Kinesin KIFC3 is essential for microtubule stability and cytokinesis in oocyte meiosis

Cell Communication and Signaling - Tập 22 Số 1
Jia‐Qian Ju1, Haolin Zhang1, Yue Wang1, Linlin Hu2, Shao‐Chen Sun1
1College of Animal Science and Technology, Nanjing Agricultural University, Nanjing 210095, China
2Key Laboratory of Research on Clinical Molecular Diagnosis for High Incidence Diseases in Western Guangxi, Reproductive Medicine, Guangxi Medical and Health Key Discipline Construction Project, Affiliated Hospital of Youjiang Medical University for Nationalities, Baise, China

Tóm tắt

AbstractKIFC3 is a member of Kinesin-14 family motor proteins, which play a variety of roles such as centrosome cohesion, cytokinesis, vesicles transportation and cell proliferation in mitosis. Here, we investigated the functional roles of KIFC3 in meiosis. Our findings demonstrated that KIFC3 exhibited expression and localization at centromeres during metaphase I, followed by translocation to the midbody at telophase I throughout mouse oocyte meiosis. Disruption of KIFC3 activity resulted in defective polar body extrusion. We observed aberrant meiotic spindles and misaligned chromosomes, accompanied by the loss of kinetochore-microtubule attachment, which might be due to the failed recruitment of BubR1/Bub3. Coimmunoprecipitation data revealed that KIFC3 plays a crucial role in maintaining the acetylated tubulin level mediated by Sirt2, thereby influencing microtubule stability. Additionally, our findings demonstrated an interaction between KIFC3 and PRC1 in regulating midbody formation during telophase I, which is involved in cytokinesis regulation. Collectively, these results underscore the essential contribution of KIFC3 to spindle assembly and cytokinesis during mouse oocyte meiosis.

Từ khóa


Tài liệu tham khảo

Von Stetina JR, Orr-Weaver TL. Developmental control of oocyte maturation and egg activation in metazoan models. Cold Spring Harb Perspect Biol. 2011;3(10):a005553.

Camlin NJ, McLaughlin EA, Holt JE. Through the smoke: use of in vivo and in vitro cigarette smoking models to elucidate its effect on female fertility. Toxicol Appl Pharmcol. 2014;281(3):266–75.

Villeneuve AM, Hillers KJ. Whence Meiosis? Cell. 2001;106(6):647–50.

Schuh M, Ellenberg J. Self-organization of MTOCs replaces centrosome function during acentrosomal spindle assembly in live mouse oocytes. Cell. 2007;130(3):484–98.

Mogessie B, Scheffler K, Schuh M. Assembly and Positioning of the Oocyte Meiotic Spindle. Annu Rev Cell Dev Biol. 2018;34:381–403.

Drutovic D, et al. RanGTP and importin β regulate meiosis I spindle assembly and function in mouse oocytes. EMBO J. 2020;39(1):e101689.

Li L, Yang X-J. Tubulin acetylation: responsible enzymes, biological functions and human diseases. Cell Mol Life Sci. 2015;72(22):4237–55.

Wloga D, Joachimiak E, Fabczak H. Tubulin post-translational modifications and Microtubule dynamics. Int J Mol Sci, 2017. 18(10).

Akera T. Tubulin post-translational modifications in meiosis. Semin Cell Dev Biol. 2023;137:38–45.

Zhang L, et al. Sirt2 functions in spindle organization and chromosome alignment in mouse oocyte meiosis. FASEB Journal: Official Publication Federation Am Soc Experimental Biology. 2014;28(3):1435–45.

Lara-Gonzalez P, Westhorpe FG, Taylor SS. The spindle assembly checkpoint. Curr Biology: CB. 2012;22(22):R966–80.

Marston AL, Wassmann K. Multiple duties for Spindle Assembly Checkpoint kinases in Meiosis. Front Cell Dev Biology. 2017;5:109.

Touati SA, Wassmann K. How oocytes try to get it right: spindle checkpoint control in meiosis. Chromosoma. 2016;125(2):321–35.

Wei L, et al. BubR1 is a spindle assembly checkpoint protein regulating meiotic cell cycle progression of mouse oocyte. Cell Cycle (Georgetown Tex). 2010;9(6):1112–21.

Li M, et al. Bub3 is a spindle assembly checkpoint protein regulating chromosome segregation during mouse oocyte meiosis. PLoS ONE. 2009;4(11):e7701.

Hu C-K, et al. KIF4 regulates midzone length during cytokinesis. Curr Biology: CB. 2011;21(10):815–24.

Cao LG, Wang YL. Signals from the spindle midzone are required for the stimulation of cytokinesis in cultured epithelial cells. Mol Biol Cell. 1996;7(2):225–32.

Mollinari C, et al. PRC1 is a microtubule binding and bundling protein essential to maintain the mitotic spindle midzone. J Cell Biol. 2002;157(7):1175–86.

Li X-H, et al. PRC1 is a critical regulator for anaphase spindle midzone assembly and cytokinesis in mouse oocyte meiosis. FEBS J. 2021;288(9):3055–67.

Camlin NJ, McLaughlin EA, Holt JE. Motoring through: the role of kinesin superfamily proteins in female meiosis. Hum Reprod Update. 2017;23(4):409–20.

She Z-Y, Yang W-X. Molecular mechanisms of kinesin-14 motors in spindle assembly and chromosome segregation. J Cell Sci. 2017;130(13):2097–110.

Decarreau J, et al. The tetrameric kinesin Kif25 suppresses pre-mitotic centrosome separation to establish proper spindle orientation. Nat Cell Biol. 2017;19(4):384–90.

So C, et al. Mechanism of spindle Pole organization and instability in human oocytes. Volume 375. New York, N.Y.): Science; 2022. p. eabj3944. 6581.

Shan M-M et al. Kinesin motor KIFC1 is required for tubulin acetylation and actin-dependent spindle migration in mouse oocyte meiosis. Development (Cambridge, England), 2022. 149(5).

Zhang YZ, et al. Aflatoxin B1 exposure disrupts organelle distribution in mouse oocytes. PeerJ. 2022;10:e13497.

Liao H, et al. KIFC3 promotes proliferation, Migration, and Invasion in Colorectal Cancer via PI3K/AKT/mTOR signaling pathway. Front Genet. 2022;13:848926.

Lu S, et al. KIFC3 regulates progression of hepatocellular carcinoma via EMT and the AKT/mTOR pathway. Exp Cell Res. 2023;426(1):113564.

Hata S, et al. The balance between KIFC3 and EG5 tetrameric kinesins controls the onset of mitotic spindle assembly. Nat Cell Biol. 2019;21(9):1138–51.

Nachbar J, et al. KIFC3 promotes mitotic progression and integrity of the central spindle in cytokinesis. Cell Cycle (Georgetown Tex). 2014;13(3):426–33.

Noda Y, et al. KIFC3, a microtubule minus end-directed motor for the apical transport of annexin XIIIb-associated Triton-insoluble membranes. J Cell Biol. 2001;155(1):77–88.

Cao Y, et al. Microtubule Minus-End binding protein CAMSAP2 and Kinesin-14 motor KIFC3 control dendritic Microtubule Organization. Curr Biol. 2020;30(5):899–e9086.

Clift D, Schuh M. A three-step MTOC fragmentation mechanism facilitates bipolar spindle assembly in mouse oocytes. Nat Commun. 2015;6:7217.

Dumont J, et al. A centriole- and RanGTP-independent spindle assembly pathway in meiosis I of vertebrate oocytes. J Cell Biol. 2007;176(3):295–305.

Moritz M, Agard DA. Gamma-tubulin complexes and microtubule nucleation. Curr Opin Struct Biol. 2001;11(2):174–81.

Blengini CS, et al. Aurora kinase A is essential for meiosis in mouse oocytes. PLoS Genet. 2021;17(4):e1009327.

Solc P, et al. Aurora kinase A drives MTOC biogenesis but does not trigger resumption of meiosis in mouse oocytes matured in vivo. Biol Reprod. 2012;87(4):85.

Kalebic N, et al. αTAT1 is the major α-tubulin acetyltransferase in mice. Nat Commun. 2013;4:1962.

Zhang L, et al. Sirt2 functions in spindle organization and chromosome alignment in mouse oocyte meiosis. Faseb j. 2014;28(3):1435–45.

Tang F, et al. Involvement of Kif4a in spindle formation and chromosome segregation in mouse oocytes. Aging Disease. 2018;9(4):623–33.

Thông tin
Thông tin xuất bản

Cell Communication and Signaling

Tập 22 Số 1

Thông tin tác giả