Potential epigenetic biomarkers for the diagnosis and prognosis of pancreatic ductal adenocarcinomas

Expert Review of Molecular Diagnostics

Volumn 13, Issue 5, 2013, Pages 431-443

  Hinton, Jesse ^a   Callan, Richard ^a   Bodine, Charlie ^a   Glasgow, Wayne ^a,b   Brower, Steve ^b,c   Jiang, Shi Wen ^a,b   Li, Jinping ^a,b  

^a MERCER UNIVERSITY SCHOOL OF MEDICINE   (United States)

^b MEMORIAL HEALTH UNIVERSITY MEDICAL CENTER   (United States)

^c BETH ISRAEL MEDICAL CENTER   (United States)

Author keywords

DNA methylation; epigenetic biomarkers; histone modification; miRNA; pancreatic ductal adenocarcinomas

Indexed keywords

CA 19-9 ANTIGEN; CARCINOEMBRYONIC ANTIGEN; FLUOROURACIL; GEMCITABINE; MESSENGER RNA; MICRORNA; MICRORNA 155; MICRORNA 15A; MICRORNA 200A; MICRORNA 200B; MUCIN 1; MUCIN 2; MUCIN 4; VORINOSTAT;

3' UNTRANSLATED REGION; APOPTOSIS; CANCER DIAGNOSIS; CANCER PROGNOSIS; CANCER RECURRENCE; CANCER SCREENING; CANCER STAGING; CANCER TISSUE; CARCINOGENICITY; CELL PROLIFERATION; CHEMORADIOTHERAPY; CHEMOSENSITIVITY; CPG ISLAND; DIAGNOSTIC TEST ACCURACY STUDY; DISEASE SPECIFIC SURVIVAL; DNA METHYLATION; DRUG EFFICACY; EARLY DIAGNOSIS; ENZYME LINKED IMMUNOSORBENT ASSAY; EPIGENETICS; FINE NEEDLE ASPIRATION BIOPSY; GOLD STANDARD; HISTONE MODIFICATION; HUMAN; IMMUNOGENICITY; MICROARRAY ANALYSIS; OVERALL SURVIVAL; PANCREAS ADENOCARCINOMA; PANCREAS JUICE; PREDICTIVE VALUE; PROGRESSION FREE SURVIVAL; REAL TIME POLYMERASE CHAIN REACTION; REVERSE TRANSCRIPTION POLYMERASE CHAIN REACTION; REVIEW; SENSITIVITY AND SPECIFICITY; SURVIVAL RATE; XENOGRAFT;

ADENOCARCINOMA; DNA METHYLATION; EARLY DETECTION OF CANCER; EPIGENESIS, GENETIC; GENE EXPRESSION PROFILING; GENE EXPRESSION REGULATION, NEOPLASTIC; HISTONES; HUMANS; MICRORNAS; NEOPLASM METASTASIS; NEOPLASM RECURRENCE, LOCAL; OLIGONUCLEOTIDE ARRAY SEQUENCE ANALYSIS; PANCREATIC DUCTS; PROGNOSIS; TUMOR MARKERS, BIOLOGICAL;

EID: 84879364361     PISSN: 14737159     EISSN: 17448352     Source Type: Journal    
DOI: 10.1586/erm.13.38     Document Type: Review

References (81)

1. Eguchi H, Ishikawa O, Ohigashi H et al. Serum REG4 level is a predictive biomarker for the response to preoperative chemoradiotherapy in patients with pancreatic cancer. Pancreas 38(7), 791-798 (2009).
2. Rosty C, Goggins M. Early detection of pancreatic carcinoma. Hematol. Oncol. Clin. North Am. 16(1), 37-52 (2002).
3. Takayama R, Nakagawa H, Sawaki A et al. Serum tumor antigen REG4 as a diagnostic biomarker in pancreatic ductal adenocarcinoma. J. Gastroenterol. 45(1), 52-59 (2010).
4. McCarthy DM, Maitra A, Argani P et al. Novel markers of pancreatic adenocarcinoma in fine-needle aspiration: mesothelin and prostate stem cell antigen labeling increases accuracy in cytologically borderline cases. Appl. Immunohistochem. Mol. Morphol. 11(3), 238-243 (2003).
5. Naito M, Terayama H, Hirai S, Qu N, Kawata S, Itoh M. Histopathology of the tubuli recti at the start of experimental autoimmune orchitis in mice. Med. Mol. Morphol. 42(4), 230-235 (2009).
6. Bedi MM, Gandhi MD, Jacob G, Lekha V, Venugopal A, Ramesh H. CA 19-9 to differentiate benign and malignant masses in chronic pancreatitis: is there any benefit? Indian J. Gastroenterol. 28(1), 24-27 (2009).
7. Chung HW, Lim JB, Jang S, Lee KJ, Park KH, Song SY. Serum high mobility group box-1 is a powerful diagnostic and prognostic biomarker for pancreatic ductal adenocarcinoma. Cancer Sci. 103(9), 1714-1721 (2012).
8. Jiang JT, Wu CP, Deng HF et al. Serum level of TSGF, CA242 and CA19-9 in pancreatic cancer. World J. Gastroenterol. 10(11), 1675-1677 (2004).
9. Sorio C, Mafficini A, Furlan F et al. Elevated urinary levels of urokinase-type plasminogen activator receptor (uPAR) in pancreatic ductal adenocarcinoma identify a clinically high-risk group. BMC Cancer 11, 448 (2011).
10. Hiraoka K, Hida Y, Miyamoto M et al. High expression of tumor-associated antigen RCAS1 in pancreatic ductal adenocarcinoma is an unfavorable prognostic marker. Int. J. Cancer 99(3), 418-423 (2002).
11. Wang F, Chen L, Ding W et al. Serum APRIL, a potential tumor marker in pancreatic cancer. Clin. Chem. Lab. Med. 49(10), 1715-1719 (2011).
12. Koprowski H, Steplewski Z, Mitchell K, Herlyn M, Herlyn D, Fuhrer P. Colorectal carcinoma antigens detected by hybridoma antibodies. Somatic Cell Genet. 5, 971 (1979).
13. Goonetilleke KS, Siriwardena AK. Systematic review of carbohydrate antigen (CA 19-9) as a biochemical marker in the diagnosis of pancreatic cancer. Eur. J. Surg. Oncol. 33(3), 266-270 (2007).
14. Winter JM, Yeo CJ, Brody JR. Diagnostic, prognostic, and predictive biomarkers in pancreatic cancer. J. Surg. Oncol. 107(1), 15-22 (2013).
15. Schlieman MG, Ho HS, Bold RJ. Utility of tumor markers in determining resectability of pancreatic cancer. Arch. Surg. 138, 951-955; discussion 955-956 (2013).
16. Safi F, Schlosser W, Kolb G, Beger HG. Diagnostic value of CA 19-9 in patients with pancreatic cancer and nonspecific gastrointestinal symptoms. J. Gastrointest. Surg. 1(2), 106-112 (1997).
17. Kim YC, Kim HJ, Park JH et al. Can preoperative CA19-9 and CEA levels predict the resectability of patients with pancreatic adenocarcinoma? J. Gastroenterol. Hepatol. 24(12), 1869-1875 (2009).
18. Pleskow DK, Berger HJ, Gyves J, Allen E, McLean A, Podolsky DK. Evaluation of a serologic marker, CA19-9, in the diagnosis of pancreatic cancer. Ann. Intern. Med. 110(9), 704-709 (1989).
19. Ferrone CR, Finkelstein DM, Thayer SP, Muzikansky A, Fernandez- delCastillo C, Warshaw AL. Perioperative CA19-9 levels can predict stage and survival in patients with resectable pancreatic adenocarcinoma. J. Clin. Oncol. 24(18), 2897-2902 (2006).
20. Jiang XT, Tao HQ, Zou SC. Detection of serum tumor markers in the diagnosis and treatment of patients with pancreatic cancer. HBPD INT 3(3), 464-468 (2004).
21. Kondo N, Murakami Y, Uemura K et al. Prognostic impact of perioperative serum CA 19-9 levels in patients with resectable pancreatic cancer. Ann. Surg. Oncol. 17(9), 2321-2329 (2010).
22. Zhang S, Wang YM, Sun CD, Lu Y, Wu LQ. Clinical value of serum CA19-9 levels in evaluating resectability of pancreatic carcinoma. World J. Gastroenterol. 14(23), 3750-3753 (2008).
23. Fujioka S, Misawa T, Okamoto T et al. Preoperative serum carcinoembryonic antigen and carbohydrate antigen 19-9 levels for the evaluation of curability and resectability in patients with pancreatic adenocarcinoma. J. Hepatobiliary. Pancreat. Surg. 14(6), 539-544 (2007).
24. Paganuzzi M, Onetto M, Marroni P et al. CA 19-9 and CA 50 in benign and malignant pancreatic and biliary diseases. Cancer 61(10), 2100-2108 (1988).
25. Kau SY, Shyr YM, Su CH, Wu CW, Lui WY. Diagnostic and prognostic values of CA 19-9 and CEA in periampullary cancers. J. Am. Coll. Surg. 188(4), 415-420 (1999).
26. Nakao A, Oshima K, Nomoto S et al. Clinical usefulness of CA-19-9 in pancreatic carcinoma. Semin. Surg. Oncol. 15(1), 15-22 (1998).
27. Michalski CW, Kleeff J, Bachmann J et al. Second-look operation for unresectable pancreatic ductal adenocarcinoma at a high-volume center. Ann. Surg. Oncol. 15(1), 186-192 (2008).
28. Verbeke CS, Menon KV. Redefining resection margin status in pancreatic cancer. HPB (Oxford) 11(4), 282-289 (2009).
29. Takahashi H, Ohigashi H, Ishikawa O et al. Serum CA19-9 alterations during preoperative gemcitabine-based chemoradiation therapy for resectable invasive ductal carcinoma of the pancreas as an indicator for therapeutic selection and survival. Ann. Surg. 251(3), 461-469 (2010).
30. Okusaka T, Yamada T, Maekawa M. Serum tumor markers for pancreatic cancer: the dawn of new era? JOP 7(4), 332-336 (2006).
31. Takehara A, Eguchi H, Ohigashi H et al. Novel tumor marker REG4 detected in serum of patients with resectable pancreatic cancer and feasibility for antibody therapy targeting REG4. Cancer Sci. 97(11), 1191-1197 (2006).
32. Zubarik R, Gordon SR, Lidofsky SD et al. Screening for pancreatic cancer in a high-risk population with serum CA 19-9 and targeted EUS: a feasibility study. Gastrointest. Endosc. 74(1), 87-95 (2011).
33. Pannala R, Basu A, Petersen GM, Chari ST. New-onset diabetes: a potential clue to the early diagnosis of pancreatic cancer. Lancet Oncol. 10(1), 88-95 (2009).
34. Moon JH, Fujiwara Y, Nakamura Y et al. REGIV as a potential biomarker for peritoneal dissemination in gastric adenocarcinoma. J. Surg. Oncol. 105(2), 189-194 (2012).
35. Hu G, Shen J, Cheng L et al. REG4 protects against acinar cell necrosis in experimental pancreatitis. Gut 60(6), 820-828 (2011).
36. Osako M, Yonezawa S, Siddiki B et al. Immunohistochemical study of mucin carbohydrates and core proteins in human pancreatic tumors. Cancer 71(7), 2191-2199 (1993).
37. Yonezawa S, Higashi M, Yamada N et al. Mucins in human neoplasms: clinical pathology, gene expression and diagnostic application. Pathol. Int. 61, 697-716 (2009).
38. Hollingsworth MA, Swanson BJ. Mucins in cancer: protection and control of the cell surface. Nat. Rev. Cancer 4(1), 45-60 (2004).
39. Kufe DW. Mucins in cancer: function, prognosis and therapy. Nat. Rev. Cancer 9(12), 874-885 (2009).
40. Andrianifahanana M, Moniaux N, Schmied BM et al. Mucin (MUC) gene expression in human pancreatic adenocarcinoma and chronic pancreatitis: a potential role of MUC4 as a tumor marker of diagnostic significance. Clin. Cancer Res. 7(12), 4033-4040 (2001).
41. Lee HK, Cho MS, Kim TH. Prognostic significance of muc4 expression in gallbladder carcinoma. World J. Surg. Oncol. 10, 224 (2012).
42. Crippa S, Fernández-Del Castillo C, Salvia R et al. Mucin-producing neoplasms of the pancreas: an analysis of distinguishing clinical and epidemiologic characteristics. Clin. Gastroenterol. Hepatol. 8(2), 213-219 (2010).
43. Cheever MA, Allison JP, Ferris AS et al. The prioritization of cancer antigens: a national cancer institute pilot project for the acceleration of translational research. Clin. Cancer Res. 15(17), 5323-5337 (2009).
44. Maker AV, Katabi N, Gonen M et al. Pancreatic cyst fluid and serum mucin levels predict dysplasia in intraductal papillary mucinous neoplasms of the pancreas. Ann. Surg. Oncol. 18(1), 199-206 (2011).
45. Yamada N, Nishida Y, Tsutsumida H et al. MUC1 expression is regulated by DNA methylation and histone H3 lysine 9 modification in cancer cells. Cancer Res. 68(8), 2708-2716 (2008).
46. Yokoyama S, Kitamoto S, Yamada N et al. The application of methylation specific electrophoresis (MSE) to DNA methylation analysis of the 5? CpG island of mucin in cancer cells. BMC Cancer 12, 67 (2012).
47. Shimizu A, Hirono S, Tani M et al. Coexpression of MUC16 and mesothelin is related to the invasion process in pancreatic ductal adenocarcinoma. Cancer Sci. 103(4), 739-746 (2012).
48. Funel N, Giovannetti E, Del Chiaro M et al. Laser microdissection and primary cell cultures improve pharmacogenetic analysis in pancreatic adenocarcinoma. Lab. Invest. 88(7), 773-784 (2008).
49. Tan AC, Jimeno A, Lin SH et al. Characterizing DNA methylation patterns in pancreatic cancer genome. Mol. Oncol. 3(5-6), 425-438 (2009).
50. Brune K, Hong SM, Li A et al. Genetic and epigenetic alterations of familial pancreatic cancers. Cancer Epidemiol. Biomarkers Prev. 17(12), 3536-3542 (2008).
51. Matsubayashi H, Canto M, Sato N et al. DNA methylation alterations in the pancreatic juice of patients with suspected pancreatic disease. Cancer Res. 66(2), 1208-1217 (2006).
52. Schutte M, Hruban RH, Geradts J et al. Abrogation of the Rb/p16 tumorsuppressive pathway in virtually all pancreatic carcinomas. Cancer Res. 57(15), 3126-3130 (1997).
53. Pedersen KS, Bamlet WR, Oberg AL et al. Leukocyte DNA methylation signature differentiates pancreatic cancer patients from healthy controls. PLoS ONE 6(3), e18223 (2011).
54. Ebrahimi B, Tucker SL, Li D, Abbruzzese JL, Kurzrock R. Cytokines in pancreatic carcinoma: correlation with phenotypic characteristics and prognosis. Cancer 101(12), 2727-2736 (2004).
55. Moniaux N, Chakraborty S, Yalniz M et al. Early diagnosis of pancreatic cancer: neutrophil gelatinase-associated lipocalin as a marker of pancreatic intraepithelial neoplasia. Br. J. Cancer 98(9), 1540-1547 (2008).
56. Dauksa A, Gulbinas A, Barauskas G, Pundzius J, Oldenburg J, El-Maarri O. Whole blood DNA aberrant methylation in pancreatic adenocarcinoma shows association with the course of the disease: a pilot study. PLoS ONE 7(5), e37509 (2012).
57. Zhang L, Gao J, Li L, Li Z, Du Y, Gong Y. The neuronal pentraxin II gene (NPTX2) inhibit proliferation and invasion of pancreatic cancer cells in vitro. Mol. Biol. Rep. 38(8), 4903-4911 (2011).
58. Sato N, Fukushima N, Maitra A et al. Discovery of novel targets for aberrant methylation in pancreatic carcinoma using high-throughput microarrays. Cancer Res. 63(13), 3735-3742 (2003).
59. Park JK, Ryu JK, Yoon WJ et al. The role of quantitative NPTX2 hypermethylation as a novel serum diagnostic marker in pancreatic cancer. Pancreas 41(1), 95-101 (2012).
60. Fujiwara K, Fujimoto N, Tabata M et al. Identification of epigenetic aberrant promoter methylation in serum DNA is useful for early detection of lung cancer. Clin. Cancer Res. 11(3), 1219-1225 (2005).
61. Griffiths EA, Gore SD. microRNA: mIR-ly regulators of DNMT? Blood 113(25), 6269-6270 (2009).
62. Giovannetti E, Funel N, Peters GJ et al. microRNA-21 in pancreatic cancer: correlation with clinical outcome and pharmacologic aspects underlying its role in the modulation of gemcitabine activity. Cancer Res. 70, 4528-4538 (2011).
63. Park JK, Lee EJ, Esau C, Schmittgen TD. Antisense inhibition of miRNA-21 or-221 arrests cell cycle, induces apoptosis, and sensitizes the effects of gemcitabine in pancreatic adenocarcinoma. Pancreas 38(7), e190-e199 (2009).
64. Zhang XJ, Ye H, Zeng CW, He B, Zhang H, Chen YQ. Dysregulation of miR-15a and miR-214 in human pancreatic cancer. J. Hematol. Oncol. 3, 46 (2010).
65. Li Y, VandenBoom TG 2nd, Kong D et al. Up-regulation of miR-200 and let-7 by natural agents leads to the reversal of epithelial-to-mesenchymal transition in gemcitabine-resistant pancreatic cancer cells. Cancer Res. 69(16), 6704-6712 (2009).
66. Ji Q, Hao X, Zhang M et al. microRNA miR-34 inhibits human pancreatic cancer tumor-initiating cells. PLoS ONE 4(8), e6816 (2009).
67. Funel N, Giovannetti E, Pollina LE et al. Critical role of laser microdissection for genetic, epigenetic and proteomic analyses in pancreatic cancer. Expert Rev. Mol. Diagn. 11(7), 695-701 (2011).
68. Nalls D, Tang SN, Rodova M, Srivastava RK, Shankar S. Targeting epigenetic regulation of miR-34a for treatment of pancreatic cancer by inhibition of pancreatic cancer stem cells. PLoS ONE 6(8), e24099 (2011).
69. Vogt M, Munding J, Grüner M et al. Frequent concomitant inactivation of miR-34a and miR-34b/c by CpG methylation in colorectal, pancreatic, mammary, ovarian, urothelial, and renal cell carcinomas and soft tissue sarcomas. Virchows Arch. 458(3), 313-322 (2011).
70. Szafranska AE, Doleshal M, Edmunds HS et al. Analysis of miRNAs in pancreatic fine-needle aspirates can classify benign and malignant tissues. Clin. Chem. 54(10), 1716-1724 (2008).
71. Habbe N, Koorstra JB, Mendell JT et al. microRNA miR-155 is a biomarker of early pancreatic neoplasia. Cancer Biol. Ther. 8(4), 340-346 (2009).
72. Morimura R, Komatsu S, Ichikawa D et al. Novel diagnostic value of circulating miR-18a in plasma of patients with pancreatic cancer. Br. J. Cancer 105(11), 1733-1740 (2011).
73. Li A, Omura N, Hong SM et al. Pancreatic cancers epigenetically silence SIP1 and hypomethylate and overexpress miR-200a/200b in association with elevated circulating miR-200a and miR-200b levels. Cancer Res. 70(13), 5226-5237 (2010).
74. Liu R, Chen X, Du Y et al. Serum miRNA expression profile as a biomarker in the diagnosis and prognosis of pancreatic cancer. Clin. Chem. 58(3), 610-618 (2012).
75. Aghdassi A, Sendler M, Guenther A et al. Recruitment of histone deacetylases HDAC1 and HDAC2 by the transcriptional repressor ZEB1 downregulates E-cadherin expression in pancreatic cancer. Gut 61(3), 439-448 (2012).
76. Manuyakorn A, Paulus R, Farrell J et al. Cellular histone modification patterns predict prognosis and treatment response in resectable pancreatic adenocarcinoma: results from RTOG 9704. J. Clin. Oncol. 28(8), 1358-1365 (2010).
77. Watanabe T, Morinaga S, Akaike M et al. The cellular level of histone H3 lysine 4 dimethylation correlates with response to adjuvant gemcitabine in Japanese pancreatic cancer patients treated with surgery. Eur. J. Surg. Oncol. 38(11), 1051-1057 (2012).
78. Kumar V, Abbas AK, Fausto N, Aster JC. Robbins and Cotran Pathologic Basis of Disease. Saunders Elsevier, PA, USA (2010).
79. Lu Z, Li Y, Takwi A et al. miR-301a as an NF-B activator in pancreatic cancer cells. EMBO J. 30(1), 57-67 (2011).
80. Zhang S, Hao J, Xie F et al. Downregulation of miR-132 by promoter methylation contributes to pancreatic cancer development. Carcinogenesis 32(8), 1183-1189 (2011).
81. Hanoun N, Delpu Y, Suriawinata AA et al. The silencing of miRNA 148a production by DNA hypermethylation is an early event in pancreatic carcinogenesis. Clin. Chem. 56(7), 1107-1118 (2010).