Abstract
The kinetochore-microtubule association is a core, conserved event that drives chromosome transmission during mitosis. Failure to establish this association on even a single chromosome results in aneuploidy leading to cell death or the development of cancer. However, although many chromosomes lacking centromeres, termed acentrics, fail to segregate, studies in a number of systems reveal robust alternative mechanisms that can drive segregation and successful poleward transport of acentrics. In contrast to the canonical mechanism that relies on end-on microtubule attachments to kinetochores, mechanisms of acentric transmission largely fall into three categories: direct attachments to other chromosomes, kinetochore-independent lateral attachments to microtubules, and long-range tether-based attachments. Here, we review these “non-canonical” methods of acentric chromosome transmission. Just as the discovery and exploration of cell cycle checkpoints provided insight into both the origins of cancer and new therapies, identifying mechanisms and structures specifically involved in acentric segregation may have a significant impact on basic and applied cancer research.
This is a preview of subscription content, log in via an institution to check access.
Similar content being viewed by others
Data availability
Not applicable
Code availability
Not applicable
Abbreviations
- APC/C:
-
Anaphase-promoting complex
- PtK cells:
-
Potorous tridactylus cells
- UFBs:
-
Ultrafine DNA bridges
- CHMP4C:
-
Charged multivesicular body protein 4C
- ESCRT-III:
-
Endosomal sorting complexes required for transport-III
References
Afonso O, Matos I, Pereira AJ, Aguiar P, Lampson MA, Maiato H (2014) Feedback control of chromosome separation by a midzone Aurora B gradient. Science 345:332–336. https://doi.org/10.1126/science.1251121
Afonso O, Castellani CM, Cheeseman LP, Ferreira JG, Orr B, Ferreira LT, Chambers JJ, Morais-de-Sá E, Maresca TJ, Maiato H (2019) Spatiotemporal control of mitotic exit during anaphase by an aurora B-Cdk1 crosstalk. eLife 8:e47646. https://doi.org/10.7554/eLife.47646
Asbury CL (2017) Anaphase a: disassembling microtubules move chromosomes toward spindle poles. Biology (Basel) 6:E15. https://doi.org/10.3390/biology6010015
Ault JG, DeMarco AJ, Salmon ED, Rieder CL (1991) Studies on the ejection properties of asters: astral microtubule turnover influences the oscillatory behavior and positioning of mono-oriented chromosomes. J Cell Sci 99:701–710
Bader JR, Vaughan KT (2010) Dynein at the kinetochore: timing, interactions and functions. Semin Cell Dev Biol 21:269–275. https://doi.org/10.1016/j.semcdb.2009.12.015
Bajer A (1958) Cine-micrographic studies on chromosome movements in beta-irradiate cells. Chromosoma 9:319–331
Bajer A (1964) Cine-micrographic studies on dicentric chromosomes. Chromosoma 15:630–651. https://doi.org/10.1007/bf00319996
Bajer A, Östergren G (1963) Observation on transverse movements within the phragmoplast. Hereditas (Lund) 50:179–195
Bajer A, Vantard M (1988) Microtubule dynamics determine chromosome lagging and transport of acentric fragments. Mutat Res 201:271–281. https://doi.org/10.1016/0027-5107(88)90016-4
Bajer A, Vantard M, Molè-Bajer J (1987) Multiple mitotic transports expressed by chromosome and particle movement. Fortschr Zool 34:171–186
Barisic M, Aguiar P, Geley S, Maiato H (2014) Kinetochore motors drive congression of peripheral polar chromosomes by overcoming random arm-ejection forces. Nat Cell Biol 16:1249–1256. https://doi.org/10.1038/ncb3060
Baxter J, Sen N, López Martínez V, Monturus de Carandini ME, Schvartzman JB, Diffley JFX, Aragón L (2011) Positive supercoiling of mitotic DNA drives decatenation by topoisomerase II in eukaryotes. Science 331:1328–1332. https://doi.org/10.1126/science/1201538
Bretscher HS, Fox DT (2016) Proliferation of double-strand break-resistant polyploid cells requires Drosophila FANCD2. Dev Cell 37:444–457. https://doi.org/10.1016/j.devcel.2016.05.004
Brinkley BR, Zinkowski RP, Mollon WL, Davis FM, Pisegna MA, Perhouse M, Rao PN (1988) Movement and segregation of kinetochores experimentally detached from mammalian chromosomes. Nature 336:251–254. https://doi.org/10.1038/336251a0
Brodsky MH, Weinert BT, Tsang G, Rong YS, McGinnis NM, Golic KG, Rio DC, Rubin GM (2004) Drosophila melongaster MNK/Chk2 and p53 regulate multiple DNA repair and apoptotic pathways following DNA damage. https://doi.org/10.1128/mcb.24.3.1219-1231.2004
Brouhard GJ, Hunt AJ (2005) Microtubule movements on the arms of mitotic chromosomes: polar ejection forces quantified in vitro. Proc Natl Acad Sci U S A 102:13903–13908. https://doi.org/10.1073/pnas.0506017102
Carlson JG (1938a) Mitotic behavior of induced chromosomal fragments lacking spindle attachments in the neuroblasts of the grasshopper. Proc Natl Acad Sci U S A 24:500–507. https://doi.org/10.1073/pnas.24.11.500
Carlson JG (1938b) Some effects of X-radiation on the neuroblast chromosomes of the grasshopper, Chortophaga viridifasciata. Genetics 23:596–609
Carlton JG, Caballe A, Agromayor M, Kloc M, Martin-Serrano J (2012) ESCRT-III governs the Aurora B-mediated abscission checkpoint through CHMP4C. Science 336:220–225. https://doi.org/10.1126/science.1217180
Chan YW, West SC (2018) A new class of ultrafine anaphase bridges generated by homologous recombination. Cell Cycle 17:2101–2109. https://doi.org/10.1080/15384101.2018.1515555
Chan KL, North PS, Hickson ID (2007) BLM is required for faithful chromosome segregation and its localization defines a class of ultrafine anaphase bridges. EMBO J 26:3397–3409. https://doi.org/10.1038/sj.emboj.7601777
Cowell JK (1982) Double minutes and homogeneously staining regions: gene amplification in mammalian cells. Annu Rev Genet 16:21–59. https://doi.org/10.1146/annurev.ge.16.120182.000321
Cox D, Yuncken C, Spriggs AI (1965) Minute chromatin bodies in malignant tumours of childhood. Lancet 286:55–58. https://doi.org/10.1016/s0140-6736(65)0-131-5
Crasta K, Ganem NJ, Dagher R, Lantermann AB, Ivanova EV, Pan Y, Nezi L, Protopopov A, Chowdhury D, Pellman D (2012) DNA breaks and chromosome pulverization from errors in mitosis. Nature 482:53–58. https://doi.org/10.1038/nature10802
Derive N, Landmann C, Montembault E, Claverie MC, Pierre-Elies P, Goutte-Gattat D, Founounou N, McCusker D, Royou A (2015) Bub3-BubR1-dependent sequestration of Cdc20Fizzy at DNA breaks facilitates the correct segregation of broken chromosomes. J Cell Biol 211:517–532. https://doi.org/10.1083/jcb.201504059
Dietz R (1972) Anaphase behavior of inversions in living cranefly spermatocytes. Chromosom Today 3:70–85
Dumont J, Oegema K, Desai A (2010) A kinetochore-independent mechanism drives anaphase chromosome separation during acentrosomal meiosis. Nat Cell Biol 12:894–901. https://doi.org/10.1038/ncb2093
Falck GC, Catalán J, Norppa H (2002) Nature of anaphase laggards and micronuclei in female cytokinesis-blocked lymphocytes. Mutagenesis 17:111–117. https://doi.org/10.1093/mutage/17.2.111
Feeney KM, Parish JL (2009) Targeting mitotic chromosomes: a conserved mechanism to ensure viral genome persistence. Proc Biol Sci 276:1535–1544. https://doi.org/10.1098/rspb.2008.1642
Fenech M, Kirsch-Volders M, Natarajan AT, Surralles J, Crott JW, Parry J, Norppa H, Eastmond DA, Tucker JD, Thomas P (2011) Molecular mechanisms of micronucleus, nucleoplasmic bridge and nuclear bud formation in mammalian and human cells. Mutagenesis 26:125–132. https://doi.org/10.1093/mutage/geq052
Fuge H (1975) Anaphase transport of akinetochoric fragments in tipulid spermatocytes. Electron microscopic observations on fragment-spindle interactions. Chromosoma 52:149–158. https://doi.org/10.1007/bf00326264
Fuge H (1990) Non-kinetochore transport phenomena, microtubule-chromosome associations, and force transmission in nuclear division. Protoplasma 158:1–9. https://doi.org/10.1007/BF01323267
Galgoczy DJ, Toczyski DP (2001) Checkpoint adaptation precedes spontaneous and damage-induced genomic instability in yeast. Mol Cell Biol 21:1710–1718. https://doi.org/10.1128/MCB.21.5.1710-1718.2001
Gerlich D, Beaudouin J, Gebhard M, Ellenberg J, Eils R (2001) Four-dimensional imaging and quantitative reconstruction to analyse complex spatiotemporal processes in live cells. Nat Cell Biol 3:852–855. https://doi.org/10.1038/ncb0901-852
Giménez-Abián JF, Clark DJ, Giménez-Martín G, Weingartner M, Giménez-Abián MI, Carballo JA, Díaz de la Espina SM, Bögre L, De la Torre C (2002) DNA catenations that link sister chromatids until the onset of anaphase are maintained by a checkpoint mechanism. Eur J Cell Biol 81:9–16. https://doi.org/10.1078/0171-9335-00226
Holm C, Goto T, Wang JC, Botstein D (1985) DNA topoisomerase II is required at the time of mitosis in yeast. Cell 41:553–563. https://doi.org/10.1016/s0092-8674(85)80028-3
Hughes SE, Hawley RS (2014) Topoisomerase II is required for the proper separation of heterochromatic regions during Drosophila melanogaster female meiosis. PLoS Genet 23:e1004650. https://doi.org/10.1371/journal.pgen.1004650
Hughes SE, Gilliland WD, Cotitta JL, Takeo S, Collins KA, Hawley RS (2009) Heterochromatic threads connect oscillating chromosomes during prometaphase I in Drosophila oocytes. PLoS Genet 5:e1000348. https://doi.org/10.1371/journal.pgen.1000348
Humphrey RM, Brinkley BR (1969) Ultrastructural studies of radiation-induced chromosome damage. J Cell Biol 42:745–753. https://doi.org/10.1083/jcb.42.3.745
Inoué S, Salmon ED (1995) Force generation by microtubule assembly/disassembly in mitosis and related movements. Mol Biol Cell 6:1619–1640. https://doi.org/10.1091/mbc.6.12.1619
Ishii K, Ogiyama Y, Chikashige Y, Soejima S, Masuda F, Kakuma T, Hiraoka Y, Takahashi K (2008) Heterochromatin integrity affects chromosome reorganization after centromere dysfunction. Science 321:1088–1091. https://doi.org/10.1126/science.1158699
Kanda T, Sullivan KF, Wahl GM (1998) Histone-GFP fusion protein enables sensitive analysis of chromosome dynamics in living mammalian cells. Curr Biol 8:377–385. https://doi.org/10.1016/s0960-9882(98)70156-3
Kanda T, Otter M, Wahl GM (2001a) Mitotic segregation of viral and cellular acentric extrachromosomal molecules by chromosome tethering. J Cell Sci 114:49–58
Kanda T, Otter M, Wahl GM (2001b) Coupling of mitotic chromosome tethering and replication competence in epstein-barr virus-based plasmids. Mol Cell Biol 21:3576–3588. https://doi.org/10.1128/MCB.21.10.3576-3588.2001
Karg T, Warecki B, Sullivan W (2015) Aurora B-mediated localized delays in nuclear envelope formation facilitate inclusion of late-segregating chromosome fragments. Mol Biol Cell 26:2227–2241. https://doi.org/10.1091/mbc.E15-01-0026
Karg T, Elting MW, Vicars H, Dumont S, Sullivan W (2017) The chromokinesin Klp3a and microtubules facilitate acentric chromosome segregation. J Cell Biol 216:1597–1608. https://doi.org/10.1083/jcb.201604079
Kaye JA, Melo JA, Cheung SK, Vaze MB, Haber JE, Toczyski DP (2004) DNA breaks promote genomic instability by impeding proper chromosome segregation. Curr Biol 14:2096–2106. https://doi.org/10.1016/j.cub.2004.10.051
Ke Y, Huh JW, Warrington R, Li B, Wu N, Leng M, Zhang J, Ball HL, Li B, Yu H (2011) PICH and BLM limit histone association with anaphase centromeric DNA threads and promote their resolution. EMBO J 30:3309–3321. https://doi.org/10.1038/emboj.2011.226
Khodjakov A, Rieder CL (1996) Kinetochores moving away from their associated pole do not exert a significant pushing force on the chromosome. J Cell Biol 135:315–327. https://doi.org/10.1083/jcb.135.2.315
Khodjakov A, Cole RW, Bajer AS, Rieder CL (1996) The force for poleward chromosome motion in Haemanthus cells acts along the length of the chromosome during metaphase but only at the kinetochore during anaphase. J Cell Biol 132:1093–1104. https://doi.org/10.1083/jcb.132.6.1093
Koo DH, Molin WT, Saski CA, Jiang J, Putta K, Jugulam M, Friebe B, Gill BS (2018) Extrachromosomal circular DNA-based amplification and transmission of herbicide resistance in crop weed Amaranthus palmeri. Proc Natl Acad Sci U S A 115:3332–3337. https://doi.org/10.1073/pnas.1719354115
Kotadia S, Montembault E, Sullivan W, Royou A (2012) Cell elongation is an adaptive response for clearing long chromatid arms from the cleavage plane. J Cell Biol 199:745–753. https://doi.org/10.1083/jcb.201208041
LaFountain JR Jr, Oldenbourg R, Cole RW, Rieder CL (2001) Microtubule flux mediates poleward motion of acentric chromosome fragments during meiosis in insect spermatocytes. Mol Biol Cell 12:4054–4065. https://doi.org/10.1091/mbc.12.12.4054
LaFountain JR Jr, Cole RW, Rieder CL (2002a) Polar ejection forces are operative in crane-fly spermatocytes, but their action is limited to the spindle periphery. Cell Motil Cytoskeleton 5:16–26. https://doi.org/10.1002/cm.10011
LaFountain JR Jr, Cole RW, Rieder CL (2002b) Partner telomeres during anaphase in crane-fly spermatocytes are connected by an elastic tether that exerts a backward force and resists poleward motion. J Cell Sci 115:1541–1549
Landmann C, Pierre-Elies P, Goutte-Gattat D, Montembault E, Claverie M-C, Royou A (2020) The Mre11-Rad50-Nbs1 complex mediates the robust recruitment of Polo to DNA lesions during mitosis in. Journal of Cell Science 133 (13):jcs244442
Leimbacher P-A, Jones SE, A-MK. Shorrocks, de Marco Zompit M, Day M, Blaauwendraad J, Bundschuh D, Bonham S, Fischer R, Fink D, Kessler BM, Oliver AW, Pearl LH, Blackford AN, Stucki M (2019) MDC1 Interacts with TOPBP1 to Maintain Chromosomal Stability during Mitosis. Molecular Cell 74 (3):571–583.e8
Liang H, Wright WH, Cheng S, He W, Berns MW (1993) Micromanipulation of chromosomes in PTK2 cells using laser microsurgery (optical scalpel) in combination with laser-induced optical force (optical tweezers). Exp Cell Res 204:110–120. https://doi.org/10.1006/excr.1993.1015
Liu Y, Nielsen CF, Yao Q, Hickson ID (2014) The origins and processing of ultrafine anaphase DNA bridges. Curr Opin Genet Dev 26:1–5. https://doi.org/10.1016/j.ge.2014.03.003
Liu S, Kwon M, Mannino M, Yang N, Renda F, Khodjakov A, Pellman D (2018) Nuclear envelope assembly defects link mitotic errors to chromothripsis. Nature 561:551–555. https://doi.org/10.1038/s41586-018-0534-z
Ly P, Teitz LS, Kim DH, Shoshani O, Skaletsky H, Fachinetti D, Page DC, Cleveland DW (2017) Selective Y centromere inactivation triggers chromosome shattering in micronuclei and repair by non-homologous end joining. Nat Cell Biol 19:68–75. https://doi.org/10.1038/ncb3450
Mackay DR, Makise M, Ullman KS (2010) Defects in nuclear pore assembly Lead to activation of an Aurora B-mediated abscission checkpoint. J Cell Biol 191:923–931. https://doi.org/10.1083/jcb.201007124
Maiato H, Gomes AM, Sousa F, Barisic M (2017) Mechanisms of chromosome congression during mitosis. Biology (Basel) 6:E13. https://doi.org/10.3390/biology6010013
Malkova A, Ivanov EL, Haber JE (1996) Double-strand break repair in the absence of RAD51 in yeast: a possible role for break-induced DNA replication. Proc Natl Acad Sci U S A 93:7131–7136. https://doi.org/10.1073/pnas.93.14.7131
McNeill PA, Berns MW (1981) Chromosome behavior after laser microirradiation of a single kinetochore in mitotic PtK2 cells. J Cell Biol 88:543–553. https://doi.org/10.1083/jcb.88.3.543
Melo JA, Cohen J, Toczyski DP (2001) Two checkpoint complexes are independently recruited to sites of DNA damage in vivo. Genes Dev 15:2809–2821. https://doi.org/10.1101/gad.903501
Merdes A, Cleveland DW (1997) Pathways of spindle pole formation: different mechanisms; conserved components. J Cell Biol 138:953–956. https://doi.org/10.1083/jcb.138.5.953
Mitchison TJ (1989) Polewards microtubule flux in the mitotic spindle: evidence from photoactivation of fluorescence. J Cell Biol 109:637–652. https://doi.org/10.1083/jcb.109.2.637
Montembault E, Claverie MC, Bouit L, Landmann C, Jenkins J, Tsankova A, Cabernard C, Royou A (2017) Myosin efflux promotes cell elongation to coordinate chromosome segregation with cell cleavage. Nat Commun 8:326. https://doi.org/10.1038/s41467-017-00337-6
Morin SJ, Eccles J, Iturriaga A, Zimmerman RS (2017) Translocations, inversions and other chromosome rearrangements. Fertil Steril 107:19–26. https://doi.org/10.1016/j.fertnstert.2016.10.013
Muscat CC, Torre-Santiago KM, Tran MV, Powers JA, Wignall SM (2015) Kinetochore-independent chromosome segregation driven by lateral microtubule bundles. eLife 4:e06462. https://doi.org/10.7554/eLife.06462
Nowsheen S, Yang ES (2012) The intersection between DNA damage response and cell death pathways. Exp Oncol 34:243–254
Ohno Y, Ogiyama Y, Kubota Y, Kubo T, Ishii K (2016) Acentric chromosome ends are prone to fusion with functional chromosome ends through a homology-directed rearrangement. Nucleic Acids Res 44:232–244. https://doi.org/10.1093/nar/gkv997
Ono M, Preece D, Duquette ML, Forer A, Berns MW (2017) Mitotic tethers connect sister chromosomes and transmit “cross-polar” force during anaphase A of mitosis in PtK2 cells. Biomed Opt Express 8:4310–4315. https://doi.org/10.1364/BOE.8.004310
Östergren G, Molè-Bajer J, Bajer A (1960) An interpretation of transport phenomena at mitosis. Ann N Y Acad Sci 90:381–408. https://doi.org/10.1111/j.1749-6632.1960.tb23258.x
Paliulis LV, Forer A (2018) A review of “tethers”: elastic connections between separating partner chromosomes in anaphase. Protoplasma 255:733–740. https://doi.org/10.1007/s00709-017-1201-1
Paliulis LV, Nicklas RB (2004) Micromanipulation of chromosomes reveals that cohesion release during cell division is gradual and does not require tension. Curr Biol 14:2124–2129. https://doi.org/10.1016/j.cub.2004.11.052
Pauletti G, Lai E, Attardi G (1990) Early appearance and long-term-persistence of the submicroscopic extrachromosomal elements (amplisomes) containing the amplified DHFR genes in human cell lines. Proc Natl Acad Sci U S A 87:2955–2959. https://doi.org/10.1073/pnas.87.8.2955
Petsalaki E, Zachos G (2019) Building bridges between chromosomes: novel insights into the abscission checkpoint. Cell Mol Life Sci 76:4291–4307. https://doi.org/10.1007/s00018-019-03224-z
Rahal R, Amon A (2008) Mitotic CDKs control the metaphase-anaphase transition and trigger spindle elongation. Genes Dev 22:1534–1548. https://doi.org/10.1101/gad.1638308
Rieder CL, Davison EA, Jensen LC, Cassimeris L, Salmon 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. https://doi.org/10.1083/jcb.103.2.581
Rocha LC, Jankowska M, Fuchs J, Mittelmann A, Techio VH, Houben A (2017a) Decondensation of chromosomal 45S rDNA sites in Lolium and Festuca genotypes does not result in karyotype instability. Protoplasma 254:285–292. https://doi.org/10.1007/s00709-016-0942-6
Rocha LC, Silva GA, Bustamante FO, Silveira RA, Mittlemann A, Techi VH (2017b) Dynamics of 45S rDNA sites in the cell cycle: fragile sites and chromosomal stability in Lolium and Festuca. Genet Mol Res 16. https://doi.org/10.4328/gmr16019156
Royou A, Macias H, Sullivan W (2005) The Drosophila Grp/Chk1 DNA damage checkpoint controls entry into anaphase. Curr Biol 15:334–339. https://doi.org/10.1016/j.cub.2005.02.026
Royou A, Gagou ME, Karess R, Sullivan W (2010) BubR1- and Polo-coated DNA tethers facilitate poleward segregation of acentric chromatids. Cell 140:235–245. https://doi.org/10.1016/j.cell.2009.12.043
Somers WG, Saint R (2003) A RhoGEF and Rho family GTPase-activating protein complex link the contractile ring to cortical microtubules at the onset of cytokinesis. Dev Cell 4:29–39. https://doi.org/10.1016/s1534-5807(02)00402-1
Stephens PJ, Greenman CD, Fu B, Yan G, Bignell GR, Mudie LJ, Pleasance ED, Lau KW, Beare D, Stebbings LA et al (2011) Massive genomic rearrangement acquired in a single catastrophic event during cancer development. Cell 144:27–40. https://doi.org/10.1016/j.cell.2010.11.055
Stich H (1953) Stoffe und Ströungen in der Spindel von Cyclops strenuous. Chromosoma 6:199–236. https://doi.org/10.1007/BF01259940
Tanaka TU (2005) Chromosome bi-orientation on the mitotic spindle. Philos Trans R Soc Lond Ser B Biol Sci 360:581–589. https://doi.org/10.1098/rstb.2004.1612
Titen SW, Golic KG (2008) Telomere loss provokes multiple pathways to apoptosis and produces genomic instability in Drosophila melanogaster. Genetics 180:1821–1831. https://doi.org/10.1534/genetics.108.093625
Tooley J, Stukenberg PT (2011) The Ndc80 complex: integrating the kinetochore’s many movements. Chromosom Res 19:377–391. https://doi.org/10.1007/s10577-010-9180-5
Udroiu I, Sgura A (2020) Quantitative relationships between acentric fragments and micronuclei: new models and implications for curve fitting. Int J Radiat Biol 96:197–205. https://doi.org/10.1080/09553002.2020.1683638
Uretz RB, Bloom W, Zirkle RE (1954) Irradiation of parts of individual cells. II Effects of an ultraviolet microbeam focused on parts of chromosomes. Science 120:197–199. https://doi.org/10.1126/science.120.3110.197
Wahl GM (1989) The importance of circular DNA in mammalian gene amplification. Cancer Res 49:1333–1340
Wandke C, Barisic M, Sigl R, Rauch V, Wolf F, Amaro AC, Tan CH, Pereira AJ, Kutay U, Maiato H, Meraldi P, Geley S (2012) Human chromokinesins promote chromosome congression and spindle microtubule dynamics during mitosis. J Cell Biol 198:847–863. https://doi.org/10.1083/jcb.201110060
Warecki B, Sullivan W (2018) Micronuclei formation is prevented by Aurora B-mediated exclusion of HP1a from late-segregating chromatin in Drosophila. Genetics 210:171–187. https://doi.org/10.1534/genetics.118.301031
Warecki B, Ling X, Bast I, Sullivan W (2020) ESCRT-III-mediated membrane fusion drives chromosome fragments through nuclear envelope channels. J Cell Biol 219:e201905091. https://doi.org/10.1083/jcb.201905091
Wignall SM, Villeneuve AM (2009) Lateral microtubule bundles promote chromosome alignment during acentrosomal oocyte meiosis. Nat Cell Biol 11:839–844. https://doi.org/10.1038/ncb1891
Zhang CZ, Spektor A, Cornils H, Francis JM, Jackson EK, Liu S, Meyerson M, Pellman D (2015) Chromothripsis from DNA damage in micronuclei. Nature. 522:179–184. https://doi.org/10.1038/nature14493
Acknowledgments
We would like to thank Alexey Khodjakov, Travis Karg, Anna Russo, and Hannah Vicars for their critical readings of the manuscript.
Funding
This work was funded by a National Institutes of Health grant NIHRO1GM120321 awarded to W.S.
Author information
Authors and Affiliations
Contributions
WS conceived this review. BW and WS assessed the published literature and wrote and revised the manuscript.
Corresponding author
Ethics declarations
Competing interests
The authors declare that they have no competing interests.
Ethics approval
Not applicable
Consent to participate
Not applicable
Consent for publication
Not applicable
Additional information
Responsible Editor: Conly Rieder
Publisher’s note
Springer Nature remains neutral with regard to jurisdictional claims in published maps and institutional affiliations.
Rights and permissions
About this article
Cite this article
Warecki, B., Sullivan, W. Mechanisms driving acentric chromosome transmission. Chromosome Res 28, 229–246 (2020). https://doi.org/10.1007/s10577-020-09636-z
Received:
Revised:
Accepted:
Published:
Issue Date:
DOI: https://doi.org/10.1007/s10577-020-09636-z