p53 target gene AEN is a nuclear exonuclease required for p53-dependent apoptosis
Abstract
DNA degradation is one of the biochemical hallmarks detected in apoptotic cells, and several nucleases have been reported to function cooperatively in this process. It has also been suggested that different sets of nucleases are activated by different stimuli, and induce distinct patterns of DNA degradation. Here we report that apoptosis-enhancing nuclease (AEN) is a novel direct target gene of p53. AEN is induced by p53 with various DNA damage, and its expression is regulated by the phosphorylation status of p53. We demonstrate that AEN is a typical exonuclease with conserved exonuclease domains Exo I-III, and it targets both single- and double-stranded DNA and RNA. AEN induces apoptosis by itself, and the conserved domains are essential for both AEN nuclease activity and its apoptosis-inducing ability. AEN possesses nuclear and nucleolar localization signals, and it translocates from the nucleolus to nucleoplasm upon apoptosis induction. We also show the dislocation of nucleophosmin in conjunction with the translocation of AEN to the nucleoplasm, indicating the ability of AEN in nucleolus disruption. In addition, AEN is shown to be required for efficient DNA fragmentation in p53-dependent apoptosis. These results suggest that AEN is an important downstream mediator of p53 in apoptosis induction.
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The p53 target gene AEN encodes for an apoptosis-enhancing nuclease that further supports apoptosis through digestion of double-stranded DNA.
“The p53 target gene AEN encodes for an apoptosis-enhancing nuclease that further supports apoptosis through digestion of double-stranded DNA.44”
From Census and evaluation of p53 target genes (2017) · cites this paper as [44]
Cites
p53, the cellular gatekeeper for growth and division
Levine, A. J. (1997) · Cell · doi:10.1016/s0092-8674(00)81871-1 · Cited by 7,693 · see citing works
Vogelstein, B., Lane, D., & Levine, A. J. (2000) · Nature · doi:10.1038/35042675 · Cited by 6,607 · see citing works
Live or let die: the cell's response to p53
Vousden, K. H., & Lü, X. (2002) · Nature reviews. Cancer · doi:10.1038/nrc864 · Cited by 3,177 · see citing works
Noxa, a BH3-Only Member of the Bcl-2 Family and Candidate Mediator of p53-Induced Apoptosis
Oda, E., Ohki, R., Murasawa, H., Nemoto, J., Shibue, T., Yamashita, T., Tokino, T., Taniguchi, T., & Tanaka, †. N. (2000) · Science · doi:10.1126/science.288.5468.1053 · Cited by 2,112 · see citing works
Self-citationActivation of the ATM Kinase by Ionizing Radiation and Phosphorylation of p53
Canman, C. E., Lim, D.-S., Cimprich, K. A., Taya, Y., Tamai, K., Sakaguchi, K., Appella, E., Kastan, M. B., & Siliciano, J. D. (1998) · Science · doi:10.1126/science.281.5383.1677 · Cited by 2,042 · see citing works
Self-citationDefinition of a consensus binding site for p53
El-Deiry, W. S., Kern, S. E., Pietenpol, J. A., Kinzler, K. W., & Vogelstein, B. (1992) · Nature Genetics · doi:10.1038/ng0492-45 · Cited by 1,985 · see citing works
Enhanced Phosphorylation of p53 by ATM in Response to DNA Damage
Banin, S., Moyal, L., Shieh, S.-Y., Taya, Y., Anderson, C. W., Chessa, L., Smorodinsky, N. I., Prives, C., Reiss, Y., Shiloh, Y., et al. (1998) · Science · doi:10.1126/science.281.5383.1674 · Cited by 1,797 · see citing works
Self-citationEndonuclease G is an apoptotic DNase when released from mitochondria
Li, L. Y., Luo, X., & Wang, X. (2001) · Nature · doi:10.1038/35083620 · Cited by 1,787 · see citing works
Rubbi, C. P., & Milner, J. (2003) · The EMBO Journal · doi:10.1093/emboj/cdg579 · Cited by 811 · see citing works
Regulation ofp53downstream genes
El‐Deiry, W. S. (1998) · Seminars in Cancer Biology · doi:10.1006/scbi.1998.0097 · Cited by 797 · see citing works
RNA-quality control by the exosome
Houseley, J. M., LaCava, J., & Tollervey, D. W. (2006) · Nature Reviews Molecular Cell Biology · doi:10.1038/nrm1964 · Cited by 645 · see citing works
Prives, C. (1998) · Cell · doi:10.1016/s0092-8674(00)81774-2 · Cited by 623 · see citing works
Nuclear targeting signal recognition: a key control point in nuclear transport?
Jans, D. A., Xiao, C.-Y., & Lam, M. H. C. (2000) · BioEssays · doi:10.1002/(sici)1521-1878(200006)22:6 · Cited by 519 · see citing works
Chronic polyarthritis caused by mammalian DNA that escapes from degradation in macrophages
Kawane, K., Ohtani, M., Miwa, K., Kizawa, T., Kanbara, Y., Yoshioka, Y., Yoshikawa, H., & Nagata, S. (2006) · Nature · doi:10.1038/nature05245 · Cited by 467 · see citing works
Degradation of chromosomal DNA during apoptosis
Nagata, S., Nagase, H., Kawane, K., Mukae, N., & Fukuyama, H. (2003) · Cell Death and Differentiation · doi:10.1038/sj.cdd.4401161 · Cited by 454 · see citing works
p53: 25 years after its discovery
Hofseth, L. J., Hussain, S. P., & Harris, C. C. (2004) · Trends in Pharmacological Sciences · doi:10.1016/j.tips.2004.02.009 · Cited by 431 · see citing works
Phosphorylation of p53 Serine 15 Increases Interaction with CBP
Lambert, P. F., Kashanchi, F., Radonovich, M. F., Shiekhattar, R., & Brady, J. N. (1998) · Journal of Biological Chemistry · doi:10.1074/jbc.273.49.33048 · Cited by 423 · see citing works
PRAK Is Essential for ras-Induced Senescence and Tumor Suppression
Sun, P., Yoshizuka, N., New, L., Moser, B. A., Li, Y., Liao, R., Xie, C., Chen, J., Deng, Q., Yamout, M., et al. (2007) · Cell · doi:10.1016/j.cell.2006.11.050 · Cited by 321 · see citing works
Trashing the genome: the role of nucleases during apoptosis
Samejima, K., & Earnshaw, W. C. (2005) · Nature Reviews Molecular Cell Biology · doi:10.1038/nrm1715 · Cited by 312 · see citing works
Saito, S., Yamaguchi, H., Higashimoto, Y., Chao, C., Xu, Y., Fornace, A. J., Appella, E., & Anderson, C. W. (2003) · Journal of Biological Chemistry · doi:10.1074/jbc.m305135200 · Cited by 253 · see citing works
Cellular stress and nucleolar function
Mayer, C., & Grummt, I. (2005) · Cell Cycle · doi:10.4161/cc.4.8.1925 · Cited by 233 · see citing works
Moser, M. J. (1997) · Nucleic Acids Research · doi:10.1093/nar/25.24.5110 · Cited by 232 · see citing works
Integration of TGF-ß and Ras/MAPK Signaling Through p53 Phosphorylation
Cordenonsi, M., Montagner, M., Adorno, M., Zacchigna, L., Martello, G., Mamidi, A., Soligo, S., Dupont, S., & Piccolo, S. (2007) · Science · doi:10.1126/science.1135961 · Cited by 202 · see citing works
Reprimo, a New Candidate Mediator of the p53-mediated Cell Cycle Arrest at the G2 Phase
Ohki, R., Nemoto, J., Murasawa, H., Oda, E., Inazawa, J., Tanaka, N., & Taniguchi, T. (2000) · Journal of Biological Chemistry · doi:10.1074/jbc.c000235200 · Cited by 201 · see citing works
Self-citationMutations in serines 15 and 20 of human p53 impair its apoptotic activity
Unger, T., Sionov, R. V., Moallem, E., Yee, C., Howley, P. M., Oren, M., & Haupt, Y. (1999) · Oncogene · doi:10.1038/sj.onc.1202656 · Cited by 190 · see citing works
Mayo, L. D., Seo, Y. R., Jackson, M. W., Smith, M. L., Guzman, J. R., Korgaonkar, C. K., & Donner, D. B. (2005) · Journal of Biological Chemistry · doi:10.1074/jbc.m503026200 · Cited by 146 · see citing works
Schaetzlein, S., Nalapareddy, K., Ju, Z., Lechel, A., Stępczyńska, A., Lilli, D. R., Clark, A. B., Rudolph, C., Kühnel, F., Wei, K., et al. (2007) · Cell · doi:10.1016/j.cell.2007.08.029 · Cited by 144 · see citing works
Cell Type- and Promoter-specific Roles of Ser18 Phosphorylation in Regulating p53 Responses
Chao, C., Hergenhahn, M., Kaeser, M. D., Wu, Z., Saito, S., Iggo, R., Hollstein, M., Appella, E., & Xu, Y. (2003) · Journal of Biological Chemistry · doi:10.1074/jbc.m306938200 · Cited by 141 · see citing works
DNA Damage-induced Translocation of the Werner Helicase Is Regulated by Acetylation
Blander, G., Zalle, N., Daniely, Y., Taplick, J., Gray, M. D., & Oren, M. (2002) · Journal of Biological Chemistry · doi:10.1074/jbc.m210479200 · Cited by 139 · see citing works
Defective apoptosis and B-cell lymphomas in mice with p53 point mutation at Ser 23
MacPherson, D., Kim, J., Kim, T., Rhee, B. K., van Oostrom, C. T., DiTullio, R. A., Venere, M., Halazonetis, T. D., Bronson, R., de Vries, A., et al. (2004) · The EMBO Journal · doi:10.1038/sj.emboj.7600363 · Cited by 124 · see citing works
Regulation of p53 Stability and Function in HCT116 Colon Cancer Cells
Kaeser, M. D., Kaeser-Pebernard, S., & Iggo, R. D. (2004) · Journal of Biological Chemistry · doi:10.1074/jbc.m311732200 · Cited by 112 · see citing works
Rowland, R. R. R., & Yoo, D. (2003) · Virus Research · doi:10.1016/s0168-1702(03)00161-8 · Cited by 111 · see citing works
Regulation of the p53 transcriptional activity
Liu, G., & Chen, X. (2005) · Journal of Cellular Biochemistry · doi:10.1002/jcb.20700 · Cited by 99 · see citing works
Tounekti, O., Belehradek, J., & Mir, L. M. (1995) · Experimental Cell Research · doi:10.1006/excr.1995.1116 · Cited by 96 · see citing works
Nucleophosmin, HDM2 and p53: Players in UV Damage Incited Nucleolar Stress Response
Kurki, S., Peltonen, K., & Laiho, M. (2004) · Cell Cycle · doi:10.4161/cc.3.8.1015 · Cited by 72 · see citing works
Ohki, R., Kawase, T., Ohta, T., Ichikawa, H., & Taya, Y. (2006) · Cancer Science · doi:10.1111/j.1349-7006.2006.00375.x · Cited by 60 · see citing works
Self-citationLife, Death, and Ubiquitin: Taming the Mule
Shmueli, A., & Oren, M. (2005) · Cell · doi:10.1016/j.cell.2005.06.018 · Cited by 53 · see citing works
Cuts can kill: the roles of apoptotic nucleases in cell death and animal development
Parrish, J. Z., & Xue, D. (2006) · Chromosoma · doi:10.1007/s00412-005-0038-0 · Cited by 48 · see citing works
Lee, J. H., Koh, Y. A., Cho, C.-K., Lee, S., Lee, Y., & Bae, S. (2005) · Biochemical and Biophysical Research Communications · doi:10.1016/j.bbrc.2005.08.264 · Cited by 29 · see citing works
Karni-Schmidt, O., Friedler, A., Zupnick, A., McKinney, K. M., Mattia, M., Beckerman, R., Bouvet, P., Sheetz, M. P., Fersht, A. R., & Prives, C. L. (2007) · Oncogene · doi:10.1038/sj.onc.1210162 · Cited by 28 · see citing works
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Census and evaluation of p53 target genes
Fischer, M. (2017) · Oncogene · doi:10.1038/onc.2016.502 · Cited by 971 · see citing works
Fischer, M., Grossmann, P., Padi, M., & DeCaprio, J. A. (2016) · Nucleic Acids Research · doi:10.1093/nar/gkw523 · Cited by 330 · see citing works
Regulation of autophagy by stress-responsive transcription factors
Pietrocola, F., Izzo, V., Niso‐Santano, M., Vacchelli, E., Galluzzi, L., Maiuri, M. C., & Kroemer, G. (2013) · Seminars in Cancer Biology · doi:10.1016/j.semcancer.2013.05.008 · Cited by 270 · see citing works
PH Domain-Only Protein PHLDA3 Is a p53-Regulated Repressor of Akt
Kawase, T., Ohki, R., Shibata, T., Tsutsumi, S., Kamimura, N., Inazawa, J., Ohta, T., Ichikawa, H., Aburatani, H., Tashiro, F., et al. (2009) · Cell · doi:10.1016/j.cell.2008.12.002 · Cited by 239 · see citing works
Self-citationTumour suppression by p53: the importance of apoptosis and cellular senescence
Zuckerman, V., Wolyniec, K., Sionov, R. V., Haupt, S., & Haupt, Y. (2009) · The Journal of Pathology · doi:10.1002/path.2584 · Cited by 210 · see citing works
He, Y., Patterson, S. E., Wang, N., Hecker, M., Martin, J. W., El‐Din, M. G., Giesy, J. P., & Wiseman, S. B. (2012) · Water Research · doi:10.1016/j.watres.2012.09.004 · Cited by 163 · see citing works
Exploring the multiple roles of guardian of the genome: P53
Feroz, W., & Sheikh, A. M. A. (2020) · Egyptian Journal of Medical Human Genetics · doi:10.1186/s43042-020-00089-x · Cited by 161 · see citing works
The transcription factor p53: Not a repressor, solely an activator.
Fischer, M., Steiner, L., & Engeland, K. (2014) · Cell Cycle · doi:10.4161/15384101.2014.949083 · Cited by 153 · see citing works
Differential genomic targeting of the transcription factor TAL1 in alternate haematopoietic lineages
Palii, C. G., Perez‐Iratxeta, C., Yao, Z., Cao, Y., Dai, F., Davison, J., Atkins, H. L., Allan, D., Dilworth, F. J., Gentleman, R. C., et al. (2010) · The EMBO Journal · doi:10.1038/emboj.2010.342 · Cited by 140 · see citing works
Cellular and nuclear degradation during apoptosis
He, B., Lü, N., & Zhou, Z. (2009) · Current Opinion in Cell Biology · doi:10.1016/j.ceb.2009.08.008 · Cited by 129 · see citing works
Lacombe, J., Chao Sima, A., Amundson, S. A., & Zenhausern, F. (2018) · PLoS ONE · doi:10.1371/journal.pone.0198851 · Cited by 99 · see citing works
UCHL1 Is a Putative Tumor Suppressor in Ovarian Cancer Cells and Contributes to Cisplatin Resistance
Jin, C., Yu, W., Lou, X., Zhou, F., Han, X., Zhao, N., & Lin, B. (2013) · Journal of Cancer · doi:10.7150/jca.6641 · Cited by 91 · see citing works
Moussay, E., Palissot, V., Vallar, L., Poirel, H. A., Wenner, T., El‐Khoury, V., Aouali, N., Moer, K. V., Leners, B., Bernardin, F., et al. (2010) · Molecular Cancer · doi:10.1186/1476-4598-9-115 · Cited by 88 · see citing works
A distinct p53 target gene set predicts for response to the selective p53–HDM2 inhibitor NVP-CGM097
Jeay, S., Gaulis, S., Ferretti, S., Bitter, H., Ito, M., Valat, T., Murakami, M., Ruetz, S., Guthy, D. A., Rynn, C., et al. (2015) · eLife · doi:10.7554/elife.06498 · Cited by 85 · see citing works
ISG20L1 is a p53 family target gene that modulates genotoxic stress-induced autophagy
Eby, K. G., Rosenbluth, J. M., Mays, D. J., Marshall, C. B., Barton, C. E., Sinha, S., Johnson, K. N., Tang, L., & Pietenpol, J. A. (2010) · Molecular Cancer · doi:10.1186/1476-4598-9-95 · Cited by 72 · see citing works
Novel p53 target gene FUCA 1 encodes a fucosidase and regulates growth and survival of cancer cells
Ezawa, I., Sawai, Y., Kawase, T., Okabe, A., Tsutsumi, S., Ichikawa, H., Kobayashi, Y., Tashiro, F., Namiki, H., Kondo, T., et al. (2016) · Cancer Science · doi:10.1111/cas.12933 · Cited by 65 · see citing works
Self-citationIER5 generates a novel hypo-phosphorylated active form of HSF1 and contributes to tumorigenesis
Asano, Y., Kawase, T., Okabe, A., Tsutsumi, S., Ichikawa, H., Tatebe, S., Kitabayashi, I., Tashiro, F., Namiki, H., Kondo, T., et al. (2016) · Scientific Reports · doi:10.1038/srep19174 · Cited by 66 · see citing works
Self-citationRashi‐Elkeles, S., Warnatz, H.-J., Elkon, R., Kupershtein, A., Chobod, Y., Paz, A., Amstislavskiy, V. S., Sultan, M., Safer, H. M., Nietfeld, W., et al. (2014) · Science Signaling · doi:10.1126/scisignal.2005032 · Cited by 57 · see citing works
Bustamante, M., Hernandéz-Ferrer, C., Tewari, A., Sarria, Y., Harrison, G. I., Puigdecanet, E., Nonell, L., Kang, W., Friedländer, M. R., Estivill, X., et al. (2019) · British Journal of Dermatology · doi:10.1111/bjd.18527 · Cited by 52 · see citing works
The role of DNA exonucleases in protecting genome stability and their impact on ageing
Mason, P. A., & Cox, L. S. (2011) · AGE · doi:10.1007/s11357-011-9306-5 · Cited by 43 · see citing works
Chiang, I., WANG, W.-S., Liu, H., Yang, S., Tang, N.-Y., & Chung, J. (2015) · Oncology Reports · doi:10.3892/or.2015.4159 · Cited by 45 · see citing works
Effects of dietary aflatoxin on the hepatic expression of apoptosis genes in growing barrows1
Rustemeyer, S. M., Lamberson, W. R., Ledoux, D. R., Wells, K. D., Austin, K. J., & Cammack, K. M. (2011) · Journal of Animal Science · doi:10.2527/jas.2010-3473 · Cited by 42 · see citing works
Watanabe, T., Suzuki, T., Natsume, M., Nakajima, M., Narumi, K., Hamada, S., Sakuma, T., Koeda, A., Oshida, K., Miyamoto, Y., et al. (2012) · Mutation Research/Genetic Toxicology and Environmental Mutagenesis · doi:10.1016/j.mrgentox.2012.04.011 · Cited by 41 · see citing works
Wang, H., Zong, Q., Shiqin, W., Zhao, C., Wu, S., & Bao, W. (2019) · Journal of Agricultural and Food Chemistry · doi:10.1021/acs.jafc.9b00613 · Cited by 36 · see citing works
Skeletal muscle-on-a-chip in microgravity as a platform for regeneration modeling and drug screening
Kim, S., Ayan, B., Shayan, M., Rando, T. A., & Huang, N. F. (2024) · Stem Cell Reports · doi:10.1016/j.stemcr.2024.06.010 · Cited by 34 · see citing works
p53-PHLDA3-Akt Network: The Key Regulators of Neuroendocrine Tumorigenesis
Chen, Y., & Ohki, R. (2020) · International Journal of Molecular Sciences · doi:10.3390/ijms21114098 · Cited by 29 · see citing works
Self-citationUlmke, P. A., Xie, Y., Sokpor, G., Pham, L., Shomroni, O., Berulava, T., Rosenbusch, J., Basu, U., Fischer, A., Nguyen, H. P., et al. (2021) · Development · doi:10.1242/dev.188276 · Cited by 29 · see citing works
Ozeki, C., Sawai, Y., Shibata, T., Kohno, T., Okamoto, K., Yokota, J., Tashiro, F., Tanuma, S., Sakai, R., Kawase, T., et al. (2011) · Journal of Biological Chemistry · doi:10.1074/jbc.m110.208587 · Cited by 28 · see citing works
Self-citationHashimoto, M., Saito, Y., Nakagawa, R., Ogahara, I., Takagi, S., Takata, S., Amitani, H., Endo, M., Yuki, H., Ramilowski, J. A., et al. (2021) · Nature Cancer · doi:10.1038/s43018-021-00177-w · Cited by 28 · see citing works
Uchiumi, F., Miyazaki, S., & Tanuma, S.-I. (2011) · Cellular and Molecular Life Sciences · doi:10.1007/s00018-011-0674-x · Cited by 27 · see citing works
Malik, A. I., Rowan‐Carroll, A., Williams, A., Lemieux, C. L., Long, A. S., Arlt, V. M., Phillips, D. H., White, P. A., & Yauk, C. L. (2013) · Mutagenesis · doi:10.1093/mutage/get031 · Cited by 25 · see citing works
TSPLASSO: A Two-Stage Prior LASSO Algorithm for Gene Selection Using Omics Data
Yang, S.-J., Chen, S., Wang, P., Chen, A.-M., & Tian, T. (2023) · IEEE journal of biomedical and health informatics · doi:10.1109/jbhi.2023.3326485 · Cited by 22 · see citing works
Breton, T. S., Kenter, L. W., Greenlaw, K., Montgomery, J., Goetz, G., Berlinsky, D. L., & Luckenbach, J. A. (2018) · Comparative Biochemistry and Physiology Part A Molecular & Integrative Physiology · doi:10.1016/j.cbpa.2018.10.024 · Cited by 23 · see citing works
Gast, M., Nageswaran, V., Kuss, A. W., Tzvetkova, A., Wang, X., Mochmann, L. H., Rad, P. R., Weiß, S., Simm, S., Zeller, T., et al. (2022) · Cells · doi:10.3390/cells11243970 · Cited by 22 · see citing works
Krishnaraj, J., Yamamoto, T., & Ohki, R. (2023) · Cancers · doi:10.3390/cancers15133399 · Cited by 22 · see citing works
Self-citationWu, S., Hsiao, Y.-T., Chen, J.-C., Lin, J.-H., Hsu, S., Hsia, T., Yang, S., Hsu, W., & Chung, J. (2014) · Molecules · doi:10.3390/molecules19056047 · Cited by 22 · see citing works
Gene Expression Signature in Patients With Symptomatic Peripheral Artery Disease
Newman, J. D., Cornwell, M., Zhou, H., Rockman, C. R., Heguy, A., Suárez, Y., Cheng, H. S., Feinberg, M. W., Hochman, J. S., Ruggles, K. V., et al. (2021) · Arteriosclerosis Thrombosis and Vascular Biology · doi:10.1161/atvbaha.120.315857 · Cited by 21 · see citing works
Exonucleases: Degrading DNA to Deal with Genome Damage, Cell Death, Inflammation and Cancer
Manils, J., Marruecos, L., & Soler, C. (2022) · Cells · doi:10.3390/cells11142157 · Cited by 19 · see citing works
Resnick‐Silverman, L., Zhou, R. W., Campbell, M. J., Leibling, I., Parsons, R. E., & Manfredi, J. J. (2023) · Cell Reports · doi:10.1016/j.celrep.2023.112216 · Cited by 17 · see citing works
Hassel, J. C., Zimmer, L., Sickmann, T., Eigentler, T., Meier, F. E., Mohr, P., Pukrop, T., Roesch, A., Vordermark, D., Wendl, C. M., et al. (2023) · Cancers · doi:10.3390/cancers15133448 · Cited by 19 · see citing works
Matrix-free human lung organoids derived from induced pluripotent stem cells to model lung injury
Budeus, B., Kroepel, C., Stasch, L. M., & Klein, D. (2024) · Stem Cell Research & Therapy · doi:10.1186/s13287-024-04106-3 · Cited by 23 · see citing works
Prevalence, causes and impact of TP53-loss phenocopying events in human tumors
Fito-Lopez, B., Salvadores, M., Álvarez‐Álvarez, M. M., & Supek, F. (2023) · BMC Biology · doi:10.1186/s12915-023-01595-1 · Cited by 18 · see citing works
Zhang, C., Zhai, S., Li, X., Zhang, Q., Wu, L., Liu, Y., Jiang, C., Zhou, H., Li, F., Zhang, S., et al. (2014) · Cell Death and Disease · doi:10.1038/cddis.2014.76 · Cited by 17 · see citing works
Long, G., Ouyang, W., Zhang, Y., Sun, G., Gan, J., Hu, Z., & Li, H. (2021) · Frontiers in Molecular Biosciences · doi:10.3389/fmolb.2021.608369 · Cited by 17 · see citing works
Ehlers, A., Florian, S., Schumacher, F., Meinl, W., Lenze, D., Hummel, M., Heise, T., Seidel, A., Glatt, H. R., & Lampen, A. (2015) · Molecular Nutrition & Food Research · doi:10.1002/mnfr.201400707 · Cited by 16 · see citing works
Saito, K., Fujiwara, T., Hatta, S., Morita, M., Ono, K., Suzuki, C., Fukuhara, N., Onishi, Y., Nakamura, Y., Kawamata, S., et al. (2019) · Molecular and Cellular Biology · doi:10.1128/mcb.00387-18 · Cited by 15 · see citing works
CT Irradiation-induced Changes of Gene Expression within Peripheral Blood Cells
Kaatsch, H. L., Majewski, M., Schrock, G., Obermair, R., Seidel, J., Nestler, K., Abend, M., Waldeck, S. S., Port, M., Ullmann, R., et al. (2020) · Health Physics · doi:10.1097/hp.0000000000001231 · Cited by 15 · see citing works
von Stromberg, K., Seddar, L., Ip, W.-H., Günther, T., Gornott, B., Weinert, S.-C., Hüppner, M., Bertzbach, L. D., & Dobner, T. (2023) · Proceedings of the National Academy of Sciences · doi:10.1073/pnas.2310770120 · Cited by 12 · see citing works
Cleavage of mRNAs by a minority of pachytene piRNAs improves sperm fitness
Cecchini, K. R., Zamani, M., Ajaykumar, N., Vega‐Badillo, J., Bagci, A., Bailey, S., Zamore, P. D., & Gainetdinov, I. V. (2026) · Nature · doi:10.1038/s41586-026-10102-9 · Cited by 11 · see citing works
Zhang, Y., Du, J., Jin, L., Pan, L., Yan, X., & Lin, S. (2023) · Frontiers in Pharmacology · doi:10.3389/fphar.2023.1326346 · Cited by 11 · see citing works
Bertucci, J. I., Bandaralage, S. M. I., & Hecker, M. (2020) · Aquatic Toxicology · doi:10.1016/j.aquatox.2020.105523 · Cited by 11 · see citing works
Sakurai, M., Watanabe, T., Suzuki, T., & Furihata, C. (2014) · Genes and Environment · doi:10.3123/jemsge.2014.005 · Cited by 10 · see citing works
Early Biomarkers Associated with P53 Signaling for Acute Radiation Injury
Li, W., Zhou, S., Jia, M., Li, X., Li, L., Wang, Q., Qi, Z., Zhou, P., Li, Y., & Wang, Z. (2022) · Life · doi:10.3390/life12010099 · Cited by 9 · see citing works
Carraro, C., Bonaguro, L., Schulte-Schrepping, J., Horne, A., Oestreich, M., Warnat‐Herresthal, S., Helbing, T., Franco, M. D., Händler, K., Mukherjee, S., et al. (2022) · eLife · doi:10.7554/elife.78012 · Cited by 9 · see citing works
Tan, F., Chen, L., Yuan, Y., He, X., Su, Y., Cao, S., Xie, C., Gu, M., & Zou, Y. (2022) · Green Synthesis and Catalysis · doi:10.1016/j.gresc.2022.09.003 · Cited by 9 · see citing works
Li, X., Chen, Y., Dong, Y., Ma, Z., Zheng, W., & Lin, Y. (2023) · Heliyon · doi:10.1016/j.heliyon.2023.e22433 · Cited by 8 · see citing works
Ma, Y., Wang, J., He, X., Liu, Y., zhen, S., An, L., Yang, Q., Niu, F., Wang, H., An, B.-R., et al. (2023) · Nucleic Acids Research · doi:10.1093/nar/gkad1210 · Cited by 8 · see citing works
Bowen, M. E., Mulligan, A. S., Sorayya, A., & Attardi, L. D. (2021) · Cell Death and Differentiation · doi:10.1038/s41418-021-00738-7 · Cited by 8 · see citing works
Lu, L., Xu, X., Du, X., Zeng, T., Yang, T., Chen, Y., Tao, Z., Zhong, S., Wen, J., & Zhou, C. (2020) · Molecular Reproduction and Development · doi:10.1002/mrd.23428 · Cited by 8 · see citing works
Haehnel, S., Rade, M., Kaiser, N. C., Reiche, K., Horn, A., Löffler, D., Blumert, C., Rapp, F., Horn, F., Meixensberger, J., et al. (2021) · FEBS Open Bio · doi:10.1002/2211-5463.13353 · Cited by 7 · see citing works
ISG20L1 acts as a co-activator of DAPK1 in the activation of the p53-dependent cell death pathway
Zou, S., Zhang, C., Xu, H., Liu, Z., Hu, Y., Wang, W., Liu, K., Wen, Q., & Song, L. (2023) · Journal of Cell Science · doi:10.1242/jcs.260915 · Cited by 7 · see citing works
Nordin, N., Majid, N. B. A., Othman, R., Omer, F. A. A., Nasharuddin, M. N. A., & Hashim, N. M. (2018) · APOPTOSIS · doi:10.1007/s10495-018-1447-x · Cited by 7 · see citing works
Brothwell, J. A., Fortney, K. R., Gao, H., Wilson, L. S., Andrews, C. F., Tran, T. M., Hu, X. Y., Batteiger, T. A., Barnes, S., Liu, Y., et al. (2022) · mBio · doi:10.1128/mbio.03125-22 · Cited by 6 · see citing works
Exploring the Genetic Associations Between the Use of Statins and Alzheimer's Disease
Lee, J., Park, S., Kim, Y., Kim, H. M., & Oh, C. (2022) · Journal of Lipid and Atherosclerosis · doi:10.12997/jla.2022.11.2.133 · Cited by 6 · see citing works
Seo, J., Park, S., Lee, D. C., Yoo, W., Yang, Y. R., Seo, H. W., Park, J. L., Joo, J., Park, K. C., & Byun, S. (2026) · Signal Transduction and Targeted Therapy · doi:10.1038/s41392-026-02688-3 · Cited by 5 · see citing works
Lee, S.-I., Kim, S. K., & Kang, S. W. (2024) · Current Issues in Molecular Biology · doi:10.3390/cimb46080536 · Cited by 5 · see citing works
Gato, W. E., Hales, D. B., McGee, S. R., & Means, J. C. (2014) · Toxicology International · doi:10.4103/0971-6580.128796 · Cited by 5 · see citing works
Cecchini, K. R., Ajaykumar, N., Bagci, A., Zamore, P. D., & Gainetdinov, I. V. (2024) · bioRxiv (Cold Spring Harbor Laboratory) · doi:10.1101/2024.11.02.621675 · Cited by 5 · see citing works
Davenport, K. M., Lockhart, K., Stoecklein, K. S., Schnabel, R. D., Spencer, T. E., & Ortega, M. S. (2025) · Journal of Dairy Science · doi:10.3168/jds.2025-26496 · Cited by 4 · see citing works
Ortega, M., Agena, E., Chen, W., Cao, H., Vasudevan, S., Shivapurkar, N., Pierobon, M., & Smith, J. P. (2025) · International Journal of Molecular Sciences · doi:10.3390/ijms262311699 · Cited by 4 · see citing works
Majerčiak, V., Alvarado-Hernandez, B., Ma, Y., Duduskar, S. N., Lobanov, A. V., Cam, M., & Zheng, Z. (2024) · mBio · doi:10.1128/mbio.03172-24 · Cited by 4 · see citing works
PHLDA3 Is an Important Downstream Mediator of p53 in Squamous Cell Carcinogenesis
Saito, M., Sada, A., Fukuyo, M., Aoki, K., Okumura, K., Tabata, Y., Chen, Y., Kaneda, A., Wakabayashi, Y., & Ohki, R. (2021) · Journal of Investigative Dermatology · doi:10.1016/j.jid.2021.09.007 · Cited by 4 · see citing works
Self-citationHuang, J., Wang, L., Jiang, M., Chen, Q., Zhang, X., Wang, Y., Jiang, Z., & Zhang, Z. (2015) · Immunologic Research · doi:10.1007/s12026-015-8701-x · Cited by 4 · see citing works
Luo, M., Ma, J., Pan, X., Zhang, X., & Yao, H. (2023) · Pathogens · doi:10.3390/pathogens13010024 · Cited by 3 · see citing works
Grzadkowski, M. R., Holly, H. D., Somers, J., & Demir, E. (2021) · BMC Bioinformatics · doi:10.1186/s12859-021-04147-y · Cited by 3 · see citing works
Gi, M., Suzuki, S., Kanki, M., Yokohira, M., Tsukamoto, T., Fujioka, M., Vachiraarunwong, A., Qiu, G., Guo, R., & Wanibuchi, H. (2024) · Archives of Toxicology · doi:10.1007/s00204-024-03755-w · Cited by 3 · see citing works
Implications of noncoding regulatory functions in the development of insulinomas
Ramos-Rodríguez, M., Subirana-Granés, M., Norris, R., Sordi, V., Fernández, Á., Fuentes-Páez, G., Pérez-González, B., Balaguer, C. B., Raurell‐Vila, H., Chowdhury, M., et al. (2024) · Cell Genomics · doi:10.1016/j.xgen.2024.100604 · Cited by 3 · see citing works
IER5 Is a p53-Regulated Activator of HSF1 That Contributes to Promotion of Cancer
Kawase, T., Chen, Y., & Ohki, R. (2019) · Heat shock proteins · doi:10.1007/978-3-030-03952-3_13 · Cited by 3 · see citing works
Self-citationWu, R. T. Y., & Cheng, W. (2015) · Elsevier eBooks · doi:10.1016/b978-0-12-418680-4.00021-x · Cited by 3 · see citing works
Biological Functions of the Duplicated GGAA-motifs in Various Human Promoter Regions
Uchiumi, F., Miyazaki, S., & Tanuma, S.-I. (2011) · YAKUGAKU ZASSHI · doi:10.1248/yakushi.131.1787 · Cited by 4 · see citing works
Pei, Z., Sun, Y., Zhang, S., Gong, C., Mao, G., Zhang, X., Meng, W., Cen, J., Li, S., Sun, M., et al. (2025) · International Immunopharmacology · doi:10.1016/j.intimp.2025.114285 · Cited by 2 · see citing works
Molecular and Cellular Effects of CT Scans in Human Adipose Mesenchymal Stem Cells
Ignatov, M. A., Markelova, E. E., Chigasova, A., Osipov, A., Buianov, I., Fedotov, Y. А., Eremin, P. S., Vorobyeva, N. Y., Zyuzikov, N., & Osipov, A. N. (2025) · International Journal of Molecular Sciences · doi:10.3390/ijms26178584 · Cited by 3 · see citing works
Kotula‐Balak, M., Duliban, M., Gurgul, A., Krakowska, I., Grzmil, P., Bilińska, B., & Wolski, J. K. (2021) · Andrologia · doi:10.1111/and.14222 · Cited by 2 · see citing works
Knops, K. (2013) · DuEPublico (University of Duisburg-Essen) · Cited by 2 · see citing works
Gast, M., Nageswaran, V., Kuss, A. W., Tzvetkova, A., Wang, X., Mochmann, L. H., Rad, P. R., Weiß, S., Simm, S., Zeller, T., et al. (2022) · Research Square · doi:10.21203/rs.3.rs-1540419/v1 · Cited by 2 · see citing works
Gast, M., Nageswaran, V., Kuss, A. W., Tzvetkova, A., Wang, X., Mochmann, L. H., Rad, P. R., Weiß, S., Simm, S., Zeller, T., et al. (2022) · Research Square · doi:10.21203/rs.3.rs-1540419/v2 · Cited by 2 · see citing works
Ghosh, A., Ghosh, A., Sinha, A., Mathai, S., Bhaumik, J., Mukhopadhyay, A., Maitra, A., Biswas, N. K., Majumder, P. P., & Sengupta, S. (2023) · Tumor Biology · doi:10.3233/tub-220035 · Cited by 1 · see citing works
Zou, Z., Ren, T., Li, J.-Q., Jiao, T., Wang, M., Huang, L., Lin, S., Wang, Y., Guo, X., Song, Y.-Y., et al. (2024) · Journal of Clinical and Translational Hepatology · doi:10.14218/jcth.2024.00111 · Cited by 1 · see citing works
Kin, K., Bhogale, S. G., Zhu, L., Thomas, D., Bertól, J. W., Zheng, W. J., Sinha, S., & Fakhouri, W. D. (2024) · Human Molecular Genetics · doi:10.1093/hmg/ddae109 · Cited by 1 · see citing works
He, Y. (2012) · HARVEST (University of Saskatchewan) · Cited by 1 · see citing works
Forgie, B. N., Prakash, R., Marno, D., Abdalbari, F. H., Zorychta, E., Noman, A. S. M., Goyeneche, A. A., Gilbert, L., Burnier, J. V., & Telleria, C. M. (2026) · bioRxiv (Cold Spring Harbor Laboratory) · doi:10.64898/2026.06.30.735544 · Cited by 1 · see citing works
Sarek, G. (2010) · Työväentutkimus Vuosikirja
Yazid, N. S. M., Hashim, N. M., Ali, H. M., & Go, R. (2021) · Sains Malaysiana · doi:10.17576/jsm-2021-5004-08
Control of AEN by NOD2.Preprint
Mamoor, S. (2023) · doi:10.31219/osf.io/6kn9e
Additional file 2 of Prevalence, causes and impact of TP53-loss phenocopying events in human tumors
Fito-Lopez, B., Salvadores, M., Alvarez, M.-M., & Supek, F. (2024) · Figshare · doi:10.6084/m9.figshare.26584569
Grzadkowski, M. R., Holly, H. D., Somers, J., & Demir, E. (2021) · Figshare · doi:10.6084/m9.figshare.14551616
Additional file 4 of Prevalence, causes and impact of TP53-loss phenocopying events in human tumors
Fito-Lopez, B., Salvadores, M., Alvarez, M.-M., & Supek, F. (2024) · Figshare · doi:10.6084/m9.figshare.26584575
Additional file 3 of Prevalence, causes and impact of TP53-loss phenocopying events in human tumors
Fito-Lopez, B., Salvadores, M., Alvarez, M.-M., & Supek, F. (2024) · Figshare · doi:10.6084/m9.figshare.26584572
Additional file 1 of Prevalence, causes and impact of TP53-loss phenocopying events in human tumors
Fito-Lopez, B., Salvadores, M., Alvarez, M.-M., & Supek, F. (2024) · Figshare · doi:10.6084/m9.figshare.26584566
- Authors
- Kawase, T., Ichikawa, H., Ohta, T., Nozaki, N., Tashiro, F., Ohki, R., & Taya, Y.
- Affiliations
- National Cancer Center Research Institute (JP)
- Kanagawa Dental University (JP)
- Tokyo University of Science (JP)
- Japan Science and Technology Agency (JP)
- Corresponding author
- Ohki, R
- Taya, Y
- Venue
- Oncogene
- Published
- 2008-02-11
- Volume
- 27
- Issue
- 27
- Pages
- 3797-3810
- ISSN
- 0950-9232 (ISSN-L)
- 1476-5594
- OpenAlex
- W1998743183
- Cited by
- 105
- References
- 41
- Citations by year
- 2026: 7 · 2025: 4 · 2024: 11 · 2023: 13 · 2022: 9 · 2021: 12 · 2020: 5 · 2019: 4 · 2018: 5 · 2017: 2 · 2016: 3 · 2015: 5 · 2014: 6 · 2013: 4 · 2012: 3
- FWCI
- 2.11
- Type
- journal article
- Language
- en
- Open access
- closed
- Locations
- Oncogene (publishedVersion)
- PubMed (publishedVersion)
- Topics
- Health Sciences › Medicine › Oncology › Cancer-related Molecular Pathways
- Life Sciences › Biochemistry, Genetics and Molecular Biology › Molecular Biology › Cell death mechanisms and regulation
- Life Sciences › Biochemistry, Genetics and Molecular Biology › Molecular Biology › DNA Repair Mechanisms
- Keywords
- AEN, p53 target genes, p53-dependent apoptosis, exonuclease activity, DNA fragmentation, p53 phosphorylation, nucleolus, nucleophosmin, DNA damage response, nucleic acid degradation
- MeSH terms
- DNA Damage, Exodeoxyribonucleases, Exonucleases, Humans, Kinetics, Mutation, Neoplasms, Phosphorylation, Gene Expression Regulation, Enzymologic, Genes, p53, Tumor Suppressor Protein p53, Apoptosis, DNA Fragmentation
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