ATR, CHK2 and BRCA1. Exp Cell Res 312:1996–2008

Pines J, Rieder CL (2001) Re-staging mitosis: a contemporary view of mitotic progression. Nat Cell Biol 3:E3–E6

Pinsky BA, Kung C, Shokat KM, Biggins S (2006) The Ipl1-Aurora protein kinase activates the spindle checkpoint by creating unattached kinetochores. Nat Cell Biol 8:78–83

Puck TT, Steffen J (1963) Life cycle analysis of mammalian cells. I. a method for localizing metabolic events within the life cycle, and its application to the action of colcemid and sublethal doses of X-irradiation. Biophys J 3:379–397

Rieder CL (1990) Formation of the astral mitotic spindle: ultrastructural basis for the centrosome–kinetochore interaction. Electron Microsc Rev 3:269–300

Rieder CL, Cole RW (1998) Entry into mitosis in vertebrate somatic cells is guarded by a chromosome damage checkpoint that reverses the cell cycle when triggered during early but not late prophase. J Cell Biol 142:1013–1022

Rieder CL, Cole RW (2000) Microscopy-induced radiation damage, microtubules, and progression through the terminal stage of G2 (prophase) in vertebrate somatic cells. Cold Spring Harb Symp Quant Biol 65:369–376

Rieder CL, Davison EA, Jensen LC, Cassimeris L, Salomon ED (1986) Oscillatory movements of monooriented chromosomes and their position relative to the spindle pole result from the ejection properties of the aster and half spindle. J Cell Biol 103:581–591

Rieder CL, Schultz A, Cole R, Sluder G (1994) Anaphase onset in vertebrate somatic cells is controlled by a checkpoint that monitors sister kinetochore attachment to the spindle. J Cell Biol 127:1301–1310

Rieder CL, Cole RW, Khodjakov A, Sluder G (1995) The checkpoint delaying anaphase in response to chromosome monorientation is mediated by an inhibitory signal produced by unattached kinetochores. J Cell Biol 130:941–948

Ris H, Tolmach LJ, Lajtha LG, Smith CL, Das NK, Zeuthen E (1963) Differential sensitivity of the cell life cycle. J Cell Comp Physiol 62(Suppl 1):141–156

Rogakou EP, Boon C, Redon C, Bonner WM (1999) Megabase chromatin domains involved in DNA double-strand breaks in vivo. J Cell Biol 146:905–916

Saekl A, Tamura S, Ito N et al (2002) Frequent impairment of the spindle assembly checkpoint in hepatocellular carcinoma. Cancer 94:2047–2054

Salmon ED, Cimini D, Cameron LA, DeLuca JG (2005) Merotelic kinetochores in mammalian tissue cells. Philos Trans R Soc Lond B Biol Sci 360:553–568

Sarkar A, Eroglu S, Poirier MG, Bupta P, Nemani A, Marko JF (2002) Dynamics of chromosome compaction during mitosis. Exp Cell Res 277:48–56

Seville LL, Shaw N, Westwell AD, Chan WC (2005) Modulation of pRB/E2F functions in the regulation of cell cycle and in cancer. Cur Cancer Drug Targets 5:159–170

Shi J, Orth JD, Mitchison T (2008) Cell type variation in response to antimitotic drugs that target microtubules and kinesin-5. Cancer Res 68:3269–3276

Shin HJ, Baek KH, Jeon AH et al (2003) Dual roles of human BubR1, a mitotic checkpoint kinase, in the monitoring of chromosomal instability. Cancer Cell 4:483–497

Shinohara M, Mikhailov AV, Aguirre-Ghiso JA, Rieder CL (2006) Extracellular signal-regulated kinase 1/2 activity is not required in mammalian cells during late G2 for timely entry into or exit from mitosis. Mol Biol Cell 17:5227–5240

Takagi M, Delia D, Chessa L et al (1998) Defective control of apoptosis, radiosensitivity, and spindle checkpoint in ataxia telangiectasia. Cancer Res 58:4923–4929

Takenaka K, Moriguchi T, Nishida E (1998) Activation of the protein kinase p38 in the spindle assembly checkpoint and mitotic arrest. Science 280:599–602

Tang J, Yang X, Liu X (2008) Phosphorylation of Plk1 at Ser326 regulates its function during mitotic progression. Oncogene 27:6635–6645

Temin HM (1968) Carcinogenesis by avian sarcoma viruses. X. The decreased requirement for insulin-replaceable activity in serum for cell multiplication. Int J Cancer 3:771–787

Thornton TM, Rincon M (2009) Non-classical p38 map kinase functions: cell cycle checkpoints and survival. Int J Biol Sci 5:44–51

Uetake Y, Sluder G (2004) Cell cycle progression after cleavage failure: mammalian somatic cells do not possess a “tetraploidy checkpoint”. J Cell Biol 165:609–615

Uetake Y, Sluder G (2010) Prolonged prometaphase blocks daughter cell proliferation despite normal completion of mitosis. Curr Biol 20:1666–1671. doi: 10.1016/j.cub2010.08.018

Uetake Y, Loncarek J, Nordberg JJ et al (2007) Cell cycle progression and de novo centriole assembly after centrosomal removal in untransformed human cells. J Cell Biol 176:173–182

Vogel C, Kienitz A, Hofmann I, Muller R, Bastians H (2004) Crosstalk of the mitotic spindle assembly checkpoint with p53 to prevent polyploidy. Oncogene 23:6845–6853

Wang Q, Liu T, Fang YL et al (2004) BubR1 deficiency results in abnormal megakaryopoiesis. Blood 103:1278–1285

Waters JC, Chen RH, Murray AW, Salmon ED (1998) Localization of Mad2 to kinetochores depends on microtubule attachment, not tension. J Cell Biol 141:1181–1191

Weinert TA, Hartwell L (1988) The RAD9 gene controls the cell cycle response to DNA damage in Saccharomyces cerevisiae. Science 241:317–322

Westendorf JM, Rao PN, Gerace L (1994) Cloning of cDNAs for M-phase phosphoproteins recognized by the MPM2 monoclonal antibody and determination of the phosphorylated epitope. Proc Nat Acad Sci USA 91:714–718

Yang Z, Kenny AE, Brito DA, Rieder CL (2009) Cells satisfy the mitotic checkpoint in Taxol, and do so faster in concentrations that stabilize syntelic attachments. J Cell Biol 186:675–684

Yen AH, Yang JL (2010) Cdc20 proteolysis requires p38 MAPK signaling and Cdh1-independent APC/C ubiquitination during spindle assembly checkpoint activation by cadmium. J Cell Physiol 223:327–334

Yu X, Minter-Dykhouse K, Malureanu L et al (2005) Chfr is required for tumor suppression and Aurora A regulation. Nat Genet 37:401–406

Zachos G, Black EJ, Walker M et al (2007) Chk1 is required for spindle checkpoint function. Dev Cell 12:247–260