HDAC inhibitors show differential epigenetic regulation and cell survival strategies on p53 mutant colon cancer cells

References

• Aggarwal, M., Saxena, R., Sinclair, E., Fu, Y., Jacobs, A., Dyba, M., … Chung, F. L. (2016). Reactivation of mutant p53 by a dietary-related compound phenethyl isothiocyanate inhibits tumor growth. Cell Death and Differentiation, 23, 1615–1627.
   PubMed Web of Science ®Google Scholar
• Bajbouj, K., Mawrin, C., Hartig, R., Schulze-Luehrmann, J., Wilisch-Neumann, A., Roessner, A., & Schneider-Stock, R. (2012). p53-dependent antiproliferative and pro-apoptotic effects of trichostatin A (TSA) in glioblastoma cells. Journal of Neuro-Oncology, 107, 503–516.
   PubMed Web of Science ®Google Scholar
• Barneda-Zahonero, B., & Parra, M. (2012). Histone deacetylases and cancer. Molecular Oncology, 6, 579–589.
   PubMed Web of Science ®Google Scholar
• Bendardaf, R., Buhmeida, A., Hilska, M., Laato, M., Syrjänen, S., Syrjänen, K., … Pyrhönen, S. (2008). VEGF-1 expression in colorectal cancer is associated with disease localization, stage, and long-term disease-specific survival. Anticancer Research, 28, 3865–3870.
   PubMed Web of Science ®Google Scholar
• Berendsen, H. J. C., Postma, J. P. M., van Gunsteren, W. F., & Hermans, J. (1981). Intermolecular forces, chapter – Interaction models for water in relation to protein hydration (pp. 331–342). Dordrecht: D. Reidel Publishing Company Dordrecht.
   Google Scholar
• Bou-Hanna, C., Jarry, A., Lode, L., Schmitz, I., Schulze-Osthoff, K., Kury, S., … Laboisse, C. L. (2015). Acute cytotoxicity of MIRA-1/NSC19630, a mutant p53-reactivating small molecule, against human normal and cancer cells via a caspase-9-dependent apoptosis. Cancer Letters, 359, 211–217.
   PubMed Web of Science ®Google Scholar
• Brady, C. A., & Attardi, L. D. (2010). p53 at a glance. Journal of Cell Science, 123, 2527–2532.
   PubMed Web of Science ®Google Scholar
• Ceccacci, E., & Minucci, S. (2016). Inhibition of histone deacetylases in cancer therapy: lessons from leukaemia. British Journal of Cancer, 114, 605–611.
   PubMed Web of Science ®Google Scholar
• Chakrabarti, A., Oehme, I., Witt, O., Oliveira, G., Sippl, W., Romier, C., … Jung, M. (2015). HDAC8: A multifaceted target for therapeutic interventions. Trends in Pharmacological Sciences, 36, 481–492.
   PubMed Web of Science ®Google Scholar
• Chen, X., Wong, P., Radany, E., & Wong, J. Y. C. (2009). HDAC inhibitor, valproic acid, induces p53-dependent radiosensitization of colon cancer cells. Cancer Biotherapy and Radiopharmaceuticals, 24, 689–699.
   PubMed Web of Science ®Google Scholar
• Ciombor, K. K., Wu, C., & Goldberg, R. M. (2015). Recent therapeutic advances in the treatment of colorectal cancer. Annual Review of Medicine, 66, 83–95.
   PubMed Web of Science ®Google Scholar
• Comeau, S. R., Gatchell, D. W., Vajda, S., & Camacho, C. J. (2004). ClusPro: An automated docking and discrimination method for the prediction of protein complexes. Bioinformatics, 20, 45–50.
   PubMed Web of Science ®Google Scholar
• Corcoran, C. A., He, Q., Huang, Y., & Sheikh, M. S. (2005). Cyclooxygenase-2 interacts with p53 and interferes with p53-dependent transcription and apoptosis. Oncogene, 24, 1634–1640.
   PubMed Web of Science ®Google Scholar
• Coward, W. R., Feghali-Bostwick, C. A., Jenkins, G., Knox, A. J., & Pang, L. (2014). A central role for G9a and EZH2 in the epigenetic silencing of cyclooxygenase-2 in idiopathic pulmonary fibrosis. The FASEB Journal, 28, 3183–3196.
   PubMed Web of Science ®Google Scholar
• Davison, T. S., Vagner, C., Kaghad, M., Ayed, A., Caput, D., & Arrowsmith, C. H. (1999). p73 and p63 are homotetramers capable of weak heterotypic interactions with each other but not with p53. The Journal of Biological Chemistry, 274, 18709–18714.
   PubMed Web of Science ®Google Scholar
• De Rosa, M., Pace, U., Rega, D., Costabile, V., Duraturo, F., Izzo, P., & Delrio, P. (2015). Genetics, diagnosis and management of colorectal cancer. Oncology Reports, 34, 1087–1096.
   PubMed Web of Science ®Google Scholar
• Eberharter, A., & Becker, P. B. (2002). Histone acetylation: A switch between repressive and permissive chromatin Second in review series on chromatin dynamics. EMBO Reports, 3, 224–229.
   PubMed Web of Science ®Google Scholar
• Elsaleh, H., Powell, B., McCaul, K., Grieu, F., Grant, R., Joseph, D., & Iacopetta, B. (2001). P53 alteration and microsatellite instability have predictive value for survival benefit from chemotherapy in stage III colorectal carcinoma. Clinical Cancer Research, 7, 1343–1349.
   PubMed Web of Science ®Google Scholar
• Famulski, W., Sulkowska, M., Wincewicz, A., Kedra, B., Pawlak, K., Zalewski, B., … Baltaziak, M. (2006). p53 correlates positively with VEGF in preoperative sera of colorectal cancer patients. Neoplasma, 53, 43–48.
   PubMed Web of Science ®Google Scholar
• Freed-Pastor, W. A., & Prives, C. (2012). Mutant p53: One name, many proteins. Genes & Development, 26, 1268–1286.
   PubMed Web of Science ®Google Scholar
• Fukuda, H., Sano, N., Muto, S., & Horikoshi, M. (2006). Simple histone acetylation plays a complex role in the regulation of gene expression. Briefings in Functional Genomics & Proteomics, 5, 190–208.
   PubMedGoogle Scholar
• Garufi, A., Pistritto, G., Cirone, M., & D’Orazi, G. (2016). Reactivation of mutant p53 by capsaicin, the major constituent of peppers. Journal of Experimental and Clinical Cancer Research, 35, 136–142.
   PubMed Web of Science ®Google Scholar
• Garufi, A., Ubertini, V., Mancini, F., D'Orazi, V., Baldari, S., Moretti, F., … D'Orazi, G. (2015). The beneficial effect of Zinc(II) on low-dose chemotherapeutic sensitivity involves p53 activation in wild-type p53-carrying colorectal cancer cells. Journal of Experimental & Clinical Cancer Research, 34, 87.
   PubMed Web of Science ®Google Scholar
• Giacomelli, C., Natali, L., Trincavelli, M. L., Daniele, S., Bertoli, A., Flamini, G., … Martini, C. (2016). New insights into the anticancer activity of carnosol: p53 reactivation in the U87MG human glioblastoma cell line. The International Journal of Biochemistry & Cell Biology, 74, 95–108.
   PubMed Web of Science ®Google Scholar
• Glaser, K. B., Staver, M. J., Waring, J. F., Stender, J., Ulrich, R. G., & Davidsen, S. K. (2003). Gene expression profiling of multiple histone deacetylase (HDAC) inhibitors: Defining a common gene set produced by HDAC inhibition in T24 and MDA carcinoma cell lines. Molecular Cancer Therapeutics, 2, 151–63.
   PubMed Web of Science ®Google Scholar
• Habold, C., Poehlmann, A., Bajbouj, K., Hartig, R., Korkmaz, K. S., Roessner, A., & Schneider-Stock, R. (2008). Trichostatin A causes p53 to switch oxidative-damaged colorectal cancer cells from cell cycle arrest into apoptosis. Journal of Cellular and Molecular Medicine, 12, 607–621.
   PubMed Web of Science ®Google Scholar
• Hagan, S., Maria Orr, C. M., & Doyle, B. (2013). Targeted therapies in colorectal cancer—an integrative view by PPPM. The EPMA Journal, 4, 3–19.
   PubMedGoogle Scholar
• Heider, U., Kaiser, M., Sterz, J., Zavrski, I., Jakob, C., Fleissner, C., … Sezer, O. (2006). Histone deacetylase inhibitors reduce VEGF production and induce growth suppression and apoptosis in human mantle cell lymphoma. European Journal of Haematology, 76, 42–50.
   PubMed Web of Science ®Google Scholar
• Hiraki, M., Hwang, S.-Y., Cao, S., Ramadhar, T. R., Byun, S., Yoon, K. W., … Lee, S. W. (2015). Small-molecule reactivation of mutant p53 to wild-type-like p53 through the p53-HSP40 regulatory axis. Chemistry & Biology, 22, 1206–1216.
   PubMedGoogle Scholar
• Hsieh, J. S., Lin, S. R., Chang, M. Y., Chen, F. M., Lu, C. Y., Huang, T. J., … Wang, J. Y. (2005). APC, K-ras, and p53 gene mutations in colorectal cancer patients: Correlation to clinicopathologic features and postoperative surveillance. The American Journal of Surgery, 71, 336–43.
   Google Scholar
• Iacopetta, B. (2003). TP53 mutation in colorectal cancer. Human Mutation, 21, 271–276.
   PubMed Web of Science ®Google Scholar
• Iacopetta, B., Russo, A., Bazan, V., Dardanoni, G., Gebbia, N., Soussi, T., … Ishioka, C. (2006). Functional categories of TP53 mutation in colorectal cancer: Results of an International Collaborative Study. Annals of Oncology, 17, 842–847.
   PubMed Web of Science ®Google Scholar
• Ines, C., Donia, O., Rahma, B., Ben Ammar, A., Sameh, A., Khalfallah, T., … Saadia, B. (2014). Implication of K-ras and p53 in colorectal cancer carcinogenesis in Tunisian population cohort. Tumor Biology, 35, 7163–7175.
   PubMed Web of Science ®Google Scholar
• Kara, O., Duman, B. B., Kara, B., Erdogan, S., Parsak, C. K., & Sakman, G. (2012). Analysis of PTEN, VEGF, HER2 and P53 status in determining colorectal cancer benefit from bevacizumab therapy. Asian Pacific Journal of Cancer Prevention, 13, 6397–401.
   PubMedGoogle Scholar
• Knickelbein, K., & Zhang, L. (2015). Mutant KRAS as a critical determinant of the therapeutic response of colorectal cancer. Genes & Diseases, 2, 4–12.
   PubMed Web of Science ®Google Scholar
• Krayem, M., Journe, F., Wiedig, M., Morandini, R., Najem, A., Salès, F., … Ghanem, G. (2016). p53 reactivation by PRIMA-1(Met) (APR-246) sensitises (V600E/K)BRAF melanoma to vemurafenib. European Journal of Cancer, 55, 98–110.
   PubMed Web of Science ®Google Scholar
• Lane, D. P., Cheok, C. F., & Lain, S. (2010). p53-based cancer therapy. Cold Spring Harbor Perspectives in Biology, 2, a001222.
   PubMed Web of Science ®Google Scholar
• Li, X. L., Zhou, J., Chen, Z. R., & Chng, W. J. (2015). p53 mutations in colorectal cancer- molecular pathogenesis and pharmacological reactivation. World Journal of Gastroenterology, 21, 84–93.
   PubMed Web of Science ®Google Scholar
• Lindahl, E., Hess, B., & Spoel, D. V. (2001). GROMACS 3.0: A package for molecular simulation and trajectory analysis. Journal of Molecular Modeling, 7, 306–317.
   Web of Science ®Google Scholar
• Liu, T., Kuljaca, S., Tee, A., & Marshall, G. M. (2006). Histone deacetylase inhibitors: Multifunctional anticancer agents. Cancer Treatment Reviews, 32, 157–165.
   PubMed Web of Science ®Google Scholar
• López, I., Oliveira, L. P., Tucci, P., Alvarez-Valín, F., Coudry, A. R., & Marín, M. (2012). Different mutation profiles associated to P53 accumulation in colorectal cancer. Gene, 499, 81–87.
   PubMed Web of Science ®Google Scholar
• Mariadason, J. M. (2008). HDACs and HDAC inhibitors in colon cancer. Epigenetics, 3, 28–37.
   PubMed Web of Science ®Google Scholar
• Marks, P. A., Miller, T., & Richon, V. M. (2003). Histone deacetylases. Current Opinion in Pharmacology, 3, 344–351.
   PubMed Web of Science ®Google Scholar
• Meng, J., Zhang, H. H., Zhou, C. X., Li, C., Zhang, F., & Mei, Q. B. (2012). The histone deacetylase inhibitor trichostatin A induces cell cycle arrest and apoptosis in colorectal cancer cells via p53-dependent and -independent pathways. Oncology Reports, 28, 384–388.
   PubMed Web of Science ®Google Scholar
• Morris, G. M., Huey, R., Lindstrom, W., Sanner, M. F., Belew, R. K., Goodsell, D. S., & Olson, A. J. (2009). Autodock4 and AutoDockTools4: Automated docking with selective receptor flexiblity. Journal of Computational Chemistry, 16, 2785–2791.
   Web of Science ®Google Scholar
• Muller, P. A. J., & Vousden, K. H. (2014). Mutant p53 in cancer: New functions and therapeutic opportunities. Cancer Cell, 25, 304–317.
   PubMed Web of Science ®Google Scholar
• Murphy, K. L., Dennis, A. P., & Rosen, J. M. (2000). A gain of function p53 mutant promotes both genomic instability and cell survival in a novel p53-null mammary epithelial cell model. The FASEB Journal, 14, 2291–302.
   PubMed Web of Science ®Google Scholar
• Naccarati, A., Polakova, V., Pardini, B., Vodickova, L., Hemminki, K., Kumar, R., & Vodicka, P. (2012). Mutations and polymorphisms in TP53 gene – An overview on the role in colorectal cancer. Mutagenesis, 27, 211–218.
   PubMed Web of Science ®Google Scholar
• Natan, E., Baloglu, C., Pagel, K., Freund, S. M., Morgner, N., Robinson, C. V., & Joerger, A. C. (2011). Interaction of the p53 DNA-binding domain with its N-terminal extension modulates the stability of the p53 tetramer. Journal of Molecular Biology, 409, 358–368.
   PubMed Web of Science ®Google Scholar
• Olivier, M., Hollstein, M., & Hainaut, P. (2010). TP53 mutations in human cancers: Origins, consequences, and clinical use. Cold Spring Harbor Perspectives in Biology, 2, a001008.
   PubMed Web of Science ®Google Scholar
• Oren, M., & Rotter, V. (2010). Mutant p53 gain-of-function in cancer. Cold Spring Harbor Perspectives in Biology, 2, a001107.
   PubMed Web of Science ®Google Scholar
• Petitjean, A., Achatz, M. I., Borresen-Dale, A. L., Hainaut, P., & Olivier, M. (2007). TP53 mutations in human cancers: Functional selection and impact on cancer prognosis and outcomes. Oncogene, 26, 2157–2165.
   PubMed Web of Science ®Google Scholar
• Pettersen, E. F., Goddard, T. D., Huang, C. C., Couch, G. S., Greenblatt, D. M., Meng, E. C., & Ferrin, T. E. (2004). UCSF Chimera–a visualization system for exploratory research and analysis. Journal of Computational Chemistry, 25, 1605–1612.
   PubMed Web of Science ®Google Scholar
• Pronk, S., Pall, S., Schulz, R., Larsson, P., Bjelkmar, P., Apostolov, R., & Lindahl, E. (2013). GROMACS 4.5: A high-throughput and highly parallel open source molecular simulation toolkit. Bioinformatics, 29, 845–854.
   PubMed Web of Science ®Google Scholar
• Ribeiro, C. J. A., Amara, J. D., Rodrigues, C. M. P., Moreira, R., & Santos, M. M. M. (2016). Spirooxadiazoline oxindoles with promising in vitro antitumor activities. MedChemComm, 7, 420–425.
   Web of Science ®Google Scholar
• Richman, S. D., Seymour, M. T., Chambers, P., Elliott, F., Daly, C. L., Meade, A. M., … Quirke, P. (2009). KRAS and BRAF mutations in advanced colorectal cancer are associated with poor prognosis but do not preclude benefit from oxaliplatin or irinotecan: Results from the MRC FOCUS trial. Journal of Clinical Oncology, 27, 5931–5937.
   PubMed Web of Science ®Google Scholar
• Ropero, S., & Esteller, M. (2007). The role of histone deacetylases (HDACs) in human cancer. Molecular Oncology, 1, 9–25.
   Web of Science ®Google Scholar
• Sachweh, M. C. C., Drummond, C. J., Higgins, M., Campbell, J., & Laín, S. (2013). Incompatible effects of p53 and HDAC inhibition on p21 expression and cell cycle progression. Cell Death & Disease, 4, e533.
   PubMed Web of Science ®Google Scholar
• Sawa, H., Murakami, H., Ohshima, Y., Murakami, M., Yamazaki, I., Tamura, Y., … Kamada, H. (2002). Histone deacetylase inhibitors such as sodium butyrate and trichostatin A inhibit vascular endothelial growth factor (VEGF) secretion from human glioblastoma cells. Brain Tumor Pathology, 19, 77–81.
   PubMedGoogle Scholar
• Shahbazian, M. D., & Grunstein, M. (2007). Functions of site-specific histone acetylation and deacetylation. Annual Review of Biochemistry, 76, 75–100.
   PubMed Web of Science ®Google Scholar
• Smith, G., Carey, F. A., Beattie, J., Wilkie, M. J., Lightfoot, T. J., Coxhead, J., … Wolf, C. R. (2002). Mutations in APC, Kirsten-ras, and p53: Alternative genetic pathways to colorectal cancer. Proceedings of the National Academy of Sciences USA, 99, 9433–9438.
   PubMed Web of Science ®Google Scholar
• Somoza, J. R., Skene, R. J., Katz, B. A., Mol, C., Ho, J. D., Jennings, A. J., … Tari, L. W. (2004). Structural snapshots of human HDAC8 provide insights into the class I histone deacetylases. Structure, 12, 1325–1334.
   PubMed Web of Science ®Google Scholar
• Sonnemann, J., Marx, C., Becker, S., Wittig, S., Palani, C. D., Kramer, O. H., & Beck, J. F. (2014). p53-dependent and p53-independent anticancer effects of different histone deacetylase inhibitors. British Journal of Cancer, 110, 656–667.
   PubMed Web of Science ®Google Scholar
• Struhl, K. (1998). Histone acetylation and transcriptional regulatory? Mechanisms. Genes & Development, 12, 599–606.
   PubMed Web of Science ®Google Scholar
• Sukhwal, A., & Sowdhamini, R. (2013). Oligomerisation status and evolutionary conservation of interfaces of protein structural domain superfamilies. Molecular BioSystems, 9, 1652–1661.
   PubMed Web of Science ®Google Scholar
• Tampakis, A., Tampaki, E. C., Nebiker, C. A., & Kouraklis, G. (2014). Histone deacetylase inhibitors and colorectal cancer: What is new? Anti-Cancer Agents in Medicinal Chemistry, 14, 1220–1227.
   PubMed Web of Science ®Google Scholar
• Tong, X., Yin, L., & Giardina, C. (2004). Butyrate suppresses Cox-2 activation in colon cancer cells through HDAC inhibition. Biochemical and Biophysical Research Communications, 317, 463–71.
   PubMed Web of Science ®Google Scholar
• Tortola, S., Marcuello, E., González, I., Reyes, G., Arribas, R., Aiza, G., … Capella, G. (1999). p53 and K-ras gene mutations correlate with tumor aggressiveness but are not of routine prognostic value in colorectal cancer. Journal of Clinical Oncology, 17, 1375–1381.
   PubMed Web of Science ®Google Scholar
• Tran, N. H., Cavalcante, L. L., Lubner, S. J., Mulkerin, D. L., LoConte, N. K., Clipson, L., … Deming, D. A. (2015). Precision medicine in colorectal cancer: The molecular profile alters treatment strategies. Therapeutic Advances in Medical Oncology, 7, 252–262.
   PubMed Web of Science ®Google Scholar
• Verdone, L., Caserta, M., & Di Mauro, E. (2005). Role of histone acetylation in the control of gene expression. Biochemistry and Cell Biology, 83, 344–353.
   PubMed Web of Science ®Google Scholar
• Vikhanskaya, F., Lee, M. K., Mazzoletti, M., Broggini, M., & Sabapathy, K. (2007). Cancer-derived p53 mutants suppress p53-target gene expression–potential mechanism for gain of function of mutant p53. Nucleic Acids Research, 35, 2093–2104.
   PubMed Web of Science ®Google Scholar
• Wang, D., & DuBois, R. N. (2010). The role of COX-2 in intestinal inflammation and colorectal cancer. Oncogene, 29, 781–788.
   PubMed Web of Science ®Google Scholar
• Wang, J. Y., Hsieh, J. S., Chang, M. Y., Huang, T. J., Chen, F. M., … Lin, S. R. (2004). Molecular detection of APC, K- ras, and p53 mutations in the serum of colorectal cancer patients as circulating biomarkers. World Journal of Surgery, 28, 721–726.
   PubMed Web of Science ®Google Scholar
• Wischhusen, J., Naumann, U., Ohgaki, H., Rastinejad, F., & Weller, M. (2003). CP-31398, a novel p53-stabilizing agent, induces p53-dependent and p53-independent glioma cell death. Oncogene, 22, 8233–8245.
   PubMed Web of Science ®Google Scholar
• Wong, R. P., Tsang, W. P., Chau, P. Y., Co, N. N., Tsang, T. Y., & Kwok, T. T. (2007). p53-R273H gains new function in induction of drug resistance through down-regulation of procaspase-3. Molecular Cancer Therapeutics, 6, 1054–1061.
   PubMed Web of Science ®Google Scholar
• Xu, W. S., Parmigiani, R. B., & Marks, P. A. (2007). Histone deacetylase inhibitors: Molecular mechanisms of action. Oncogene, 26, 5541–5552.
   PubMed Web of Science ®Google Scholar
• Yan, W., Liu, S., Xu, E., Zhang, J., Zhang, Y., Chen, X., & Chen, X. (2013). Histone deacetylase inhibitors suppress mutant p53 transcription via histone deacetylase 8. Oncogene, 32, 599–609.
   PubMed Web of Science ®Google Scholar
• Zache, N., Lambert, J. M., Rökaeus, N., Shen, J., Hainaut, P., Bergman, J., & Bykov, V. J. (2008). Mutant p53 targeting by the low molecular weight compound STIMA-1. Molecular Oncology, 2, 70–80.
   PubMed Web of Science ®Google Scholar
• Zilfou, J. T., & Lowe, S. W. (2009). Tumor Suppressive Functions of p53, Cold Spring Harbor Perspectives in Biology (p. a001883).
   PubMed Web of Science ®Google Scholar