Salivary DNA Methylation as an Epigenetic Biomarker for Head and Neck Cancer. Part II: A Cancer Risk Meta-Analysis
Abstract
:1. Introduction
2. Materials and Methods
2.1. Protocol and Registration
2.2. Search Strategy, Study Selection, and Data Extraction
2.3. Selection Criteria
2.4. Assessment of Study Quality
2.5. Statistical Analysis
3. Results
3.1. Study Selection and Characteristics of Included Studies
3.2. Study Quality
3.3. Association between Salivary DNA Promoter Hypermethylation and HNC Risk
3.4. Meta-Regression and Subgroup Analysis
3.5. Association between p16 Promoter Hypermethylation and HNC Risk
3.6. Association between MGMT Promoter Hypermethylation and HNC Risk
3.7. Association between DAPK Promoter Hypermethylation and HNC Risk
3.8. Association between TIMP3 Promoter Hypermethylation and HNC Risk
3.9. Association between RASSF1A Promoter Hypermethylation and HNC Risk
3.10. Association between APC Promoter Hypermethylation and HNC Risk
4. Discussion
5. Conclusions
Supplementary Materials
Author Contributions
Funding
Institutional Review Board Statement
Informed Consent Statement
Conflicts of Interest
References
- Castilho, R.M.; Squarize, C.H.; Almeida, L.O. Epigenetic modifications and head and neck cancer: Implications for tumor progression and resistance to therapy. Int. J. Mol. Sci. 2017, 18, 1506. [Google Scholar] [CrossRef] [PubMed]
- Pfeifer, G.P. Defining driver DNA methylation changes in human cancer. Int. J. Mol. Sci. 2018, 19, 1166. [Google Scholar] [CrossRef] [Green Version]
- Laird, P.W. The power and the promise of DNA methylation markers. Nat. Rev. Cancer 2003, 3, 253–266. [Google Scholar] [CrossRef]
- Hulbert, A.; Jusue-Torres, I.; Stark, A.; Chen, C.; Rodgers, K.; Lee, B.; Griffin, C.; Yang, A.; Huang, P.; Wrangle, J.; et al. Early detection of lung cancer using DNA promoter hypermethylation in plasma and sputum. Clin. Cancer Res. 2017, 23, 1998–2005. [Google Scholar] [CrossRef] [Green Version]
- Patai, Á.V.; Valcz, G.; Hollósi, P.; Kalmár, A.; Peterfia, B.; Wichmann, B.; Spisák, S.; Barták, B.K.; Leiszter, K.; Tóth, K.; et al. Comprehensive DNA methylation analysis reveals a common ten-gene methylation signature in colorectal adenomas and carcinomas. PLoS ONE 2015, 10, e0133836. [Google Scholar] [CrossRef]
- Glodzik, D.; Bosch, A.; Hartman, J.; Aine, M.; Vallon-Christersson, J.; Reuterswärd, C.; Karlsson, A.; Mitra, S.; Niméus, E.; Holm, K.; et al. Comprehensive molecular comparison of BRCA1 hypermethylated and BRCA1 mutated triple negative breast cancers. Nat. Commun. 2020, 11, 1–15. [Google Scholar] [CrossRef]
- Chou, J.L.; Huang, R.L.; Shay, J.; Chen, L.Y.; Lin, S.J.; Yan, P.S.; Chao, W.T.; Lai, Y.H.; Lai, Y.L.; Chao, T.K.; et al. Hypermethylation of the TGF-β target, ABCA1 is associated with poor prognosis in ovarian cancer patients. Clin. Epigenet. 2015, 7, 1. [Google Scholar] [CrossRef] [PubMed] [Green Version]
- Gaździcka, J.; Gołąbek, K.; Strzelczyk, J.K.; Ostrowska, Z. Epigenetic modifications in head and neck cancer. Biochem. Genet. 2020, 58, 213–244. [Google Scholar] [CrossRef] [PubMed] [Green Version]
- Schröck, A.; Leisse, A.; De Vos, L.; Gevensleben, H.; Dröge, F.; Franzen, A.; Wachendörfer, M.; Schröck, F.; Ellinger, J.; Teschke, M.; et al. Free-circulating methylated DNA in blood for diagnosis, staging, prognosis, and monitoring of head and neck squamous cell carcinoma patients: An observational prospective cohort study. Clin. Chem. 2017, 63, 1288–1296. [Google Scholar] [CrossRef] [PubMed]
- Liyanage, C.; Wathupola, A.; Muraleetharan, S.; Perera, K.; Punyadeera, C.; Udagama, P. Promoter hypermethylation of tumor-suppressor genes p16INK4a, RASSF1A, TIMP3, and PCQAP/MED15 in salivary DNA as a quadruple biomarker panel for early detection of oral and oropharyngeal cancers. Biomolecules 2019, 9, 148. [Google Scholar] [CrossRef] [PubMed] [Green Version]
- Sanchez-Cespedes, M.; Esteller, M.; Wu, L.; Nawroz-Danish, H.; Yoo, G.H.; Koch, W.M.; Jen, J.; Herman, J.G.; Sidransky, D. Gene promoter hypermethylation in tumors and serum of head and neck cancer patients. Cancer Res. 2000, 60, 892–895. [Google Scholar]
- McInnes, M.; Moher, D.; Thombs, B.D.; McGrath, T.A.; Bossuyt, P.M.; Clifford, T.; Cohen, J.F.; Deeks, J.J.; Gatsonis, C.; Hooft, L.; et al. Preferred Reporting Items for a Systematic Review and Meta-analysis of Diagnostic Test Accuracy Studies. JAMA 2018, 319, 388–396. [Google Scholar] [CrossRef] [PubMed]
- Rapado-González, Ó.; Martínez-Reglero, C.; Salgado-Barreira, Á.; Muinelo-Romay, L.; Muinelo-Lorenzo, J.; López-López, R.; Díaz-Lagares, Á.; Suárez-Cunqueiro, M. Salivary DNA methylation as an epigenetic biomarker for head and neck cancer. Part I: A diagnostic accuracy meta-analysis. J. Pers. Med. 2021, 11, 568. [Google Scholar] [CrossRef]
- Wells, G.A.; Shea, B.; O’Connell, D.; Peterson, J.; Welch, V.; Losos, M.; Tugwell, P. The Newcastle-Ottawa Scale (NOS) for assessing the quality of nonrandomized studies in meta-analysis. Available online: http://www.ohri.ca/programs/clinical_epidemiology/oxford.asp (accessed on 16 December 2019).
- Egger, M.; Smith, G.D.; Schneider, M.; Minder, C. Bias in meta-analysis detected by a simple, graphical test. BMJ 1997, 315, 629–634. [Google Scholar] [CrossRef] [Green Version]
- Begg, C.B.; Mazumdar, M. Operating characteristics of a rank correlation test for publication bias. Biometrics 1994, 50, 1088. [Google Scholar] [CrossRef] [PubMed]
- Guerrero-Preston, R.; Soudry, E.; Acero, J.; Orera, M.; Moreno-López, L.A.; Macía-Colón, G.; Jaffe, A.; Berdasco, M.; Ili, C.; Brebi-Mieville, P.; et al. NID2 and HOXA9 promoter hypermethylation as biomarkers for prevention and early detection in oral cavity squamous cell carcinoma tissues and saliva. Cancer Prev. Res. 2011, 4, 1061–1072. [Google Scholar] [CrossRef] [PubMed] [Green Version]
- Claus, R.; Wilop, S.; Hielscher, T.; Sonnet, M.; Dahl, E.; Galm, O.; Jost, E.; Plass, C. A systematic comparison of quantitative high-resolution DNA methylation analysis and methylation-specific PCR. Epigenetics 2012, 7, 772–780. [Google Scholar] [CrossRef] [Green Version]
- Lee, E.-S.; Issa, J.-P.; Roberts, D.B.; Williams, M.D.; Weber, R.S.; Kies, M.S.; El-Naggar, A.K. Quantitative promoter hypermethylation analysis of cancer-related genes in salivary gland carcinomas: Comparison with methylation-specific PCR technique and clinical significance. Clin. Cancer Res. 2008, 14, 2664–2672. [Google Scholar] [CrossRef] [Green Version]
- Padhi, S.S.; Roy, S.; Kar, M.; Saha, A.; Roy, S.; Adhya, A.; Baisakh, M.; Banerjee, B. Role of CDKN2A/p16 expression in the prognostication of oral squamous cell carcinoma. Oral Oncol. 2017, 73, 27–35. [Google Scholar] [CrossRef]
- Kulkarni, V.; Saranath, D. Concurrent hypermethylation of multiple regulatory genes in chewing tobacco associated oral squamous cell carcinomas and adjacent normal tissues. Oral Oncol. 2004, 40, 145–153. [Google Scholar] [CrossRef]
- Su, P.F.; Huang, W.L.; Wu, H.T.; Wu, C.H.; Liu, T.Y.; Kao, S.Y. p16INK4A promoter hypermethylation is associated with invasiveness and prognosis of oral squamous cell carcinoma in an age-dependent manner. Oral Oncol. 2010, 46, 734–739. [Google Scholar] [CrossRef] [PubMed]
- Shi, H.; Chen, X.; Lu, C.; Gu, C.; Jiang, H.; Meng, R.; Niu, X.; Huang, Y.; Lu, M. Association between P16INK4a promoter methylation and HNSCC: A meta-analysis of 21 published studies. PLoS ONE 2015, 10, e0122302. [Google Scholar] [CrossRef] [Green Version]
- Zhou, C.; Shen, Z.; Ye, D.; Li, Q.; Deng, H.; Liu, H.; Li, J. The association and clinical significance of CDKN2A promoter methylation in head and neck squamous cell carcinoma: A meta-analysis. Cell. Physiol. Biochem. 2018, 50, 868–882. [Google Scholar] [CrossRef]
- Zhao, J.J.; Li, H.Y.; Wang, D.; Yao, H.; Sun, D.W. Abnormal MGMT promoter methylation may contribute to the risk of esophageal cancer: A meta-analysis of cohort studies. Tumor Biol. 2014, 35, 10085–10093. [Google Scholar] [CrossRef] [PubMed]
- Matsuda, S.; Mafune, A.; Kohda, N.; Hama, T.; Urashima, M. Associations among smoking, MGMT hypermethylation, TP53-mutations, and relapse in head and neck squamous cell carcinoma. PLoS ONE 2020, 15, e0231932. [Google Scholar] [CrossRef] [PubMed]
- Zuo, C.; Ai, L.; Ratliff, P.; Suen, J.Y.; Hanna, E.; Brent, T.P.; Fan, C.Y. O6-methylguanine-DNA methyltransferase gene: Epigenetic silencing and prognostic value in head and neck squamous cell carcinoma. Cancer Epidemiol. Biomark. Prev. 2004, 13, 967–975. [Google Scholar]
- Cohen, O.; Kimchi, A. DAP-kinase: From functional gene cloning to establishment of its role in apoptosis and cancer. Cell Death Differ. 2001, 8, 6–15. [Google Scholar] [CrossRef] [Green Version]
- Šupić, G.; Kozomara, R.; Branković-Magić, M.; Jović, N.; Magić, Z. Gene hypermethylation in tumor tissue of advanced oral squamous cell carcinoma patients. Oral Oncol. 2009, 45, 1051–1057. [Google Scholar] [CrossRef]
- Dammann, R.H.; Steinmann, K.; Sandner, A.; Schagdarsurengin, U. Frequent promoter hypermethylation of tumor-related genes in head and neck squamous cell carcinoma. Oncol. Rep. 2009, 22, 1519–1526. [Google Scholar] [CrossRef] [Green Version]
- Cai, F.; Xiao, X.; Niu, X.; Zhong, Y. Association between promoter methylation of DAPK gene and HNSCC: A meta-analysis. PLoS ONE 2017, 12, e0173194. [Google Scholar] [CrossRef]
- Su, C.W.; Lin, C.W.; Yang, W.E.; Yang, S.F. TIMP-3 as a therapeutic target for cancer. Ther. Adv. Med. Oncol. 2019, 11. [Google Scholar] [CrossRef] [Green Version]
- Rettori, M.M.; De Carvalho, A.C.; Longo, A.L.B.; De Oliveira, C.Z.; Kowalski, L.P.; Carvalho, A.L.; Vettore, A.L. TIMP3 and CCNA1 hypermethylation in HNSCC is associated with an increased incidence of second primary tumors. J. Transl. Med. 2013, 11, 316. [Google Scholar] [CrossRef] [Green Version]
- Sun, W.; Zaboli, D.; Wang, H.; Liu, Y.; Arnaoutakis, D.; Khan, T.; Khan, Z.; Koch, W.M.; Califano, J.A. Detection of TIMP3 promoter hypermethylation in salivary rinse as an independent predictor of local recurrence-free survival in head and neck cancer. Clin. Cancer Res. 2012, 18, 1082–1091. [Google Scholar] [CrossRef] [Green Version]
- Dubois, F.; Bergot, E.; Zalcman, G.; Levallet, G. RASSF1A, puppeteer of cellular homeostasis, fights tumorigenesis, and metastasis—An updated review. Cell Death Dis. 2019, 10, 1–13. [Google Scholar] [CrossRef]
- Raos, D.; Ulamec, M.; Bojanac, A.K.; Bulic-Jakus, F.; Jezek, D.; Sincic, N. Epigenetically inactivated RASSF1A as a tumor biomarker. Bosn. J. Basic Med. Sci. 2020. [Google Scholar] [CrossRef]
- Meng, R.W.; Li, Y.C.; Chen, X.; Huang, Y.X.; Shi, H.; Du, D.D.; Niu, X.; Lu, C.; Lu, M.X. Aberrant methylation of RASSF1A closely associated with HNSCC, a meta-Analysis. Sci. Rep. 2016, 6, 20756. [Google Scholar] [CrossRef] [Green Version]
- Zhang, L.; Shay, J.W. Multiple roles of APC and its therapeutic implications in colorectal cancer. J. Natl. Cancer Inst. 2017, 109, 109. [Google Scholar] [CrossRef] [PubMed] [Green Version]
- Uesugi, H.; Uzawa, K.; Kawasaki, K.; Shimada, K.; Moriya, T.; Tada, A.; Shiiba, M.; Tanzawa, H. Status of reduced expression and hypermethylation of the APC tumor suppressor gene in human oral squamous cell carcinoma. Int. J. Mol. Med. 2005, 15, 597–602. [Google Scholar] [CrossRef] [PubMed]
- Rettori, M.M.; De Carvalho, A.C.; Longo, A.L.B.; De Oliveira, C.Z.; Kowalski, L.P.; Carvalho, A.; Vettore, A.L. Prognostic significance of TIMP3 hypermethylation in post-treatment salivary rinse from head and neck squamous cell carcinoma patients. Carcinogenesis 2012, 34, 20–27. [Google Scholar] [CrossRef] [PubMed] [Green Version]
- Nagata, S.; Hamada, T.; Yamada, N.; Yokoyama, S.; Kitamoto, S.; Kanmura, Y.; Nomura, M.; Kamikawa, Y.; Yonezawa, S.; Sugihara, K. Aberrant DNA methylation of tumor-related genes in oral rinse. Cancer 2012, 118, 4298–4308. [Google Scholar] [CrossRef]
- Righini, C.A.; De Fraipont, F.; Timsit, J.-F.; Faure, C.; Brambilla, E.; Reyt, E.; Favrot, M.-C. Tumor-specific methylation in saliva: A promising biomarker for early detection of head and neck cancer recurrence. Clin. Cancer Res. 2007, 13, 1179–1185. [Google Scholar] [CrossRef] [PubMed] [Green Version]
- López, F.; Sampedro, T.; Llorente, J.L.; Dominguez, F.; Hermsen, M.; Suárez, C.; Álvarez-Marcos, C. Utility of MS-MLPA in DNA methylation profiling in primary laryngeal squamous cell carcinoma. Oral Oncol. 2014, 50, 291–297. [Google Scholar] [CrossRef]
- Chen, K.; Sawhney, R.; Khan, M.; Benninger, M.S.; Hou, Z.; Sethi, S.; Stephen, J.K.; Worsham, M.J. Methylation of multiple genes as diagnostic and therapeutic markers in primary head and neck squamous cell carcinoma. Arch. Otolaryngol. Head Neck Surg. 2007, 133, 1131–1138. [Google Scholar] [CrossRef] [PubMed] [Green Version]
- Seike, M.; Gemma, A.; Hosoya, Y.; Hemmi, S.; Taniguchi, Y.; Fukuda, Y.; Yamanaka, N.; Kudoh, S. Increase in the frequency of p16INK4 gene inactivation by hypermethylation in lung cancer during the process of metastasis and its relation to the status of p53. Clin. Cancer Res. 2000, 6, 4307–4313. [Google Scholar] [PubMed]
- Wahab, A.H.A.; El-Mezayen, H.A.; Sharad, H.; Rahman, S.A. Promoter hypermethylation of RASSF1A, MGMT, and HIC-1 genes in benign and malignant colorectal tumors. Tumor Biol. 2011, 32, 845–852. [Google Scholar] [CrossRef] [PubMed]
- Masson, D.; Rioux-Leclercq, N.; Fergelot, P.; Jouan, F.; Mottier, S.; Théoleyre, S.; Bach-Ngohou, K.; Patard, J.J.; Denis, M. Loss of expression of TIMP3 in clear cell renal cell carcinoma. Eur. J. Cancer 2010, 46, 1430–1437. [Google Scholar] [CrossRef]
- Van Der Auwera, I.; Bovie, C.; Svensson, C.; Trinh, X.B.; Limame, R.; Van Dam, P.; Van Laere, S.J.; Van Marck, E.A.; Dirix, L.Y.; Vermeulen, P.B. Quantitative methylation profiling in tumor and matched morphologically normal tissues from breast cancer patients. BMC Cancer 2010, 10, 97. [Google Scholar] [CrossRef] [Green Version]
- Krassenstein, R.; Sauter, E.; Dulaimi, E.; Battagli, C.; Ehya, H.; Klein-Szanto, A.; Cairns, P. Detection of breast cancer in nipple aspirate fluid by CpG island hypermethylation. Clin. Cancer Res. 2004, 10, 28–32. [Google Scholar] [CrossRef] [PubMed] [Green Version]
- Mittag, F.; Kuester, D.; Vieth, M.; Peters, B.; Stolte, B.; Roessner, A.; Schneider-Stock, R. DAPK promotor methylation is an early event in colorectal carcinogenesis. Cancer Lett. 2006, 240, 69–75. [Google Scholar] [CrossRef]
- Belinsky, S.A.; Klinge, D.M.; Dekker, J.D.; Smith, M.W.; Bocklage, T.J.; Gilliland, F.D.; Crowell, R.E.; Karp, D.D.; Stidley, C.A.; Picchi, M.A. Gene promoter methylation in plasma and sputum increases with lung cancer risk. Clin. Cancer Res. 2005, 11, 6505–6511. [Google Scholar] [CrossRef] [Green Version]
- Shi, D.-T.; Han, M.; Gao, N.; Tian, W.; Chen, W. Association of RASSF1A promoter methylation with gastric cancer risk: A meta-analysis. Tumor Biol. 2013, 35, 943–948. [Google Scholar] [CrossRef] [PubMed]
- Chen, R.; Zheng, Y.; Zhuo, L.; Wang, S. Association between MGMT promoter methylation and risk of breast and gynecologic cancers: A systematic review and meta-Analysis. Sci. Rep. 2017, 7, 12783. [Google Scholar] [CrossRef] [Green Version]
- Cao, J.; Li, Z.; Yang, L.; Liu, C.; Luan, X. Association between tissue inhibitor of metalloproteinase-3 gene methylation and gastric cancer risk: A meta-Analysis. Genet. Test. Mol. Biomark. 2016, 20, 427–431. [Google Scholar] [CrossRef] [PubMed]
- Tang, B.; Li, Y.; Qi, G.; Yuan, S.; Wang, Z.; Yu, S.; Li, B.; He, S. Clinicopathological significance of cdkn2a promoter hypermethylation frequency with pancreatic cancer. Sci. Rep. 2015, 5, srep13563. [Google Scholar] [CrossRef] [PubMed] [Green Version]
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Rapado-González, Ó.; Martínez-Reglero, C.; Salgado-Barreira, Á.; Santos, M.A.; López-López, R.; Díaz-Lagares, Á.; Suárez-Cunqueiro, M.M. Salivary DNA Methylation as an Epigenetic Biomarker for Head and Neck Cancer. Part II: A Cancer Risk Meta-Analysis. J. Pers. Med. 2021, 11, 606. https://doi.org/10.3390/jpm11070606
Rapado-González Ó, Martínez-Reglero C, Salgado-Barreira Á, Santos MA, López-López R, Díaz-Lagares Á, Suárez-Cunqueiro MM. Salivary DNA Methylation as an Epigenetic Biomarker for Head and Neck Cancer. Part II: A Cancer Risk Meta-Analysis. Journal of Personalized Medicine. 2021; 11(7):606. https://doi.org/10.3390/jpm11070606
Chicago/Turabian StyleRapado-González, Óscar, Cristina Martínez-Reglero, Ángel Salgado-Barreira, María Arminda Santos, Rafael López-López, Ángel Díaz-Lagares, and María Mercedes Suárez-Cunqueiro. 2021. "Salivary DNA Methylation as an Epigenetic Biomarker for Head and Neck Cancer. Part II: A Cancer Risk Meta-Analysis" Journal of Personalized Medicine 11, no. 7: 606. https://doi.org/10.3390/jpm11070606