Implications of Genetic and Epigenetic Alterations of CDKN2A (p16 INK4a ) in Cancer

Aguilo, 2011, Long noncoding RNA, polycomb, and the ghosts haunting INK4b-ARF-INK4a expression, Cancer Res., 71, 5365, 10.1158/0008-5472.CAN-10-4379 Alevizos, 2012, Review of the molecular profile and modern prognostic markers for gastric lymphoma: how do they affect clinical practice?, Can. J. Surg., 55, 117, 10.1503/cjs.002310 Al-Kaabi, 2014, p16INK4A and p14ARF gene promoter hypermethylation as prognostic biomarker in oral and oropharyngeal squamous cell carcinoma: a review, Dis. Markers, 2014, 260549, 10.1155/2014/260549 Ameri, 2011, Prognostic value of promoter hypermethylation of retinoic acid receptor beta (RARB) and CDKN2 (p16/MTS1) in prostate cancer, Chin. J. Cancer Res., 23, 306, 10.1007/s11670-011-0306-x Asokan, 2014, Promoter hypermethylation profile of tumour suppressor genes in oral leukoplakia and oral squamous cell carcinoma, J. Clin. Diagn. Res., 8, ZC09 Bhagat, 2014, Epigenetic alteration of p16 and retinoic acid receptor beta genes in the development of epithelial ovarian carcinoma, Tumour Biol., 35, 9069, 10.1007/s13277-014-2136-1 Bishop, 2013, Human papillomavirus-related carcinomas of the sinonasal tract, Am. J. Surg. Pathol., 37, 185, 10.1097/PAS.0b013e3182698673 Bostick, 2007, UHRF1 plays a role in maintaining DNA methylation in mammalian cells, Science, 317, 1760, 10.1126/science.1147939 Bracken, 2007, The Polycomb group proteins bind throughout the INK4A-ARF locus and are disassociated in senescent cells, Genes Dev., 21, 525, 10.1101/gad.415507 Cancer Genome Atlas, N., 2015, Comprehensive genomic characterization of head and neck squamous cell carcinomas, Nature, 517, 576, 10.1038/nature14129 Cao, 2002, Role of histone H3 lysine 27 methylation in Polycomb-group silencing, Science, 298, 1039, 10.1126/science.1076997 Ceol, 2011, The histone methyltransferase SETDB1 is recurrently amplified in melanoma and accelerates its onset, Nature, 471, 513, 10.1038/nature09806 Chan, 2002, CpG island methylation in aberrant crypt foci of the colorectum, Am. J. Pathol., 160, 1823, 10.1016/S0002-9440(10)61128-5 Chen, 2012, UVA-induced epigenetic regulation of P16(INK4a) in human epidermal keratinocytes and skin tumor derived cells, Photochem. Photobiol. Sci., 11, 180, 10.1039/C1PP05197K Chen, 2012, Aberrant DNA methylation of P16, MGMT, and hMLH1 genes in combination with MTHFR C677T genetic polymorphism and folate intake in esophageal squamous cell carcinoma, Asian Pac. J. Cancer Prev., 13, 5303, 10.7314/APJCP.2012.13.10.5303 Chung, 2015, Genomic alterations in head and neck squamous cell carcinoma determined by cancer gene-targeted sequencing, Ann. Oncol., 26, 1216, 10.1093/annonc/mdv109 Collado, 2007, Cellular senescence in cancer and aging, Cell, 130, 223, 10.1016/j.cell.2007.07.003 Collins, 1997, The cell cycle and cancer, Proc. Natl. Acad. Sci. U. S. A., 94, 2776, 10.1073/pnas.94.7.2776 Crea, 2009, Epigenetic mechanisms of irinotecan sensitivity in colorectal cancer cell lines, Mol. Cancer Ther., 8, 1964, 10.1158/1535-7163.MCT-09-0027 De Gruijl, 1999, Skin cancer and solar UV radiation, Eur. J. Cancer, 35, 2003, 10.1016/S0959-8049(99)00283-X Dulaimi, 2004, Promoter hypermethylation profile of kidney cancer, Clin. Cancer Res., 10, 3972, 10.1158/1078-0432.CCR-04-0175 Dyson, 1989, The human papilloma virus-16 E7 oncoprotein is able to bind to the retinoblastoma gene product, Science, 243, 934, 10.1126/science.2537532 El-Naggar, 1997, Methylation, a major mechanism of p16/CDKN2 gene inactivation in head and neck squamous carcinoma, Am. J. Pathol., 151, 1767 Fahey, 1997, Broccoli sprouts: an exceptionally rich source of inducers of enzymes that protect against chemical carcinogens, Proc. Natl. Acad. Sci. U. S. A., 94, 10367, 10.1073/pnas.94.19.10367 Feng, 2009, The transcription factor ZBP-89 suppresses p16 expression through a histone modification mechanism to affect cell senescence, FEBS J., 276, 4197, 10.1111/j.1742-4658.2009.07128.x Gil, 2006, Regulation of the INK4b-ARF-INK4a tumour suppressor locus: all for one or one for all, Nat. Rev. Mol. Cell Biol., 7, 667, 10.1038/nrm1987 Gillison, 2012, Tobacco smoking and increased risk of death and progression for patients with p16-positive and p16-negative oropharyngeal cancer, J. Clin. Oncol., 30, 2102, 10.1200/JCO.2011.38.4099 Gomez-Sanchez, 2013, Epigenetic induction of the Ink4a/Arf locus prevents Schwann cell overproliferation during nerve regeneration and after tumorigenic challenge, Brain, 136, 2262, 10.1093/brain/awt130 Gullett, 2010, Cancer prevention with natural compounds, Semin. Oncol., 37, 258, 10.1053/j.seminoncol.2010.06.014 Hanahan, 2011, Hallmarks of cancer: the next generation, Cell, 144, 646, 10.1016/j.cell.2011.02.013 Hassler, 2012, Antineoplastic activity of the DNA methyltransferase inhibitor 5-aza-2'-deoxycytidine in anaplastic large cell lymphoma, Biochimie, 94, 2297, 10.1016/j.biochi.2012.05.029 Hauptman, 2013, Long non-coding RNA in cancer, Int. J. Mol. Sci., 14, 4655, 10.3390/ijms14034655 He, 2015, Aberrant gene promoter methylation of p16, FHIT, CRBP1, WWOX, and DLC-1 in Epstein-Barr virus-associated gastric carcinomas, Med. Oncol., 32, 92, 10.1007/s12032-015-0525-y Hennessy, 2009, Ovarian cancer, Lancet, 374, 1371, 10.1016/S0140-6736(09)61338-6 Huang, 2007, Promoter hypermethylation of multiple genes in gastric lymphoma, Leuk. Lymphoma, 48, 1988, 10.1080/10428190701573224 Jayson, 2014, Ovarian cancer, Lancet, 384, 1376, 10.1016/S0140-6736(13)62146-7 Jiao, 2007, K-ras mutation and p16 and preproenkephalin promoter hypermethylation in plasma DNA of pancreatic cancer patients: in relation to cigarette smoking, Pancreas, 34, 55, 10.1097/01.mpa.0000246665.68869.d4 Jonsson, 2010, High frequency of p16(INK4A) promoter methylation in NRAS-mutated cutaneous melanoma, J. Investig. Dermatol., 130, 2809, 10.1038/jid.2010.216 Kensler, 2013, Keap1-nrf2 signaling: a target for cancer prevention by sulforaphane, Top. Curr. Chem., 329, 163, 10.1007/128_2012_339 Kim, 2010, Promoter methylation of specific genes is associated with the phenotype and progression of colorectal adenocarcinomas, Ann. Surg. Oncol., 17, 1767, 10.1245/s10434-009-0901-y Klajic, 2014, DNA methylation status of key cell-cycle regulators such as CDKNA2/p16 and CCNA1 correlates with treatment response to doxorubicin and 5-fluorouracil in locally advanced breast tumors, Clin. Cancer Res., 20, 6357, 10.1158/1078-0432.CCR-14-0297 Kobalka, 2015, p16INK4A expression is frequently increased in periorbital and ocular squamous lesions, Diagn. Pathol., 10, 175, 10.1186/s13000-015-0396-8 Kollmann, 2011, c-JUN prevents methylation of p16(INK4a) (and Cdk6): the villain turned bodyguard, Oncotarget, 2, 422, 10.18632/oncotarget.279 Kostaki, 2014, High-frequency p16(INK) (4A) promoter methylation is associated with histone methyltransferase SETDB1 expression in sporadic cutaneous melanoma, Exp. Dermatol., 23, 332, 10.1111/exd.12398 Kuwabara, 2011, Genetic pathways of multiple esophageal squamous cell carcinomas, Oncol. Rep., 25, 453 Lee, 2015, Different prognostic effect of CpG island methylation according to sex in colorectal cancer patients treated with adjuvant FOLFOX, Clin. Epigenetics, 7, 63, 10.1186/s13148-015-0106-0 Li, 2013, FOXA1 mediates p16(INK4a) activation during cellular senescence, EMBO J., 32, 858, 10.1038/emboj.2013.35 Li, 2013, Epigenetic regulation of multiple tumor-related genes leads to suppression of breast tumorigenesis by dietary genistein, PLoS One, 8, e54369, 10.1371/journal.pone.0054369 Liang, 2014, Integrative identification of Epstein-Barr virus-associated mutations and epigenetic alterations in gastric cancer, Gastroenterology, 147, 10.1053/j.gastro.2014.08.036 Majid, 2008, Genistein induces the p21WAF1/CIP1 and p16INK4a tumor suppressor genes in prostate cancer cells by epigenetic mechanisms involving active chromatin modification, Cancer Res., 68, 2736, 10.1158/0008-5472.CAN-07-2290 Marchetti, 1997, Alterations of P16 (MTS1) in node-positive non-small cell lung carcinomas, J. Pathol., 181, 178, 10.1002/(SICI)1096-9896(199702)181:2<178::AID-PATH741>3.0.CO;2-5 Markopoulos, 2012, Current aspects on oral squamous cell carcinoma, Open Dent. J., 6, 126, 10.2174/1874210601206010126 Matsusaka, 2014, DNA methylation in gastric cancer, related to Helicobacter pylori and Epstein-Barr virus, World J. Gastroenterol., 20, 3916, 10.3748/wjg.v20.i14.3916 Mclaughlin-Drubin, 2013, Tumor suppressor p16INK4A is necessary for survival of cervical carcinoma cell lines, Proc. Natl. Acad. Sci. U. S. A., 110, 16175, 10.1073/pnas.1310432110 Molyneux, 2012, Burkitt's lymphoma, Lancet, 379, 1234, 10.1016/S0140-6736(11)61177-X Moore, 2001, Genetic profile of 22 pancreatic carcinoma cell lines. Analysis of K-ras, p53, p16 and DPC4/Smad4, Virchows Arch., 439, 798, 10.1007/s004280100474 Munger, 2013, p16 in HPV-associated cancers, Oncotarget, 4, 1864, 10.18632/oncotarget.1523 Nabel, 2002, CDKs and CKIs: molecular targets for tissue remodelling, Nat. Rev. Drug Discov., 1, 587, 10.1038/nrd869 Nady, 2011, Recognition of multivalent histone states associated with heterochromatin by UHRF1 protein, J. Biol. Chem., 286, 24300, 10.1074/jbc.M111.234104 Nandakumar, 2011, (−)-Epigallocatechin-3-gallate reactivates silenced tumor suppressor genes, Cip1/p21 and p16INK4a, by reducing DNA methylation and increasing histones acetylation in human skin cancer cells, Carcinogenesis, 32, 537, 10.1093/carcin/bgq285 Nanni, 2006, Epithelial-restricted gene profile of primary cultures from human prostate tumors: a molecular approach to predict clinical behavior of prostate cancer, Mol. Cancer Res., 4, 79, 10.1158/1541-7786.MCR-05-0098 Nehls, 2008, p16 methylation does not affect protein expression in cervical carcinogenesis, Eur. J. Cancer, 44, 2496, 10.1016/j.ejca.2008.07.014 Ott, 2007, JunB is a gatekeeper for B-lymphoid leukemia, Oncogene, 26, 4863, 10.1038/sj.onc.1210285 Pauck, 2014, Depletion of the cdk inhibitor p16INK4a differentially affects proliferation of established cervical carcinoma cells, J. Virol., 88, 5256, 10.1128/JVI.03817-13 Peng, 2014, The relationship between P16 gene promoter methylation and gastric cancer: a meta-analysis based on Chinese patients, J. Cancer Res. Ther., 10, 292 Pomerantz, 1998, The Ink4a tumor suppressor gene product, p19Arf, interacts with MDM2 and neutralizes MDM2's inhibition of p53, Cell, 92, 713, 10.1016/S0092-8674(00)81400-2 Portela, 2010, Epigenetic modifications and human disease, Nat. Biotechnol., 28, 1057, 10.1038/nbt.1685 Qu, 2013, Gene methylation in gastric cancer, Clin. Chim. Acta, 424, 53, 10.1016/j.cca.2013.05.002 Quelle, 1995, Alternative reading frames of the INK4a tumor suppressor gene encode two unrelated proteins capable of inducing cell cycle arrest, Cell, 83, 993, 10.1016/0092-8674(95)90214-7 Qureshi, 2012, A novel p16(INK4A) mutation associated with esophageal squamous cell carcinoma in a high risk population, Biomarkers, 17, 552, 10.3109/1354750X.2012.699556 Rajendran, 2015, Nrf2 status affects tumor growth, HDAC3 gene promoter associations, and the response to sulforaphane in the colon, Clin. Epigenetics, 7, 102, 10.1186/s13148-015-0132-y Robaina, 2015, Quantitative analysis of CDKN2A methylation, mRNA, and p16(INK4a) protein expression in children and adolescents with Burkitt lymphoma: biological and clinical implications, Leuk. Res., 39, 248, 10.1016/j.leukres.2014.11.023 Salo-Mullen, 2015, Identification of germline genetic mutations in patients with pancreatic cancer, Cancer, 10.1002/cncr.29664 Sarkar, 2015, Epigenetic regulation in human melanoma: past and future, Epigenetics, 10, 103, 10.1080/15592294.2014.1003746 Sato, 2010, ANRIL is implicated in the regulation of nucleus and potential transcriptional target of E2F1, Oncol. Rep., 24, 701 Scandura, 2011, Phase 1 study of epigenetic priming with decitabine prior to standard induction chemotherapy for patients with AML, Blood, 118, 1472, 10.1182/blood-2010-11-320093 Scheffner, 1993, The HPV-16 E6 and E6-AP complex functions as a ubiquitin-protein ligase in the ubiquitination of p53, Cell, 75, 495, 10.1016/0092-8674(93)90384-3 Serrano, 1993, A new regulatory motif in cell-cycle control causing specific inhibition of cyclin D/CDK4, Nature, 366, 704, 10.1038/366704a0 Siegel, 2015, Cancer statistics, 2015, CA Cancer J. Clin., 65, 5, 10.3322/caac.21254 Tallen, 2014, Keep-ING balance: tumor suppression by epigenetic regulation, FEBS Lett., 588, 2728, 10.1016/j.febslet.2014.03.011 Tam, 2013, CDKN2A/p16 inactivation mechanisms and their relationship to smoke exposure and molecular features in non-small-cell lung cancer, J. Thorac. Oncol., 8, 1378, 10.1097/JTO.0b013e3182a46c0c Valdez, 2015, Comparison of the cytotoxicity of cladribine and clofarabine when combined with fludarabine and busulfan in AML cells: enhancement of cytotoxicity with epigenetic modulators, Exp. Hematol., 43, 10.1016/j.exphem.2015.02.001 Veganzones, 2015, Combined methylation of p16 and hMLH1 (CMETH2) discriminates a subpopulation with better prognosis in colorectal cancer patients with microsatellite instability tumors, Tumour Biol., 36, 3853, 10.1007/s13277-014-3027-1 Vidaurreta, 2008, Inactivation of p16 by CpG hypermethylation in renal cell carcinoma, Urol. Oncol., 26, 239, 10.1016/j.urolonc.2007.01.018 Wang, 2012, The acetylation of transcription factor HBP1 by p300/CBP enhances p16INK4A expression, Nucleic Acids Res., 40, 981, 10.1093/nar/gkr818 Wang, 2014, Role of p16 gene promoter methylation in gastric carcinogenesis: a meta-analysis, Mol. Biol. Rep., 41, 4481, 10.1007/s11033-014-3319-y Weinberg, 1995, The retinoblastoma protein and cell cycle control, Cell, 81, 323, 10.1016/0092-8674(95)90385-2 Wilson, 2010, Epigenetic antagonism between polycomb and SWI/SNF complexes during oncogenic transformation, Cancer Cell, 18, 316, 10.1016/j.ccr.2010.09.006 Witcher, 2009, Epigenetic silencing of the p16(INK4a) tumor suppressor is associated with loss of CTCF binding and a chromatin boundary, Mol. Cell, 34, 271, 10.1016/j.molcel.2009.04.001 Wu, 2007, The zinc finger repressor, ZBP-89, recruits histone deacetylase 1 to repress vimentin gene expression, Genes Cells, 12, 905, 10.1111/j.1365-2443.2007.01104.x Wu, 2013, Epigallocatechin-3-gallate and trichostatin A synergistically inhibit human lymphoma cell proliferation through epigenetic modification of p16INK4a, Oncol. Rep., 30, 2969, 10.3892/or.2013.2734 Yang, 2002, Molecular cloning of ESET, a novel histone H3-specific methyltransferase that interacts with ERG transcription factor, Oncogene, 21, 148, 10.1038/sj.onc.1204998 Yap, 2010, Molecular interplay of the noncoding RNA ANRIL and methylated histone H3 lysine 27 by polycomb CBX7 in transcriptional silencing of INK4a, Mol. Cell, 38, 662, 10.1016/j.molcel.2010.03.021 Yoruker, 2012, Promoter and histone methylation and p16(INK4A) gene expression in colon cancer, Exp. Ther. Med., 4, 865, 10.3892/etm.2012.683 Zhang, 2013, Epidemiology of esophageal cancer, World J. Gastroenterol., 19, 5598, 10.3748/wjg.v19.i34.5598 Zhang, 2014, FOXA1 antagonizes EZH2-mediated CDKN2A repression in carcinogenesis, Biochem. Biophys. Res. Commun., 453, 172, 10.1016/j.bbrc.2014.09.092 Zhang, 2010, Transcription factor ZBP-89 in cancer growth and apoptosis, Biochim. Biophys. Acta, 1806, 36