Methylation analysis of plasma cell-free DNA for breast cancer early detection using bisulfite next-generation sequencing

Tumor Biology

Volumn 37, Issue 10, 2016, Pages 13111-13119

  Li, Zibo ^a   Guo, Xinwu ^b   Tang, Lili ^a   Peng, Limin ^b   Chen, Ming ^b   Luo, Xipeng ^b   Wang, Shouman ^a   Xiao, Zhi ^a   Deng, Zhongping ^b,c,d   Dai, Lizhong ^b,c,d   Xia, Kun ^a   Wang, Jun ^a  

^a CENTRAL SOUTH UNIVERSITY   (China)

^b Sanway Gene Technology Inc   (China)

^c Research Center for Technologies of Nucleic Acid Based Diagnostics of Infectious Diseases and Cancer   (China)

^d Research Center for Technologies of Nucleic Acid Based Diagnostics and Therapeutics   (China)

Author keywords

Breast cancer; Cell free DNA; Methylation; Microfludic PCR; Next generation sequencing; Plasma

Indexed keywords

BIOLOGICAL MARKER; CIRCULATING CELL FREE DNA; DNA; EPIDERMAL GROWTH FACTOR RECEPTOR; PLATELET DERIVED GROWTH FACTOR BETA RECEPTOR; TRANSCRIPTION FACTOR SOX17; UNCLASSIFIED DRUG; WERNER SYNDROME ATP DEPENDENT HELICASE; HYDROGEN SULFITE; SULFITE; TUMOR MARKER;

ADULT; ARTICLE; BISULFITE SEQUENCING; BREAST CANCER; CANCER DIAGNOSIS; CANCER PATIENT; CONTROLLED STUDY; CPG ISLAND; DNA METHYLATION; EARLY DIAGNOSIS; FEMALE; HUMAN; HUMAN TISSUE; MAJOR CLINICAL STUDY; MICROFLUIDIC ANALYSIS; NEXT GENERATION SEQUENCING; NON INVASIVE MEASUREMENT; POLYMERASE CHAIN REACTION; PROMOTER REGION; QUANTITATIVE ANALYSIS; BLOOD; BREAST NEOPLASMS; CANCER STAGING; CASE CONTROL STUDY; CHEMISTRY; COMPARATIVE STUDY; EARLY CANCER DIAGNOSIS; GENETICS; HIGH THROUGHPUT SEQUENCING; MIDDLE AGED; PROCEDURES; PROGNOSIS;

BIOMARKERS, TUMOR; BREAST NEOPLASMS; CASE-CONTROL STUDIES; DNA METHYLATION; DNA, NEOPLASM; EARLY DETECTION OF CANCER; FEMALE; HIGH-THROUGHPUT NUCLEOTIDE SEQUENCING; HUMANS; MIDDLE AGED; NEOPLASM STAGING; PROGNOSIS; SULFITES;

EID: 84979620819     PISSN: 10104283     EISSN: 14230380     Source Type: Journal    
DOI: 10.1007/s13277-016-5190-z     Document Type: Article

References (41)

1. Torre LA, Bray F, Siegel RL, Ferlay J, Lortet-Tieulent J, Jemal A. Global cancer statistics, 2012. CA Cancer J Clin. 2015;65(2):87–108. doi:10.3322/caac.21262.
2. Fan L, Strasser-Weippl K, Li JJ, St Louis J, Finkelstein DM, Yu KD, Chen WQ, Shao ZM, Goss PE. Breast cancer in China. Lancet Oncol. 2014;15(7):e279–89. doi:10.1016/S1470-2045(13)70567-9.
3. Chen W, Zheng R, Baade PD, Zhang S, Zeng H, Bray F, Jemal A, Yu XQ, He J. Cancer statistics in China, 2015. CA Cancer J Clin. 2016. doi:10.3322/caac.21338.
4. Radpour R, Barekati Z, Kohler C, Lv Q, Burki N, Diesch C, Bitzer J, Zheng H, Schmid S, Zhong XY. Hypermethylation of tumor suppressor genes involved in critical regulatory pathways for developing a blood-based test in breast cancer. PLoS One. 2011;6(1):e16080. doi:10.1371/journal.pone.0016080.
5. Ogino S, Lochhead P, Chan AT, Nishihara R, Cho E, Wolpin BM, Meyerhardt JA, Meissner A, Schernhammer ES, Fuchs CS, Giovannucci E. Molecular pathological epidemiology of epigenetics: emerging integrative science to analyze environment, host, and disease. Modern Pathol Off J US Can Acad Pathol Inc. 2013;26(4):465–84. doi:10.1038/modpathol.2012.214.
6. Rhee JK, Kim K, Chae H, Evans J, Yan P, Zhang BT, Gray J, Spellman P, Huang TH, Nephew KP, Kim S. Integrated analysis of genome-wide DNA methylation and gene expression profiles in molecular subtypes of breast cancer. Nucleic Acids Res. 2013;41(18):8464–74. doi:10.1093/nar/gkt643.
7. Heyn H, Esteller M. DNA methylation profiling in the clinic: applications and challenges. Nat Rev Genet. 2012;13(10):679–92. doi:10.1038/nrg3270.
8. Noehammer C, Pulverer W, Hassler MR, Hofner M, Wielscher M, Vierlinger K, Liloglou T, McCarthy D, Jensen TJ, Nygren A, Gohlke H, Trooskens G, Braspenning M, Van Criekinge W, Egger G, Weinhaeusel A. Strategies for validation and testing of DNA methylation biomarkers. Epigenomics. 2014;6(6):603–22. doi:10.2217/epi.14.43.
9. Massihnia D, Perez A, Bazan V, Bronte G, Castiglia M, Fanale D, Barraco N, Cangemi A, Di Piazza F, Calo V, Rizzo S, Cicero G, Pantuso G, Russo A. A headlight on liquid biopsies: a challenging tool for breast cancer management. Tumour Biol J Int Soc Oncodev Biol Med. 2016. doi:10.1007/s13277-016-4856-x.
10. Crowley E, Di Nicolantonio F, Loupakis F, Bardelli A. Liquid biopsy: monitoring cancer-genetics in the blood. Nat Rev Clin Oncol. 2013;10(8):472–84. doi:10.1038/nrclinonc.2013.110.
11. Thakur BK, Zhang H, Becker A, Matei I, Huang Y, Costa-Silva B, Zheng Y, Hoshino A, Brazier H, Xiang J, Williams C, Rodriguez-Barrueco R, Silva JM, Zhang W, Hearn S, Elemento O, Paknejad N, Manova-Todorova K, Welte K, Bromberg J, Peinado H, Lyden D. Double-stranded DNA in exosomes: a novel biomarker in cancer detection. Cell Res. 2014;24(6):766–9. doi:10.1038/cr.2014.44.
12. Elshimali YI, Khaddour H, Sarkissyan M, Wu Y, Vadgama JV. The clinical utilization of circulating cell free DNA (CCFDNA) in blood of cancer patients. Int J Mol Sci. 2013;14(9):18925–58. doi:10.3390/ijms140918925.
13. Schwarzenbach H, Pantel K. Circulating DNA as biomarker in breast cancer. Breast Cancer Res: BCR. 2015;17(1):136. doi:10.1186/s13058-015-0645-5.
14. Fackler MJ, Lopez Bujanda Z, Umbricht C, Teo WW, Cho S, Zhang Z, Visvanathan K, Jeter S, Argani P, Wang C, Lyman JP, de Brot M, Ingle JN, Boughey J, McGuire K, King TA, Carey LA, Cope L, Wolff AC, Sukumar S. Novel methylated biomarkers and a robust assay to detect circulating tumor DNA in metastatic breast cancer. Cancer Res. 2014;74(8):2160–70. doi:10.1158/0008-5472.CAN-13-3392.
15. Guerrero-Preston R, Hadar T, Ostrow KL, Soudry E, Echenique M, Ili-Gangas C, Perez G, Perez J, Brebi-Mieville P, Deschamps J, Morales L, Bayona M, Sidransky D, Matta J. Differential promoter methylation of kinesin family member 1a in plasma is associated with breast cancer and DNA repair capacity. Oncol Rep. 2014;32(2):505–12. doi:10.3892/or.2014.3262.
16. Chan KC, Jiang P, Chan CW, Sun K, Wong J, Hui EP, Chan SL, Chan WC, Hui DS, Ng SS, Chan HL, Wong CS, Ma BB, Chan AT, Lai PB, Sun H, Chiu RW, Lo YM. Noninvasive detection of cancer-associated genome-wide hypomethylation and copy number aberrations by plasma DNA bisulfite sequencing. Proc Natl Acad Sci U S A. 2013;110(47):18761–8. doi:10.1073/pnas.1313995110.
17. Vaca-Paniagua F, Oliver J, Nogueira da Costa A, Merle P, McKay J, Herceg Z, Holmila R. Targeted deep DNA methylation analysis of circulating cell-free DNA in plasma using massively parallel semiconductor sequencing. Epigenomics. 2015;7(3):353–62. doi:10.2217/epi.14.94.
18. Li Z, Guo X, Wu Y, Li S, Yan J, Peng L, Xiao Z, Wang S, Deng Z, Dai L, Yi W, Xia K, Tang L, Wang J. Methylation profiling of 48 candidate genes in tumor and matched normal tissues from breast cancer patients. Breast Cancer Res Treat. 2015;149(3):767–79. doi:10.1007/s10549-015-3276-8.
19. Kampfrath T, Levinson SS. Brief critical review: statistical assessment of biomarker performance. Clin Chim Acta Int J Clin Chem. 2013;419:102–7. doi:10.1016/j.cca.2013.02.006.
20. Holdman XB, Welte T, Rajapakshe K, Pond A, Coarfa C, Mo Q, Huang S, Hilsenbeck SG, Edwards DP, Zhang X, Rosen JM. Upregulation of EGFR signaling is correlated with tumor stroma remodeling and tumor recurrence in FGFR1-driven breast cancer. Breast Cancer Res: BCR. 2015;17:141. doi:10.1186/s13058-015-0649-1.
21. Voss M, Paterson J, Kelsall IR, Martin-Granados C, Hastie CJ, Peggie MW, Cohen PT. Ppm1E is an in cellulo AMP-activated protein kinase phosphatase. Cell Signal. 2011;23(1):114–24. doi:10.1016/j.cellsig.2010.08.010.
22. Rodenhiser DI, Andrews J, Kennette W, Sadikovic B, Mendlowitz A, Tuck AB, Chambers AF. Epigenetic mapping and functional analysis in a breast cancer metastasis model using whole-genome promoter tiling microarrays. Breast Cancer Res: BCR. 2008;10(4):R62. doi:10.1186/bcr2121.
23. Rauscher GH, Kresovich JK, Poulin M, Yan L, Macias V, Mahmoud AM, Al-Alem U, Kajdacsy-Balla A, Wiley EL, Tonetti D, Ehrlich M. Exploring DNA methylation changes in promoter, intragenic, and intergenic regions as early and late events in breast cancer formation. BMC Cancer. 2015;15:816. doi:10.1186/s12885-015-1777-9.
24. Scartozzi M, Bearzi I, Mandolesi A, Giampieri R, Faloppi L, Galizia E, Loupakis F, Zaniboni A, Zorzi F, Biscotti T, Labianca R, Falcone A, Cascinu S. Epidermal growth factor receptor (EGFR) gene promoter methylation and cetuximab treatment in colorectal cancer patients. Br J Cancer. 2011;104(11):1786–90. doi:10.1038/bjc.2011.161.
25. Montero AJ, Diaz-Montero CM, Mao L, Youssef EM, Estecio M, Shen L, Issa JP. Epigenetic inactivation of EGFR by CpG island hypermethylation in cancer. Cancer Biol Ther. 2006;5(11):1494–501.
26. Weng X, Zhang H, Ye J, Kan M, Liu F, Wang T, Deng J, Tan Y, He L, Liu Y. Hypermethylated epidermal growth factor receptor (EGFR) promoter is associated with gastric cancer. Sci Report. 2015;5:10154. doi:10.1038/srep10154.
27. Varley KE, Mitra RD. Bisulfite patch PCR enables multiplexed sequencing of promoter methylation across cancer samples. Genome Res. 2010;20(9):1279–87. doi:10.1101/gr.101212.109.
28. Danese E, Minicozzi AM, Benati M, Montagnana M, Paviati E, Salvagno GL, Lima-Oliveira G, Gusella M, Pasini F, Lippi G, Guidi GC. Comparison of genetic and epigenetic alterations of primary tumors and matched plasma samples in patients with colorectal cancer. PLoS One. 2015;10(5):e0126417. doi:10.1371/journal.pone.0126417.
29. Fu D, Ren C, Tan H, Wei J, Zhu Y, He C, Shao W, Zhang J. Sox17 promoter methylation in plasma DNA is associated with poor survival and can be used as a prognostic factor in breast cancer. Medicine. 2015;94(11):e637. doi:10.1097/MD.0000000000000637.
30. Kloten V, Becker B, Winner K, Schrauder MG, Fasching PA, Anzeneder T, Veeck J, Hartmann A, Knuchel R, Dahl E. Promoter hypermethylation of the tumor-suppressor genes ITIH5, DKK3, and RASSF1A as novel biomarkers for blood-based breast cancer screening. Breast Cancer Res: BCR. 2013;15(1):R4. doi:10.1186/bcr3375.
31. Deng J, Liang H, Ying G, Dong Q, Zhang L, Yu J, Fan D, Hao X. Clinical significance of the methylated cytosine-phosphate-guanine sites of protocadherin-10 promoter for evaluating the prognosis of gastric cancer. J Am Coll Surg. 2014;219(5):904–13. doi:10.1016/j.jamcollsurg.2014.06.014.
32. Warton K, Lin V, Navin T, Armstrong NJ, Kaplan W, Ying K, Gloss B, Mangs H, Nair SS, Hacker NF, Sutherland RL, Clark SJ, Samimi G. Methylation-capture and next-generation sequencing of free circulating DNA from human plasma. BMC Genomics. 2014;15:476. doi:10.1186/1471-2164-15-476.
33. Redshaw N, Huggett JF, Taylor MS, Foy CA, Devonshire AS. Quantification of epigenetic biomarkers: an evaluation of established and emerging methods for DNA methylation analysis. BMC Genomics. 2014;15:1174. doi:10.1186/1471-2164-15-1174.
34. Yang R, Pfutze K, Zucknick M, Sutter C, Wappenschmidt B, Marme F, Qu B, Cuk K, Engel C, Schott S, Schneeweiss A, Brenner H, Claus R, Plass C, Bugert P, Hoth M, Sohn C, Schmutzler R, Bartram CR, Burwinkel B. DNA methylation array analyses identified breast cancer-associated HYAL2 methylation in peripheral blood. Int J Cancer J Int Cancer. 2015;136(8):1845–55. doi:10.1002/ijc.29205.
35. Harrison K, Hoad G, Scott P, Simpson L, Horgan GW, Smyth E, Heys SD, Haggarty P. Breast cancer risk and imprinting methylation in blood. Clin Epigenetics. 2015;7(1):92. doi:10.1186/s13148-015-0125-x.
36. Jing F, Yuping W, Yong C, Jie L, Jun L, Xuanbing T, Lihua H. CpG island methylator phenotype of multigene in serum of sporadic breast carcinoma. Tumour Biol J Int Soc Oncodev Biol Med. 2010;31(4):321–31. doi:10.1007/s13277-010-0040-x.
37. Yang P, Ma J, Zhang B, Duan H, He Z, Zeng J, Zeng X, Li D, Wang Q, Xiao Y, Liu C, Xiao Q, Chen L, Zhu X, Xing X, Li Z, Zhang S, Zhang Z, Ma L, Wang E, Zhuang Z, Zheng Y, Chen W. CpG site-specific hypermethylation of p16INK4alpha in peripheral blood lymphocytes of PAH-exposed workers. Cancer epidemiology, biomarkers & prevention: a publication of the American Association for Cancer Research, cosponsored by the American Society of Preventive Oncology. 2012;21(1):182–90. doi:10.1158/1055-9965.EPI-11-0784.
38. Moskalev EA, Jandaghi P, Fallah M, Manoochehri M, Botla SK, Kolychev OV, Nikitin EA, Bubnov VV, von Knebel DM, Strobel O, Hackert T, Buchler MW, Giese N, Bauer A, Muley T, Warth A, Schirmacher P, Haller F, Hoheisel JD, Riazalhosseini Y. GHSR DNA hypermethylation is a common epigenetic alteration of high diagnostic value in a broad spectrum of cancers. Oncotarget. 2015;6(6):4418–27. doi:10.18632/oncotarget.2759.
39. Sang Q, Li X, Wang H, Wang H, Zhang S, Feng R, Xu Y, Li Q, Zhao X, Xing Q, Jin L, He L, Wang L. Quantitative methylation level of the EPHX1 promoter in peripheral blood DNA is associated with polycystic ovary syndrome. PLoS One. 2014;9(2):e88013. doi:10.1371/journal.pone.0088013.
40. Wang D, Cui W, Wu X, Qu Y, Wang N, Shi B, Hou P. RUNX3 site-specific hypermethylation predicts papillary thyroid cancer recurrence. Am J Cancer Res. 2014;4(6):725–37.
41. van Vlodrop IJ, Niessen HE, Derks S, Baldewijns MM, van Criekinge W, Herman JG, van Engeland M. Analysis of promoter CpG island hypermethylation in cancer: location, location, location! Clin Cancer Res Off J Am Assoc Cancer Res. 2011;17(13):4225–31. doi:10.1158/1078-0432.CCR-10-3394.