Promoter hypermethylation of cysteine dioxygenase type 1 in patients with non‑small cell lung cancer

Yin,Wei; Wang,Xiang; Li,Yunping; Wang,Bin; Song,Mingzhe; Hulbert,Alicia; Chen,Chen; Yu,Fenglei

doi:10.3892/ol.2020.11592

Promoter hypermethylation of cysteine dioxygenase type 1 in patients with non‑small cell lung cancer

Authors:
- Wei Yin
- Xiang Wang
- Yunping Li
- Bin Wang
- Mingzhe Song
- Alicia Hulbert
- Chen Chen
- Fenglei Yu
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Affiliations: Department of Thoracic Surgery, The Second Xiangya Hospital of Central South University, Changsha, Hunan 410011, P.R. China, Department of Ophthalmology, The Second Xiangya Hospital of Central South University, Changsha, Hunan 410011, P.R. China, Department of Surgery, University of Illinois at Chicago School of Medicine, Chicago, IL 60607, USA
Published online on: May 6, 2020 https://doi.org/10.3892/ol.2020.11592
Pages: 967-973

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Abstract

In the present study, promoter hypermethylation of cysteine dioxygenase type 1 (CDO1) was evaluated in non‑small cell lung cancer (NSCLC) tissues to assess the value of CDO1 as a novel biomarker to improve the diagnosis of NSCLC. Tumor tissue samples and corresponding normal lung tissue samples from 42 patients with NSCLC were obtained at the Department of Thoracic Surgery, The Second Xiangya Hospital (Changsha, China). Conventional methylation‑specific PCR (cMSP) and methylation‑on‑beads followed by quantitative methylation‑specific PCR (MOB‑qMSP) were used to analyze the tumor and normal lung tissue samples. Using these two methods, promoter DNA hypermethylation of the CDO1 gene was detected in 59.4 and 71.0% of tumor tissues of patients with NSCLC and in 9.4 and 0% of normal lung tissue, respectively. Compared with the rate of methylation in the well‑differentiated NSCLC tissues (15.4 and 55.6%, respectively), the rate of CDO1 gene promoter methylation was higher in the poorly differentiated tissues (89.5 and 92.3%, respectively). Overall, it was demonstrated that the MOB‑qMSP method had a higher positive detection rate for CDO1 hypermethylation compared with the cMSP method. In conclusion, CDO1 gene promoter hypermethylation was more frequently observed in NSCLC tissues compared with in normal lung tissues, and a high methylation frequency of the CDO1 gene in biopsy specimens of NSCLC was associated with the degree of differentiation.

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1	Ferlay J, Soerjomataram I, Dikshit R, Eser S, Mathers C, Rebelo M, Parkin DM, Forman D and Bray F: Cancer incidence and mortality worldwide: Sources, methods and major patterns in GLOBOCAN 2012. Int J Cancer. 136:E359–E386. 2015. View Article : Google Scholar : PubMed/NCBI
2	Chen W, Zheng R, Baade PD, Zhang S, Zeng H, Bray F, Jemal A, Yu XQ and He J: Cancer statistics in China, 2015. CA Cancer J Clin. 66:115–132. 2016. View Article : Google Scholar : PubMed/NCBI
3	Wender R, Fontham ET, Barrera E Jr, Colditz GA, Church TR, Ettinger DS, Etzioni R, Flowers CR, Gazelle GS, Kelsey DK, et al: American Cancer Society lung cancer screening guidelines. CA Cancer J Clin. 63:107–117. 2013. View Article : Google Scholar : PubMed/NCBI
4	Miller KD, Siegel RL, Lin CC, Mariotto AB, Kramer JL, Rowland JH, Stein KD, Alteri R and Jemal A: Cancer treatment and survivorship statistics, 2016. CA Cancer J Clin. 66:271–289. 2016. View Article : Google Scholar : PubMed/NCBI
5	Sharma S, Kelly TK and Jones PA: Epigenetics in cancer. Carcinogenesis. 31:27–36. 2010. View Article : Google Scholar : PubMed/NCBI
6	Sandoval J, Peiró-Chova L, Pallardó FV and García-Giménez JL: Epigenetic biomarkers in laboratory diagnostics: Emerging approaches and opportunities. Expert Rev Mol Diagn. 13:457–471. 2013. View Article : Google Scholar : PubMed/NCBI
7	Kim Y and Kim D-H: CpG island hypermethylation as a biomarker for the early detection of lung cancer. Cancer Epigenetics. Humana Press. (NY, USA). 141–171. 2015. View Article : Google Scholar
8	Leygo C, Williams M, Jin HC, Chan MWY, Chu WK, Grusch M and Cheng YY: DNA methylation as a noninvasive epigenetic biomarker for the detection of cancer. Dis Markers. 2017:37265952017. View Article : Google Scholar : PubMed/NCBI
9	Herman JG, Graff JR, Myöhänen S, Nelkin BD and Baylin SB: Methylation-specific PCR: A novel PCR assay for methylation status of CpG islands. Proc Natl Acad Sci USA. 93:9821–9826. 1996. View Article : Google Scholar : PubMed/NCBI
10	Navarro E, Serrano-Heras G, Castaño MJ and Solera J: Real-time PCR detection chemistry. Clin Chim Acta. 439:231–250. 2015. View Article : Google Scholar : PubMed/NCBI
11	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. 23:1998–2005. 2017. View Article : Google Scholar : PubMed/NCBI
12	Brait M, Ling S, Nagpal JK, Chang X, Park HL, Lee J, Okamura J, Yamashita K, Sidransky D and Kim MS: Cysteine dioxygenase 1 is a tumor suppressor gene silenced by promoter methylation in multiple human cancers. PLoS One. 7:e449512012. View Article : Google Scholar : PubMed/NCBI
13	Minatani N, Waraya M, Yamashita K, Kikuchi M, Ushiku H, Kojo K, Ema A, Nishimiya H, Kosaka Y, Katoh H, et al: Prognostic significance of promoter DNA hypermethylation of cysteine dioxygenase 1 (CDO1) gene in primary breast cancer. PLoS One. 11:e01448622016. View Article : Google Scholar : PubMed/NCBI
14	Choi JI, Cho E-H, Kim SB, Kim R, Kwon J, Park M, Shin HJ, Ryu HS, Park SH and Lee KH: Promoter methylation of cysteine dioxygenase type 1: Gene silencing and tumorigenesis in hepatocellular carcinoma. Ann Hepatobiliary Pancreat Surg. 21:181–187. 2017. View Article : Google Scholar : PubMed/NCBI
15	Igarashi K, Yamashita K, Katoh H, Kojima K, Ooizumi Y, Nishizawa N, Nishiyama R, Kawamata H, Tajima H, Kaizu T, et al: Prognostic significance of promoter DNA hypermethylation of the cysteine dioxygenase 1 (CDO1) gene in primary gallbladder cancer and gallbladder disease. PLoS One. 12:e01881782017. View Article : Google Scholar : PubMed/NCBI
16	Vedeld HM, Andresen K, Eilertsen IA, Nesbakken A, Seruca R, Gladhaug IP, Thiis-Evensen E, Rognum TO, Boberg KM and Lind GE: The novel colorectal cancer biomarkers CDO1, ZSCAN18 and ZNF331 are frequently methylated across gastrointestinal cancers. Int J Cancer. 136:844–853. 2015. View Article : Google Scholar : PubMed/NCBI
17	Meller S, Zipfel L, Gevensleben H, Dietrich J, Ellinger J, Majores M, Stein J, Sailer V, Jung M, Kristiansen G, et al: CDO1 promoter methylation is associated with gene silencing and is a prognostic biomarker for biochemical recurrence-free survival in prostate cancer patients. Epigenetics. 11:871–880. 2016. View Article : Google Scholar : PubMed/NCBI
18	Kwon J, Park M, Kim JH, Lee HW, Kang MC and Park JH: Epigenetic regulation of the novel tumor suppressor cysteine dioxygenase 1 in esophageal squamous cell carcinoma. Tumour Biol. 36:7449–7456. 2015. View Article : Google Scholar : PubMed/NCBI
19	Feng N, Wang Y, Zheng M, Yu X, Lin H, Ma RN, Shi O, Zheng X, Gao M, Yu H, et al: Genome-wide analysis of DNA methylation and their associations with long noncoding RNA/mRNA expression in non-small-cell lung cancer. Epigenomics. 9:137–153. 2017. View Article : Google Scholar
20	Goldstraw P, Chansky K, Crowley J, Rami-Porta R, Asamura H, Eberhardt WE, Nicholson AG, Groome P, Mitchell A, Bolejack V, et al; International Association for the Study of Lung Cancer Staging and Prognostic Factors Committee, Advisory Boards, Participating Institutions; International Association for the Study of Lung Cancer Staging and Prognostic Factors Committee Advisory Boards and Participating Institutions, . The IASLC Lung Cancer Staging Project: Proposals for Revision of the TNM Stage Groupings in the Forthcoming (Eighth) Edition of the TNM Classification for Lung Cancer. J Thorac Oncol. 11:39–51. 2016. View Article : Google Scholar : PubMed/NCBI
21	Kwon YJ, Lee SJ, Koh JS, Kim SH, Lee HW, Kang MC, Bae JB, Kim YJ and Park JH: Genome-wide analysis of DNA methylation and the gene expression change in lung cancer. J Thorac Oncol. 7:20–33. 2012. View Article : Google Scholar : PubMed/NCBI
22	Wrangle J, Machida EO, Danilova L, Hulbert A, Franco N, Zhang W, Glöckner SC, Tessema M, Van Neste L, Easwaran H, et al: Functional identification of cancer-specific methylation of CDO1, HOXA9, and TAC1 for the diagnosis of lung cancer. Clin Cancer Res. 20:1856–1864. 2014. View Article : Google Scholar : PubMed/NCBI
23	Ooki A, Maleki Z, Tsay JJ, Goparaju C, Brait M, Turaga N, Nam HS, Rom WN, Pass HI, Sidransky D, et al: A Panel of Novel Detection and Prognostic Methylated DNA Markers in Primary Non-Small Cell Lung Cancer and Serum DNA. Clin Cancer Res. 23:7141–7152. 2017. View Article : Google Scholar : PubMed/NCBI
24	Diaz-Lagares A, Mendez-Gonzalez J, Hervas D, Saigi M, Pajares MJ, Garcia D, Crujerias AB, Pio R, Montuenga LM, Zulueta J, et al: A Novel Epigenetic Signature for Early Diagnosis in Lung Cancer. Clin Cancer Res. 22:3361–3371. 2016. View Article : Google Scholar : PubMed/NCBI
25	Brait M, Ling S, Nagpal JK, Chang X, Park HL, Lee J, Okamura J, Yamashita K, Sidransky D and Kim MS: Cysteine dioxygenase 1 is a tumor suppressor gene silenced by promoter methylation in multiple human cancers. PLoS One. 7:e449512012. View Article : Google Scholar : PubMed/NCBI
26	Ramalho-Carvalho J, Henrique R and Jerónimo C: Methylation-specific PCR. DNA Methylation Protocols. 1708. Tost J: Springer, Humana Press; New York, NY: pp. 447–472. 2018, View Article : Google Scholar
27	Holmes EE, Jung M, Meller S, Leisse A, Sailer V, Zech J, Mengdehl M, Garbe LA, Uhl B, Kristiansen G, et al: Performance evaluation of kits for bisulfite-conversion of DNA from tissues, cell lines, FFPE tissues, aspirates, lavages, effusions, plasma, serum, and urine. PLoS One. 9:e939332014. View Article : Google Scholar : PubMed/NCBI
28	López-Otín C, Blasco MA, Partridge L, Serrano M and Kroemer G: The hallmarks of aging. Cell. 153:1194–1217. 2013. View Article : Google Scholar : PubMed/NCBI
29	Derhovanessian E, Solana R, Larbi A and Pawelec G: Immunity, ageing and cancer. Immun Ageing. 5:112008. View Article : Google Scholar : PubMed/NCBI
30	Rodier F and Campisi J: Four faces of cellular senescence. J Cell Biol. 192:547–556. 2011. View Article : Google Scholar : PubMed/NCBI
31	Bakulski KM and Fallin MDJE: Epigenetic epidemiology: Promises for public health research. Environ Mol Mutagen. 55:171–183. 2014. View Article : Google Scholar : PubMed/NCBI
32	Levine ME, Hosgood HD, Chen B, Absher D, Assimes T and Horvath S: DNA methylation age of blood predicts future onset of lung cancer in the women's health initiative. Aging (Albany NY). 7:690–700. 2015. View Article : Google Scholar : PubMed/NCBI
33	Breitling LP, Yang R, Korn B, Burwinkel B and Brenner H: Tobacco-smoking-related differential DNA methylation: 27K discovery and replication. Am J Hum Genet. 88:450–457. 2011. View Article : Google Scholar : PubMed/NCBI