cAMP response element-binding (CREB) protein is a cellular transcription factor that mediates responses to different physiological and pathological signals. Using a model of human neuronal cells we demonstrate herein, that CREB is phosphorylated after oxidative stress induced by hydrogen peroxide. This phosphorylation is largely independent of PKA and of the canonical phosphoacceptor site at ser-133, and is accompanied by an upregulation of CREB expression at both mRNA and protein levels. In accordance with previous data, we show that CREB upregulation promotes cell survival and that its silencing results in an increment of apoptosis after oxidative stress. Interestingly, we also found that CREB promotes DNA repair after treatment with hydrogen peroxide. Using a cDNA microarray we found that CREB is responsible for the regulation of many genes involved in DNA repair and cell survival after oxidative injury. In summary, the neuroprotective effect mediated by CREB appears to follow three essential steps following oxidative injury. First, the upregulation of CREB expression that allows sufficient level of activated and phosphorylated protein is the primordial event that promotes the induction of genes of the DNA Damage Response. Then and when the DNA repair is effective, CREB induces detoxification and survival genes. This kinetics seems to be important to completely resolve oxidative-induced neuronal damages. © 2016, Springer Science+Business Media New York.
|Título:||Oxidative stress-induced CREB upregulation promotes DNA damage repair prior to neuronal cell death protection|
|Autor:||Pregi, N.; Belluscio, L.M.; Berardino, B.G.; Castillo, D.S.; Cánepa, E.T.|
|Filiación:||Laboratorio de Neuroepigenética, Departamento de Química Biológica, Facultad de Ciencias Exactas y Naturales, Universidad de Buenos Aires, IQuiBiCEN–CONICET (Consejo Nacional de Investigaciones Científicas y Técnicas), Ciudad Universitaria Pabellón II Piso 4, Buenos Aires, C1428EHA, Argentina|
|Palabras clave:||Apoptosis; CREB transcription factor; DNA damage response; Genotoxic stress; Neuronal cells; Phosphorylation; caspase 3; cyclic AMP responsive element binding protein; hydrogen peroxide; CREB1 protein, human; cyclic AMP dependent protein kinase; cyclic AMP responsive element binding protein; apoptosis; Article; cell cycle; cell death; cell survival; controlled study; DNA content; DNA damage; DNA damage response; DNA repair; flow cytometry; fluorescence microscopy; human; human cell; nerve cell; nerve cell differentiation; neuroblastoma cell; neuroprotection; oxidative stress; protein phosphorylation; regulatory mechanism; reporter gene; upregulation; cell death; DNA damage; genetics; metabolism; nerve cell; phosphorylation; tumor cell line; upregulation; Cell Death; Cell Line, Tumor; Cyclic AMP Response Element-Binding Protein; Cyclic AMP-Dependent Protein Kinases; DNA Damage; DNA Repair; Humans; Neurons; Oxidative Stress; Phosphorylation; Up-Regulation|
|Página de inicio:||9|
|Página de fin:||24|
|Título revista:||Molecular and Cellular Biochemistry|
|Título revista abreviado:||Mol. Cell. Biochem.|
|CAS:||caspase 3, 169592-56-7; cyclic AMP responsive element binding protein, 130428-87-4, 130939-96-7; hydrogen peroxide, 7722-84-1; cyclic AMP dependent protein kinase; CREB1 protein, human; Cyclic AMP Response Element-Binding Protein; Cyclic AMP-Dependent Protein Kinases|
- Hachem, L.D., Mothe, A.J., Tator, C.H., Effect of BDNF and other potential survival factors in models of in vitro oxidative stress on adult spinal cord-derived neural stem/progenitor cells (2015) Biores Open Access, 4 (1), pp. 146-159. , COI: 1:CAS:528:DC%2BC28Xntlait78%3D, PID: 26309791
- Kulkarni, A., McNeill, D.R., Gleichmann, M., XRCC1 protects against the lethality of induced oxidative DNA damage in nondividing neural cells (2008) Nucleic Acids Res, 36, pp. 5111-5121. , COI: 1:CAS:528:DC%2BD1cXhtVGkt7zO, PID: 18682529
- Belaidi, A.A., Bush, A.I., Iron neurochemistry in Alzheimer’s disease and Parkinson’s disease: targets for therapeutics (2015) J Neurochem
- Cleary, J.P., Walsh, D.M., Hofmeister, J.J., Natural oligomers of the amyloid-beta protein specifically disrupt cognitive function (2005) Nat Neurosci, 8, pp. 79-84. , COI: 1:CAS:528:DC%2BD2MXhtFWmsw%3D%3D, PID: 15608634
- Leon, J., Sakumi, K., Castillo, E., 8-Oxoguanine accumulation in mitochondrial DNA causes mitochondrial dysfunction and impairs neuritogenesis in cultured adult mouse cortical neurons under oxidative conditions (2016) Sci Rep, 6, p. 22086. , COI: 1:CAS:528:DC%2BC28Xjt1ertL0%3D, PID: 26912170
- Migliore, L., Coppedè, F., Environmental-induced oxidative stress in neurodegenerative disorders and aging (2009) Mutat Res, 674, pp. 73-84. , COI: 1:CAS:528:DC%2BD1MXjtF2htb4%3D, PID: 18952194
- Pregi, N., Vittori, D., Pérez, G., Effect of erythropoietin on staurosporine-induced apoptosis and differentiation of SH-SY5Y neuroblastoma cells (2006) Biochim Biophys Acta, 1763, pp. 238-246. , COI: 1:CAS:528:DC%2BD28XisF2js74%3D, PID: 16500719
- Bartek, J., Lukas, J., DNA damage checkpoints: from initiation to recovery or adaptation (2007) Curr Opin Cell Biol, 19, pp. 238-245. , COI: 1:CAS:528:DC%2BD2sXjt1Sksrg%3D, PID: 17303408
- Yang, S.-P., Bae, D.-G., Kang, H.J., Co-accumulation of vascular endothelial growth factor with beta-amyloid in the brain of patients with Alzheimer’s disease (2004) Neurobiol Aging, 25, pp. 283-290. , PID: 15123332
- Dell’Orco, M., Milani, P., Arrigoni, L., Hydrogen peroxide-mediated induction of SOD1 gene transcription is independent from Nrf2 in a cellular model of neurodegeneration (2016) Biochim Biophys Acta, 1859, pp. 315-323. , PID: 26619801
- Jackson, S.P., The DNA-damage response: new molecular insights and new approaches to cancer therapy (2009) Biochem Soc Trans, 37, pp. 483-494. , COI: 1:CAS:528:DC%2BD1MXmtFSgur4%3D, PID: 19442242
- Sedelnikova, O.A., Redon, C.E., Dickey, J.S., Role of oxidatively induced DNA lesions in human pathogenesis (2010) Mutat Res, 704, pp. 152-159. , COI: 1:CAS:528:DC%2BC3cXmtFamu7o%3D, PID: 20060490
- Lu, W., Ogasawara, M.A., Huang, P., Models of reactive oxygen species in cancer (2007) Drug Discov Today Dis Models, 4, pp. 67-73. , PID: 18591999
- Lala, P.K., Chakraborty, C., Role of nitric oxide in carcinogenesis and tumour progression (2001) Lancet Oncol, 2, pp. 149-156. , COI: 1:CAS:528:DC%2BD3MXmsVymtbc%3D, PID: 11902565
- Hussain, S., Witt, E., Huber, P.A.J., Direct interaction of the Fanconi anaemia protein FANCG with BRCA2/FANCD1 (2003) Hum Mol Genet, 12, pp. 2503-2510. , COI: 1:CAS:528:DC%2BD3sXnsVekt7Y%3D, PID: 12915460
- Tartier, L., Gilchrist, S., Burdak-Rothkamm, S., Cytoplasmic irradiation induces mitochondrial-dependent 53BP1 protein relocalization in irradiated and bystander cells (2007) Cancer Res, 67, pp. 5872-5879. , COI: 1:CAS:528:DC%2BD2sXmsFCqtrk%3D, PID: 17575156
- Kurfurstova, D., Bartkova, J., Vrtel, R., DNA damage signalling barrier, oxidative stress and treatment-relevant DNA repair factor alterations during progression of human prostate cancer (2016) Mol Oncol, , PID: 26987799
- Simoneau, A., Ricard, É., Weber, S., Chromosome-wide histone deacetylation by sirtuins prevents hyperactivation of DNA damage-induced signaling upon replicative stress (2016) Nucleic Acids Res, , PID: 26748095
- Bellacosa, A., Drohat, A.C., Role of base excision repair in maintaining the genetic and epigenetic integrity of CpG sites (2015) DNA Rep (Amst), 32, pp. 33-42. , COI: 1:CAS:528:DC%2BC2MXnvFSisrg%3D
- Chou, W.-C., Hu, L.-Y., Hsiung, C.-N., Shen, C.-Y., Initiation of the ATM-Chk2 DNA damage response through the base excision repair pathway (2015) Carcinogenesis, 36, pp. 832-840. , COI: 1:CAS:528:DC%2BC28Xht1CisL7M, PID: 26025911
- Maynard, S., Schurman, S.H., Harboe, C., Base excision repair of oxidative DNA damage and association with cancer and aging (2009) Carcinogenesis, 30, pp. 2-10. , COI: 1:CAS:528:DC%2BD1MXhtVaqu74%3D, PID: 18978338
- Lonze, B.E., Ginty, D.D., Function and regulation of CREB family transcription factors in the nervous system (2002) Neuron, 35, pp. 605-623. , COI: 1:CAS:528:DC%2BD38XmslSlsLY%3D, PID: 12194863
- Sakamoto, K., Karelina, K., Obrietan, K., CREB: a multifaceted regulator of neuronal plasticity and protection (2011) J Neurochem, 116, pp. 1-9. , COI: 1:CAS:528:DC%2BC3MXis1Whuw%3D%3D, PID: 21044077
- Gonzalez, G.A., Montminy, M.R., Cyclic AMP stimulates somatostatin gene transcription by phosphorylation of CREB at serine 133 (1989) Cell, 59, pp. 675-680. , COI: 1:CAS:528:DyaK3cXkvFOkuw%3D%3D, PID: 2573431
- Gonzalez, G.A., Yamamoto, K.K., Fischer, W.H., A cluster of phosphorylation sites on the cyclic AMP-regulated nuclear factor CREB predicted by its sequence (1989) Nature, 337, pp. 749-752. , COI: 1:CAS:528:DyaL1MXmt1Onsrk%3D, PID: 2521922
- Shi, Y., Venkataraman, S.L., Dodson, G.E., Direct regulation of CREB transcriptional activity by ATM in response to genotoxic stress (2004) Proc Natl Acad Sci USA, 101, pp. 5898-5903. , COI: 1:CAS:528:DC%2BD2cXjsFKns7w%3D, PID: 15073328
- Sakamoto, K., Huang, B.-W., Iwasaki, K., Regulation of genotoxic stress response by homeodomain-interacting protein kinase 2 through phosphorylation of cyclic AMP response element-binding protein at serine 271 (2010) Mol Biol Cell, 21, pp. 2966-2974. , COI: 1:CAS:528:DC%2BC3cXhtlGlt7nE, PID: 20573984
- Trinh, A.T., Kim, S.H., Chang, H., Cyclin-dependent kinase 1-dependent phosphorylation of cAMP response element-binding protein decreases chromatin occupancy (2013) J Biol Chem, 288, pp. 23765-23775. , COI: 1:CAS:528:DC%2BC3sXht1yiu7%2FI, PID: 23814058
- St-Pierre, J., Drori, S., Uldry, M., Suppression of reactive oxygen species and neurodegeneration by the PGC-1 transcriptional coactivators (2006) Cell, 127, pp. 397-408. , COI: 1:CAS:528:DC%2BD28XhtFOkt7rM, PID: 17055439
- Lee, B., Cao, R., Choi, Y.-S., The CREB/CRE transcriptional pathway: protection against oxidative stress-mediated neuronal cell death (2009) J Neurochem, 108, pp. 1251-1265. , COI: 1:CAS:528:DC%2BD1MXivFels7Y%3D, PID: 19141071
- Tan, Y.-W., Zhang, S.-J., Hoffmann, T., Bading, H., Increasing levels of wild-type CREB up-regulates several activity-regulated inhibitor of death (AID) genes and promotes neuronal survival (2012) BMC Neurosci, 13, p. 48. , COI: 1:CAS:528:DC%2BC38Xhsl2jsb%2FI, PID: 22607375
- Mosmann, T., Rapid colorimetric assay for cellular growth and survival: application to proliferation and cytotoxicity assays (1983) J Immunol Methods, 65, pp. 55-63. , COI: 1:STN:280:DyaL2c%2FovFSmtw%3D%3D, PID: 6606682
- Carcagno, A.L., Giono, L.E., Marazita, M.C., E2F1 induces p19INK4d, a protein involved in the DNA damage response, following UV irradiation (2012) Mol Cell Biochem, 366, pp. 123-129. , COI: 1:CAS:528:DC%2BC38XotFWqsb4%3D, PID: 22476863
- Ceruti, J.M., Scassa, M.E., Fló, J.M., Induction of p19INK4d in response to ultraviolet light improves DNA repair and confers resistance to apoptosis in neuroblastoma cells (2005) Oncogene, 24, pp. 4065-4080. , COI: 1:CAS:528:DC%2BD2MXlt1Knu7g%3D, PID: 15750620
- Varone, C.L., Giono, L.E., Ochoa, A., Transcriptional regulation of 5-aminolevulinate synthase by phenobarbital and cAMP-dependent protein kinase (1999) Arch Biochem Biophys, 372, pp. 261-270. , COI: 1:CAS:528:DyaK1MXnvFekt7k%3D, PID: 10600163
- Verdeil, G., Puthier, D., Nguyen, C., Gene profiling approach to establish the molecular bases for partial versus full activation of naïve CD8 T lymphocytes (2002) Ann N Y Acad Sci, 975, pp. 68-76. , COI: 1:CAS:528:DC%2BD3sXht1yhu74%3D, PID: 12538155
- Sherman, B.T., Huang, D.W., Tan, Q., DAVID knowledgebase: a gene-centered database integrating heterogeneous gene annotation resources to facilitate high-throughput gene functional analysis (2007) BMC Bioinform, 8, p. 426
- Yamamoto, K.K., Gonzalez, G.A., Biggs, W.H., Montminy, M.R., Phosphorylation-induced binding and transcriptional efficacy of nuclear factor CREB (1988) Nature, 334, pp. 494-498. , COI: 1:CAS:528:DyaL1cXls1Gqtb8%3D, PID: 2900470
- Lee, H.J., Mignacca, R.C., Sakamoto, K.M., Transcriptional activation of egr-1 by granulocyte-macrophage colony-stimulating factor but not interleukin 3 requires phosphorylation of cAMP response element-binding protein (CREB) on serine 133 (1995) J Biol Chem, 270, pp. 15979-15983. , COI: 1:CAS:528:DyaK2MXmvVGnsro%3D, PID: 7608156
- Yi, C., He, C., DNA repair by reversal of DNA damage (2013) Cold Spring Harb Perspect Biol, 5, p. 12575. , PID: 23284047
- Huang, D.W., Sherman, B.T., Tan, Q., DAVID bioinformatics resources: expanded annotation database and novel algorithms to better extract biology from large gene lists (2007) Nucleic Acids Res, 35, pp. W169-W175. , PID: 17576678
- Huang, D.W., Sherman, B.T., Lempicki, R.A., Systematic and integrative analysis of large gene lists using DAVID bioinformatics resources (2009) Nat Protoc, 4, pp. 44-57. , COI: 1:CAS:528:DC%2BD1cXhsFCkurnI
- Zou, J., Crews, F., CREB and NF-kappaB transcription factors regulate sensitivity to excitotoxic and oxidative stress induced neuronal cell death (2006) Cell Mol Neurobiol, 26, pp. 385-405. , COI: 1:CAS:528:DC%2BD28Xhtleksb7F, PID: 16633891
- Volakakis, N., Kadkhodaei, B., Joodmardi, E., NR4A orphan nuclear receptors as mediators of CREB-dependent neuroprotection (2010) Proc Natl Acad Sci USA, 107, pp. 12317-12322. , COI: 1:CAS:528:DC%2BC3cXovFyitb0%3D, PID: 20566846
- Andreoli, C., Leopardi, P., Rossi, S., Crebelli, R., Processing of DNA damage induced by hydrogen peroxide and methyl methanesulfonate in human lymphocytes: analysis by alkaline single cell gel electrophoresis and cytogenetic methods (1999) Mutagenesis, 14, pp. 497-504. , COI: 1:CAS:528:DyaK1MXmtlOjtrw%3D, PID: 10473654
- Mantha, A.K., Sarkar, B., Tell, G., A short review on the implications of base excision repair pathway for neurons: relevance to neurodegenerative diseases (2014) Mitochondrion, 16, pp. 38-49. , COI: 1:CAS:528:DC%2BC3sXhvFGiu7bE, PID: 24220222
- Yang, J.-L., Tadokoro, T., Keijzers, G., Neurons efficiently repair glutamate-induced oxidative DNA damage by a process involving CREB-mediated up-regulation of apurinic endonuclease 1 (2010) J Biol Chem, 285, pp. 28191-28199. , COI: 1:CAS:528:DC%2BC3cXhtVOnsLjK, PID: 20573957
- Li, C., Hu, Z., Lu, J., Genetic polymorphisms in DNA base-excision repair genes ADPRT, XRCC1, and APE1 and the risk of squamous cell carcinoma of the head and neck (2007) Cancer, 110, pp. 867-875. , COI: 1:CAS:528:DC%2BD2sXhtVajsrfF, PID: 17614107
- Wittschieben, B.Ø., Iwai, S., Wood, R.D., DDB1-DDB2 (xeroderma pigmentosum group E) protein complex recognizes a cyclobutane pyrimidine dimer, mismatches, apurinic/apyrimidinic sites, and compound lesions in DNA (2005) J Biol Chem, 280, pp. 39982-39989. , COI: 1:CAS:528:DC%2BD2MXht1Gjs7%2FK, PID: 16223728
- Miao, F., Bouziane, M., Dammann, R., 3-Methyladenine-DNA glycosylase (MPG protein) interacts with human RAD23 proteins (2000) J Biol Chem, 275, pp. 28433-28438. , COI: 1:CAS:528:DC%2BD3cXms1CrurY%3D, PID: 10854423
- Grombacher, T., Mitra, S., Kaina, B., Induction of the alkyltransferase (MGMT) gene by DNA damaging agents and the glucocorticoid dexamethasone and comparison with the response of base excision repair genes (1996) Carcinogenesis, 17, pp. 2329-2336. , COI: 1:CAS:528:DyaK28XnsVOqtbY%3D, PID: 8968045
- Shiyanov, P., Nag, A., Raychaudhuri, P., Cullin 4A associates with the UV-damaged DNA-binding protein DDB (1999) J Biol Chem, 274, pp. 35309-35312. , COI: 1:CAS:528:DyaK1MXotVGgt70%3D, PID: 10585395
- Groisman, R., Polanowska, J., Kuraoka, I., The ubiquitin ligase activity in the DDB2 and CSA complexes is differentially regulated by the COP9 signalosome in response to DNA damage (2003) Cell, 113, pp. 357-367. , COI: 1:CAS:528:DC%2BD3sXjslOlur0%3D, PID: 12732143
---------- APA ----------Pregi, N., Belluscio, L.M., Berardino, B.G., Castillo, D.S. & Cánepa, E.T.
. Oxidative stress-induced CREB upregulation promotes DNA damage repair prior to neuronal cell death protection. Molecular and Cellular Biochemistry, 425(1-2), 9-24.
---------- CHICAGO ----------Pregi, N., Belluscio, L.M., Berardino, B.G., Castillo, D.S., Cánepa, E.T.
"Oxidative stress-induced CREB upregulation promotes DNA damage repair prior to neuronal cell death protection"
. Molecular and Cellular Biochemistry 425, no. 1-2
(2017) : 9-24.
---------- MLA ----------Pregi, N., Belluscio, L.M., Berardino, B.G., Castillo, D.S., Cánepa, E.T.
"Oxidative stress-induced CREB upregulation promotes DNA damage repair prior to neuronal cell death protection"
. Molecular and Cellular Biochemistry, vol. 425, no. 1-2, 2017, pp. 9-24.
---------- VANCOUVER ----------Pregi, N., Belluscio, L.M., Berardino, B.G., Castillo, D.S., Cánepa, E.T. Oxidative stress-induced CREB upregulation promotes DNA damage repair prior to neuronal cell death protection. Mol. Cell. Biochem. 2017;425(1-2):9-24.