Table of Contents Author Guidelines Submit a Manuscript
Neural Plasticity
Volume 2015, Article ID 242158, 12 pages
http://dx.doi.org/10.1155/2015/242158
Research Article

Expression of p53 Target Genes in the Early Phase of Long-Term Potentiation in the Rat Hippocampal CA1 Area

1Novosibirsk State University, Pirogova Street 2, Novosibirsk 630090, Russia
2Institute of Molecular Biology and Biophysics SB RAMS, Timakova Street 2, Novosibirsk 630117, Russia
3International Tomography Center (ITC) SB RAS, Institutskaya Street 3-A, Novosibirsk 630090, Russia
4Laboratory of Biomedical Informatics, Design Technological Institute of Digital Techniques SB RAS, Akademika Rzhanova Street 6, Novosibirsk 630090, Russia

Received 17 October 2014; Accepted 27 January 2015

Academic Editor: Michel Baudry

Copyright © 2015 Vladimir O. Pustylnyak et al. This is an open access article distributed under the Creative Commons Attribution License, which permits unrestricted use, distribution, and reproduction in any medium, provided the original work is properly cited.

Linked References

  1. K. G. Reymann and J. U. Frey, “The late maintenance of hippocampal LTP: requirements, phases, ‘synaptic tagging’, ‘late-associativity’ and implications,” Neuropharmacology, vol. 52, no. 1, pp. 24–40, 2007. View at Publisher · View at Google Scholar · View at Scopus
  2. C. M. Alberini, “Transcription factors in long-term memory and synaptic plasticity,” Physiological Reviews, vol. 89, no. 1, pp. 121–145, 2009. View at Publisher · View at Google Scholar · View at Scopus
  3. V. O. Pustylnyak, P. D. Lisachev, M. B. Shtark, and O. I. Epstein, “Regulation of S100B gene in rat hippocampal CA1 area during long term potentiation,” Brain Research, vol. 1394, pp. 33–39, 2011. View at Publisher · View at Google Scholar · View at Scopus
  4. O. Laptenko and C. Prives, “Transcriptional regulation by p53: one protein, many possibilities,” Cell Death and Differentiation, vol. 13, no. 6, pp. 951–961, 2006. View at Publisher · View at Google Scholar · View at Scopus
  5. K. H. Vousden and C. Prives, “Blinded by the Light: the growing complexity of p53,” Cell, vol. 137, no. 3, pp. 413–431, 2009. View at Publisher · View at Google Scholar · View at Scopus
  6. K. Kuribayashi and W. S. El-Deiry, “Regulation of programmed cell death by the p53 pathway,” Advances in Experimental Medicine and Biology, vol. 615, pp. 201–221, 2008. View at Publisher · View at Google Scholar · View at Scopus
  7. A. Tedeschi and S. Di Giovanni, “The non-apoptotic role of p53 in neuronal biology: enlightening the dark side of the moon,” The EMBO Reports, vol. 10, no. 6, pp. 576–583, 2009. View at Publisher · View at Google Scholar · View at Scopus
  8. S. Solá, M. M. Aranha, and C. M. P. Rodrigues, “Driving apoptosis-relevant proteins toward neural differentiation,” Molecular Neurobiology, vol. 46, no. 2, pp. 316–331, 2012. View at Publisher · View at Google Scholar · View at Scopus
  9. Z. Li, J. Jo, J. M. Jia et al., “Caspase-3 activation via mitochondria is required for long-term depression and AMPA receptor internalization,” Cell, vol. 141, no. 5, pp. 859–871, 2010. View at Publisher · View at Google Scholar · View at Scopus
  10. N. V. Gulyaeva, I. E. Kudryashov, and I. V. Kudryashova, “Caspase activity is essential for long-term potentiation,” Journal of Neuroscience Research, vol. 73, no. 6, pp. 853–864, 2003. View at Publisher · View at Google Scholar · View at Scopus
  11. M. Agostini, P. Tucci, J. R. Steinert et al., “microRNA-34a regulates neurite outgrowth, spinal morphology, and function,” Proceedings of the National Academy of Sciences of the United States of America, vol. 108, no. 52, pp. 21099–21104, 2011. View at Publisher · View at Google Scholar · View at Scopus
  12. H. Nishiyama, T. Knöpfel, S. Endo, and S. Itohara, “Glial protein S100B modulates long-term neuronal synaptic plasticity,” Proceedings of the National Academy of Sciences of the United States of America, vol. 99, no. 6, pp. 4037–4042, 2002. View at Publisher · View at Google Scholar · View at Scopus
  13. J. McAfoose and B. T. Baune, “Evidence for a cytokine model of cognitive function,” Neuroscience and Biobehavioral Reviews, vol. 33, no. 3, pp. 355–366, 2009. View at Publisher · View at Google Scholar · View at Scopus
  14. P. D. Lisachev, M. B. Shtark, O. O. Sokolova, V. O. Pustylnyak, M. Y. Salakhutdinova, and O. I. Epstein, “A comparison of the dynamics of S100B, S100A1, and S100A6 mRNA expression in Hippocampal CA1 area of rats during long-term potentiation and after low-frequency stimulation,” Cardiovascular Psychiatry and Neurology, vol. 2010, Article ID 720958, 6 pages, 2010. View at Publisher · View at Google Scholar · View at Scopus
  15. L. T. Vassilev, B. T. Vu, B. Graves et al., “In vivo activation of the p53 pathway by small-molecule antagonists of MDM2,” Science, vol. 303, no. 5659, pp. 844–848, 2004. View at Publisher · View at Google Scholar · View at Scopus
  16. B. Huang and L. T. Vassilev, “Reduced transcriptional activity in the p53 pathway of senescent cells revealed by the MDM2 antagonist nutlin-3,” Aging, vol. 1, no. 10, pp. 845–854, 2009. View at Google Scholar · View at Scopus
  17. L. A. Carvajal, P.-J. Hamard, C. Tonnessen, and J. J. Manfredi, “E2F7, a novel target, is up-regulated by p53 and mediates DNA damage-dependent transcriptional repression,” Genes & Development, vol. 26, no. 14, pp. 1533–1545, 2012. View at Publisher · View at Google Scholar · View at Scopus
  18. D. Michael and M. Oren, “The p53-Mdm2 module and the ubiquitin system,” Seminars in Cancer Biology, vol. 13, no. 1, pp. 49–58, 2003. View at Publisher · View at Google Scholar · View at Scopus
  19. Y. Ofir-Rosenfeld, K. Boggs, D. Michael, M. B. Kastan, and M. Oren, “Mdm2 regulates p53 mRNA translation through inhibitory interactions with ribosomal protein L26,” Molecular Cell, vol. 32, no. 2, pp. 180–189, 2008. View at Publisher · View at Google Scholar · View at Scopus
  20. S. Nag, J. Qin, K. S. Srivenugopal, M. Wang, and R. Zhang, “The MDM2-p53 pathway revisited,” Journal of Biomedical Research, vol. 27, no. 4, pp. 254–271, 2013. View at Publisher · View at Google Scholar
  21. M. C. Moroni, E. S. Hickman, E. L. Denchi et al., “Apaf-1 is a transcriptional target for E2F and p53,” Nature Cell Biology, vol. 3, no. 6, pp. 552–558, 2001. View at Publisher · View at Google Scholar · View at Scopus
  22. A. I. Robles, N. A. Bemmels, A. B. Foraker, and C. C. Harris, “APAF-1 is a transcriptional target of p53 in DNA damage-induced apoptosis,” Cancer Research, vol. 61, no. 18, pp. 6660–6664, 2001. View at Google Scholar · View at Scopus
  23. T. Miyashita, S. Krajewski, M. Krajewska et al., “Tumor suppressor p53 is a regulator of bcl-2 and bax gene expression in vitro and in vivo,” Oncogene, vol. 9, no. 6, pp. 1799–1805, 1994. View at Google Scholar · View at Scopus
  24. K. Nakano and K. H. Vousden, “PUMA, a novel proapoptotic gene, is induced by p53,” Molecular Cell, vol. 7, no. 3, pp. 683–694, 2001. View at Publisher · View at Google Scholar · View at Scopus
  25. J. K. Sax, P. Fei, M. E. Murphy, E. Bernhard, S. J. Korsmeyer, and W. S. El-Deiry, “BID regulation by p53 contributes to chemosensitivity,” Nature Cell Biology, vol. 4, no. 11, pp. 842–849, 2002. View at Publisher · View at Google Scholar · View at Scopus
  26. W. H. Hoffman, S. Biade, J. T. Zilfou, J. Chen, and M. Murphy, “Transcriptional repression of the anti-apoptotic survivin gene by wild type p53,” The Journal of Biological Chemistry, vol. 277, no. 5, pp. 3247–3257, 2002. View at Publisher · View at Google Scholar · View at Scopus
  27. K. Löhr, C. Möritz, A. Contente, and M. Dobbelstein, “p21/CDKN1A mediates negative regulation of transcription by p53,” The Journal of Biological Chemistry, vol. 278, no. 35, pp. 32507–32516, 2003. View at Publisher · View at Google Scholar · View at Scopus
  28. J.-P. Rouault, N. Falette, F. Guehenneux et al., “Identification of BTG2, an antiproliferative p53-dependent component of the DNA damage cellular response pathway,” Nature Genetics, vol. 14, no. 4, pp. 482–486, 1996. View at Publisher · View at Google Scholar · View at Scopus
  29. S. A. Innocente, J. L. A. Abrahamson, J. P. Cogswell, and J. M. Lee, “p53 regulates a G2 checkpoint through cyclin B1,” Proceedings of the National Academy of Sciences of the United States of America, vol. 96, no. 5, pp. 2147–2152, 1999. View at Publisher · View at Google Scholar · View at Scopus
  30. K. Okamoto and D. Beach, “Cyclin G is a transcriptional target of the p53 tumor suppressor protein,” The EMBO Journal, vol. 13, no. 20, pp. 4816–4822, 1994. View at Google Scholar · View at Scopus
  31. K. Rother, R. Kirschner, K. Sänger, L. Böhlig, J. Mössner, and K. Engeland, “p53 downregulates expression of the G1/S cell cycle phosphatase Cdc25A,” Oncogene, vol. 26, no. 13, pp. 1949–1953, 2007. View at Publisher · View at Google Scholar · View at Scopus
  32. S. S. Clair, L. Giono, S. Varmeh-Ziaie et al., “DNA damage-induced downregulation of Cdc25C is mediated by p53 via two independent mechanisms: one involves direct binding to the cdc25C promoter,” Molecular Cell, vol. 16, no. 5, pp. 725–736, 2004. View at Publisher · View at Google Scholar · View at Scopus
  33. C. Badie, J. E. Itzhaki, M. J. Sullivan, A. J. Carpenter, and A. C. G. Porter, “Repression of CDK1 and other genes with CDE and CHR promoter elements during DNA damage-induced G2/M arrest in human cells,” Molecular and Cellular Biology, vol. 20, no. 7, pp. 2358–2366, 2000. View at Publisher · View at Google Scholar · View at Scopus
  34. W. S. El-Deiry, T. Tokino, T. Waldman et al., “Topological control of p21WAF1/CIP1 expression in normal and neoplastic tissues,” Cancer Research, vol. 55, no. 13, pp. 2910–2919, 1995. View at Google Scholar · View at Scopus
  35. F. J. Stott, S. Bates, M. C. James et al., “The alternative product from the human CDKN2A locus, p14(ARF), participates in a regulatory feedback loop with p53 and MDM2,” The EMBO Journal, vol. 17, no. 17, pp. 5001–5014, 1998. View at Publisher · View at Google Scholar · View at Scopus
  36. T. Matsui, Y. Katsuno, T. Inoue et al., “Negative regulation of Chk2 expression by p53 is dependent on the CCAAT-binding transcription factor NF-Y,” The Journal of Biological Chemistry, vol. 279, no. 24, pp. 25093–25100, 2004. View at Publisher · View at Google Scholar · View at Scopus
  37. A. Martoriati, G. Doumont, M. Alcalay, E. Bellefroid, P. G. Pelicci, and J.-C. Marine, “Dapk1, encoding an activator of a p19ARF-p53-mediated apoptotic checkpoint, is a transcription target of p53,” Oncogene, vol. 24, no. 8, pp. 1461–1466, 2005. View at Publisher · View at Google Scholar · View at Scopus
  38. E. J. Peterson, O. Bögler, and S. M. Taylor, “p53-mediated repression of DNA methyltransferase 1 expression by specific DNA binding,” Cancer Research, vol. 63, no. 20, pp. 6579–6582, 2003. View at Google Scholar · View at Scopus
  39. J. H. Ludes-Meyers, M. A. Subler, C. V. Shivakumar et al., “Transcriptional activation of the human epidermal growth factor receptor promoter by human p53,” Molecular and Cellular Biology, vol. 16, no. 11, pp. 6009–6019, 1996. View at Google Scholar · View at Scopus
  40. J. Yu, V. Baron, D. Mercola, T. Mustelin, and E. D. Adamson, “A network of p73, p53 and Egr1 is required for efficient apoptosis in tumor cells,” Cell Death and Differentiation, vol. 14, no. 3, pp. 436–446, 2007. View at Publisher · View at Google Scholar · View at Scopus
  41. L. B. Owen-Schaub, W. Zhang, J. C. Cusack et al., “Wild-type human p53 and a temperature-sensitive mutant induce Fas/APO-1 expression,” Molecular and Cellular Biology, vol. 15, no. 6, pp. 3032–3040, 1995. View at Google Scholar · View at Scopus
  42. M. Müller, S. Wilder, D. Bannasch et al., “p53 activates the CD95 (APO-1/Fas) gene in response to DNA damage by anticancer drugs,” The Journal of Experimental Medicine, vol. 188, no. 11, pp. 2033–2045, 1998. View at Publisher · View at Google Scholar · View at Scopus
  43. T. Fukazawa, T. Fujiwara, Y. Morimoto et al., “Differential involvement of the CD95 (Fas/APO-1) receptor/ligand system on apoptosis induced by the wild-type p53 gene transfer in human cancer cells,” Oncogene, vol. 18, no. 13, pp. 2189–2199, 1999. View at Publisher · View at Google Scholar · View at Scopus
  44. M. L. Smith, I. T. Chen, Q. Zhan et al., “Interaction of the p53-regulated protein gadd45 with proliferating cell nuclear antigen,” Science, vol. 266, no. 5189, pp. 1376–1380, 1994. View at Publisher · View at Google Scholar · View at Scopus
  45. U. Santhanam, A. Ray, and P. B. Sehgal, “Repression of the interleukin 6 gene promoter by p53 and the retinoblastoma susceptibility gene product,” Proceedings of the National Academy of Sciences of the United States of America, vol. 88, no. 17, pp. 7605–7609, 1991. View at Publisher · View at Google Scholar · View at Scopus
  46. A. Zauberman, D. Flusberg, Y. Haupt, Y. Barak, and M. Oren, “A functional p53-responsive intronic promoter is contained within the human mdm2 gene,” Nucleic Acids Research, vol. 23, no. 14, pp. 2584–2592, 1995. View at Publisher · View at Google Scholar · View at Scopus
  47. J. Chen and I. Sadowski, “Identification of the mismatch repair genes PMS2 and MLH1 as p53 target genes by using serial analysis of binding elements,” Proceedings of the National Academy of Sciences of the United States of America, vol. 102, no. 13, pp. 4813–4818, 2005. View at Publisher · View at Google Scholar · View at Scopus
  48. S. J. Scherer, S. M. Maier, M. Seifert et al., “p53 and c-Jun functionally synergize in the regulation of the DNA repair gene hMSH2 in response to UV,” The Journal of Biological Chemistry, vol. 275, no. 48, pp. 37469–37473, 2000. View at Publisher · View at Google Scholar · View at Scopus
  49. K. H. Moberg, W. A. Tyndall, and D. J. Hall, “Wild-type murine p53 represses transcription from the murine c-myc promotor in a human glial cell line,” Journal of Cellular Biochemistry, vol. 49, no. 2, pp. 208–215, 1992. View at Publisher · View at Google Scholar · View at Scopus
  50. G. F. Morris, J. R. Bischoff, and M. B. Mathews, “Transcriptional activation of the human proliferating-cell nuclear antigen promoter by p53,” Proceedings of the National Academy of Sciences of the United States of America, vol. 93, no. 2, pp. 895–899, 1996. View at Publisher · View at Google Scholar · View at Scopus
  51. E. Oda, R. Ohki, H. Murasawa et al., “Noxa, a BH3-only member of the Bcl-2 family and candidate mediator of p53-induced apoptosis,” Science, vol. 288, no. 5468, pp. 1053–1058, 2000. View at Publisher · View at Google Scholar · View at Scopus
  52. M. Fiscella, H. Zhang, S. Fan et al., “Wip1, a novel human protein phosphatase that is induced in response to ionizing radiation in a p53-dependent manner,” Proceedings of the National Academy of Sciences of the United States of America, vol. 94, no. 12, pp. 6048–6053, 1997. View at Publisher · View at Google Scholar · View at Scopus
  53. C. Li, M. Lin, and J. Liu, “Identification of PRC1 as the p53 target gene uncovers a novel function of p53 in the regulation of cytokinesis,” Oncogene, vol. 23, no. 58, pp. 9336–9347, 2004. View at Publisher · View at Google Scholar · View at Scopus
  54. M. Zhan, D. Yu, J. Liu, J. Hannay, and R. E. Pollock, “Transcriptional repression of protein kinase Cα via Sp1 by wild type p53 is involved in inhibition of multidrug resistance 1 P-glycoprotein phosphorylation,” The Journal of Biological Chemistry, vol. 280, no. 6, pp. 4825–4833, 2005. View at Publisher · View at Google Scholar · View at Scopus
  55. V. Stambolic, D. MacPherson, D. Sas et al., “Regulation of PTEN transcription by p53,” Molecular Cell, vol. 8, no. 2, pp. 317–325, 2001. View at Publisher · View at Google Scholar · View at Scopus
  56. P. S. Kho, Z. Wang, L. Zhuang et al., “p53-regulated transcriptional program associated with genotoxic stress-induced apoptosis,” Journal of Biological Chemistry, vol. 279, no. 20, pp. 21183–21192, 2004. View at Publisher · View at Google Scholar · View at Scopus
  57. Y. Shiio, T. Yamamoto, and N. Yamaguchi, “Negative regulation of Rb expression by the p53 gene product,” Proceedings of the National Academy of Sciences of the United States of America, vol. 89, no. 12, pp. 5206–5210, 1992. View at Google Scholar · View at Scopus
  58. A. V. Budanov and M. Karin, “p53 target genes sestrin1 and sestrin2 connect genotoxic stress and mTOR signaling,” Cell, vol. 134, no. 3, pp. 451–460, 2008. View at Publisher · View at Google Scholar · View at Scopus
  59. R. Ohki, J. Nemoto, H. Murasawa et al., “Reprimo, a new candidate mediator of the p53-mediated cell cycle arrest at the G2 phase,” The Journal of Biological Chemistry, vol. 275, no. 30, pp. 22627–22630, 2000. View at Publisher · View at Google Scholar · View at Scopus
  60. J. Lin, Q. Yang, Z. Yan et al., “Inhibiting S100B restores p53 levels in primary malignant melanoma cancer cells,” The Journal of Biological Chemistry, vol. 279, no. 32, pp. 34071–34077, 2004. View at Publisher · View at Google Scholar · View at Scopus
  61. L. Brown, P. P. Ongusaha, H.-G. Kim et al., “CDIP, a novel pro-apoptotic gene, regulates TNFα-mediated apoptosis in a p53-dependent manner,” The EMBO Journal, vol. 26, no. 14, pp. 3410–3422, 2007. View at Publisher · View at Google Scholar · View at Scopus
  62. R. Zhao, K. Gish, M. Murphy et al., “Analysis of p53-regulated gene expression patterns using oligonucleotide arrays,” Genes & Development, vol. 14, no. 8, pp. 981–993, 2000. View at Google Scholar · View at Scopus
  63. C. D. Lopez, Y. Ao, L. H. Rohde et al., “Proapoptotic p53-interacting protein 53BP2 is induced by UV irradiation but suppressed by p53,” Molecular and Cellular Biology, vol. 20, no. 21, pp. 8018–8025, 2000. View at Publisher · View at Google Scholar · View at Scopus
  64. D. C. Harmes, E. Bresnick, E. A. Lubin et al., “Positive and negative regulation of deltaN-p63 promoter activity by p53 and deltaN-p63-alpha contributes to differential regulation of p53 target genes,” Oncogene, vol. 22, no. 48, pp. 7607–7616, 2003. View at Publisher · View at Google Scholar · View at Scopus
  65. T. J. Grob, U. Novak, C. Maisse et al., “Human ΔNp73 regulates a dominant negative feedback loop for TAp73 and p53,” Cell Death and Differentiation, vol. 8, no. 12, pp. 1213–1223, 2001. View at Publisher · View at Google Scholar · View at Scopus
  66. X. Chen, Y. Zheng, J. Zhu, J. Jiang, and J. Wang, “p73 is transcriptionally regulated by DNA damage, p53, and p73,” Oncogene, vol. 20, no. 6, pp. 769–774, 2001. View at Publisher · View at Google Scholar · View at Scopus
  67. D. Israeli, E. Tessler, Y. Haupt et al., “A novel p53-inducible gene, PAG608, encodes a nuclear zinc finger protein whose overexpression promotes apoptosis,” The EMBO Journal, vol. 16, no. 14, pp. 4384–4392, 1997. View at Publisher · View at Google Scholar · View at Scopus
  68. P. D. Lisachev, V. O. Pustylnyak, M. B. Shtark, and O. I. Epstein, “Induction of S100B gene expression in long-term potentiation in the hippocampal CA1 field depends on activity of NMDA receptors,” Bulletin of Experimental Biology and Medicine, vol. 154, no. 4, pp. 485–488, 2013. View at Publisher · View at Google Scholar · View at Scopus
  69. O. O. Sokolova, M. B. Shtark, P. D. Lisachev, V. O. Pustylnyak, I. R. Pan, and O. I. Epstein, “Expression of S100B and S100A6 genes during long-term posttetanic potentiation in the hippocampus,” Bulletin of Experimental Biology and Medicine, vol. 148, no. 2, pp. 227–229, 2009. View at Publisher · View at Google Scholar · View at Scopus
  70. Y. Y. Huang and E. R. Kandel, “Recruitment of long-lasting and protein kinase A-dependent long-term potentiation in the CA1 region of hippocampus requires repeated tetanization,” Learning & Memory, vol. 1, no. 1, pp. 74–82, 1994. View at Google Scholar · View at Scopus
  71. L. Biderman, J. L. Manley, and C. Prives, “Mdm2 and MdmX as regulators of gene expression,” Genes & Cancer, vol. 3, no. 3-4, pp. 264–273, 2012. View at Publisher · View at Google Scholar · View at Scopus
  72. C. S. Park, R. Gong, J. Stuart, and S.-J. Tang, “Molecular network and chromosomal clustering of genes involved in synaptic plasticity in the hippocampus,” Journal of Biological Chemistry, vol. 281, no. 40, pp. 30195–30211, 2006. View at Publisher · View at Google Scholar · View at Scopus
  73. J. E. Ploski, K. W. Park, J. Ping, M. S. Monsey, and G. E. Schafe, “Identification of plasticity-associated genes regulated by Pavlovian fear conditioning in the lateral amygdala,” Journal of Neurochemistry, vol. 112, no. 3, pp. 636–650, 2010. View at Publisher · View at Google Scholar · View at Scopus
  74. M. M. Ryan, S. E. Mason-Parker, W. P. Tate, W. C. Abraham, and J. M. Williams, “Rapidly induced gene networks following induction of long-term potentiation at perforant path synapses in vivo,” Hippocampus, vol. 21, no. 5, pp. 541–553, 2011. View at Publisher · View at Google Scholar · View at Scopus
  75. M. M. Ryan, B. Ryan, M. Kyrke-Smith et al., “Temporal profiling of gene networks associated with the late phase of long-term potentiation in vivo,” PLoS ONE, vol. 7, no. 7, Article ID e40538, 2012. View at Publisher · View at Google Scholar · View at Scopus
  76. E. S. Lein, X. Zhao, and F. H. Gage, “Defining a molecular atlas of the hippocampus using DNA microarrays and high-throughput in situ hybridization,” The Journal of Neuroscience, vol. 24, no. 15, pp. 3879–3889, 2004. View at Publisher · View at Google Scholar · View at Scopus
  77. E. D. Leonardo, J. W. Richardson-Jones, E. Sibille, A. Kottman, and R. Hen, “Molecular heterogeneity along the dorsal-ventral axis of the murine hippocampal CA1 field: a microarray analysis of gene expression,” Neuroscience, vol. 137, no. 1, pp. 177–186, 2006. View at Publisher · View at Google Scholar · View at Scopus
  78. N. Maggio and M. Segal, “Unique regulation of long term potentiation in the rat ventral hippocampus,” Hippocampus, vol. 17, no. 1, pp. 10–25, 2007. View at Publisher · View at Google Scholar · View at Scopus
  79. T. Riley, E. Sontag, P. Chen, and A. Levine, “Transcriptional control of human p53-regulated genes,” Nature Reviews Molecular Cell Biology, vol. 9, no. 5, pp. 402–412, 2008. View at Publisher · View at Google Scholar · View at Scopus
  80. E. Miyamoto, “Molecular mechanism of neuronal plasticity: induction and maintenance of long-term potentiation in the hippocampus,” Journal of Pharmacological Sciences, vol. 100, no. 5, pp. 433–442, 2006. View at Publisher · View at Google Scholar · View at Scopus
  81. V. P. Sukhatme, X. M. Cao, L. C. Chang et al., “A zinc finger-encoding gene coregulated with c-fos during growth and differentiation, and after cellular depolarization,” Cell, vol. 53, no. 1, pp. 37–43, 1988. View at Publisher · View at Google Scholar · View at Scopus
  82. A. Quiñones, K. U. Dobberstein, and N. G. Rainov, “The egr-1 gene is induced by DNA-damaging agents and non-genotoxic drugs in both normal and neoplastic human cells,” Life Sciences, vol. 72, no. 26, pp. 2975–2992, 2003. View at Publisher · View at Google Scholar · View at Scopus
  83. I. de Belle, R.-P. Huang, Y. Fan, C. Liu, D. Mercola, and E. D. Adamson, “P53 and Egr-1 additively suppress transformed growth in HT1080 cells but Egr-1 counteracts p53-dependent apoptosis,” Oncogene, vol. 18, no. 24, pp. 3633–3642, 1999. View at Publisher · View at Google Scholar · View at Scopus
  84. M. Pignatelli, R. Luna-Medina, A. Pérez-Rendón, A. Santos, and A. Perez-Castillo, “The transcription factor early growth response factor-1 (EGR-1) promotes apoptosis of neuroblastoma cells,” The Biochemical Journal, vol. 373, no. 3, pp. 739–746, 2003. View at Publisher · View at Google Scholar · View at Scopus
  85. E. Bálint, S. Bates, and K. H. Vousden, “Mdm2 binds p73α without targeting degradation,” Oncogene, vol. 18, no. 27, pp. 3923–3929, 1999. View at Publisher · View at Google Scholar · View at Scopus