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Tytuł pozycji:

MDC1 is essential for G2/M transition and spindle assembly in mouse oocytes.

Tytuł:
MDC1 is essential for G2/M transition and spindle assembly in mouse oocytes.
Autorzy:
Leem J; Department of Integrative Biotechnology, Sungkyunkwan University, Suwon, Korea.
Oh JS; Department of Integrative Biotechnology, Sungkyunkwan University, Suwon, Korea. .; Biomedical Institute for Convergence at SKKU (BICS), Sungkyunkwan University, Suwon, Korea. .
Źródło:
Cellular and molecular life sciences : CMLS [Cell Mol Life Sci] 2022 Mar 23; Vol. 79 (4), pp. 200. Date of Electronic Publication: 2022 Mar 23.
Typ publikacji:
Journal Article
Język:
English
Imprint Name(s):
Publication: Basel : Springer
Original Publication: Basel ; Boston : Birkhauser, c1997-
MeSH Terms:
Cell Cycle Proteins*/metabolism
Oocytes*/metabolism
Animals ; Cell Cycle ; Cell Division ; DNA Damage ; Mammals/metabolism ; Mice
References:
Bartek J, Lukas J (2007) DNA damage checkpoints: from initiation to recovery or adaptation. Curr Opin Cell Biol 19(2):238–245. https://doi.org/10.1016/j.ceb.2007.02.009. (PMID: 10.1016/j.ceb.2007.02.00917303408)
Blackford AN, Jackson SP (2017) ATM, ATR, and DNA-PK: the trinity at the heart of the DNA damage response. Mol Cell 66(6):801–817. https://doi.org/10.1016/j.molcel.2017.05.015. (PMID: 10.1016/j.molcel.2017.05.01528622525)
Bartek J, Lukas J (2003) Chk1 and Chk2 kinases in checkpoint control and cancer. Cancer Cell 3(5):421–429. https://doi.org/10.1016/s1535-6108(03)00110-7. (PMID: 10.1016/s1535-6108(03)00110-712781359)
Lou Z, Minter-Dykhouse K, Wu X, Chen J (2003) MDC1 is coupled to activated CHK2 in mammalian DNA damage response pathways. Nature 421(6926):957–961. https://doi.org/10.1038/nature01447. (PMID: 10.1038/nature0144712607004)
Stewart GS, Wang B, Bignell CR, Taylor AM, Elledge SJ (2003) MDC1 is a mediator of the mammalian DNA damage checkpoint. Nature 421(6926):961–966. https://doi.org/10.1038/nature01446. (PMID: 10.1038/nature0144612607005)
Panier S, Boulton SJ (2014) Double-strand break repair: 53BP1 comes into focus. Nat Rev Mol Cell Biol 15(1):7–18. https://doi.org/10.1038/nrm3719. (PMID: 10.1038/nrm371924326623)
Polo SE, Jackson SP (2011) Dynamics of DNA damage response proteins at DNA breaks: a focus on protein modifications. Genes Dev 25(5):409–433. https://doi.org/10.1101/gad.2021311. (PMID: 10.1101/gad.2021311213639603049283)
Stucki M, Clapperton JA, Mohammad D, Yaffe MB, Smerdon SJ, Jackson SP (2005) MDC1 directly binds phosphorylated histone H2AX to regulate cellular responses to DNA double-strand breaks. Cell 123(7):1213–1226. https://doi.org/10.1016/j.cell.2005.09.038. (PMID: 10.1016/j.cell.2005.09.03816377563)
Celeste A, Fernandez-Capetillo O, Kruhlak MJ, Pilch DR, Staudt DW, Lee A, Bonner RF, Bonner WM, Nussenzweig A (2003) Histone H2AX phosphorylation is dispensable for the initial recognition of DNA breaks. Nat Cell Biol 5(7):675–679. https://doi.org/10.1038/ncb1004. (PMID: 10.1038/ncb100412792649)
Han SJ, Chen R, Paronetto MP, Conti M (2005) Wee1B is an oocyte-specific kinase involved in the control of meiotic arrest in the mouse. Curr Biol 15(18):1670–1676. https://doi.org/10.1016/j.cub.2005.07.056. (PMID: 10.1016/j.cub.2005.07.05616169490)
Morgan DO (1995) Principles of CDK regulation. Nature 374(6518):131–134. https://doi.org/10.1038/374131a0. (PMID: 10.1038/374131a07877684)
Adhikari D, Busayavalasa K, Zhang J, Hu M, Risal S, Bayazit MB, Singh M, Diril MK, Kaldis P, Liu K (2016) Inhibitory phosphorylation of Cdk1 mediates prolonged prophase I arrest in female germ cells and is essential for female reproductive lifespan. Cell Res 26(11):1212–1225. https://doi.org/10.1038/cr.2016.119. (PMID: 10.1038/cr.2016.119277670955099868)
Holt JE, Tran SM, Stewart JL, Minahan K, Garcia-Higuera I, Moreno S, Jones KT (2011) The APC/C activator FZR1 coordinates the timing of meiotic resumption during prophase I arrest in mammalian oocytes. Development 138(5):905–913. https://doi.org/10.1242/dev.059022. (PMID: 10.1242/dev.05902221270054)
Reis A, Chang HY, Levasseur M, Jones KT (2006) APCcdh1 activity in mouse oocytes prevents entry into the first meiotic division. Nat Cell Biol 8(5):539–540. (PMID: 10.1038/ncb1406)
Carroll J, Marangos P (2013) The DNA damage response in mammalian oocytes. Front Genet 4:117. https://doi.org/10.3389/fgene.2013.00117. (PMID: 10.3389/fgene.2013.00117238051523690358)
Marangos P, Carroll J (2012) Oocytes progress beyond prophase in the presence of DNA damage. Curr Biol 22(11):989–994. https://doi.org/10.1016/j.cub.2012.03.063. (PMID: 10.1016/j.cub.2012.03.06322578416)
Collins JK, Jones KT (2016) DNA damage responses in mammalian oocytes. Reproduction 152(1):R15-22. https://doi.org/10.1530/REP-16-0069. (PMID: 10.1530/REP-16-006927069010)
Collins JK, Lane SIR, Merriman JA, Jones KT (2015) DNA damage induces a meiotic arrest in mouse oocytes mediated by the spindle assembly checkpoint. Nat Commun 6:8553. https://doi.org/10.1038/ncomms9553. (PMID: 10.1038/ncomms955326522232)
Marangos P, Stevense M, Niaka K, Lagoudaki M, Nabti I, Jessberger R, Carroll J (2015) DNA damage-induced metaphase I arrest is mediated by the spindle assembly checkpoint and maternal age. Nat Commun 6:8706. https://doi.org/10.1038/ncomms9706. (PMID: 10.1038/ncomms970626522734)
Mayer A, Baran V, Sakakibara Y, Brzakova A, Ferencova I, Motlik J, Kitajima TS, Schultz RM, Solc P (2016) DNA damage response during mouse oocyte maturation. Cell Cycle 15(4):546–558. https://doi.org/10.1080/15384101.2015.1128592. (PMID: 10.1080/15384101.2015.1128592267452375056612)
Subramanian GN, Greaney J, Wei Z, Becherel O, Lavin M, Homer HA (2020) Oocytes mount a noncanonical DNA damage response involving APC-Cdh1-mediated proteolysis. J Cell Biol 219 (4). doi: https://doi.org/10.1083/jcb.201907213.
Eliezer Y, Argaman L, Kornowski M, Roniger M, Goldberg M (2014) Interplay between the DNA damage proteins MDC1 and ATM in the regulation of the spindle assembly checkpoint. J Biol Chem 289(12):8182–8193. https://doi.org/10.1074/jbc.M113.532739. (PMID: 10.1074/jbc.M113.532739245098553961647)
Barra V, Fachinetti D (2018) The dark side of centromeres: types, causes and consequences of structural abnormalities implicating centromeric DNA. Nat Commun 9(1):4340. https://doi.org/10.1038/s41467-018-06545-y. (PMID: 10.1038/s41467-018-06545-y303375346194107)
Bai GY, Choe MH, Kim JS, Oh JS (2020) Mis12 controls cyclin B1 stabilization via Cdc14B-mediated APC/C(Cdh1) regulation during meiotic G2/M transition in mouse oocytes. Development 147 (8). doi: https://doi.org/10.1242/dev.185322.
Homer H, Gui L, Carroll J (2009) A spindle assembly checkpoint protein functions in prophase I arrest and prometaphase progression. Science 326(5955):991–994. https://doi.org/10.1126/science.1175326. (PMID: 10.1126/science.1175326199655103428834)
Holt JE, Weaver J, Jones KT (2010) Spatial regulation of APCCdh1-induced cyclin B1 degradation maintains G2 arrest in mouse oocytes. Development 137(8):1297–1304. https://doi.org/10.1242/dev.047555. (PMID: 10.1242/dev.04755520223764)
Soderberg O, Gullberg M, Jarvius M, Ridderstrale K, Leuchowius KJ, Jarvius J, Wester K, Hydbring P, Bahram F, Larsson LG, Landegren U (2006) Direct observation of individual endogenous protein complexes in situ by proximity ligation. Nat Methods 3(12):995–1000. https://doi.org/10.1038/nmeth947. (PMID: 10.1038/nmeth94717072308)
Schuh M, Ellenberg J (2007) Self-organization of MTOCs replaces centrosome function during acentrosomal spindle assembly in live mouse oocytes. Cell 130(3):484–498. https://doi.org/10.1016/j.cell.2007.06.025. (PMID: 10.1016/j.cell.2007.06.02517693257)
Coster G, Hayouka Z, Argaman L, Strauss C, Friedler A, Brandeis M, Goldberg M (2007) The DNA damage response mediator MDC1 directly interacts with the anaphase-promoting complex/cyclosome. J Biol Chem 282(44):32053–32064. https://doi.org/10.1074/jbc.M705890200. (PMID: 10.1074/jbc.M70589020017827148)
Townsend K, Mason H, Blackford AN, Miller ES, Chapman JR, Sedgwick GG, Barone G, Turnell AS, Stewart GS (2009) Mediator of DNA damage checkpoint 1 (MDC1) regulates mitotic progression. J Biol Chem 284(49):33939–33948. https://doi.org/10.1074/jbc.M109.009191. (PMID: 10.1074/jbc.M109.009191198260032797164)
Krenning L, Feringa FM, Shaltiel IA, van den Berg J, Medema RH (2014) Transient activation of p53 in G2 phase is sufficient to induce senescence. Mol Cell 55(1):59–72. https://doi.org/10.1016/j.molcel.2014.05.007. (PMID: 10.1016/j.molcel.2014.05.00724910099)
Mullers E, Silva Cascales H, Jaiswal H, Saurin AT, Lindqvist A (2014) Nuclear translocation of Cyclin B1 marks the restriction point for terminal cell cycle exit in G2 phase. Cell Cycle 13(17):2733–2743. https://doi.org/10.4161/15384101.2015.945831. (PMID: 10.4161/15384101.2015.945831254863604615111)
Wiebusch L, Hagemeier C (2010) p53- and p21-dependent premature APC/C-Cdh1 activation in G2 is part of the long-term response to genotoxic stress. Oncogene 29(24):3477–3489. https://doi.org/10.1038/onc.2010.99. (PMID: 10.1038/onc.2010.9920383190)
Clift D, Schuh M (2015) A three-step MTOC fragmentation mechanism facilitates bipolar spindle assembly in mouse oocytes. Nat Commun 6:7217. https://doi.org/10.1038/ncomms8217. (PMID: 10.1038/ncomms821726147444)
Rai R, Phadnis A, Haralkar S, Badwe RA, Dai H, Li K, Lin SY (2008) Differential regulation of centrosome integrity by DNA damage response proteins. Cell Cycle 7(14):2225–2233. https://doi.org/10.4161/cc.7.14.6303. (PMID: 10.4161/cc.7.14.630318635967)
Namgoong S, Kim NH (2018) Meiotic spindle formation in mammalian oocytes: implications for human infertility. Biol Reprod 98(2):153–161. https://doi.org/10.1093/biolre/iox145. (PMID: 10.1093/biolre/iox14529342242)
Joukov V, Walter JC, De Nicolo A (2014) The Cep192-organized aurora A-Plk1 cascade is essential for centrosome cycle and bipolar spindle assembly. Mol Cell 55(4):578–591. https://doi.org/10.1016/j.molcel.2014.06.016. (PMID: 10.1016/j.molcel.2014.06.016250428044245277)
Li Z, Shao C, Kong Y, Carlock C, Ahmad N, Liu X (2017) DNA Damage Response-Independent Role for MDC1 in Maintaining Genomic Stability. Molecular and cellular biology 37 (9). https://doi.org/10.1128/MCB.00595-16.
Grant Information:
NRF-2017R1A6A1A03015642 Basic Science Research Program through the National Research Foundation of Korea (NRF); NRF-2019R1I1A2A01041413 Basic Science Research Program through the National Research Foundation of Korea (NRF)
Contributed Indexing:
Keywords: APC/C-Cdh1; DNA damage; G2/M transition; MDC1; Oocytes; Spindle assembly
Substance Nomenclature:
0 (Cell Cycle Proteins)
Entry Date(s):
Date Created: 20220323 Date Completed: 20220404 Latest Revision: 20220405
Update Code:
20240104
DOI:
10.1007/s00018-022-04241-1
PMID:
35320416
Czasopismo naukowe
Mammalian oocytes are particularly susceptible to accumulating DNA damage. However, unlike mitotic cells in which DNA damage induces G2 arrest by activating the ATM-Chk1/2-Cdc25 pathway, oocytes readily enter M-phase immediately following DNA damage. This implies a lack of a robust canonical G2/M DNA damage checkpoint in oocytes. Here we show that MDC1 plays a non-canonical role in controlling G2/M transition by regulating APC/C-Cdh1-mediated cyclin B1 degradation in response to DNA damage in mouse oocytes. Depletion of MDC1 impaired M-phase entry by decreasing cyclin B1 levels via the APC/C-Cdh1 pathway. Notably, the APC/C-Cdh1 regulation mediated by MDC1 was achieved by a direct interaction between MDC1 and APC/C-Cdh1. This interaction was transiently disrupted after DNA damage with a concomitant increase in Cdh1 levels, which, in turn, decreased cyclin B1 levels and delayed M-phase entry. Moreover, MDC1 depletion impaired spindle assembly by decreasing the integrity of microtubule organizing centers (MTOCs). Therefore, our results demonstrate that MDC1 is an essential molecule in regulating G2/M transition in response to DNA damage and in regulating spindle assembly in mouse oocytes. These results provide new insights into the regulation of the G2/M DNA damage checkpoint and cell cycle control in oocytes.
(© 2022. The Author(s), under exclusive licence to Springer Nature Switzerland AG.)

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