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CHAMP1-POGZ counteracts the inhibitory effect of 53BP1 on homologous recombination and affects PARP inhibitor resistance.

التفاصيل البيبلوغرافية
العنوان: CHAMP1-POGZ counteracts the inhibitory effect of 53BP1 on homologous recombination and affects PARP inhibitor resistance.
المؤلفون: Fujita H; Department of Molecular Oncology, Institute of Development, Aging and Cancer, Tohoku University, 4-1 Seiryo-machi, Aoba-ku, Sendai, Miyagi, 980-8575, Japan., Ikeda M; Department of Molecular Oncology, Institute of Development, Aging and Cancer, Tohoku University, 4-1 Seiryo-machi, Aoba-ku, Sendai, Miyagi, 980-8575, Japan., Ui A; Department of Molecular Oncology, Institute of Development, Aging and Cancer, Tohoku University, 4-1 Seiryo-machi, Aoba-ku, Sendai, Miyagi, 980-8575, Japan.; IDAC Fellow Laboratory, Institute of Development, Aging and Cancer, Tohoku University, 4-1 Seiryo-machi, Aoba-ku, Sendai, Miyagi, 980-8575, Japan., Ouchi Y; Department of Molecular Oncology, Institute of Development, Aging and Cancer, Tohoku University, 4-1 Seiryo-machi, Aoba-ku, Sendai, Miyagi, 980-8575, Japan., Mikami Y; Department of Molecular Oncology, Institute of Development, Aging and Cancer, Tohoku University, 4-1 Seiryo-machi, Aoba-ku, Sendai, Miyagi, 980-8575, Japan., Kanno SI; IDAC Fellow Laboratory, Institute of Development, Aging and Cancer, Tohoku University, 4-1 Seiryo-machi, Aoba-ku, Sendai, Miyagi, 980-8575, Japan., Yasui A; IDAC Fellow Laboratory, Institute of Development, Aging and Cancer, Tohoku University, 4-1 Seiryo-machi, Aoba-ku, Sendai, Miyagi, 980-8575, Japan., Tanaka K; Department of Molecular Oncology, Institute of Development, Aging and Cancer, Tohoku University, 4-1 Seiryo-machi, Aoba-ku, Sendai, Miyagi, 980-8575, Japan. kozo.tanaka.d2@tohoku.ac.jp.
المصدر: Oncogene [Oncogene] 2022 May; Vol. 41 (19), pp. 2706-2718. Date of Electronic Publication: 2022 Apr 07.
نوع المنشور: Journal Article
اللغة: English
بيانات الدورية: Publisher: Nature Publishing Group Country of Publication: England NLM ID: 8711562 Publication Model: Print-Electronic Cited Medium: Internet ISSN: 1476-5594 (Electronic) Linking ISSN: 09509232 NLM ISO Abbreviation: Oncogene Subsets: MEDLINE
أسماء مطبوعة: Publication: <2002->: Basingstoke : Nature Publishing Group
Original Publication: Basingstoke, Hampshire, UK : Scientific & Medical Division, MacMillan Press, c1987-
مواضيع طبية MeSH: DNA Breaks, Double-Stranded* , Poly(ADP-ribose) Polymerase Inhibitors*/pharmacology, BRCA1 Protein/metabolism ; Chromosomal Proteins, Non-Histone/metabolism ; DNA/metabolism ; DNA End-Joining Repair ; DNA Repair ; Homologous Recombination ; Humans ; Phosphoproteins/genetics ; Transposases/metabolism ; Tumor Suppressor p53-Binding Protein 1/metabolism
مستخلص: DNA double-strand break (DSB) repair-pathway choice regulated by 53BP1 and BRCA1 contributes to genome stability. 53BP1 cooperates with the REV7-Shieldin complex and inhibits DNA end resection to block homologous recombination (HR) and affects the sensitivity to inhibitors for poly (ADP-ribose) polymerases (PARPs) in BRCA1-deficient cells. Here, we show that a REV7 binding protein, CHAMP1 (chromosome alignment-maintaining phosphoprotein 1), has an opposite function of REV7 in DSB repair and promotes HR through DNA end resection together with POGZ (POGO transposable element with ZNF domain). CHAMP1 was recruited to laser-micro-irradiation-induced DSB sites and promotes HR, but not NHEJ. CHAMP1 depletion suppressed the recruitment of BRCA1, but not the recruitment of 53BP1, suggesting that CHAMP1 regulates DSB repair pathway in favor of HR. Depletion of either CHAMP1 or POGZ impaired the recruitment of phosphorylated RPA2 and CtIP (CtBP-interacting protein) at DSB sites, implying that CHAMP1, in complex with POGZ, promotes DNA end resection for HR. Furthermore, loss of CHAMP1 and POGZ restored the sensitivity to a PARP inhibitor in cells depleted of 53BP1 together with BRCA1. These data suggest that CHAMP1and POGZ counteract the inhibitory effect of 53BP1 on HR by promoting DNA end resection and affect the resistance to PARP inhibitors.
(© 2022. The Author(s), under exclusive licence to Springer Nature Limited.)
References: Ceccaldi R, Rondinelli B, D’Andrea AD. Repair pathway choices and consequences at the double-strand break. Trends Cell Biol. 2016;26:52–64. (PMID: 2643758610.1016/j.tcb.2015.07.009)
Chapman JR, Taylor MR, Boulton SJ. Playing the end game: DNA double-strand break repair pathway choice. Mol Cell. 2012;47:497–510. (PMID: 2292029110.1016/j.molcel.2012.07.029)
Chen H, Lisby M, Symington LS. RPA coordinates DNA end resection and prevents formation of DNA hairpins. Mol Cell. 2013;50:589–600. (PMID: 2370682210.1016/j.molcel.2013.04.032)
Zhu Z, Chung WH, Shim EY, Lee SE, Ira G. Sgs1 helicase and two nucleases Dna2 and Exo1 resect DNA double-strand break ends. Cell. 2008;134:981–94. (PMID: 18805091266251610.1016/j.cell.2008.08.037)
Kowalczykowski SC. An Overview of the molecular mechanisms of recombinational DNA repair. Cold Spring Harb Perspect Biol. 2015;7:a016410.
Sartori AA, Lukas C, Coates J, Mistrik M, Fu S, Bartek J, et al. Human CtIP promotes DNA end resection. Nature. 2007;450:509–14. (PMID: 17965729240943510.1038/nature06337)
You Z, Shi LZ, Zhu Q, Wu P, Zhang YW, Basilio A, et al. CtIP links DNA double-strand break sensing to resection. Mol Cell. 2009;36:954–69. (PMID: 20064462280741510.1016/j.molcel.2009.12.002)
Escribano-Diaz C, Orthwein A, Fradet-Turcotte A, Xing M, Young JT, Tkac J, et al. A cell cycle-dependent regulatory circuit composed of 53BP1-RIF1 and BRCA1-CtIP controls DNA repair pathway choice. Mol Cell. 2013;49:872–83. (PMID: 2333330610.1016/j.molcel.2013.01.001)
Yoshida K, Miki Y. Role of BRCA1 and BRCA2 as regulators of DNA repair, transcription, and cell cycle in response to DNA damage. Cancer Sci. 2004;95:866–71. (PMID: 1554650310.1111/j.1349-7006.2004.tb02195.x)
Rose M, Burgess JT, O’Byrne K, Richard DJ, Bolderson E. PARP inhibitors: clinical relevance, mechanisms of action and tumor resistance. Front Cell Dev Biol. 2020;8:564601. (PMID: 33015058750909010.3389/fcell.2020.564601)
Itoh G, Kanno S, Uchida KS, Chiba S, Sugino S, Watanabe K, et al. CAMP (C13orf8, ZNF828) is a novel regulator of kinetochore-microtubule attachment. EMBO J. 2011;30:130–44. (PMID: 2106339010.1038/emboj.2010.276)
Hara K, Taharazako S, Ikeda M, Fujita H, Mikami Y, Kikuchi S, et al. Dynamic feature of mitotic arrest deficient 2-like protein 2 (MAD2L2) and structural basis for its interaction with chromosome alignment-maintaining phosphoprotein (CAMP). J Biol Chem. 2017;292:17658–67. (PMID: 2888730710.1074/jbc.M117.804237)
Sale JE. REV7/MAD2L2: the multitasking maestro emerges as a barrier to recombination. EMBO J. 2015;34:1609–11. (PMID: 25896508447539610.15252/embj.201591697)
Murakumo Y, Roth T, Ishii H, Rasio D, Numata S, Croce CM, et al. A human REV7 homolog that interacts with the polymerase zeta catalytic subunit hREV3 and the spindle assembly checkpoint protein hMAD2. J Biol Chem. 2000;275:4391–7. (PMID: 1066061010.1074/jbc.275.6.4391)
Pfleger CM, Salic A, Lee E, Kirschner MW. Inhibition of Cdh1-APC by the MAD2-related protein MAD2L2: a novel mechanism for regulating Cdh1. Genes Dev. 2001;15:1759–64. (PMID: 1145982531274010.1101/gad.897901)
Chen J, Fang G. MAD2B is an inhibitor of the anaphase-promoting complex. Genes Dev. 2001;15:1765–70. (PMID: 1145982631273710.1101/gad.898701)
Boersma V, Moatti N, Segura-Bayona S, Peuscher MH, van der Torre J, Wevers BA, et al. MAD2L2 controls DNA repair at telomeres and DNA breaks by inhibiting 5’ end resection. Nature. 2015;521:537–40. (PMID: 25799990448129610.1038/nature14216)
Xu G, Chapman JR, Brandsma I, Yuan J, Mistrik M, Bouwman P, et al. REV7 counteracts DNA double-strand break resection and affects PARP inhibition. Nature. 2015;521:541–4. (PMID: 25799992467131610.1038/nature14328)
Gupta R, Somyajit K, Narita T, Maskey E, Stanlie A, Kremer M, et al. DNA repair network analysis reveals shieldin as a key regulator of NHEJ and PARP inhibitor sensitivity. Cell. 2018;173:972–88. (PMID: 29656893810809310.1016/j.cell.2018.03.050)
Mirman Z, Lottersberger F, Takai H, Kibe T, Gong Y, Takai K, et al. 53BP1-RIF1-shieldin counteracts DSB resection through CST- and Polalpha-dependent fill-in. Nature. 2018;560:112–6. (PMID: 30022158607255910.1038/s41586-018-0324-7)
Noordermeer SM, Adam S, Setiaputra D, Barazas M, Pettitt SJ, Ling AK, et al. The shieldin complex mediates 53BP1-dependent DNA repair. Nature. 2018;560:117–21. (PMID: 30022168614100910.1038/s41586-018-0340-7)
Ghezraoui H, Oliveira C, Becker JR, Bilham K, Moralli D, Anzilotti C, et al. 53BP1 cooperation with the REV7-shieldin complex underpins DNA structure-specific NHEJ. Nature. 2018;560:122–7. (PMID: 30046110698921710.1038/s41586-018-0362-1)
Dev H, Chiang TW, Lescale C, de Krijger I, Martin AG, Pilger D, et al. Shieldin complex promotes DNA end-joining and counters homologous recombination in BRCA1-null cells. Nat Cell Biol. 2018;20:954–65. (PMID: 30022119614544410.1038/s41556-018-0140-1)
Isidor B, Kury S, Rosenfeld JA, Besnard T, Schmitt S, Joss S, et al. De Novo Truncating Mutations in the Kinetochore-Microtubules Attachment Gene CHAMP1 Cause Syndromic Intellectual Disability. Hum Mutat. 2016;37:354–8. (PMID: 2675139510.1002/humu.22952)
Fanti L, Pimpinelli S. HP1: a functionally multifaceted protein. Curr Opin Genet Dev. 2008;18:169–74. (PMID: 1832987110.1016/j.gde.2008.01.009)
Zeng W, Ball AR Jr., Yokomori K. HP1: heterochromatin binding proteins working the genome. Epigenetics. 2010;5:287–92. (PMID: 2042174310.4161/epi.5.4.11683)
Yearim A, Gelfman S, Shayevitch R, Melcer S, Glaich O, Mallm JP, et al. HP1 is involved in regulating the global impact of DNA methylation on alternative splicing. Cell Rep. 2015;10:1122–34. (PMID: 2570481510.1016/j.celrep.2015.01.038)
Abe Y, Sako K, Takagaki K, Hirayama Y, Uchida KS, Herman JA, et al. HP1-assisted Aurora B kinase activity prevents chromosome segregation errors. Dev Cell. 2016;36:487–97. (PMID: 26954544494907210.1016/j.devcel.2016.02.008)
Nozawa RS, Nagao K, Masuda HT, Iwasaki O, Hirota T, Nozaki N, et al. Human POGZ modulates dissociation of HP1alpha from mitotic chromosome arms through Aurora B activation. Nat Cell Biol. 2010;12:719–27. (PMID: 2056286410.1038/ncb2075)
Baude A, Aaes TL, Zhai B, Al-Nakouzi N, Oo HZ, Daugaard M, et al. Hepatoma-derived growth factor-related protein 2 promotes DNA repair by homologous recombination. Nucleic Acids Res. 2016;44:2214–26. (PMID: 2672138710.1093/nar/gkv1526)
Gudmundsdottir B, Gudmundsson KO, Klarmann KD, Singh SK, Sun L, Singh S, et al. POGZ Is required for silencing mouse embryonic beta-like hemoglobin and human fetal hemoglobin expression. Cell Rep. 2018;23:3236–48. (PMID: 29898395730196610.1016/j.celrep.2018.05.043)
Hempel M, Cremer K, Ockeloen CW, Lichtenbelt KD, Herkert JC, Denecke J, et al. De Novo mutations in CHAMP1 cause intellectual disability with severe speech impairment. Am J Hum Genet. 2015;97:493–500. (PMID: 26340335456498610.1016/j.ajhg.2015.08.003)
Tanaka AJ, Cho MT, Retterer K, Jones JR, Nowak C, Douglas J, et al. De novo pathogenic variants in CHAMP1 are associated with global developmental delay, intellectual disability, and dysmorphic facial features. Cold Spring Harb Mol Case Stud. 2016;2:a000661. (PMID: 27148580484984410.1101/mcs.a000661)
Ye Y, Cho MT, Retterer K, Alexander N, Ben-Omran T, Al-Mureikhi M, et al. De novo POGZ mutations are associated with neurodevelopmental disorders and microcephaly. Cold Spring Harb Mol Case Stud. 2015;1:a000455. (PMID: 27148570485088510.1101/mcs.a000455)
Lee YJ, Park SJ, Ciccone SL, Kim CR, Lee SH. An in vivo analysis of MMC-induced DNA damage and its repair. Carcinogenesis. 2006;27:446–53. (PMID: 1625817610.1093/carcin/bgi254)
Clairmont CS, Sarangi P, Ponnienselvan K, Galli LD, Csete I, Moreau L, et al. TRIP13 regulates DNA repair pathway choice through REV7 conformational change. Nat Cell Biol. 2020;22:87–96. (PMID: 31915374733636810.1038/s41556-019-0442-y)
Adachi N, So S, Koyama H. Loss of nonhomologous end joining confers camptothecin resistance in DT40 cells. Implications for the repair of topoisomerase I-mediated DNA damage. J Biol Chem. 2004;279:37343–8. (PMID: 1521803410.1074/jbc.M313910200)
Pierce AJ, Johnson RD, Thompson LH, Jasin M. XRCC3 promotes homology-directed repair of DNA damage in mammalian cells. Genes Dev. 1999;13:2633–8. (PMID: 1054154931709410.1101/gad.13.20.2633)
Ogiwara H, Ui A, Otsuka A, Satoh H, Yokomi I, Nakajima S, et al. Histone acetylation by CBP and p300 at double-strand break sites facilitates SWI/SNF chromatin remodeling and the recruitment of non-homologous end joining factors. Oncogene. 2011;30:2135–46. (PMID: 2121777910.1038/onc.2010.592)
Willmore E, de Caux S, Sunter NJ, Tilby MJ, Jackson GH, Austin CA, et al. A novel DNA-dependent protein kinase inhibitor, NU7026, potentiates the cytotoxicity of topoisomerase II poisons used in the treatment of leukemia. Blood. 2004;103:4659–65. (PMID: 1501036910.1182/blood-2003-07-2527)
Marechal A, Zou L. RPA-coated single-stranded DNA as a platform for post-translational modifications in the DNA damage response. Cell Res. 2015;25:9–23. (PMID: 2540347310.1038/cr.2014.147)
Cruz-Garcia A, Lopez-Saavedra A, Huertas P. BRCA1 accelerates CtIP-mediated DNA-end resection. Cell Rep. 2014;9:451–9. (PMID: 2531097310.1016/j.celrep.2014.08.076)
Caron MC, Sharma AK, O’Sullivan J, Myler LR, Ferreira MT, Rodrigue A, et al. Poly(ADP-ribose) polymerase-1 antagonizes DNA resection at double-strand breaks. Nat Commun. 2019;10:2954. (PMID: 31273204660962210.1038/s41467-019-10741-9)
Bunting SF, Callen E, Wong N, Chen HT, Polato F, Gunn A, et al. 53BP1 inhibits homologous recombination in Brca1-deficient cells by blocking resection of DNA breaks. Cell. 2010;141:243–54. (PMID: 20362325285757010.1016/j.cell.2010.03.012)
Bouwman P, Aly A, Escandell JM, Pieterse M, Bartkova J, van der Gulden H, et al. 53BP1 loss rescues BRCA1 deficiency and is associated with triple-negative and BRCA-mutated breast cancers. Nat Struct Mol Biol. 2010;17:688–95. (PMID: 20453858291250710.1038/nsmb.1831)
Bochum S, Berger S, Martens UM. Olaparib. Recent Results Cancer Res. 2018;211:217–33. (PMID: 3006977010.1007/978-3-319-91442-8_15)
Vermeulen M, Eberl HC, Matarese F, Marks H, Denissov S, Butter F, et al. Quantitative interaction proteomics and genome-wide profiling of epigenetic histone marks and their readers. Cell. 2010;142:967–80. (PMID: 2085001610.1016/j.cell.2010.08.020)
Hein MY, Hubner NC, Poser I, Cox J, Nagaraj N, Toyoda Y, et al. A human interactome in three quantitative dimensions organized by stoichiometries and abundances. Cell. 2015;163:712–23. (PMID: 2649661010.1016/j.cell.2015.09.053)
Simonetta M, de Krijger I, Serrat J, Moatti N, Fortunato D, Hoekman L, et al. H4K20me2 distinguishes pre-replicative from post-replicative chromatin to appropriately direct DNA repair pathway choice by 53BP1-RIF1-MAD2L2. Cell Cycle. 2018;17:124–36. (PMID: 29160738581543810.1080/15384101.2017.1404210)
Tomida J, Takata KI, Bhetawal S, Person MD, Chao HP, Tang DG et al. FAM35A associates with REV7 and modulates DNA damage responses of normal and BRCA1-defective cells. EMBO J. 2018;37:e99543.
Sharma S, Hicks JK, Chute CL, Brennan JR, Ahn JY, Glover TW, et al. REV1 and polymerase zeta facilitate homologous recombination repair. Nucleic Acids Res. 2012;40:682–91. (PMID: 2192616010.1093/nar/gkr769)
Bluhm A, Casas-Vila N, Scheibe M, Butter F. Reader interactome of epigenetic histone marks in birds. Proteomics. 2016;16:427–36. (PMID: 2670308710.1002/pmic.201500217)
Stessman HAF, Willemsen MH, Fenckova M, Penn O, Hoischen A, Xiong B, et al. Disruption of POGZ Is associated with intellectual disability and autism spectrum disorders. Am J Hum Genet. 2016;98:541–52. (PMID: 26942287489024110.1016/j.ajhg.2016.02.004)
White J, Beck CR, Harel T, Posey JE, Jhangiani SN, Tang S, et al. POGZ truncating alleles cause syndromic intellectual disability. Genome Med. 2016;8:3. (PMID: 26739615470230010.1186/s13073-015-0253-0)
Tan B, Zou Y, Zhang Y, Zhang R, Ou J, Shen Y, et al. A novel de novo POGZ mutation in a patient with intellectual disability. J Hum Genet. 2016;61:357–9. (PMID: 2676387910.1038/jhg.2015.156)
Deciphering Developmental Disorders S. Prevalence and architecture of de novo mutations in developmental disorders. Nature. 2017;542:433–8. (PMID: 10.1038/nature21062)
Rulten SL, Caldecott KW. DNA strand break repair and neurodegeneration. DNA Repair (Amst). 2013;12:558–67. (PMID: 10.1016/j.dnarep.2013.04.008)
Sack LM, Davoli T, Li MZ, Li Y, Xu Q, Naxerova K, et al. Profound tissue specificity in proliferation control underlies cancer drivers and aneuploidy patterns. Cell. 2018;173:499–514. (PMID: 29576454664328310.1016/j.cell.2018.02.037)
Garrity M, Kavus H, Rojas-Vasquez M, Valenzuela I, Larson A, Reed S et al. Neurodevelopmental phenotypes in individuals with pathogenic variants in CHAMP1. Cold Spring Harb Mol Case Stud. 2021;7:a006092.
Fradet-Turcotte A, Canny MD, Escribano-Diaz C, Orthwein A, Leung CC, Huang H, et al. 53BP1 is a reader of the DNA-damage-induced H2A Lys 15 ubiquitin mark. Nature. 2013;499:50–54. (PMID: 23760478395540110.1038/nature12318)
Daugaard M, Baude A, Fugger K, Povlsen LK, Beck H, Sorensen CS, et al. LEDGF (p75) promotes DNA-end resection and homologous recombination. Nat Struct Mol Biol. 2012;19:803–10. (PMID: 2277310310.1038/nsmb.2314)
Stewart GS, Wang B, Bignell CR, Taylor AM, Elledge SJ. MDC1 is a mediator of the mammalian DNA damage checkpoint. Nature. 2003;421:961–6. (PMID: 1260700510.1038/nature01446)
Silverman J, Takai H, Buonomo SB, Eisenhaber F, de Lange T. Human Rif1, ortholog of a yeast telomeric protein, is regulated by ATM and 53BP1 and functions in the S-phase checkpoint. Genes Dev. 2004;18:2108–19. (PMID: 1534249051528910.1101/gad.1216004)
Unno J, Itaya A, Taoka M, Sato K, Tomida J, Sakai W, et al. FANCD2 binds CtIP and regulates DNA-end resection during DNA interstrand crosslink repair. Cell Rep. 2014;7:1039–47. (PMID: 2479443010.1016/j.celrep.2014.04.005)
Lan L, Ui A, Nakajima S, Hatakeyama K, Hoshi M, Watanabe R, et al. The ACF1 complex is required for DNA double-strand break repair in human cells. Mol Cell. 2010;40:976–87. (PMID: 2117266210.1016/j.molcel.2010.12.003)
Lan L, Nakajima S, Komatsu K, Nussenzweig A, Shimamoto A, Oshima J, et al. Accumulation of Werner protein at DNA double-strand breaks in human cells. J Cell Sci. 2005;118:4153–62. (PMID: 1614123410.1242/jcs.02544)
Nakajima S, Lan L, Kanno S, Usami N, Kobayashi K, Mori M, et al. Replication-dependent and -independent responses of RAD18 to DNA damage in human cells. J Biol Chem. 2006;281:34687–95. (PMID: 1698029610.1074/jbc.M605545200)
Ikeda M, Tanaka K. Plk1 bound to Bub1 contributes to spindle assembly checkpoint activity during mitosis. Sci Rep. 2017;7:8794. (PMID: 28821799556274610.1038/s41598-017-09114-3)
Hino M, Iemura K, Ikeda M, Itoh G, Tanaka K. Chromosome alignment-maintaining phosphoprotein CHAMP1 plays a role in cell survival through regulating Mcl-1 expression. Cancer Sci. 2021;112:3711–21. (PMID: 34107118840943310.1111/cas.15018)
المشرفين على المادة: 0 (BRCA1 Protein)
0 (CHAMP1 protein, human)
0 (Chromosomal Proteins, Non-Histone)
0 (POGZ protein, human)
0 (Phosphoproteins)
0 (Poly(ADP-ribose) Polymerase Inhibitors)
0 (Tumor Suppressor p53-Binding Protein 1)
9007-49-2 (DNA)
EC 2.7.7.- (Transposases)
تواريخ الأحداث: Date Created: 20220408 Date Completed: 20220510 Latest Revision: 20221022
رمز التحديث: 20231215
DOI: 10.1038/s41388-022-02299-6
PMID: 35393543
قاعدة البيانات: MEDLINE
الوصف
تدمد:1476-5594
DOI:10.1038/s41388-022-02299-6