Protein regulator of cytokinesis 1 regulates chromosome dynamics and cytoplasmic division during mouse oocyte meiotic maturation and early embryonic development.
chromosome dynamics
cytoplasmic division
early embryo development
oocyte meiosis
protein regulator of cytokinesis 1
Journal
The FEBS journal
ISSN: 1742-4658
Titre abrégé: FEBS J
Pays: England
ID NLM: 101229646
Informations de publication
Date de publication:
12 2020
12 2020
Historique:
received:
26
11
2019
revised:
01
06
2020
accepted:
15
06
2020
pubmed:
21
6
2020
medline:
25
5
2021
entrez:
21
6
2020
Statut:
ppublish
Résumé
In contrast to the homeokinesis of mitosis, asymmetric division of cytoplasm is the conspicuous feature of meiosis in mammalian oocytes. Protein regulator of cytokinesis 1 (PRC1) is an important regulator during mitotic spindle assembly and cytoplasmic division, but its functions in oocyte meiosis and early embryo development have not been fully elucidated. In this study, we detected PRC1 expression and localization and revealed a nuclear, spindle midzone-related dynamic pattern throughout meiotic and mitotic progressions. Treatment of oocytes with the reagents taxol or nocodazole disturbed the distribution of PRC1 in metaphase II oocytes. Further, PRC1 depletion led to failure of first polar body (PB1) extrusion and spindle migration, aneuploidy and defective kinetochore-microtubule attachment and spindle assembly. Overexpression of PRC1 resulted in PB1 extrusion failure, aneuploidy and serious defects of spindle assembly. To investigate PRC1 function in early embryos, we injected Prc1 morpholino into zygotes and 2-cell stage embryos. Depletion of PRC1 in zygotes impaired 4-cell, morula and blastocyst formation. Loss of PRC1 in single or double blastomeres in 2-cell stage embryos significantly impaired cell division, indicating its indispensable role in early embryo development. Co-immunoprecipitation showed that PRC1 interacts with polo-like kinase 1 (PLK1), and functional knockdown and rescue experiments demonstrated that PRC1 recruits PLK1 to the spindle midzone to regulate cytoplasmic division during meiosis. Finally, kinesin family member 4 knockdown downregulates PRC1 expression and leads to PRC1 localization failure. Taken together, our data suggest PRC1 plays an important role during oocyte maturation and early embryonic development by regulating chromosome dynamics and cytoplasmic division.
Substances chimiques
Cell Cycle Proteins
0
Kif4 protein, mouse
EC 3.6.1.-
Kinesins
EC 3.6.4.4
Types de publication
Journal Article
Research Support, Non-U.S. Gov't
Langues
eng
Sous-ensembles de citation
IM
Pagination
5130-5147Informations de copyright
© 2020 Federation of European Biochemical Societies.
Références
Bennabi I, Terret ME & Verlhac MH (2016) Meiotic spindle assembly and chromosome segregation in oocytes. J Cell Biol 215, 611-619.
di Pietro F, Echard A & Morin X (2016) Regulation of mitotic spindle orientation: an integrated view. EMBO Rep 17, 1106-1130.
Field C, Li R & Oegema K (1999) Cytokinesis in eukaryotes: a mechanistic comparison. Curr Opin Cell Biol 11, 68-80.
Oliferenko S, Chew TG & Balasubramanian MK (2009) Positioning cytokinesis. Genes Dev 23, 660-674.
Douglas ME & Mishima M (2010) Still entangled: assembly of the central spindle by multiple microtubule modulators. Semin Cell Dev Biol 21, 899-908.
Hornick JE, Karanjeet K, Collins ES & Hinchcliffe EH (2010) Kinesins to the core: The role of microtubule-based motor proteins in building the mitotic spindle midzone. Semin Cell Dev Biol 21, 290-299.
Jiang W, Jimenez G, Wells NJ, Hope TJ, Wahl GM, Hunter T & Fukunaga R (1998) PRC1: a human mitotic spindle-associated CDK substrate protein required for cytokinesis. Mol Cell 2, 877-885.
Subramanian R, Wilson-Kubalek EM, Arthur CP, Bick MJ, Campbell EA, Darst SA, Milligan RA & Kapoor TM (2010) Insights into antiparallel microtubule crosslinking by PRC1, a conserved nonmotor microtubule binding protein. Cell 142, 433-443.
Kapitein LC, Janson ME, van den Wildenberg SM, Hoogenraad CC, Schmidt CF & Peterman EJ (2008) Microtubule-driven multimerization recruits ase1p onto overlapping microtubules. Curr Biol 18, 1713-1717.
Mollinari C, Kleman JP, Jiang W, Schoehn G, Hunter T & Margolis RL (2002) PRC1 is a microtubule binding and bundling protein essential to maintain the mitotic spindle midzone. J Cell Biol 157, 1175-1186.
Zhu C, Lau E, Schwarzenbacher R, Bossy-Wetzel E & Jiang W (2006) Spatiotemporal control of spindle midzone formation by PRC1 in human cells. Proc Natl Acad Sci USA 103, 6196-6201.
Courtheoux T, Gay G, Gachet Y & Tournier S (2009) Ase1/Prc1-dependent spindle elongation corrects merotely during anaphase in fission yeast. J Cell Biol 187, 399-412.
Zhang JY, Lv S, Niu HM & Lei AM (2018) [Research progress on the asymmetric division in mammalian oocytes]. Yi chuan = Hereditas 40, 279-291.
Fabritius AS, Ellefson ML & McNally FJ (2011) Nuclear and spindle positioning during oocyte meiosis. Curr Opin Cell Biol 23, 78-84.
Chaigne A, Verlhac MH & Terret ME (2012) Spindle positioning in mammalian oocytes. Exp Cell Res 318, 1442-1447.
Glotzer M (2001) Animal cell cytokinesis. Annu Rev Cell Dev Biol 17, 351-386.
Barr FA & Gruneberg U (2007) Cytokinesis: placing and making the final cut. Cell 131, 847-860.
Yi K & Li R (2012) Actin cytoskeleton in cell polarity and asymmetric division during mouse oocyte maturation. Cytoskeleton 69, 727-737.
Mullen TJ & Wignall SM (2017) Interplay between microtubule bundling and sorting factors ensures acentriolar spindle stability during C. elegans oocyte meiosis. PLoS Genet 13, e1006986.
Mishima M (2017) Preparation of centralspindlin as an active heterotetramer of kinesin and GTPase activating protein subunits for in vitro structural and functional assays. Methods Cell Biol 137, 371-385.
Lee KY, Esmaeili B, Zealley B & Mishima M (2015) Direct interaction between centralspindlin and PRC1 reinforces mechanical resilience of the central spindle. Nat Commun 6, 7290.
Adriaans IE, Basant A, Ponsioen B, Glotzer M & Lens SMA (2019) PLK1 plays dual roles in centralspindlin regulation during cytokinesis. J Cell Biol 218, 1250-1264.
Hu CK, Ozlu N, Coughlin M, Steen JJ & Mitchison TJ (2012) Plk1 negatively regulates PRC1 to prevent premature midzone formation before cytokinesis. Mol Biol Cell 23, 2702-2711.
Zhu C & Jiang W (2005) Cell cycle-dependent translocation of PRC1 on the spindle by Kif4 is essential for midzone formation and cytokinesis. Proc Natl Acad Sci USA 102, 343-348.
Heath CM & Wignall SM (2019) Chromokinesin Kif4 promotes proper anaphase in mouse oocyte meiosis. Mol Biol Cell 30, 1691-1704.
Guo J, Zhang T, Guo Y, Sun T, Li H, Zhang X, Yin H, Cao G, Yin Y, Wang H et al. (2018) Oocyte stage-specific effects of MTOR determine granulosa cell fate and oocyte quality in mice. Proc Natl Acad Sci USA 115, E5326-E5333.
Solc P, Kitajima TS, Yoshida S, Brzakova A, Kaido M, Baran V, Mayer A, Samalova P, Motlik J & Ellenberg J (2015) Multiple requirements of PLK1 during mouse oocyte maturation. PLoS One 10, e0116783.
Zhang Z, Chen C, Ma L, Yu Q, Li S, Abbasi B, Yang J, Rui R & Ju S (2017) Plk1 is essential for proper chromosome segregation during meiosis I/meiosis II transition in pig oocytes. Reprod Biol Endocrinol 15, 69.
Wolfe BA, Takaki T, Petronczki M & Glotzer M (2009) Polo-like kinase 1 directs assembly of the HsCyk-4 RhoGAP/Ect2 RhoGEF complex to initiate cleavage furrow formation. PLoS Biol 7, e1000110.
Neef R, Gruneberg U, Kopajtich R, Li X, Nigg EA, Sillje H & Barr FA (2007) Choice of Plk1 docking partners during mitosis and cytokinesis is controlled by the activation state of Cdk1. Nat Cell Biol 9, 436-444.
Poser E, Caous R, Gruneberg U & Barr FA (2019) Aurora A promotes chromosome congression by activating the condensin-dependent pool of KIF4A. J Cell Biol 219, e201905194.
Nguyen PA, Field CM & Mitchison TJ (2018) Prc1E and Kif4A control microtubule organization within and between large Xenopus egg asters. Mol Biol Cell 29, 304-316.
Schuyler SC, Liu JY & Pellman D (2003) The molecular function of Ase1p: evidence for a MAP-dependent midzone-specific spindle matrix. Microtubule-associated proteins. J Cell Biol 160, 517-528.
Verni F, Somma MP, Gunsalus KC, Bonaccorsi S, Belloni G, Goldberg ML & Gatti M (2004) Feo, the Drosophila homolog of PRC1, is required for central-spindle formation and cytokinesis. Curr Biol 14, 1569-1575.
Loiodice I, Staub J, Setty TG, Nguyen NP, Paoletti A & Tran PT (2005) Ase1p organizes antiparallel microtubule arrays during interphase and mitosis in fission yeast. Mol Biol Cell 16, 1756-1768.
Yamashita A, Sato M, Fujita A, Yamamoto M & Toda T (2005) The roles of fission yeast ase1 in mitotic cell division, meiotic nuclear oscillation, and cytokinesis checkpoint signaling. Mol Biol Cell 16, 1378-1395.
Liu J, Wang Z, Jiang K, Zhang L, Zhao L, Hua S, Yan F, Yang Y, Wang D, Fu C et al. (2009) PRC1 cooperates with CLASP1 to organize central spindle plasticity in mitosis. J Biol Chem 284, 23059-23071.
Mollinari C, Kleman JP, Saoudi Y, Jablonski SA, Perard J, Yen TJ & Margolis RL (2005) Ablation of PRC1 by small interfering RNA demonstrates that cytokinetic abscission requires a central spindle bundle in mammalian cells, whereas completion of furrowing does not. Mol Biol Cell 16, 1043-1055.
Fu C, Yan F, Wu F, Wu Q, Whittaker J, Hu H, Hu R & Yao X (2007) Mitotic phosphorylation of PRC1 at Thr470 is required for PRC1 oligomerization and proper central spindle organization. Cell Res 17, 449-457.
Zhang Y, Wan X, Wang HH, Pan MH, Pan ZN & Sun SC (2019) RAB35 depletion affects spindle formation and actin-based spindle migration in mouse oocyte meiosis. Mol Hum Reprod 25, 359-372.
Leader B, Lim H, Carabatsos MJ, Harrington A, Ecsedy J, Pellman D, Maas R & Leder P (2002) Formin-2, polyploidy, hypofertility and positioning of the meiotic spindle in mouse oocytes. Nat Cell Biol 4, 921-928.
Verlhac MH, Lefebvre C, Guillaud P, Rassinier P & Maro B (2000) Asymmetric division in mouse oocytes: with or without Mos. Curr Biol 10, 1303-1306.
Rampioni Vinciguerra GL, Citron F, Segatto I, Belletti B, Vecchione A & Baldassarre G (2019) p27kip1 at the crossroad between actin and microtubule dynamics. Cell Div 14, 2.
Godin JD, Thomas N, Laguesse S, Malinouskaya L, Close P, Malaise O, Purnelle A, Raineteau O, Campbell K, Fero M et al. (2012) p27(Kip1) is a microtubule-associated protein that promotes microtubule polymerization during neuron migration. Dev Cell 23, 729-744.
Perchey RT, Serres MP, Nowosad A, Creff J, Callot C, Gay A, Manenti S, Margolis RL, Hatzoglou A & Besson A (2018) p27(Kip1) regulates the microtubule bundling activity of PRC1. Biochim Biophys Acta 1865, 1630-1639.
Manandhar G, Schatten H & Sutovsky P (2005) Centrosome reduction during gametogenesis and its significance. Biol Reprod 72, 2-13.
Schuh M & Ellenberg J (2007) Self-organization of MTOCs replaces centrosome function during acentrosomal spindle assembly in live mouse oocytes. Cell 130, 484-498.
Clift D & Schuh M (2015) A three-step MTOC fragmentation mechanism facilitates bipolar spindle assembly in mouse oocytes. Nat Commun 6, 7217.
Polak B, Risteski P, Lesjak S & Tolic IM (2017) PRC1-labeled microtubule bundles and kinetochore pairs show one-to-one association in metaphase. EMBO Rep 18, 217-230.
Zhan P, Zhang B, Xi GM, Wu Y, Liu HB, Liu YF, Xu WJ, Zhu QQ, Cai F, Zhou ZJ et al. (2017) PRC1 contributes to tumorigenesis of lung adenocarcinoma in association with the Wnt/beta-catenin signaling pathway. Mol Cancer 16, 108.
Liu X, Li Y, Meng L, Liu XY, Peng A, Chen Y, Liu C, Chen H, Sun S, Miao X et al. (2018) Reducing protein regulator of cytokinesis 1 as a prospective therapy for hepatocellular carcinoma. Cell Death Dis 9, 534.
Shimo A, Nishidate T, Ohta T, Fukuda M, Nakamura Y & Katagiri T (2007) Elevated expression of protein regulator of cytokinesis 1, involved in the growth of breast cancer cells. Cancer Sci 98, 174-181.
Kanehira M, Katagiri T, Shimo A, Takata R, Shuin T, Miki T, Fujioka T & Nakamura Y (2007) Oncogenic role of MPHOSPH1, a cancer-testis antigen specific to human bladder cancer. Can Res 67, 3276-3285.
Chen J, Rajasekaran M, Xia H, Zhang X, Kong SN, Sekar K, Seshachalam VP, Deivasigamani A, Goh BK, Ooi LL et al. (2016) The microtubule-associated protein PRC1 promotes early recurrence of hepatocellular carcinoma in association with the Wnt/beta-catenin signalling pathway. Gut 65, 1522-1534.
Crest J, Concha-Moore K & Sullivan W (2012) RhoGEF and positioning of rappaport-like furrows in the early Drosophila embryo. Curr Biol 22, 2037-2041.
Hernandez-Ortega S, Sanchez-Botet A, Quandt E, Masip N, Gasa L, Verde G, Jimenez J, Levin RS, Rutaganira FU, Burlingame AL et al. (2019) Phosphoregulation of the oncogenic protein regulator of cytokinesis 1 (PRC1) by the atypical CDK16/CCNY complex. Exp Mol Med 51, 44.
Ban R, Irino Y, Fukami K & Tanaka H (2004) Human mitotic spindle-associated protein PRC1 inhibits MgcRacGAP activity toward Cdc42 during the metaphase. J Biol Chem 279, 16394-16402.
Gruneberg U, Neef R, Li X, Chan EH, Chalamalasetty RB, Nigg EA & Barr FA (2006) KIF14 and citron kinase act together to promote efficient cytokinesis. J Cell Biol 172, 363-372.
Sharma A, Tiwari M, Gupta A, Pandey AN, Yadav PK & Chaube SK (2018) Journey of oocyte from metaphase-I to metaphase-II stage in mammals. J Cell Physiol 233, 5530-5536.
Barr FA, Sillje HH & Nigg EA (2004) Polo-like kinases and the orchestration of cell division. Nat Rev Mol Cell Biol 5, 429-440.
Jackman M, Lindon C, Nigg EA & Pines J (2003) Active cyclin B1-Cdk1 first appears on centrosomes in prophase. Nat Cell Biol 5, 143-148.
Lenart P, Petronczki M, Steegmaier M, Di Fiore B, Lipp JJ, Hoffmann M, Rettig WJ, Kraut N & Peters JM (2007) The small-molecule inhibitor BI 2536 reveals novel insights into mitotic roles of polo-like kinase 1. Curr Biol 17, 304-315.
Hu CK, Coughlin M, Field CM & Mitchison TJ (2011) KIF4 regulates midzone length during cytokinesis. Curr Biol 21, 815-824.
Samejima K, Samejima I, Vagnarelli P, Ogawa H, Vargiu G, Kelly DA, de Lima Alves F, Kerr A, Green LC, Hudson DF et al. (2012) Mitotic chromosomes are compacted laterally by KIF4 and condensin and axially by topoisomerase IIalpha. J Cell Biol 199, 755-770.
Kurasawa Y, Earnshaw WC, Mochizuki Y, Dohmae N & Todokoro K (2004) Essential roles of KIF4 and its binding partner PRC1 in organized central spindle midzone formation. EMBO J 23, 3237-3248.
Tang F, Pan MH, Lu Y, Wan X, Zhang Y & Sun SC (2018) Involvement of Kif4a in spindle formation and chromosome segregation in mouse oocytes. Aging Dis 9, 623-633.
Camlin NJ, McLaughlin EA & Holt JE (2017) Kif4 Is Essential for Mouse Oocyte Meiosis. PLoS One 12, e0170650.
Zhou CJ, Wang XY, Han Z, Wang DH, Ma YZ & Liang CG (2019) Loss of CENPF leads to developmental failure in mouse embryos. Cell Cycle 18, 2784-2799.
Lu A, Zhou CJ, Wang DH, Han Z, Kong XW, Ma YZ, Yun ZZ & Liang CG (2017) Cytoskeleton-associated protein 5 and clathrin heavy chain binding regulates spindle assembly in mouse oocytes. Oncotarget 8, 17491-17503.