Physiological concentrations of glucocorticoids induce pathological DNA double-strand breaks.
DNA topoisomerase II
DSB repair
TDP2/EAPII/TTRAP
cortisol
dexamethasone
early transcriptional response
glucocorticoid
signal-induced transcription
Journal
Genes to cells : devoted to molecular & cellular mechanisms
ISSN: 1365-2443
Titre abrégé: Genes Cells
Pays: England
ID NLM: 9607379
Informations de publication
Date de publication:
Jan 2023
Jan 2023
Historique:
revised:
15
11
2022
received:
03
10
2022
accepted:
15
11
2022
pubmed:
24
11
2022
medline:
19
1
2023
entrez:
23
11
2022
Statut:
ppublish
Résumé
Steroid hormones induce the transcription of target genes by activating nuclear receptors. Early transcriptional response to various stimuli, including hormones, involves the active catalysis of topoisomerase II (TOP2) at transcription regulatory sequences. TOP2 untangles DNAs by transiently generating double-strand breaks (DSBs), where TOP2 covalently binds to DSB ends. When TOP2 fails to rejoin, called "abortive" catalysis, the resulting DSBs are repaired by tyrosyl-DNA phosphodiesterase 2 (TDP2) and non-homologous end-joining (NHEJ). A steroid, cortisol, is the most important glucocorticoid, and dexamethasone (Dex), a synthetic glucocorticoid, is widely used for suppressing inflammation in clinics. We here revealed that clinically relevant concentrations of Dex and physiological concentrations of cortisol efficiently induce DSBs in G
Substances chimiques
Transcription Factors
0
DNA-Binding Proteins
0
Glucocorticoids
0
Nuclear Proteins
0
Hydrocortisone
WI4X0X7BPJ
Phosphoric Diester Hydrolases
EC 3.1.4.-
DNA Topoisomerases, Type II
EC 5.99.1.3
DNA
9007-49-2
Types de publication
Journal Article
Langues
eng
Sous-ensembles de citation
IM
Pagination
53-67Subventions
Organisme : JSPS KAKENHI
ID : 19H04267
Organisme : JSPS KAKENHI
ID : 19K20449
Organisme : JSPS KAKENHI
ID : 20KK0186
Organisme : JSPS KAKENHI
ID : 18H03992
Organisme : JSPS KAKENHI
ID : 16H06306
Organisme : JSPS KAKENHI
ID : 20K16280
Organisme : JSPS KAKENHI
ID : 20K21525
Organisme : JSPS KAKENHI
ID : 21K07148
Organisme : NCI NIH HHS
ID : R01 CA149385
Pays : United States
Organisme : JSPS KAKENHI
ID : 16H12595
Informations de copyright
© 2022 Molecular Biology Society of Japan and John Wiley & Sons Australia, Ltd.
Références
Akagawa, R., Trinh, H. T., Saha, L. K., Tsuda, M., Hirota, K., Yamada, S., Shibata, A., Kanemaki, M. T., Nakada, S., Takeda, S., & Sasanuma, H. (2020). UBC13-mediated ubiquitin signaling promotes removal of blocking adducts from DNA double-Strand breaks. IScience, 23(4), 101027. https://doi.org/10.1016/j.isci.2020.101027
Al Mahmud, M. R., Ishii, K., Bernal-Lozano, C., Delgado-Sainz, I., Toi, M., Akamatsu, S., Fukumoto, M., Watanabe, M., Takeda, S., Ledesma, F. C., & Sasanuma, H. (2020). TDP2 suppresses genomic instability induced by androgens in the epithelial cells of prostate glands. Genes to Cells: Devoted to Molecular & Cellular Mechanisms, 25(7), 450-465. https://doi.org/10.1111/gtc.12770
Álvarez-Quilón, A., Serrano-Benítez, A., Ariel Lieberman, J., Quintero, C., Sánchez-Gutiérrez, D., Escudero, L. M., & Cortés-Ledesma, F. (2014). ATM specifically mediates repair of double-strand breaks with blocked DNA ends. Nature Communications, 5, 3347. https://doi.org/10.1038/ncomms4347
Austin, C. A., Lee, K. C., Swan, R. L., Khazeem, M. M., Manville, C. M., Cridland, P., Treumann, A., Porter, A., Morris, N. J., & Cowell, I. G. (2018). TOP2B: The first thirty years. International Journal of Molecular Sciences, 19(9), 2765. https://doi.org/10.3390/ijms19092765
Boija, A., Klein, I. A., Sabari, B. R., Dall'Agnese, A., Coffey, E. L., Zamudio, A. V., Li, C. H., Shrinivas, K., Manteiga, J. C., Hannett, N. M., Abraham, B. J., Afeyan, L. N., Guo, Y. E., Rimel, J. K., Fant, C. B., Schuijers, J., Lee, T. I., Taatjes, D. J., & Young, R. A. (2018). Transcription factors activate genes through the phase-separation capacity of their activation domains. Cell, 175(7), 1842-1855.e16. https://doi.org/10.1016/j.cell.2018.10.042
Buick, J. K., Moffat, I., Williams, A., Swartz, C. D., Recio, L., Hyduke, D. R., Li, H. H., Fornace, A. J., Jr., Aubrecht, J., & Yauk, C. L. (2015). Integration of metabolic activation with a predictive toxicogenomics signature to classify genotoxic versus nongenotoxic chemicals in human TK6 cells. Environmental and Molecular Mutagenesis, 56(6), 520-534. https://doi.org/10.1002/em.21940
Bunch, H. (2017). RNA polymerase II pausing and transcriptional regulation of the HSP70 expression. European Journal of Cell Biology, 96(8), 739-745. https://doi.org/10.1016/j.ejcb.2017.09.003
Bunch, H., Zheng, X., Burkholder, A., Dillon, S. T., Motola, S., Birrane, G., Ebmeier, C. C., Levine, S., Fargo, D., Hu, G., Taatjes, D. J., & Calderwood, S. K. (2014). TRIM28 regulates RNA polymerase II promoter-proximal pausing and pause release. Nature Structural & Molecular Biology, 21(10), 876-883. https://doi.org/10.1038/nsmb.2878
Bunch, H., Lawney, B. P., Lin, Y.-F., Asaithamby, A., Murshid, A., Wang, Y. E., Chen, B. P., & Calderwood, S. K. (2015). Transcriptional elongation requires DNA break-induced signalling. Nature Communications, 6, 10191. https://doi.org/10.1038/ncomms10191
Cain, D. W., & Cidlowski, J. A. (2020). After 62 years of regulating immunity, dexamethasone meets COVID-19. Nature Reviews. Immunology, 20(10), 587-588. https://doi.org/10.1038/s41577-020-00421-x
Calderwood, S. K. (2016). A critical role for topoisomerase IIb and DNA double strand breaks in transcription. Transcription, 7(3), 75-83. https://doi.org/10.1080/21541264.2016.1181142
Canela, A., Maman, Y., Huang, S.-Y. N., Wutz, G., Tang, W., Zagnoli-Vieira, G., Callen, E., Wong, N., Day, A., Peters, J. M., Caldecott, K. W., Pommier, Y., & Nussenzweig, A. (2019). Topoisomerase II-induced chromosome breakage and translocation is determined by chromosome architecture and transcriptional activity. Molecular Cell, 75(2), 252-266.e8. https://doi.org/10.1016/j.molcel.2019.04.030
Chappell, C. (2002). Involvement of human polynucleotide kinase in double-strand break repair by non-homologous end joining. The EMBO Journal, 21(11), 2827-2832. https://doi.org/10.1093/emboj/21.11.2827
Fellows, M. D., & O'Donovan, M. R. (2010). Etoposide, cadmium chloride, benzo[a]pyrene, cyclophosphamide and colchicine tested in the in vitro mammalian cell micronucleus test (MNvit) in the presence and absence of cytokinesis block using L5178Y mouse lymphoma cells and 2-aminoanthracene tested in MNvit in the absence of cytokinesis block using TK6 cells at AstraZeneca UK, in support of OECD draft test guideline 487. Mutation Research, 702(2), 163-170. https://doi.org/10.1016/j.mrgentox.2009.09.003
Ghosh, D., & Raghavan, S. C. (2021). Nonhomologous end joining: New accessory factors fine tune the machinery. Trends in Genetics: TIG, 37(6), 582-599. https://doi.org/10.1016/j.tig.2021.03.001
Gollapudi, B. B., White, P. A., & Honma, M. (2019). The IWGT in vitro mammalian cell gene mutation (MCGM) assays working group-introductory remarks & consensus statements. Mutation Research, 848, 403061. https://doi.org/10.1016/j.mrgentox.2019.05.017
Gómez-Herreros, F., Schuurs-Hoeijmakers, J. H. M., McCormack, M., Greally, M. T., Rulten, S., Romero-Granados, R., Counihan, T. J., Chaila, E., SCJ, E., Delanty, N., Cortes-Ledesma, F., de Brouwer, A. P., Cavalleri, G. L., El-khamisy, S. F., de Vries, B. B., & Caldecott, K. W. (2014). TDP2 protects transcription from abortive topoisomerase activity and is required for normal neural function. Nature Genetics, 46(5), 516-521. https://doi.org/10.1038/ng.2929
Goodwin, J. F., Kothari, V., Drake, J. M., Zhao, S., Dylgjeri, E., Dean, J. L., Schiewer, M. J., McNair, C., Jones, J. K., Aytes, A., Magee, M. S., Snook, A. E., Zhu, Z., Den RB, B. R. C., Gomella, L. G., Graham, N. A., Vashisht, A. A., Wohlschlegel, J. A., Graeber, T. G., … Knudsen, K. E. (2015). DNA-PKcs-mediated transcriptional regulation drives prostate cancer progression and metastasis. Cancer Cell, 28(1), 97-113. https://doi.org/10.1016/j.ccell.2015.06.004
Guess, A., Agrawal, S., Wei, C.-C., Ransom, R. F., Benndorf, R., & Smoyer, W. E. (2010). Dose- and time-dependent glucocorticoid receptor signaling in podocytes. American Journal of Physiology. Renal Physiology, 299(4), F845-F853. https://doi.org/10.1152/ajprenal.00161.2010
Haffner, M. C., Aryee, M. J., Toubaji, A., Esopi, D. M., Albadine, R., Gurel, B., Isaacs, W. B., Bova, G. S., Liu, W., Xu, J., Meeker, A. K., Netto, G., AMD, M., Nelson, W. G., & Yegnasubramanian, S. (2010). Androgen-induced TOP2B-mediated double-strand breaks and prostate cancer gene rearrangements. Nature Genetics, 42(8), 668-675. https://doi.org/10.1038/ng.613
Heming, N., Sivanandamoorthy, S., Meng, P., Bounab, R., & Annane, D. (2018). Immune effects of corticosteroids in sepsis. Frontiers in Immunology, 9, 1736. https://doi.org/10.3389/fimmu.2018.01736
Hoa, N. N., Kobayashi, J., Omura, M., Hirakawa, M., Yang, S.-H., Komatsu, K., Paull, T. T., Takeda, S., & Sasanuma, H. (2015). BRCA1 and CtIP are both required to recruit Dna2 at double-Strand breaks in homologous recombination. PLoS One, 10(4), e0124495. https://doi.org/10.1371/journal.pone.0124495
Hoa, N. N., Shimizu, T., Zhou, Z. W., Wang, Z.-Q., Deshpande, R. A., Paull, T. T., Akter, S., Tsuda, M., Furuta, R., Tsutsui, K., Takeda, S., & Sasanuma, H. (2016). Mre11 is essential for the removal of lethal topoisomerase 2 covalent cleavage complexes. Molecular Cell, 64(5), 1010. https://doi.org/10.1016/j.molcel.2016.11.028
Huang, W., Kalhorn, T. F., Baillie, M., Shen, D. D., & Thummel, K. E. (2007). Determination of free and total cortisol in plasma and urine by liquid chromatography-tandem mass spectrometry. Therapeutic Drug Monitoring, 29(2), 215-224. https://doi.org/10.1097/FTD.0b013e31803d14c0
Itou, J., Takahashi, R., Sasanuma, H., Tsuda, M., Morimoto, S., Matsumoto, Y., Ishii, T., Sato, F., Takeda, S., & Toi, M. (2020). Estrogen induces mammary ductal dysplasia via the upregulation of Myc expression in a DNA-repair-deficient condition. IScience, 23(2), 100821. https://doi.org/10.1016/j.isci.2020.100821
Jao, C. Y., & Salic, A. (2008). Exploring RNA transcription and turnover in vivo by using click chemistry. Proceedings of the National Academy of Sciences of the United States of America, 105(41), 15779-15784. https://doi.org/10.1073/pnas.0808480105
Joshi, R. S., Piña, B., & Roca, J. (2012). Topoisomerase II is required for the production of long pol II gene transcripts in yeast. Nucleic Acids Research, 40(16), 7907-7915. https://doi.org/10.1093/nar/gks626
Ju, B.-G., Lunyak, V. V., Perissi, V., Garcia-Bassets, I., Rose, D. W., Glass, C. K., & Rosenfeld, M. G. (2006). A topoisomerase IIbeta-mediated dsDNA break required for regulated transcription. New York, N.Y: Science (Vol. 312, pp. 1798-1802). https://doi.org/10.1126/science.1127196
Karras, G. I., Yi, S., Sahni, N., Fischer, M., Xie, J., Vidal, M., D'Andrea, A. D., Whitesell, L., & Lindquist, S. (2017). HSP90 shapes the consequences of human genetic variation. Cell, 168(5), 856-866.e12. https://doi.org/10.1016/j.cell.2017.01.023
King, I. F., Yandava, C. N., Mabb, A. M., Hsiao, J. S., Huang, H.-S., Pearson, B. L., Calabrese, J. M., Starmer, J., Parker, J. S., Magnuson, T., Chamberlain, S. J., Philpot, B. D., & Zylka, M. J. (2013). Topoisomerases facilitate transcription of long genes linked to autism. Nature, 501(7465), 58-62. https://doi.org/10.1038/nature12504
Kouzine, F., Levens, D., & Baranello, L. (2014). DNA topology and transcription. Nucleus (Austin, Tex.), 5(3), 195-202. https://doi.org/10.4161/nucl.28909
Lai, C.-H., Park, K.-S., Lee, D.-H., Alberobello, A. T., Raffeld, M., Pierobon, M., Pin, E., Petricoin, E. F., Wang, Y., & Giaccone, G. (2014). HSP-90 inhibitor ganetespib is synergistic with doxorubicin in small cell lung cancer. Oncogene, 33(40), 4867-4876. https://doi.org/10.1038/onc.2013.439
Ledesma, F. C., El Khamisy, S. F., Zuma, M. C., Osborn, K., & Caldecott, K. W. (2009). A human 5′-tyrosyl DNA phosphodiesterase that repairs topoisomerase-mediated DNA damage. Nature, 461(7264), 674-678. https://doi.org/10.1038/nature08444
Li, C., Sun, S.-Y., Khuri, F. R., & Li, R. (2011). Pleiotropic functions of EAPII/TTRAP/TDP2: Cancer development, chemoresistance and beyond. Cell Cycle (Georgetown, Tex.), 10(19), 3274-3283. https://doi.org/10.4161/cc.10.19.17763
Li, H.-H., Chen, R., Hyduke, D. R., Williams, A., Frötschl, R., Ellinger-Ziegelbauer, H., O'Lone, R., Yauk, C. L., Aubrecht, J., & Fornace, A. J. (2017). Development and validation of a high-throughput transcriptomic biomarker to address 21st century genetic toxicology needs. Proceedings of the National Academy of Sciences of the United States of America, 114(51), E10881-E10889. https://doi.org/10.1073/pnas.1714109114
Madabhushi, R. (2018). The roles of DNA topoisomerase IIβ in transcription. International Journal of Molecular Sciences, 19(7), 1917. https://doi.org/10.3390/ijms19071917
Madabhushi, R., Gao, F., Pfenning, A. R., Pan, L., Yamakawa, S., Seo, J., Rueda, R., Phan, T. X., Yamakawa, H., Pao, P. C., Stott, R. T., Gjoneska, E., Nott, A., Cho, S., Kellis, M., & Tsai, L.-H. (2015). Activity-induced DNA breaks govern the expression of neuronal early-response genes. Cell, 161(7), 1592-1605. https://doi.org/10.1016/j.cell.2015.05.032
McKinnon, P. J. (2016). Topoisomerases and the regulation of neural function. Nature Reviews Neuroscience, 17(11), 673-679. https://doi.org/10.1038/nrn.2016.101
Miyaji, M., Furuta, R., Hosoya, O., Sano, K., Hara, N., Kuwano, R., Kang, J., Tateno, M., Tsutsui, K. M., & Tsutsui, K. (2020). Topoisomerase IIβ targets DNA crossovers formed between distant homologous sites to induce chromatin opening. Scientific Reports, 10(1), 18550. https://doi.org/10.1038/s41598-020-75004-w
Morgan, B. P., Swick, A. G., Hargrove, D. M., LaFlamme, J. A., Moynihan, M. S., Carroll, R. S., Martin, K. A., Lee, E., Decosta, D., & Bordner, J. (2002). Discovery of potent, nonsteroidal, and highly selective glucocorticoid receptor antagonists. Journal of Medicinal Chemistry, 45(12), 2417-2424. https://doi.org/10.1021/jm0105530
Morimoto, S., Tsuda, M., Bunch, H., Sasanuma, H., Austin, C., & Takeda, S. (2019). Type II DNA topoisomerases cause spontaneous double-Strand breaks in genomic DNA. Genes, 10(11), 868. https://doi.org/10.3390/genes10110868
Naito, Y., Hino, K., Bono, H., & Ui-Tei, K. (2015). CRISPRdirect: Software for designing CRISPR/Cas guide RNA with reduced off-target sites. Bioinformatics, 31(7), 1120-1123. https://doi.org/10.1093/bioinformatics/btu743
Nitiss, J. L. (2009). Targeting DNA topoisomerase II in cancer chemotherapy. Nature Reviews. Cancer, 9(5), 338-350. https://doi.org/10.1038/nrc2607
Pommier, Y., Sun, Y., Huang, S. N., & Nitiss, J. L. (2016). Roles of eukaryotic topoisomerases in transcription, replication and genomic stability. Nature Reviews Molecular Cell Biology, 17(11), 703-721. https://doi.org/10.1038/nrm.2016.111
Pommier, Y., Nussenzweig, A., Takeda, S., & Austin, C. (2022). Human topoisomerases and their roles in genome stability and organization. Nature Reviews. Molecular Cell Biology, 23(6), 407-427. https://doi.org/10.1038/s41580-022-00452-3
Puc, J., Aggarwal, A. K., & Rosenfeld, M. G. (2017). Physiological functions of programmed DNA breaks in signal-induced transcription. Nature Reviews. Molecular Cell Biology, 18(8), 471-476. https://doi.org/10.1038/nrm.2017.43
Robins, P., & Lindahl, T. (1996). DNA ligase IV from HeLa cell nuclei. Journal of Biological Chemistry, 271(39), 24257-24261. https://doi.org/10.1074/jbc.271.39.24257
Russell, G., & Lightman, S. (2019). The human stress response. Nature Reviews. Endocrinology, 15(9), 525-534. https://doi.org/10.1038/s41574-019-0228-0
Sano, K., Miyaji-Yamaguchi, M., Tsutsui, K. M., & Tsutsui, K. (2008). Topoisomerase IIbeta activates a subset of neuronal genes that are repressed in AT-rich genomic environment. PLoS One, 3(12), e4103. https://doi.org/10.1371/journal.pone.0004103
Sasanuma, H., Tsuda, M., Morimoto, S., Saha, L. K., Rahman, M. M., Kiyooka, Y., Fujiike, H., Cherniack, A. D., Itou, J., Moreu, E. C., Toi, M., Nakada, S., Tanaka, H., Tsutsui, K., Yamada, S., Nussenzweig, A., & Takeda, S. (2018). BRCA1 ensures genome integrity by eliminating estrogen-induced pathological topoisomerase II-DNA complexes. Proceedings of the National Academy of Sciences, 115(45), E10642-E10651. https://doi.org/10.1073/pnas.1803177115
Scheer, F. A. J. L., Van Paassen, B., Van Montfrans, G. A., Fliers, E., Van Someren, E. J. W., Van Heerikhuize, J. J., & Buijs, R. M. (2002). Human basal cortisol levels are increased in hospital compared to home setting. Neuroscience Letters, 333(2), 79-82. https://doi.org/10.1016/S0304-3940(02)00988-6
Sciascia, N., Wu, W., Zong, D., Sun, Y., Wong, N., John, S., Wangsa, D., Ried, T., Bunting, S. F., Pommier, Y., & Nussenzweig, A. (2020). Suppressing proteasome mediated processing of topoisomerase II DNA-protein complexes preserves genome integrity. eLife, 9, e53. https://doi.org/10.7554/eLife.53447
Singh, H., Singh, J. R., Dhillon, V. S., Bali, D., & Paul, H. (1994). In vitro and in vivo genotoxicity evaluation of hormonal drugs II. Dexamethasone. Mutation Research, 308(1), 89-97. https://doi.org/10.1016/0027-5107(94)90201-1
Spoorenberg, S. M. C., Deneer, V. H. M., Grutters, J. C., Pulles, A. E., Voorn, G. P. P., Rijkers, G. T., WJW, B., & van de Garde, E. M. W. (2014). Pharmacokinetics of oral vs. intravenous dexamethasone in patients hospitalized with community-acquired pneumonia. British Journal of Clinical Pharmacology, 78(1), 78-83. https://doi.org/10.1111/bcp.12295
Stortz, M., Pecci, A., Presman, D. M., & Levi, V. (2020). Unraveling the molecular interactions involved in phase separation of glucocorticoid receptor. BMC Biology, 18(1), 59. https://doi.org/10.1186/s12915-020-00788-2
Strehl, C., Ehlers, L., Gaber, T., & Buttgereit, F. (2019). Glucocorticoids-all-Rounders tackling the versatile players of the immune system. Frontiers in Immunology, 10, 1744. https://doi.org/10.3389/fimmu.2019.01744
Tubbs, A., & Nussenzweig, A. (2017). Endogenous DNA damage as a source of genomic instability in cancer. Cell, 168(4), 644-656. https://doi.org/10.1016/j.cell.2017.01.002
Weijtens, O., Schoemaker, R. C., Cohen, A. F., Romijn, F. P., Lentjes, E. G., van Rooij, J., & van Meurs, J. C. (1998). Dexamethasone concentration in vitreous and serum after oral administration. American Journal of Ophthalmology, 125(5), 673-679. https://doi.org/10.1016/s0002-9394(98)00003-8
Wong, R. H. F., Chang, I., Hudak, C. S. S., Hyun, S., Kwan, H.-Y., & Sul, H. S. (2009). A role of DNA-PK for the metabolic gene regulation in response to insulin. Cell, 136(6), 1056-1072. https://doi.org/10.1016/j.cell.2008.12.040
Yauk, C. L., Buick, J. K., Williams, A., Swartz, C. D., Recio, L., Li, H.-H., Fornace, A. J., Jr., Thomson, E. M., & Aubrecht, J. (2016). Application of the TGx-28.65 transcriptomic biomarker to classify genotoxic and non-genotoxic chemicals in human TK6 cells in the presence of rat liver S9. Environmental and Molecular Mutagenesis, 57(4), 243-260. https://doi.org/10.1002/em.22004
Yu, T., MacPhail, S. H., Banáth, J. P., Klokov, D., & Olive, P. L. (2006). Endogenous expression of phosphorylated histone H2AX in tumors in relation to DNA double-strand breaks and genomic instability. DNA Repair, 5(8), 935-946. https://doi.org/10.1016/j.dnarep.2006.05.040