Diagnostic and prognostic biomarkers in pancreatic carcinoma

International Journal of Clinical and Experimental Pathology

Volumn 2, Issue 1, 2009, Pages 1-10

  Liang, John J ^a   Kimchi, Eric T ^a   Staveley O'Carroll, Kevin F ^a   Tan, Dongfeng ^b  

^a PENN STATE MILTON S HERSHEY MEDICAL CENTER   (United States)

^b UNIVERSITY OF TEXAS MD ANDERSON CANCER CENTER   (United States)

Author keywords

Molecular biomarkers; Pancreatic ductal carcinoma

Indexed keywords

EID: 65549110878     PISSN: None     EISSN: 19362625     Source Type: Journal    
DOI: None     Document Type: Review

References (80)

1. Chua YJ and Cunningham D. Adjuvant treatment for resectable pancreatic cancer. J Clin Oncol 2005; 23:4532-4537.
2. Chen CH, Tseng LJ, Yang CC, Yeh YH and Mo LR. The accuracy of endoscopic ultrasound, endoscopic retrograde cholangiopancreatography, computed tomography, and transabdominal ultrasound in the detection and staging of primary ampullary tumors. Hepatogastroenterology 2001;48:1750-1753.
3. Tascilar M, Skinner HG, Rosty C, Sohn T, Wilentz RE, Offerhaus GJ, Adsay V, Abrams RA, Cameron JL, Kern SE, Yeo CJ, Hruban RH and Goggins M. The SMAD4 protein and prognosis of pancreatic ductal adenocarcinoma. Clin Cancer Res 2001;7:4115-4121.
4. Jhala NC, Jhala DN, Chhieng DC, Eloubeidi MA and Eltoum IA. Endoscopic ultrasound-guided fine-needle aspiration. A cytopathologist's perspective. Am J Clin Pathol 2003;120:351-367.
5. Volmar KE, Vollmer RT, Jowell PS, Nelson RC and Xie HB. Pancreatic FNA in 1000 cases: a comparison of imaging modalities. Gastrointest Endosc 2005;61:854-861.
6. Schwartz MR. Endoscopic ultrasound-guided fine-needle aspiration. Cancer 2004;102:203-206.
7. Shin HJ, Lahoti S and Sneige N. Endoscopic ultrasound-guided fine-needle aspiration in 179 cases: the M. D. Anderson Cancer Center experience. Cancer 2002;96:174-180.
8. Eloubeidi MA, Jhala D, Chhieng DC, Chen VK, Eltoum I, Vickers S, Mel Wilcox C and Jhala N. Yield of endoscopic ultrasound-guided fine-needle aspiration biopsy in patients with suspected pancreatic carcinoma. Cancer 2003;99:285-292.
9. Jhala NC, Jhala D, Eltoum I, Vickers SM, Wilcox CM, Chhieng DC and Eloubeidi MA. Endoscopic ultrasound-guided fine-needle aspiration biopsy: a powerful tool to obtain samples from small lesions. Cancer 2004;102:239-246.
10. Klapman JB, Logrono R, Dye CE and Waxman I. Clinical impact of on-site cytopathology interpretation on endoscopic ultrasound-guided fine needle aspiration. Am J Gastroenterol 2003;98:1289-1294.
11. Baeckstrom D, Hansson GC, Nilsson O, Johansson C, Gendler SJ, Lindholm L: Purification and characterization of a membrane-bound and a secreted mucin-type glycoprotein carrying the carcinoma-associated sialyl-Lea epitope on distinct core proteins. J Biol Chem 1991;266:21537-21547.
12. Baeckstrom D, Nilsson O, Price MR, Lindholm L and Hansson GC. Discrimination of MUC1 mucins from other sialyl-Le(a)-carrying glycoproteins produced by colon carcinoma cells using a novel monoclonal antibody. Cancer Res 1993;53:755-761.
13. Ho JJ, Siddiki B and Kim YS. Association of sialyl-Lewis(a) and sialyl-Lewis(x) with MUC-1 apomucin in a pancreatic cancer cell line. Cancer Res 1995;55:3659-3663.
14. Steinberg W. The clinical utility of the CA 19-9 tumor-associated antigen. Am J Gastroenterol 1990;85:350-355.
15. Ritts RE and Pitt HA. CA 19-9 in pancreatic cancer. Surg Oncol Clin N Am 1998;7:93-101.
16. Ziske C, Schlie C, Gorschluter M, Glasmacher A, Mey U, Strehl J, Sauerbruch T and Schmidt-Wolf IG. Prognostic value of CA 19-9 levels in patients with inoperable adenocarcinoma of the pancreas treated with gemcitabine. Br J Cancer 2003;89:1413-1417.
17. Ferrone CR, Finkelstein DM, Thayer SP, Muzikansky A, Fernandez-delCastillo C and Warshaw AL. Perioperative CA19-9 levels can predict stage and survival in patients with resectable pancreatic adenocarcinoma. J Clin Oncol 2006;24:2897-2902.
18. Kilic M, Gocmen E, Tez M, Ertan T, Keskek M and Koc M. Value of preoperative serum CA 19-9 levels in predicting resectability for pancreatic cancer. Can J Surg 2006;49:241-244.
19. Boeck S, Stieber P, Holdenrieder S, Wilkowski R and Heinemann V. Prognostic and therapeutic significance of carbohydrate antigen 19-9 as tumor marker in patients with pancreatic cancer. Oncology 2006;70:255-264.
20. Tessler DA, Catanzaro A, Velanovich V, Havstad S and Goel S. Predictors of cancer in patients with suspected pancreatic malignancy without a tissue diagnosis. Am J Surg 2006;191:191-197.
21. Boeck S, Schulz C, Stieber P, Holdenrieder S, Weckbach S and Heinemann V. Assessing prognosis in metastatic pancreatic cancer by the serum tumor marker CA 19-9: pretreatment levels or kinetics during chemotherapy? Onkologie 2007;30:39-42.
22. Locker GY, Hamilton S, Harris J, Jessup JM, Kemeny N, Macdonald JS, Somerfield MR, Hayes DF and Bast RC Jr. ASCO 2006 update of recommendations for the use of tumor markers in gastrointestinal cancer. J Clin Oncol 2006;24:5313-5327.
23. Andrianifahanana M, Moniaux N, Schmied BM, Ringel J, Friess H, Hollingsworth MA, Buchler MW, Aubert JP and Batra SK. 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 2001; 7:4033-4040.
24. Burdick MD, Harris A, Reid CJ, Iwamura T and Hollingsworth MA. Oligosaccharides expressed on MUC1 produced by pancreatic and colon tumor cell lines. J Biol Chem 1997;272:24198-24202.
25. Beum PV, Singh J, Burdick M, Hollingsworth MA and Cheng PW. Expression of core 2 beta-1,6-N-acetylglucosaminyltransferase in a human pancreatic cancer cell line results in altered expression of MUC1 tumor-associated epitopes. J Biol Chem 1999;274:24641-24648.
26. Gold DV, Modrak DE, Ying Z, Cardillo TM, Sharkey RM and Goldenberg DM. New MUC1 serum immunoassay differentiates pancreatic cancer from pancreatitis. J Clin Oncol 2006;24: 252-258.
27. Saitou M, Goto M, Horinouchi M, Tamada S, Nagata K, Hamada T, Osako M, Takao S, Batra SK, Aikou T, Imai K and Yonezawa S. MUC4 expression is a novel prognostic factor in patients with invasive ductal carcinoma of the pancreas. J Clin Pathol 2005;58:845-852.
28. Singh AP, Moniaux N, Chauhan SC, Meza JL and Batra SK. Inhibition of MUC4 expression suppresses pancreatic tumor cell growth and metastasis. Cancer Res 2004;64:622-630.
29. Prall F, Nollau P, Neumaier M, Haubeck HD, Drzeniek Z, Helmchen U, Loning T and Wagener C. CD66a (BGP), an adhesion molecule of the carcinoembryonic antigen family, is expressed in epithelium, endothelium, and myeloid cells in a wide range of normal human tissues. J Histochem Cytochem 1996;44:35-41.
30. Simeone DM, Ji B, Banerjee M, Arumugam T, Li D, Anderson MA, Bamberger AM, Greenson J, Brand RE, Ramachandran V and Logsdon CD. CEACAM1, a novel serum biomarker for pancreatic cancer. Pancreas 2007;34:436-443.
31. Logsdon CD, Simeone DM, Binkley C, Arumugam T, Greenson JK, Giordano TJ, Misek DE, Kuick R and Hanash S. Molecular profiling of pancreatic adenocarcinoma and chronic pancreatitis identifies multiple genes differentially regulated in pancreatic cancer. Cancer Res 2003;63:2649-2657.
32. Bootcov MR, Bauskin AR, Valenzuela SM, Moore AG, Bansal M, He XY, Zhang HP, Donnellan M, Mahler S, Pryor K, Walsh BJ, Nicholson RC, Fairlie WD, Por SB, Robbins JM and Breit SN. MIC-1, a novel macrophage inhibitory cytokine, is a divergent member of the TGF-beta superfamily. Proc Natl Acad Sci USA 1997;94:11514-11519.
33. Koopmann J, Buckhaults P, Brown DA, Zahurak ML, Sato N, Fukushima N, Sokoll LJ, Chan DW, Yeo CJ, Hruban RH, Breit SN, Kinzler KW, Vogelstein B and Goggins M. Serum macrophage inhibitory cytokine 1 as a marker of pancreatic and other periampullary cancers. Clin Cancer Res 2004;10:2386-2392.
34. Buckhaults P, Rago C, St Croix B, Romans KE, Saha S, Zhang L, Vogelstein B and Kinzler KW. Secreted and cell surface genes expressed in benign and malignant colorectal tumors. Cancer Res 2001;61:6996-7001.
35. Welsh JB, Sapinoso LM, Su AI, Kern SG, Wang-Rodriguez J, Moskaluk CA, Frierson HF Jr. and Hampton GM. Analysis of gene expression identifies candidate markers and pharmacological targets in prostate cancer. Cancer Res 2001;61:5974-5978.
36. Lee DH, Yang Y, Lee SJ, Kim KY, Koo TH, Shin SM, Song KS, Lee YH, Kim YJ, Lee JJ, Choi I and Lee JH. Macrophage inhibitory cytokine-1 induces the invasiveness of gastric cancer cells by up-regulating the urokinase-type plasminogen activator system. Cancer Res 2003;63:4648-4655.
37. Koopmann J, Rosenzweig CN, Zhang Z, Canto MI, Brown DA, Hunter M, Yeo C, Chan DW, Breit SN and Goggins M. Serum markers in patients with resectable pancreatic adenocarcinoma: macrophage inhibitory cytokine 1 versus CA19-9. Clin Cancer Res 2006;12:442-446.
38. Brentnall TA, Bronner MP, Byrd DR, Haggitt RC and Kimmey MB. Early diagnosis and treatment of pancreatic dysplasia in patients with a family history of pancreatic cancer. Ann Intern Med 1999;131:247-255.
39. Canto MI, Goggins M, Yeo CJ, Griffin C, Axilbund JE, Brune K, Ali SZ, Jagannath S, Petersen GM, Fishman EK, Piantadosi S, Giardiello FM and Hruban RH. Screening for pancreatic neoplasia in high-risk individuals: an EUS-based approach. Clin Gastroenterol Hepatol 2004;2: 606-621.
40. Mulcahy HE, Lyautey J, Lederrey C, qi Chen X, Anker P, Alstead EM, Ballinger A, Farthing MJ and Stroun M. A prospective study of K-ras mutations in the plasma of pancreatic cancer patients. Clin Cancer Res 1998;4:271-275.
41. Yamada T, Nakamori S, Ohzato H, Oshima S, Aoki T, Higaki N, Sugimoto K, Akagi K, Fujiwara Y, Nishisho I, Sakon M, Gotoh M and Monden M. Detection of K-ras gene mutations in plasma DNA of patients with pancreatic adenocarcinoma: correlation with clinicopathological features. Clin Cancer Res 1998; 4:1527-1532.
42. Kalthoff H, Schmiegel W, Roeder C, Kasche D, Schmidt A, Lauer G, Thiele HG, Honold G, Pantel K and Riethmuller G et al. p53 and K-AS alterations in pancreatic epithelial cell lesions. Oncogene 1993;8:289-298.
43. Schutte M, Hruban RH, Geradts J, Maynard R, Hilgers W, Rabindran SK, Moskaluk CA, Hahn SA, Schwarte-Waldhoff I, Schmiegel W, Baylin SB, Kern SE and Herman JG. Abrogation of the Rb/p16 tumor-suppressive pathway in virtually all pancreatic carcinomas. Cancer Res 1997; 57:3126-3130.
44. Berger DH, Chang H, Wood M, Huang L, Heath CW, Lehman T and Ruggeri BA. Mutational activation of K-ras in nonneoplastic exocrine pancreatic lesions in relation to cigarette smoking status. Cancer 1999;85:326-332.
45. Tada M, Komatsu Y, Kawabe T, Sasahira N, Isayama H, Toda N, Shiratori Y and Omata M. Quantitative analysis of K-ras gene mutation in pancreatic tissue obtained by endoscopic ultrasonography-guided fine needle aspiration: clinical utility for diagnosis of pancreatic tumor. Am J Gastroenterol 2002;97:2263-2270.
46. Shi C, Eshleman SH, Jones D, Fukushima N, Hua L, Parker AR, Yeo CJ, Hruban RH, Goggins MG and Eshleman JR. LigAmp for sensitive detection of single-nucleotide differences. Nat Methods 2004;1:141-147.
47. Dressman D, Yan H, Traverso G, Kinzler KW and Vogelstein B. Transforming single DNA molecules into fluorescent magnetic particles for detection and enumeration of genetic variations. Proc Natl Acad Sci USA 2003;100: 8817-8822.
48. Diehl F, Li M, Dressman D, He Y, Shen D, Szabo S, Diaz LA Jr, Goodman SN, David KA, Juhl H, Kinzler KW and Vogelstein B. Detection and quantification of mutations in the plasma of patients with colorectal tumors. Proc Natl Acad Sci USA 2005;102:16368-16373.
49. Caldas C, Hahn SA, da Costa LT, Redston MS, Schutte M, Seymour AB, Weinstein CL, Hruban RH, Yeo CJ and Kern SE. Frequent somatic mutations and homozygous deletions of the p16 (MTS1) gene in pancreatic adenocarcinoma. Nat Genet 1994;8:27-32.
50. Sturm PD, Hruban RH, Ramsoekh TB, Noorduyn LA, Tytgat GN, Gouma DJ and Offerhaus GJ. The potential diagnostic use of K-ras codon 12 and p53 alterations in brush cytology from the pancreatic head region. J Pathol 1998;186:247-253.
51. Yan L, McFaul C, Howes N, Leslie J, Lancaster G, Wong T, Threadgold J, Evans J, Gilmore I, Smart H, Lombard M, Neoptolemos J and Greenhalf W. Molecular analysis to detect pancreatic ductal adenocarcinoma in high-risk groups. Gastroenterology 2005;128:2124-2130.
52. Ehmann M, Felix K, Hartmann D, Schnolzer M, Nees M, Vorderwulbecke S, Bogumil R, Buchler MW and Friess H. Identification of potential markers for the detection of pancreatic cancer through comparative serum protein expression profiling. Pancreas 2007;34:205-214.
53. Ishizone S, Yamauchi K, Kawa S, Suzuki T, Shimizu F, Harada O, Sugiyama A, Miyagawa S, Fukuda M and Nakayama J. Clinical utility of quantitative RT-PCR targeted to alpha1,4-N-acetylglucosaminyltransferase mRNA for detection of pancreatic cancer. Cancer Sci 2006;97:119-126.
54. Hoffmann K, Kerner C, Wilfert W, Mueller M, Thiery J, Hauss J and Witzigmann H. Detection of disseminated pancreatic cells by amplification of cytokeratin-19 with quantitative RT-PCR in blood, bone marrow and peritoneal lavage of pancreatic carcinoma patients. World J Gastroenterol 2007;13:257-263.
55. Giovannetti E, Del Tacca M, Mey V, Funel N, Nannizzi S, Ricci S, Orlandini C, Boggi U, Campani D, Del Chiaro M, Iannopollo M, Bevilacqua G, Mosca F and Danesi R. Transcription analysis of human equilibrative nucleoside transporter-1 predicts survival in pancreas cancer patients treated with gemcitabine. Cancer Res 2006;66:3928-3935.
56. Lee EJ, Gusev Y, Jiang J, Nuovo GJ, Lerner MR, Frankel WL, Morgan DL, Postier RG, Brackett DJ and Schmittgen TD. Expression profiling identifies microRNA signature in pancreatic cancer. Int J Cancer 2007;120:1046-1054.
57. Chadeneau C, Hay K, Hirte HW, Gallinger S and Bacchetti S. Telomerase activity associated with acquisition of malignancy in human colorectal cancer. Cancer Res 1995;55:2533-2536.
58. Kanaya T, Kyo S, Takakura M, Ito H, Namiki M and Inoue M. hTERT is a critical determinant of telomerase activity in renal-cell carcinoma. Int J Cancer 1998;78:539-543.
59. Lantuejoul S, Soria JC, Moro-Sibilot D, Morat L, Veyrenc S, Lorimier P, Brichon PY, Sabatier L, Brambilla C and Brambilla E. Differential expression of telomerase reverse transcriptase (hTERT) in lung tumours. Br J Cancer 2004; 90:1222-1229.
60. Liu YC, Chen CJ, Wu HS, Chan DC, Yu JC, Yang AH, Cheng YL, Lee SC and Harn HJ. Telomerase and c-myc expression in hepatocellular carcinomas. Eur J Surg Oncol 2004;30:384-390.
61. Niiyama H, Mizumoto K, Sato N, Nagai E, Mibu R, Fukui T, Kinoshita M and Tanaka M. Quantitative analysis of hTERT mRNA expression in colorectal cancer. Am J Gastroenterol 2001;96:1895-1900.
62. Yoo J, Park SY, Kang SJ, Kim BK, Shim SI and Kang CS. Expression of telomerase activity, human telomerase RNA, and telomerase reverse transcriptase in gastric adenocarcinomas. Mod Pathol 2003;16:700-707.
63. Mishra G, Zhao Y, Sweeney J, Pineau BC, Case D, Ho C, Blackstock AW, Geisinger K, Howerton R, Levine E, Shen P and Ibdah J. Determination of qualitative telomerase activity as an adjunct to the diagnosis of pancreatic adenocarcinoma by EUS-guided fine-needle aspiration. Gastrointest Endosc 2006;63:648-654.
64. Bhattacharyya S, Siegel ER, Petersen GM, Chari ST, Suva LJ and Haun RS. Diagnosis of pancreatic cancer using serum proteomic profiling. Neoplasia 2004;6:674-686.
65. Koopmann J, Zhang Z, White N, Rosenzweig J, Fedarko N, Jagannath S, Canto MI, Yeo CJ, Chan DW and Goggins M. Serum diagnosis of pancreatic adenocarcinoma using surface-enhanced laser desorption and ionization mass spectrometry. Clin Cancer Res 2004;10:860-868.
66. Scarlett CJ, Smith RC, Saxby A, Nielsen A, Samra JS, Wilson SR and Baxter RC. Proteomic classification of pancreatic adenocarcinoma tissue using protein chip technology. Gastroenterology 2006; 130:1670-1678.
67. Lin F, Shi J, Liu H, Hull ME, Dupree W, Prichard JW, Brown RE, Zhang J, Wang HL and Schuerch C. Diagnostic utility of S100P and von Hippel-Lindau gene product (pVHL) in pancreatic adenocarcinoma-with implication of their roles in early tumorigenesis. Am J Surg Pathol 2008; 32:78-91.
68. Tsiambas E, Karameris A, Dervenis C, Lazaris AC, Giannakou N, Gerontopoulos K and Patsouris E. HER2/neu expression and gene alterations in pancreatic ductal adenocarcinoma: a comparative immunohistochemistry and chromogenic in situ hybridization study based on tissue microarrays and computerized image analysis. Jop 2006;7:283-294.
69. Wright JH, Wang X, Manning G, LaMere BJ, Le P, Zhu S, Khatry D, Flanagan PM, Buckley SD, Whyte DB, Howlett AR, Bischoff JR, Lipson KE and Jallal B. The STE20 kinase HGK is broadly expressed in human tumor cells and can modulate cellular transformation, invasion, and adhesion. Mol Cell Biol 2003;23:2068-2082.
70. Hiyama E, Kodama T, Shinbara K, Iwao T, Itoh M, Hiyama K, Shay JW, Matsuura Y and Yokoyama T. Telomerase activity is detected in pancreatic cancer but not in benign tumors. Cancer Res 1997;57:326-331.
71. Suehara N, Mizumoto K, Tanaka M, Niiyama H, Yokohata K, Tominaga Y, Shimura H, Muta T and Hamasaki N. Telomerase activity in pancreatic juice differentiates ductal carcinoma from adenoma and pancreatitis. Clin Cancer Res 1997;3:2479-2483.
72. Ohuchida K, Mizumoto K, Yamada D, Yamaguchi H, Konomi H, Nagai E, Yamaguchi K, Tsuneyoshi M and Tanaka M. Quantitative analysis of human telomerase reverse transcriptase in pancreatic cancer. Clin Cancer Res 2006;12:2066-2069.
73. Matsubayashi H, Canto M, Sato N, Klein A, Abe T, Yamashita K, Yeo CJ, Kalloo A, Hruban R and Goggins M. DNA methylation alterations in the pancreatic juice of patients with suspected pancreatic disease. Cancer Res 2006;66: 1208-1217.
74. Chen R, Pan S, Yi EC, Donohoe S, Bronner MP, Potter JD, Goodlett DR, Aebersold R and Brentnall TA. Quantitative proteomic profiling of pancreatic cancer juice. Proteomics 2006;6: 3871-3879.
75. Chen R, Pan S, Cooke K, Moyes KW, Bronner MP, Goodlett DR, Aebersold R and Brentnall TA. Comparison of pancreas juice proteins from cancer versus pancreatitis using quantitative proteomic analysis. Pancreas 2007;34:70-79.
76. Kosmahl M, Pauser U, Peters K, Sipos B, Luttges J, Kremer B and Kloppel G. Cystic neoplasms of the pancreas and tumor-like lesions with cystic features: a review of 418 cases and a classification proposal. Virchows Arch 2004;445:168-178.
77. Pelaez-Luna M and Chari ST. Cyst fluid analysis to diagnose pancreatic cystic lesions: an as yet unfulfilled promise. Gastroenterology 2006;130:1007-1009; discussion 1009.
78. van der Waaij LA, van Dullemen HM and Porte RJ. Cyst fluid analysis in the differential diagnosis of pancreatic cystic lesions: a pooled analysis. Gastrointest Endosc 2005;62:383-389.
79. Kobayashi M, Ueyama Y, Nakanishi H, Ishida H, Takahashi E, Nakamura S, Koshikawa T and Yatabe Y. Immunocytochemical detection using CDX2: An aid for discerning tumor involvement in ascites cytology. Cancer 2006;108:114-118.
80. Moparty B, Logrono R, Nealon WH, Waxman I, Raju GS, Pasricha PJ and Bhutani MS. The role of endoscopic ultrasound and endoscopic ultrasound-guided fine-needle aspiration in distinguishing pancreatic cystic lesions. Diagn Cytopathol 2007;35:18-25.