Novel methylation biomarker panel for the early detection of pancreatic cancer

Clinical Cancer Research

Volumn 19, Issue 23, 2013, Pages 6544-6555

  Yi, Joo Mi ^a,d   Guzzetta, Angela A ^b   Bailey, Vasudev J ^b   Downing, Stephanie R ^b   Neste, Leander Van ^c   Chiappinelli, Katherine B ^a   Keeley, Brian P ^b   Stark, Alejandro ^b   Herrera, Alexander ^b   Wolfgang, Christopher ^b   Pappou, Emmanouil P ^b   Iacobuzio Donahue, Christine A ^a   Goggins, Michael G ^a   Herman, James G ^a   Wang, Tza Huei ^a,b   Baylin, Stephen B ^a   Ahuja, Nita ^a,b  

^a DEPARTMENT OF PATHOLOGY   (United States)

^b JOHNS HOPKINS UNIVERSITY SCHOOL OF MEDICINE   (United States)

^c MDxHealth   (Belgium)

^d Dongnam Institute of Radiological and Medical Science   (South Korea)

Author keywords

[No Author keywords available]

Indexed keywords

ADAMTS1 PROTEIN; DNA; NANOPARTICLE; TRANSCRIPTOME; TUMOR MARKER;

ADAMTS1 GENE; ARTICLE; ASCL2 GENE; BNC1 GENE; BNIP3 GENE; CANCER CELL; CANCER GENETICS; CANCER STAGING; CONTROLLED STUDY; DISEASE MARKER; DNA METHYLATION; EARLY CANCER; EARLY DIAGNOSIS; EVL GENE; FEMALE; GENE; GENE EXPRESSION; GENE FREQUENCY; GENE IDENTIFICATION; HUMAN; HUMAN CELL; HUMAN TISSUE; MAJOR CLINICAL STUDY; MALE; PANCREAS CANCER; PNMT GENE; PRIORITY JOURNAL; SENSITIVITY AND SPECIFICITY; TFPI2 GENE; TWIST1 GENE;

ADAM PROTEINS; CARCINOMA IN SITU; CELL LINE, TUMOR; CELL MOVEMENT; CELL PROLIFERATION; CPG ISLANDS; DNA; DNA METHYLATION; DNA-BINDING PROTEINS; EARLY DETECTION OF CANCER; EPIGENESIS, GENETIC; FEMALE; GENE EXPRESSION PROFILING; GENE EXPRESSION REGULATION, NEOPLASTIC; HUMANS; MALE; MOLECULAR DIAGNOSTIC TECHNIQUES; PANCREATIC NEOPLASMS; PROMOTER REGIONS, GENETIC; PROPORTIONAL HAZARDS MODELS; SENSITIVITY AND SPECIFICITY; SEQUENCE ANALYSIS, DNA; TRANSCRIPTION FACTORS; TRANSCRIPTOME; TUMOR MARKERS, BIOLOGICAL;

EID: 84890276015     PISSN: 10780432     EISSN: 15573265     Source Type: Journal    
DOI: 10.1158/1078-0432.CCR-12-3224     Document Type: Article

References (59)

1. Jemal A, Siegel R, Ward E, Hao Y, Xu J, Thun MJ. Cancer statistics, 2009. CA Cancer J Clin 2009;59:225-49.
2. Klapman J, Malafa MP. Early detection of pancreatic cancer: why, who, and how to screen. Cancer Control 2008;15:280-7.
3. Siegel R, Ward E, Brawley O, Jemal A. Cancer statistics, 2011: the impact of eliminating socioeconomic and racial disparities on premature cancer deaths. A Cancer J Clin 2011;61:212-36.
4. Gemmel C, Eickhoff A, Helmstädter L, Riemann JF. Pancreatic cancer screening: state of the art. Expert Rev Gastroenterol Hepatol 2009;3:89-96.
5. Yeo CJ, Cameron JL, Sohn TA, Lillemoe KD, Pitt HA, Talamini MA, et al. Six hundred fifty consecutive pancreaticoduodenectomies in the 1990s: pathology, complications, and outcomes. Ann Surg 1997;226:248-57.
6. Winter JM, Cameron JL, Campbell KA, Arnold MA, Chang DC, Coleman J, et al. 1423 pancreaticoduodenectomies for pancreatic cancer: a single-institution experience. J Gastrointest Surg 2006;10:1199-211.
7. Greenhalf W, Neoptolemos JP. Increasing survival rates of patients with pancreatic cancer by earlier identification. Nat Clin Prac Oncol 2006;3:346-7.
8. Misek DE, Patwa TH, Lubman DM, Simeone DM. Early detection and biomarkers in pancreatic cancer. J Natl Compr Cancer Netw 2007;5:1034-41.
9. Michael G. Molecular markers of early pancreatic cancer. J Clin Oncol 2005;23:4524-31.
10. Wilentz RE, Hruban RH. Pathology of cancer of the pancreas. Surg Oncol Clin N Am 1998;7:43-65.
11. Ueki T, Toyota M, Sohn T, Yeo CJ, Issa JP, Hruban RH, et al. Hypermethylation of multiple genes in pancreatic adenocarcinoma. Cancer Res 2000;60:1835-9.
12. Jones S, Zhang X, Parsons DW, Lin JC-H, Leary RJ, Angenendt P, et al. Core signaling pathways in human pancreatic cancers revealed by global genomic analyses. Science 2008;321:1801-6.
13. Jones PA, Baylin SB. The epigenomics of cancer. Cell 2007;128:683-92.
14. Laird PW. The power andthe promise of DNA methylation markers. Nat Rev Cancer 2003;3:253-66.
15. Jemal A, Center MM, De Santis C, Ward EM. Global patterns of cancer incidence and mortality rates and trends. Cancer Epidemiol Biomarkers Prev 2010;19:1893-907.
16. Jemal A, Ward E, Thun M. Declining death rates reflect progress against cancer. PLoS One 2010;5:e9584.
17. Glockner SC, Dhir M, Yi JM, McGarvey KE, Van Neste L, Louwagie J, et al. Methylation of TFPI2 in stool DNA: a potential novel biomarker for the detection of colorectal cancer. Cancer Res 2009;69:4691-9.
18. Melotte V, Lentjes MH, Van Den Bosch SM, Hellebrekers DM, De Hoon JP, Wouters KA, et al. N-Myc downstream-regulated gene 4 (NDRG4): a candidate tumor suppressor gene and potential biomarker for colorectal cancer. J Natl Cancer Inst 2009;101:916-27.
19. Anglim PP, Galler JS, Koss MN, Hagen JA, Turla S, Campan M, et al. Identification of a panel of sensitive and specific DNA methylation markers for squamous cell lung cancer. Mol Cancer 2008;7:62.
20. Hoque MO. DNA methylation changes in prostate cancer: current developments and future clinical implementation. Expert Rev Mol Diagn 2009;9:243-57.
21. Koopmann J, Rosenzweig CN, Zhang Z, Canto MI, Brown DA, Hunter M, et al. Serum markers in patients with resectable pancreatic adenocarcinoma: macrophage inhibitory cytokine 1 versus CA19-9. Clin Cancer Res 2006;12:442-6.
22. Larghi A, Verna EC, Lecca PG, Costamagna G. Screening for pancreatic cancer in high-risk individuals: a call for endoscopic ultrasound. Clin Cancer Res 2009;15:1907-14.
23. Canto MI, Goggins M, Yeo CJ, Griffin C, Axilbund JE, Brune K, et al. Screening for pancreatic neoplasia in high-risk individuals: an EUS-based approach. Clin Gastroenterol Hepatol 2004;2:606-21.
24. Rhee I, Bachman KE, Park BH, Jair KW, Yen RW, Schuebel KE, et al. DNMT1 and DNMT3b cooperate to silence genes in human cancer cells. Nature 2002;416:552-6.
25. Schuebel KE, Chen W, Cope L, Glöckner SC, Suzuki H, Yi JM, et al. Comparing the DNA hypermethylome with gene mutations in human colorectal cancer. PLoS Genet 2007;3:1709-23.
26. Herman JG, Graff JR, Myohanen S, Nelkin BD, Baylin SB. Methylationspecific PCR: a novel PCR assay for methylation status of CpG islands. Proc Natl Acad Sci U S A 1996;93:9821-6.
27. Livak KJ, Schmittgen TD. Analysis of relative gene expression data using real-time quantitative PCR and the 2 (-Delta Delta C (T)) Method. Methods 2001;25:402-8.
28. Bailey VJ, Zhang Y, Keeley BP, Yin C, Pelosky KL, Brock M, et al. Single-tube analysis of DNA methylation with silica superparamagnetic beads. Clin Chem 2010;56:1022-5.
29. Bailey VJ, Easwaran H, Zhang Y, Griffiths E, Belinsky SA, Herman JG, et al. MS-qFRET: a quantum dot-based method for analysis of DNA methylation. Genome Res 2009;19:1455-61.
30. Bailey VJ, Keeley BP, Razavi CR, Griffiths E, Carraway HE, Wang TH. DNA methylation detection using MS-qFRET, a quantum dot-based nanoassay. Methods 2010;52:237-41.
31. R: a language and environment for statistical computing. 2nd ed. Vienna, Austria: R Development Core Team; 2011.
32. Chan TA, Glockner S, Yi JM, Chen W, Van Neste L, Cope L, et al. Convergence of mutation and epigenetic alterations identifies common genes in cancer that predict for poor prognosis. PLoS Med 2008;5:0823-38.
33. Yi JM, Dhir M, Van Neste L, Downing SR, Jeschke J, Glöckner SC, et al. Genomic and epigenomic integration identifies a prognostic signature in colon cancer. Clin Cancer Res 2011;17:1535-45.
34. Hruban RH, Goggins M, Parsons J, Kern SE. Progression model for pancreatic cancer. Clin Cancer Res 2000;6:2969-72.
35. Hruban RH, Canto MI, Yeo CJ. Prevention of pancreatic cancer and strategies for management of familial pancreatic cancer. Dig Dis 2001;19:76-84.
36. Issa JP, Ahuja N, Toyota M, Bronner MP, Brentnall TA. Accelerated age-related CpG island methylation in ulcerative colitis. Cancer Res 2001;61:3573-7.
37. Dhir M, Montgomery E, Glöckner S, Schuebel K, Hooker C, Herman J, et al. Epigenetic regulation of WNT signaling pathway genes in inflammatory bowel disease (IBD) associated neoplasia. J Gastrointest Surg 2008;12:1745-53.
38. Hahn MA, Hahn T, Lee D-H, Esworthy RS, Kim B-W, Riggs AD, et al. Methylation of polycomb target genes in intestinal cancer is mediated by inflammation. Cancer Res 2008;68:10280-9.
39. Rhodes DR, Yu J, Shanker K, Deshpande N, Varambally R, Ghosh D, et al. ONCOMINE: a cancer microarray database and integrated datamining platform. Neoplasia 2004;6:1-6.
40. Fry LC, Monkemuller K, Malfertheiner P. Molecular markers of pancreatic cancer: development and clinical relevance. Langenbecks Arch Surg 2008;393:883-90.
41. Ballehaninna UK, Chamberlain RS. The clinical utility of serum CA19-9 in the diagnosis, prognosis and management of pancreatic adenocarcinoma: an evidence based appraisal. J Gastrointest Oncol 2012;3:105-19.
42. Sidransky D. Emerging molecular markers of cancer. Nat Rev Cancer 2002;2:210-9.
43. Jeschke J, Van Neste L, Glockner SC, Dhir M, Calmon MF, Deregowski V, et al. Biomarkers for detection and prognosis of breast cancer identified by a functional hypermethylome screen. Epigenetics 2012;7:701-9.
44. Wang J, Zhang S, Schultz RM, Tseng H. Search for basonuclin target genes. Biochem Biophys Res Commun 2006;348:1261-71.
45. Shames DS, Girard L, Gao B, Sato M, Lewis CM, Shivapurkar N, et al. A genome-wide screen for promoter methylation in lung cancer identifies novel methylation markers for multiple malignancies. PLoS Med 2006;3:e486.
46. Porter S, Clark IM, Kevorkian L, Edwards DR. The ADAMTS metalloproteinases. Biochem J 2005;386:15-27.
47. Masui T, Hosotani R, Tsuji S, Miyamoto Y, Yasuda S, Ida J, et al. Expression of METH-1 and METH-2 in pancreatic cancer. Clin Cancer Res 2001;7:3437-43.
48. Porter S, Scott SD, Sassoon EM, Williams MR, Jones JL, Girling AC, et al. Dysregulated expression of adamalysin-thrombospondin genes in human breast carcinoma. Clin Cancer Res 2004;10:2429-40.
49. Choi JE, Kim DS, Kim EJ, Chae MH, Cha SI, Kim CH, et al. Aberrant methylation of ADAMTS1 in non-small cell lung cancer. Cancer Genet Cytogenet 2008;187:80-4.
50. Yegnasubramanian S, Wu Z, Haffner MC, Esopi D, Aryee MJ, Badrinath R, et al. Chromosome-wide mapping of DNA methylation patterns in normal and malignant prostate cells reveals pervasive methylation of gene-associated and conserved intergenic sequences. BMC Genomics 2011;12:313.
51. Ahlquist T, Lind GE, Costa VL, Meling GI, Vatn M, Hoff GS, et al. Gene methylation profiles of normal mucosa, and benign and malignant colorectal tumors identify early onset markers. Mol Cancer 2008;7:94.
52. Vazquez F, Hastings G, Ortega MA, Lane TF, Oikemus S, Lombardo M, et al. METH-1, a human ortholog of ADAMTS-1, and METH-2 are members of a new family of proteins with angio-inhibitory activity. J Biol Chem 1999;274:23349-57.
53. Vincent A, Herman J, Schulick R, Hruban RH, Goggins M. Pancreatic cancer. Lancet 2011;378:607-20.
54. Winter JM, Brennan MF, Tang LH, D'Angelica MI, Dematteo RP, Fong Y, et al. Survival after resection of pancreatic adenocarcinoma: results from a single institution over three decades. Ann Surg Oncol 2012;19:165-75.
55. Jemal A, Siegel R, Xu J, Ward E. Cancer statistics, 2010. CA Cancer J Clin 2010;60:277-300.
56. Sato N, Maitra A, Fukushima N, Van Heek NT, Matsubayashi H, Iacobuzio-Donahue CA, et al. Frequent hypomethylation of multiple genes overexpressed in pancreatic ductal adenocarcinoma. Cancer Res 2003;63:4158-66.
57. Brune K, Hong SM, Li A, Yashida S, Abe T, Griffith M, et al. Genetic and epigenetic alterations of familiar pancreatic cancers. Cancer Epidemiol Biomarkers Prev 2008;17:3536-42.
58. Jones SN, Hruban RH, Kamiyama M, Borges M, Zhang X, Parsons DW, et al. Exomic sequencing identifies PALB2 as a pancreatic cancer susceptibility gene. Science 2009;324:217.
59. Wu J, Matthaei H, Maitra A, Dal Molin M, Wood LD, Eshleman JR, et al. Recurrent GNAS mutations define an unexpected pathway for pancreatic cyst development. Sci Transl Med 2011;3:92ra66-92ra66.