Regulation of the human AP-endonuclease (APE1/Ref-1) expression by the tumor suppressor p53 in response to DNA damage

Zaky, A.; Busso, C.; Izumi, T.; Chattopadhyay, R.; Bassiouny, A.; Mitra, S.; Bhakat, K. K.

doi:10.1093/nar/gkm1173

Cited by 111Cancer-related Molecular PathwaysDNA Repair MechanismsCell death mechanisms and regulation

Regulation of the human AP-endonuclease (APE1/Ref-1) expression by the tumor suppressor p53 in response to DNA damage

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Zaky, A., Busso, C., Izumi, T., Chattopadhyay, R., Bassiouny, A., Mitra, S., Bhakat, K. K.·2008·Nucleic Acids Research

DOI 10.1093/nar/gkm1173PMC PMC2275136

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Abstract

The human AP-endonuclease (APE1/Ref-1), an essential multifunctional protein, plays a central role in the repair of oxidative base damage via the DNA base excision repair (BER) pathway. The mammalian AP-endonuclease (APE1) overexpression is often observed in tumor cells, and confers resistance to various anticancer drugs; its downregulation sensitizes tumor cells to those agents via induction of apoptosis. Here we show that wild type (WT) but not mutant p53 negatively regulates APE1 expression. Time-dependent decrease was observed in APE1 mRNA and protein levels in the human colorectal cancer line HCT116 p53(+/+), but not in the isogenic p53 null mutant after treatment with camptothecin, a DNA topoisomerase I inhibitor. Furthermore, ectopic expression of WTp53 in the p53 null cells significantly reduced both endogenous APE1 and APE1 promoter-dependent luciferase expression in a dose-dependent fashion. Chromatin immunoprecipitation assays revealed that endogenous p53 is bound to the APE1 promoter region that includes a Sp1 site. We show here that WTp53 interferes with Sp1 binding to the APE1 promoter, which provides a mechanism for the downregulation of APE1. Taken together, our results demonstrate that WTp53 is a negative regulator of APE1 expression, so that repression of APE1 by p53 could provide an additional pathway for p53-dependent induction of apoptosis in response to DNA damage.

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After DNA damage, p53 can negatively regulate APE1 and MGMT by sequestering the Sp1 transcription factor needed for promoter activation.
“Following DNA damage, p53 can act as a negative regulator of APE150 and MGMT5 by sequestering the Sp1 transcription factor required for promoter activation.”
From Combination therapy in a xenograft model of glioblastoma: Enhancement of the antitumor activity of temozolomide by an MDM2 antagonist (2017) · cites this paper as [50]

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Down-regulation of Apurinic/Apyrimidinic Endonuclease 1/Redox Factor-1 Expression by Soy Isoflavones Enhances Prostate Cancer Radiotherapy In vitro and In vivo
Raffoul, J. J., Banerjee, S., Singh‐Gupta, V., et al. (2007) · Cancer Research · doi:10.1158/0008-5472.can-06-2147 · Cited by 106 · see citing works
Retracted
WAF1, a potential mediator of p53 tumor suppression
El-Deiry, W. S., Tokino, T., Velculescu, V. E., Levy, D. B., Parsons, R., Trent, J. M., Lin, D., Mercer, W. E., Kinzler, K. W., & Vogelstein, B. (1993) · Cell · doi:10.1016/0092-8674(93)90500-p · Cited by 8,321 · see citing works
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
Tumor suppressor p53 is a direct transcriptional activator of the human bax gene
Toshiyuki, M., & Reed, J. C. (1995) · Cell · doi:10.1016/0092-8674(95)90412-3 · Cited by 4,063 · see citing works
p53: puzzle and paradigm.Preprint
Ko, L. J., & Prives, C. L. (1996) · Genes & Development · doi:10.1101/gad.10.9.1054 · Cited by 2,338 · see citing works
PUMA, a Novel Proapoptotic Gene, Is Induced by p53
Nakano, K., & Vousden, K. H. (2001) · Molecular Cell · doi:10.1016/s1097-2765(01)00214-3 · Cited by 2,315 · see citing works
Potent and specific inhibition of mammalian histone deacetylase both in vivo and in vitro by trichostatin A.
Yoshida, M., Kijima, M., Akita, M., & Beppu, T. (1990) · Journal of Biological Chemistry · doi:10.1016/s0021-9258(17)44885-x · Cited by 1,856 · see citing works
REPAIR OF OXIDATIVE DAMAGE TO DNA: Enzymology and Biology
Demple, B., & Harrison, L. (1994) · Annual Review of Biochemistry · doi:10.1146/annurev.bi.63.070194.004411 · Cited by 1,495 · see citing works
PUMA Induces the Rapid Apoptosis of Colorectal Cancer Cells
Yu, J., Zhang, L., Hwang, P. M., Kinzler, K. W., & Vogelstein, B. (2001) · Molecular Cell · doi:10.1016/s1097-2765(01)00213-1 · Cited by 1,282 · see citing works
A Chemical Inhibitor of p53 That Protects Mice from the Side Effects of Cancer Therapy
Komarov, P. G., Komarova, E. A., Kondratov, R. V., Christov-Tselkov, K., Coon, J. S., Chernov, M. V., & Gudkov, A. V. (1999) · Science · doi:10.1126/science.285.5434.1733 · Cited by 1,270 · see citing works
Is a p53-Regulated Inhibitor of G2/M Progression
Hermeking, H., Lengauer, C., Polyak, K., He, T.-C., Zhang, L., Thiagalingam, S., Kinzler, K. W., & Vogelstein, B. (1997) · Molecular Cell · doi:10.1016/s1097-2765(00)80002-7 · Cited by 1,251 · see citing works
Identification and characterization of Ref‐1, a nuclear protein that facilitates AP‐1 DNA‐binding activity.
Xanthoudakis, S., & Curran, T. (1992) · The EMBO Journal · doi:10.1002/j.1460-2075.1992.tb05097.x · Cited by 708 · see citing works
Several hydrophobic amino acids in the p53 amino-terminal domain are required for transcriptional activation, binding to mdm-2 and the adenovirus 5 E1B 55-kD protein.Preprint
Lin, J., Chen, J., Elenbaas, B., & Levine, A. J. (1994) · Genes & Development · doi:10.1101/gad.8.10.1235 · Cited by 652 · see citing works
Going APE over ref-1
Evans, A. R., Limp-Foster, M., & Kelley, M. R. (2000) · Mutation Research/DNA Repair · doi:10.1016/s0921-8777(00)00046-x · Cited by 532 · see citing works
Human survivin is negatively regulated by wild-type p53 and participates in p53-dependent apoptotic pathway
Mirza, A., McGuirk, M., Hockenberry, T., Wu, Q. J., Ashar, H. R., Black, S., Wen, S. F., Wang, L., Kirschmeier, P. T., Bishop, W. R., et al. (2002) · Oncogene · doi:10.1038/sj.onc.1205353 · Cited by 530 · see citing works
Identification of redox/repair protein Ref-1 as a potent activator of p53.Preprint
Jayaraman, L., Murthy, K. G. K., Zhu, C., Curran, T., Xanthoudakis, S., & Prives, C. L. (1997) · Genes & Development · doi:10.1101/gad.11.5.558 · Cited by 479 · see citing works
Activation of apurinic/apyrimidinic endonuclease in human cells by reactive oxygen species and its correlation with their adaptive response to genotoxicity of free radicals
Ramana, C. V., Boldogh, I. R., Izumi, T., & MITRA, S. P. (1998) · Proceedings of the National Academy of Sciences · doi:10.1073/pnas.95.9.5061 · Cited by 409 · see citing works
Self-citation
The Intracellular Localization of APE1/Ref-1: More than a Passive Phenomenon?
Tell, G., Damante, G., Caldwell, D. B., & Kelley, M. R. (2005) · Antioxidants and Redox Signaling · doi:10.1089/ars.2005.7.367 · Cited by 376 · see citing works
A role for p53 in base excision repair
Zhou, J., Ahn, J., Wilson, S. H., & Prives, C. (2001) · The EMBO Journal · doi:10.1093/emboj/20.4.914 · Cited by 333 · see citing works
The p53 functional circuit
Jin, S. V., & Levine, A. J. (2001) · Journal of Cell Science · doi:10.1242/jcs.114.23.4139 · Cited by 310 · see citing works
A Vital Role for Ape1/Ref1 Protein in Repairing Spontaneous DNA Damage in Human Cells
Fung, H., & Demple, B. (2005) · Molecular Cell · doi:10.1016/j.molcel.2004.12.029 · Cited by 284 · see citing works
Cooperative effects of genes controlling the G2/M checkpointPreprint
Chan, T. A.-T., Hwang, P. M., Hermeking, H., Kinzler, K. W., & Vogelstein, B. (2000) · Genes & Development · doi:10.1101/gad.14.13.1584 · Cited by 262 · see citing works
Human apurinic endonuclease 1 (APE1) expression and prognostic significance in osteosarcoma: Enhanced sensitivity of osteosarcoma to DNA damaging agents using silencing RNA APE1 expression inhibition
Wang, D., Luo, M., & Kelley, M. R. (2004) · Molecular Cancer Therapeutics · doi:10.1158/1535-7163.679.3.6 · Cited by 240 · see citing works
Wild-type p53 suppresses angiogenesis in human leiomyosarcoma and synovial sarcoma by transcriptional suppression of vascular endothelial growth factor expression.
Zhang, L., Yu, D., Hu, M., Xiong, S., Lang, A., Ellis, L. M., & Pollock, R. E. (2000) · PubMed · Cited by 230 · see citing works
Adenoviral expression of p53 represses telomerase activity through down-regulation of human telomerase reverse transcriptase transcription.
Kanaya, T., Kyo, S., Hamada, K., Takakura, M., Kitagawa, Y., Harada, H., & Inoue, M. (2000) · PubMed · Cited by 222 · see citing works
Wild-type p53 negatively regulates the expression of a microtubule-associated protein.Preprint
Murphy, M. E., Hinman, A. M., & Levine, A. J. (1996) · Genes & Development · doi:10.1101/gad.10.23.2971 · Cited by 221 · see citing works
Two essential but distinct functions of the mammalian abasic endonuclease
Izumi, T., Brown, D. B., Naidu, C. V., Bhakat, K. K., MacInnes, M. A., Saitō, H., Chen, D. J., & MITRA, S. P. (2005) · Proceedings of the National Academy of Sciences · doi:10.1073/pnas.0500986102 · Cited by 221 · see citing works
Self-citation
Transcriptional repression mediated by the p53 tumour suppressor
Ho, J., & Benchimol, S. (2003) · Cell Death and Differentiation · doi:10.1038/sj.cdd.4401191 · Cited by 200 · see citing works
Altered expression of Ape1/ref-1 in germ cell tumors and overexpression in NT2 cells confers resistance to bleomycin and radiation.
Robertson, K. A., Bullock, H. A., Xu, Y., Tritt, R., Zimmerman, E., Ulbright, T. M., Foster, R. S., Einhorn, L. H., & Kelley, M. R. (2001) · PubMed · Cited by 194 · see citing works
Elevated and altered expression of the multifunctional DNA base excision repair and redox enzyme Ape1/ref-1 in prostate cancer.
Kelley, M. R., Cheng, L., Foster, R. S., Tritt, R., Jiang, J., Broshears, J. R., & Koch, M. O. (2001) · PubMed · Cited by 193 · see citing works
p53-Mediated Repression of Alpha-Fetoprotein Gene Expression by Specific DNA Binding
Lee, K. C., Crowe, A. J., & Barton, M. (1999) · Molecular and Cellular Biology · doi:10.1128/mcb.19.2.1279 · Cited by 176 · see citing works
Acetylation of Human 8-Oxoguanine-DNA Glycosylase by p300 and Its Role in 8-Oxoguanine Repair In Vivo
Bhakat, K. K., Mokkapati, S. K., Boldogh, I. R., Hazra, T. K., & MITRA, S. P. (2006) · Molecular and Cellular Biology · doi:10.1128/mcb.26.5.1654-1665.2006 · Cited by 176 · see citing works
Self-citation
Role of acetylated human AP‐endonuclease (APE1/Ref‐1) in regulation of the parathyroid hormone gene
Bhakat, K. K., Izumi, T., Yang, S., Hazra, T. K., & MITRA, S. P. (2003) · The EMBO Journal · doi:10.1093/emboj/cdg595 · Cited by 171 · see citing works
Self-citation
Repression of the insulin receptor promoter by the tumor suppressor gene product p53: a possible mechanism for receptor overexpression in breast cancer.
Webster, N. J. G., Resnik, J. L., Reichart, D. B., Strauss, B. E., Haas, M., & Seely, B. L. (1996) · PubMed · Cited by 150 · see citing works
Induction of Sp1-p53 DNA-binding heterocomplexes during granulocyte/macrophage colony-stimulating factor-dependent proliferation in human erythroleukemia cell line TF-1.
Borellini, F., & Glazer, R. I. (1993) · Journal of Biological Chemistry · doi:10.1016/s0021-9258(18)53046-5 · Cited by 147 · see citing works
Choreography of oxidative damage repair in mammalian genomes1,2 1Guest Editor: Miral Dizdaroglu 2This article is part of a series of reviews on “Oxidative DNA Damage and Repair.” The full list of papers may be found on the homepage of the journal.
MITRA, S. P., Izumi, T., Boldogh, I. R., Bhakat, K. K., Hill, J. W., & Hazra, T. K. (2002) · Free Radical Biology and Medicine · doi:10.1016/s0891-5849(02)00819-5 · Cited by 146 · see citing works
Self-citation
The Insulin-Like Growth Factor I Receptor as a Physiologically Relevant Target of p53 in Apoptosis Caused by Interleukin-3 Withdrawal
di Prisco, M., Hongo, A., Rizzo, M. G., et al. (1997) · Molecular and Cellular Biology · doi:10.1128/mcb.17.3.1084 · Cited by 142 · see citing works
p53 is involved in regulation of the DNA repair gene O6-methylguanine-DNA methyltransferase (MGMT) by DNA damaging agents
Grombacher, T., Eichhorn, U., & Kaina, B. (1998) · Oncogene · doi:10.1038/sj.onc.1202000 · Cited by 141 · see citing works
Apurinic endonuclease (Ref-1) is induced in mammalian cells by oxidative stress and involved in clastogenic adaptation.
Grösch, S., Fritz, G., & Kaina, B. (1998) · PubMed · Cited by 137 · see citing works
A redox factor protein, ref1, is involved in negative gene regulation by extracellular calcium.
Okazaki, T., Chung, U., Nishishita, T., Ebisu, S., Usuda, S., Mishiro, S., Xanthoudakis, S., Igarashi, T., & Ogata, E. (1994) · Journal of Biological Chemistry · doi:10.1016/s0021-9258(18)46865-2 · Cited by 134 · see citing works
Alterations in the expression of the DNA repair/redox enzyme APE/ref-1 in epithelial ovarian cancers.
Moore, D. H., Michael, H. T., Tritt, R., et al. (2000) · PubMed · Cited by 131 · see citing works
Tumor-suppressor p53 and the cell cycle
Perry, M. E., & Levine, A. J. (1993) · Current Opinion in Genetics & Development · doi:10.1016/s0959-437x(05)80340-5 · Cited by 118 · see citing works
Nuclear expression of human apurinic/apyrimidinic endonuclease (HAP1/Ref-1) in head-and-neck cancer is associated with resistance to chemoradiotherapy and poor outcome
Koukourakis, M. I., Giatromanolaki, A. N., Kakolyris, S., Sivridis, E., Georgoulias, V., Funtzilas, G., Hickson, I. D., Gatter, K. C., & Harris, A. L. (2001) · International Journal of Radiation Oncology*Biology*Physics · doi:10.1016/s0360-3016(00)01561-3 · Cited by 113 · see citing works
Pifithrin-α Inhibits p53 Signaling after Interaction of the Tumor Suppressor Protein with hsp90 and Its Nuclear Translocation
Murphy, P. J. M., Galigniana, M. D., Morishima, Y., Harrell, J. M., Kwok, R. P. S., Ljungman, M. E., & Pratt, W. B. (2004) · Journal of Biological Chemistry · doi:10.1074/jbc.m403539200 · Cited by 108 · see citing works
Levels of the DNA repair enzyme human apurinic/apyrimidinic endonuclease (APE1, APEX, Ref-1) are associated with the intrinsic radiosensitivity of cervical cancers
Herring, C. J., West, C., Wilks, D., et al. (1998) · British Journal of Cancer · doi:10.1038/bjc.1998.641 · Cited by 97 · see citing works
Intracellular trafficking and regulation of mammalian AP-endonuclease 1 (APE1), an essential DNA repair protein
MITRA, S., Izumi, T., Boldogh, I., Bhakat, K. K., Chattopadhyay, R., & Szczęsny, B. (2006) · DNA repair · doi:10.1016/j.dnarep.2006.10.010 · Cited by 96 · see citing works
Self-citation
Wild-type p53 suppresses transcription of the human O6-methylguanine-DNA methyltransferase gene.
Harris, L. C., Remack, J. S., Houghton, P. J., & Brent, T. P. (1996) · PubMed · Cited by 95 · see citing works
The apurinic/apyrimidinic endonuclease (APE/ref-1) DNA repair enzyme is elevated in premalignant and malignant cervical cancer.
Xu, Y., Moore, D. H., Broshears, J. R., Liu, L., Wilson, T., & Kelley, M. R. (1997) · PubMed · Cited by 93 · see citing works
Enforced expression of wild-type p53 curtails the transcription of the O(6)-methylguanine-DNA methyltransferase gene in human tumor cells and enhances their sensitivity to alkylating agents.
Srivenugopal, K. S., Shou, J., Mullapudi, S., Lang, F. F., Rao, J. S., & Ali‐Osman, F. (2001) · PubMed · Cited by 88 · see citing works
Loss of Ref-1 protein expression precedes DNA fragmentation in apoptotic neurons
Walton, M. R., Lawlor, P. A., Sirimanne, E. S., et al. (1997) · Molecular Brain Research · doi:10.1016/s0169-328x(96)00291-4 · Cited by 87 · see citing works
Prognostic significance of Ape1/ref-1 subcellular localization in non-small cell lung carcinomas.
Puglisi, F., Aprile, G., Minisini, A. M., Barbone, F., Cataldi, P., Tell, G., Kelley, M. R., Damante, G., Beltrami, C. A., & Loreto, C. D. (2001) · PubMed · Cited by 85 · see citing works
Expression and subcellular localization of human AP endonuclease 1 (HAP1/Ref‐1) protein: a basis for its role in human disease
Kakolyris, Kaklamanis, Giatromanolaki, Koukourakis, Hickson, I. D., Barzilay, Turley, Leek, R., Kanavaros, Georgoulias, et al. (1998) · Histopathology · doi:10.1046/j.1365-2559.1998.00541.x · Cited by 83 · see citing works
Negative Regulation of the Major Human AP-Endonuclease, a Multifunctional Protein,
Izumi, T., Henner, W. D., & MITRA, S. P. (1996) · Biochemistry · doi:10.1021/bi961995u · Cited by 73 · see citing works
Self-citation
Ref‐1/Ape is critical for formation of the hypoxia‐inducible transcriptional complex on the hypoxic response element of the rat pulmonary artery endothelial cell VEGF gene
Ziel, K. A., Campbell, C. C., Wilson, G. L., & Gillespie, M. N. (2004) · The FASEB Journal · doi:10.1096/fj.03-1160fje · Cited by 70 · see citing works
Down-regulation of apurinic/apyrimidinic endonuclease expression is associated with the induction of apoptosis in differentiating myeloid leukemia cells.
Robertson, K. A., Hill, D. P., Xu, Y., Liu, L., Van Epps, S., Hockenbery, D. M., Park, Wilson, T., & Kelley, M. R. (1997) · PubMed · Cited by 68 · see citing works
Transcriptional Regulation of the Human DNA Polymerase δ Catalytic Subunit Gene POLD1 by p53 Tumor Suppressor and Sp1
Li, B., & Lee, M. Y. W. (2001) · Journal of Biological Chemistry · doi:10.1074/jbc.m101167200 · Cited by 65 · see citing works
TSH controls Ref-1 nuclear translocation in thyroid cells
Tell, G., Pellizzari, L., Pucillo, C. E. M., Puglisi, F., Cesselli, D., Kelley, M. R., Loreto, C. D., & Damante, G. (2000) · Journal of Molecular Endocrinology · doi:10.1677/jme.0.0240383 · Cited by 61 · see citing works
Hypersensitivity phenotypes associated with genetic and synthetic inhibitor-induced base excision repair deficiency
HORTON, J., & Wilson, S. H. (2006) · DNA repair · doi:10.1016/j.dnarep.2006.10.016 · Cited by 61 · see citing works
Implication of Ref-1 in the repression of renin gene transcription by intracellular calcium
Fuchs, S., Philippe, J., Corvol, P. L., & Pinet, F. (2003) · Journal of Hypertension · doi:10.1097/00004872-200302000-00024 · Cited by 60 · see citing works
p53 in cancer: A paradigm for modern management of cancer
Steele, R. J., & Lane, D. P. (2005) · The Surgeon · doi:10.1016/s1479-666x(05)80041-1 · Cited by 59 · see citing works
Divergent Regulation of the Growth-promoting GeneIEX-1 by the p53 Tumor Suppressor and Sp1
Im, H., Pittelkow, M. R., & Kumar, R. (2002) · Journal of Biological Chemistry · doi:10.1074/jbc.m109414200 · Cited by 58 · see citing works
Studies of apurinic/apyrimidinic endonuclease/ref-1 expression in epithelial ovarian cancer: correlations with tumor progression and platinum resistance.
Freitas, S., Moore, D. H., Michael, H., & Kelley, M. R. (2003) · PubMed · Cited by 46 · see citing works
Key Role of a Downstream Specificity Protein 1 Site in Cell Cycle-regulated Transcription of the AP Endonuclease Gene APE1/APEX in NIH3T3 Cells
Fung, H., Bennett, R. A. O., & Demple, B. (2001) · Journal of Biological Chemistry · doi:10.1074/jbc.m106423200 · Cited by 44 · see citing works
Characterization of the Promoter Region of the Human Apurinic Endonuclease Gene (APE)
Harrison, L., Ascione, A. G., Wilson, D. M., et al. (1995) · Journal of Biological Chemistry · doi:10.1074/jbc.270.10.5556 · Cited by 34 · see citing works
Pifithrin-α, an inhibitor of p53 transactivation, alters the inflammatory process and delays tendon healing following acute injury
Marsolais, D., Côt́e, C. H., & Frenette, J. (2006) · American Journal of Physiology-Regulatory, Integrative and Comparative Physiology · doi:10.1152/ajpregu.00411.2005 · Cited by 15 · see citing works

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Authors: Zaky, A., Busso, C., Izumi, T., Chattopadhyay, R., Bassiouny, A., Mitra, S., & Bhakat, K. K.
Affiliations: The University of Texas Medical Branch at Galveston (US)
Louisiana State University (US)
Corresponding author: Bhakat, K. K.
ORCID: Zaky, A.
Izumi, T.
Bassiouny, A.
Mitra, S.
Bhakat, K. K.
Venue: Nucleic Acids Research
Publisher: Oxford University Press (OUP)
Published: 2008-01-10
Volume: 36
Issue: 5
Pages: 1555-1566
ISSN: 0305-1048 (ISSN-L)
1362-4962
DOI: 10.1093/nar/gkm1173
PMC: PMC2275136
OpenAlex: W2106130941
Cited by: 111
References: 65
Citations by year: 2026: 1 · 2025: 8 · 2024: 3 · 2023: 1 · 2022: 1 · 2021: 4 · 2020: 7 · 2019: 4 · 2018: 4 · 2017: 6 · 2016: 10 · 2015: 4 · 2014: 5 · 2013: 14 · 2012: 5
FWCI: 5.99
Type: journal article
Language: en
Open access: gold
doi.org
Licence: cc-by-nc
Locations: Nucleic Acids Research (publishedVersion, cc-by-nc)
PubMed Central (publishedVersion, cc-by-nc)
PubMed (publishedVersion)
Funders: American Heart Association
University of Oxford
National Institutes of Health
National Cancer Institute (CA98664, R01 CA53791, R56CA098664, R01CA053791, R01CA098664)
National Institute of Environmental Health Sciences (R01 ES 08457, R01ES008457)
Topics: Health Sciences › Medicine › Oncology › Cancer-related Molecular Pathways
Life Sciences › Biochemistry, Genetics and Molecular Biology › Molecular Biology › DNA Repair Mechanisms
Life Sciences › Biochemistry, Genetics and Molecular Biology › Molecular Biology › Cell death mechanisms and regulation
Keywords: APE1/Ref-1, p53, transcriptional regulation, Sp1, DNA base excision repair, oxidative DNA damage, DNA damage response, apoptosis, camptothecin, colorectal cancer, chemoresistance
MeSH terms: DNA Damage, Humans, Mutation, Promoter Regions, Genetic, RNA, Messenger, Down-Regulation, Gene Expression Regulation, Enzymologic, Tumor Suppressor Protein p53, Sp1 Transcription Factor, Response Elements, DNA-(Apurinic or Apyrimidinic Site) Lyase, Cell Line, Tumor

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Regulation of the human AP-endonuclease (APE1/Ref-1) expression by the tumor suppressor p53 in response to DNA damage

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