4D live tracing reveals distinct movement trajectories of meiotic chromosomes

Peng Xie , Shiqi Zhu , Jin Zhang , Xinrui Wang , Xu Jiang , Feng Xiong , Linjin Chen , Ke Fang , Yuanhui Ji , Beihong Zheng , Lincui Da , Hua Cao , Yan Sun , Zhuojuan Luo , Chengqi Lin

Life Medicine ›› 2024, Vol. 3 ›› Issue (6) : lnae038

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Life Medicine ›› 2024, Vol. 3 ›› Issue (6) : lnae038 DOI: 10.1093/lifemedi/lnae038
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4D live tracing reveals distinct movement trajectories of meiotic chromosomes

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Abstract

Proper chromosome alignment at the spindle equator is a prerequisite for accurate chromosome segregation during cell division. However, the chromosome movement trajectories prior to alignment remain elusive. Here, we established a 4D imaging analysis framework to visualize chromosome dynamics and develop a deep-learning model for chromosome movement trajectory classification. Our data reveal that chromosomes follow at least three distinct movement trajectories (retracing, congressing, and quasi-static) to arrive at the equator. We further revealed the distinct roles of multiple kinesin superfamily proteins (KIFs) in coordinating and maintaining the chromosome movement trajectories. In summary, we have presented an efficient and unbiased approach to studying chromosome dynamics during cell division, thereby uncovering a variety of chromosome movement trajectories that precede alignment.

Keywords

chromosome segregation / chromosome movement trajectory / live imaging / deep learning

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Peng Xie, Shiqi Zhu, Jin Zhang, Xinrui Wang, Xu Jiang, Feng Xiong, Linjin Chen, Ke Fang, Yuanhui Ji, Beihong Zheng, Lincui Da, Hua Cao, Yan Sun, Zhuojuan Luo, Chengqi Lin. 4D live tracing reveals distinct movement trajectories of meiotic chromosomes. Life Medicine, 2024, 3(6): lnae038 DOI:10.1093/lifemedi/lnae038

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References

[1]

Charalambous C , Webster A , Schuh M . Aneuploidy in mammalian oocytes and the impact of maternal ageing. Nat Rev Mol Cell Biol 2023; 24: 27- 44.

[2]

Wu JC , Akhmanova A . Microtubule-organizing centers. Annu Rev Cell Dev Biol 2017; 33: 51- 75.

[3]

Kitajima TS , Ohsugi M , Ellenberg J . Complete kinetochore tracking reveals error-prone homologous chromosome biorientation in mammalian oocytes. Cell 2011; 146: 568- 81.

[4]

Hirokawa N , Noda Y , Tanaka Y , et al. Kinesin superfamily motor proteins and intracellular transport. Nat Rev Mol Cell Biol 2009; 10: 682- 96.

[5]

Cross RA , McAinsh A . Prime movers: the mechanochemistry of mitotic kinesins. Nat Rev Mol Cell Biol 2014; 15: 257- 71.

[6]

Kapitein LC , Peterman EJG , Kwok BH , et al. The bipolar mitotic kinesin Eg5 moves on both microtubules that it crosslinks. Nature 2005; 435: 114- 8.

[7]

Ganem NJ , Compton DA . The KinI kinesin Kif2a is required for bipolar spindle assembly through a functional relationship with MCAK. J Cell Biol 2004; 166: 473- 8.

[8]

Henkin G , Brito C , Thomas C , et al. The minus-end depolymerase KIF2A drives flux-like treadmilling of γTuRC-uncapped microtubules. J Cell Biol 2023; 222: e202304020.

[9]

Ditchfield C , Johnson VL , Tighe A , et al. Aurora B couples chromosome alignment with anaphase by targeting BubR1, Mad2, and Cenp-E to kinetochores. J Cell Biol 2003; 161: 267- 80.

[10]

Maiato H , Gomes AM , Sousa F , et al. Mechanisms of chromosome congression during mitosis. Biology-Basel 2017; 6: 13.

[11]

Peng HC , Bria A , Zhou Z , et al. Extensible visualization and analysis for multidimensional images using Vaa3D. Nat Protoc 2014; 9: 193- 208.

[12]

Graves A , Liwicki M , Fernández S , et al. A novel connectionist system for unconstrained handwriting recognition. IEEE Trans Pattern Anal Mach Intell 2009; 31: 855- 68.

[13]

Abiodun OI , Jantan A , Omolara AE , et al. State-of-the-art in artificial neural network applications: a survey. Heliyon 2018; 4: e00938.

[14]

Rath O , Kozielski F . Kinesins and cancer. Nat Rev Cancer 2012; 12: 527- 39.

[15]

Verhey KJ , Hammond JW . Traffic control: regulation of kinesin motors. Nat Rev Mol Cell Biol 2009; 10: 765- 77.

[16]

Camlin NJ , McLaughlin EA , Holt JE . Kif4 is essential for mouse oocyte meiosis. PLoS One 2017; 12: e0170650.

[17]

Chen MH , Liu Y , Wang YL , et al. KIF2A regulates the spindle assembly and the metaphase I-anaphase I transition in mouse oocyte. Sci Rep 2016; 6: 39337.

[18]

FitzHarris G . A shift from kinesin 5-dependent metaphase spindle function during preimplantation development in mouse. Development 2009; 136: 2111- 9.

[19]

Gui L , Homer H . Spindle assembly checkpoint signalling is uncoupled from chromosomal position in mouse oocytes. Development 2012; 139: 1941- 6.

[20]

Heath CM , Wignall SM . Chromokinesin Kif4 promotes proper anaphase in mouse oocyte meiosis. Mol Biol Cell 2019; 30: 1691- 704.

[21]

Mailhes JB , Mastromatteo C , Fuseler JW . Transient exposure to the Eg5 kinesin inhibitor monastrol leads to syntelic orientation of chromosomes and aneuploidy in mouse oocytes. Mutat Res 2004; 559: 153- 67.

[22]

So C , Menelaou K , Uraji J , et al. Mechanism of spindle pole organization and instability in human oocytes. Science 2022; 375: eabj3944.

[23]

Tang F , Pan MH , Wan X , et al. Kif18a regulates Sirt2-mediated tubulin acetylation for spindle organization during mouse oocyte meiosis. Cell Div 2018; 13: 9.

[24]

Yi ZY , Ma XS , Liang QX , et al. Kif2a regulates spindle organization and cell cycle progression in meiotic oocytes. Sci Rep 2016; 6: 38574.

[25]

So C , Menelaou K , Uraji J , et al. Mechanism of spindle pole organization and instability in human oocytes. Science 2022; 375: 631.

[26]

Risteski P , Bozan D , Jagric M , et al. Length-dependent poleward flux of sister kinetochore fibers promotes chromosome alignment. Cell Rep 2022; 40: 111169.

[27]

Klaasen SJ , Truong MA , van Jaarsveld RH , et al. Nuclear chromosome locations dictate segregation error frequencies. Nature 2022; 607: 604- 9.

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