Proteomic strategies in the search for novel pancreatic cancer biomarkers and drug targets: recent advances and clinical impact

References

• Vincent A, Herman J, Schulick R, et al. Pancreatic cancer. Lancet. 2011;378(9791):607–620.
   PubMed Web of Science ®Google Scholar
• Chue BM. Five-year survival of metastatic pancreatic carcinoma: a study of courage and hope. Gastrointest Cancer Res. 2009;3(5):208–211.
   Google Scholar
• Lowenfels AB, Maisonneuve P. Epidemiology and risk factors for pancreatic cancer. Best Pract Res Clin Gastroenterol. 2006;20(2):197–209.
   PubMed Web of Science ®Google Scholar
• Bosetti C, Lucenteforte E, Silverman DT, et al. Cigarette smoking and pancreatic cancer: an analysis from the international pancreatic cancer case-control consortium (Panc4). Ann Oncol. 2012;23(7):1880–1888.
   PubMed Web of Science ®Google Scholar
• Ryan DP, Hong TS, Bardeesy N. Pancreatic adenocarcinoma. N Engl J Med. 2014;371(11):1039–1049.
   PubMed Web of Science ®Google Scholar
• Takahashi Y, Takeuchi T, Sakamoto J, et al. The usefulness of CEA and/or CA19-9 in monitoring for recurrence in gastric cancer patients: a prospective clinical study. Gastric Cancer. 2003;6(3):142–145.
   PubMedGoogle Scholar
• Maestranzi S, Przemioslo R, Mitchell H, et al. The effect of benign and malignant liver disease on the tumour markers CA19-9 and CEA. Ann Clin Biochem. 1998;35(1):99–103.
   PubMedGoogle Scholar
• Li D, Xie K, Wolff R, et al. Pancreatic cancer. Lancet. 2004;363(9414):1049–1057.
   PubMed Web of Science ®Google Scholar
• Rozenblum E, Schutte M, Goggins M, et al. Tumor-suppressive pathways in pancreatic carcinoma. Cancer Res. 1997;57(9):1731–1734.
   PubMed Web of Science ®Google Scholar
• Schutte M, Hruban RH, Geradts J, et al. Abrogation of the Rb/p16 tumor-suppressive pathway in virtually all pancreatic carcinomas. Cancer Res. 1997;57(15):3126–3130.
   PubMed Web of Science ®Google Scholar
• Shields JM, Pruitt K, McFall A, et al. Understanding Ras:‘it ain’t over’til it’s over’. Trends Cell Biol. 2000;10(4):147–154.
   PubMed Web of Science ®Google Scholar
• Fernandez-Medarde A, Santos E. Ras in cancer and developmental diseases. Genes Cancer. 2011;2(3):344–358.
   PubMedGoogle Scholar
• Koorstra JM, Feldmann G, Habbe N, et al. Morphogenesis of pancreatic cancer: role of pancreatic intraepithelial neoplasia (PanINs). Langenbeck’s Arch Surg. 2008;393(4):561–570.
   PubMed Web of Science ®Google Scholar
• Cowgill SM, Muscarella P. The genetics of pancreatic cancer. Am J Surg. 2003;186(3):279–286.
   PubMed Web of Science ®Google Scholar
• Boja ES, Rodriguez H. The path to clinical proteomics research: integration of proteomics, genomics, clinical laboratory and regulatory science. Korean J Lab Med. 2011;31(2):61–71.
   PubMedGoogle Scholar
• Adam BL, Vlahou A, Semmes OJ, et al. Proteomic approaches to biomarker discovery in prostate and bladder cancers. Proteomics. 2001;1(10):1264–1270.
   PubMed Web of Science ®Google Scholar
• Hu S, Arellano M, Boontheung P, et al. Salivary proteomics for oral cancer biomarker discovery. Clin Cancer Res. 2008;14(19):6246–6252.
   PubMed Web of Science ®Google Scholar
• De Wit M, Fijneman RJ, Verheul HM, et al. Proteomics in colorectal cancer translational research: biomarker discovery for clinical applications. Clin Biochem. 2013;46(6):466–479.
   PubMed Web of Science ®Google Scholar
• Pontén F, Schwenk JM, Asplund A, et al. The Human Protein Atlas as a proteomic resource for biomarker discovery. J Intern Med. 2011;270(5):428–446.
   PubMed Web of Science ®Google Scholar
• Surlin V, Bintintan V, Petrariu FD, et al. Prognostic factors in resectable pancreatic cancer. Rev Med Chir Soc Med Nat Iasi. 2014;118(4):924–931.
   PubMedGoogle Scholar
• Whipple AO, Parsons WB, Mullins CR. Treatment of Carcinoma of the Ampulla of Vater. Ann Surg. 1935;102(4):763–779.
   PubMedGoogle Scholar
• Winter JM, Brennan MF, Tang LH, et al. Survival after resection of pancreatic adenocarcinoma: results from a single institution over three decades. Ann Surg Oncol. 2012;19(1):169–175.
   PubMed Web of Science ®Google Scholar
• Oettle H, Neuhaus P, Hochhaus A, et al. Adjuvant chemotherapy with gemcitabine and long-term outcomes among patients with resected pancreatic cancer: the CONKO-001 randomized trial. Jama. 2013;310(14):1473–1481.
   PubMed Web of Science ®Google Scholar
• Schniewind B, Christgen M, Kurdow R, et al. Resistance of pancreatic cancer to gemcitabine treatment is dependent on mitochondria‐mediated apoptosis. Int J Cancer. 2004;109(2):182–188.
   PubMed Web of Science ®Google Scholar
• Lee JJ, Huang J, England CG, et al. Predictive modeling of in vivo response to gemcitabine in pancreatic cancer. PLoS Comput Biol. 2013;9(9):e1003231.
   PubMedGoogle Scholar
• Samulitis BK, Pond KW, Pond E, et al. Gemcitabine resistant pancreatic cancer cell lines acquire an invasive phenotype with collateral hypersensitivity to histone deacetylase inhibitors. Cancer Biol Ther. 2015;16(1):43–51.
   PubMed Web of Science ®Google Scholar
• Ciliberto D, Botta C, Correale P, et al. Role of gemcitabine-based combination therapy in the management of advanced pancreatic cancer: a meta-analysis of randomised trials. Eur J Cancer. 2013;49(3):593–603.
   PubMed Web of Science ®Google Scholar
• Von Hoff DD, Ervin T, Arena FP, et al. Increased survival in pancreatic cancer with nab-paclitaxel plus gemcitabine. N Engl J Med. 2013;369(18):1691–1703.
   PubMed Web of Science ®Google Scholar
• Conroy T, Desseigne F, Ychou M, et al. FOLFIRINOX versus gemcitabine for metastatic pancreatic cancer. N Engl J Med. 2011;364(19):1817–1825.
   PubMed Web of Science ®Google Scholar
• Boone BA, Steve J, Krasinskas AM, et al. Outcomes with FOLFIRINOX for borderline resectable and locally unresectable pancreatic cancer. J Surg Oncol. 2013;108(4):236–241.
   PubMed Web of Science ®Google Scholar
• Falchook GS, Ordonez NG, Bastida CC, et al. Effect of the RET inhibitor vandetanib in a patient with RET fusion-positive metastatic non-small-cell lung cancer. J Clin Oncol. 2014. doi:10.1200/JCO.2013.50.5016. [Epub ahead of print]
   Google Scholar
• Costello E, Greenhalf W, Neoptolemos JP. New biomarkers and targets in pancreatic cancer and their application to treatment. Nat Rev Gastroenterol Hepatol. 2012;9(8):435–444.
   PubMed Web of Science ®Google Scholar
• Kessler ER, Eckhardt SG, Pitts TM, et al. Phase I trial of vandetanib in combination with gemcitabine and capecitabine in patients with advanced solid tumors with an expanded cohort in pancreatic and biliary cancers. Invest New Drugs. 2015;34(2):176–183.
   Google Scholar
• Moore MJ, Goldstein D, Hamm J, et al. Erlotinib plus gemcitabine compared with gemcitabine alone in patients with advanced pancreatic cancer: a phase III trial of the National Cancer Institute of Canada Clinical Trials Group. J Clin Oncol. 2007;25(15):1960–1966.
   PubMed Web of Science ®Google Scholar
• Hurwitz HI, Uppal N, Wagner SA, et al. Randomized, double-blind, phase ii study of ruxolitinib or placebo in combination with capecitabine in patients with metastatic pancreatic cancer for whom therapy with gemcitabine has failed. J Clin Oncol. 2015;33(34):4039–4047.
   PubMed Web of Science ®Google Scholar
• ENCODE Project Consortium. An integrated encyclopedia of DNA elements in the human genome. Nature. 2012;489(7414):57–74.
   PubMed Web of Science ®Google Scholar
• Wittmann‐Liebold B, Graack H, Pohl T. Two‐dimensional gel electrophoresis as tool for proteomics studies in combination with protein identification by mass spectrometry. Proteomics. 2006;6(17):4688–4703.
   PubMed Web of Science ®Google Scholar
• Cellulaire B. Two-dimensional gel electrophoresis in proteomics: old, old fashioned, but it still climbs up the mountains. Proteomics. 2002;2:3–10.
   Web of Science ®Google Scholar
• Theodoridis GA, Gika HG, Want EJ, et al. Liquid chromatography–mass spectrometry based global metabolite profiling: a review. Anal Chim Acta. 2012;711:7–16.
   PubMed Web of Science ®Google Scholar
• Mullen W, Albalat A, Gonzalez J, et al. Performance of different separation methods interfaced in the same MS‐reflection TOF detector: A comparison of performance between CE versus HPLC for biomarker analysis. Electrophoresis. 2012;33(4):567–574.
   PubMed Web of Science ®Google Scholar
• Tu C, Rudnick PA, Martinez MY, et al. Depletion of abundant plasma proteins and limitations of plasma proteomics. J Proteome Res. 2010;9(10):4982–4991.
   PubMed Web of Science ®Google Scholar
• McKinney KQ, Lee JG, Sindram D, et al. Identification of differentially expressed proteins from primary versus metastatic pancreatic cancer cells using subcellular proteomics. Cancer Genom Proteom. 2012;9(5):257–263.
   PubMed Web of Science ®Google Scholar
• Britton D, Zen Y, Quaglia A, et al. Quantification of pancreatic cancer proteome and phosphorylome: indicates molecular events likely contributing to cancer and activity of drug targets. PloS One. 2014;9(3):e90948.
   Web of Science ®Google Scholar
• Ong SE, Blagoev B, Kratchmarova I, et al. Stable isotope labeling by amino acids in cell culture, SILAC, as a simple and accurate approach to expression proteomics. Mol Cell Proteomics. 2002;1(5):376–386.
   PubMed Web of Science ®Google Scholar
• Gygi SP, Rist B, Gerber SA, et al. Quantitative analysis of complex protein mixtures using isotope-coded affinity tags. Nat Biotechnol. 1999;17(10):994–999.
   PubMed Web of Science ®Google Scholar
• Wiese S, Reidegeld KA, Meyer HE, et al. Protein labeling by iTRAQ: a new tool for quantitative mass spectrometry in proteome research. Proteomics. 2007;7(3):340–350.
   PubMed Web of Science ®Google Scholar
• Thompson A, Schäfer J, Kuhn K, et al. Tandem mass tags: a novel quantification strategy for comparative analysis of complex protein mixtures by MS/MS. Anal Chem. 2003;75(8):1895–1904.
   PubMed Web of Science ®Google Scholar
• Zhu W, Smith JW, Huang CM. Mass spectrometry-based label-free quantitative proteomics. J Biomed Biotechnol. 2010;2010:1–6.
   Google Scholar
• Kosanam H, Prassas I, Chrystoja CC, et al. Laminin, gamma 2 (LAMC2): a promising new putative pancreatic cancer biomarker identified by proteomic analysis of pancreatic adenocarcinoma tissues. Mol Cell Proteomics. 2013;12(10):2820–2832.
   PubMed Web of Science ®Google Scholar
• Scheltema RA, Hauschild JP, Lange O, et al. The Q Exactive HF, a Benchtop mass spectrometer with a pre-filter, high-performance quadrupole and an ultra-high-field Orbitrap analyzer. Mol Cell Proteomics. 2014;13(12):3698–3708.
   PubMed Web of Science ®Google Scholar
• LaConti JJ, Laiakis EC, Mays AD, et al. Distinct serum metabolomics profiles associated with malignant progression in the KrasG12D mouse model of pancreatic ductal adenocarcinoma. BMC Genomics. 2015;16(Suppl 1):S1-2164-16-S1-S1. Epub 2015 Jan 15.
   PubMedGoogle Scholar
• Lin L, Lin H, Zhang M, et al. Types, principle, and characteristics of tandem high-resolution mass spectrometry and its applications. RSC Adv. 2015;5(130):107623–107636.
   Web of Science ®Google Scholar
• Ansari D, Aronsson L, Sasor A, et al. The role of quantitative mass spectrometry in the discovery of pancreatic cancer biomarkers for translational science. J Transl Med. 2014;12:87-5876-12-87.
   Web of Science ®Google Scholar
• Pan S, Chen R, Crispin DA, et al. Protein alterations associated with pancreatic cancer and chronic pancreatitis found in human plasma using global quantitative proteomics profiling. J Proteome Res. 2011;10(5):2359–2376.
   PubMed Web of Science ®Google Scholar
• Ohmine K, Kawaguchi K, Ohtsuki S, et al. Quantitative targeted proteomics of pancreatic cancer: deoxycytidine kinase protein level correlates to progression-free survival of patients receiving gemcitabine treatment. Mol Pharm. 2015;12(9):3282–3291.
   PubMed Web of Science ®Google Scholar
• Singh CK, Kaur S, George J, et al. Molecular signatures of sanguinarine in human pancreatic cancer cells: A large scale label-free comparative proteomics approach. Oncotarget. 2015;6(12):10335–10348.
   PubMed Web of Science ®Google Scholar
• Radon TP, Massat NJ, Jones R, et al. Identification of a three-biomarker panel in urine for early detection of pancreatic adenocarcinoma. Clin Cancer Res. 2015;21(15):3512–3521.
   PubMed Web of Science ®Google Scholar
• Kim MS, Zhong Y, Yachida S, et al. Heterogeneity of pancreatic cancer metastases in a single patient revealed by quantitative proteomics. Mol Cell Proteomics. 2014;13(11):2803–2811.
   PubMed Web of Science ®Google Scholar
• Nie S, Lo A, Wu J, et al. Glycoprotein biomarker panel for pancreatic cancer discovered by quantitative proteomics analysis. J Proteome Res. 2014;13(4):1873–1884.
   PubMed Web of Science ®Google Scholar
• Wang W, Liu X, Liu L, et al. Identification of proteins implicated in the development of pancreatic cancer-associated diabetes mellitus by iTRAQ-based quantitative proteomics. J Proteomics. 2013;84:52–60.
   PubMed Web of Science ®Google Scholar
• Takadate T, Onogawa T, Fukuda T, et al. Novel prognostic protein markers of resectable pancreatic cancer identified by coupled shotgun and targeted proteomics using formalin‐fixed paraffin‐embedded tissues. Int J Cancer. 2013;132(6):1368–1382.
   PubMed Web of Science ®Google Scholar
• Yoneyama T, Ohtsuki S, Ono M, et al. Quantitative targeted absolute proteomics-based large-scale quantification of proline-hydroxylated α-fibrinogen in plasma for pancreatic cancer diagnosis. J Proteome Res. 2013;12(2):753–762.
   PubMed Web of Science ®Google Scholar
• Chen J, Wu W, Tang HK, et al. Analysis of pancreatic cancer peripheral blood by comparative proteomics. Zhonghua Wai Ke Za Zhi. 2013;51(1):62–65.
   PubMedGoogle Scholar
• Wang WB, Zhao YP, Liao Q, et al. Validation of candidate immunogenic membrane antigens of human pancreatic cancer screened by proteomics. Zhonghua Wai Ke Za Zhi. 2012;50(3):260–263.
   PubMedGoogle Scholar
• Harsha H, Kandasamy K, Ranganathan P, et al. A compendium of potential biomarkers of pancreatic cancer. PLoS Med. 2009;6(4):343.
   Google Scholar
• Deer EL, Gonzalez-Hernandez J, Coursen JD, et al. Phenotype and genotype of pancreatic cancer cell lines. Pancreas. 2010;39(4):425–435.
   PubMed Web of Science ®Google Scholar
• Kim Y, Han D, Min H, et al. Comparative proteomic profiling of pancreatic ductal adenocarcinoma cell lines. Mol Cells. 2014;37(12):888.
   PubMed Web of Science ®Google Scholar
• Liu X, Zhang M, Go VL, et al. Membrane proteomic analysis of pancreatic cancer cells. J Biomed. Sci. 2010;17:74. doi:10.1186/1423-0127-17-74.
   Google Scholar
• Grippo PJ, Munshi HG, editors. Pancreatic cancer and tumor microenvironment [Internet]. Trivandrum (India): Transworld Research Network; 2012. Available from: http://www.ncbi.nlm.nih.gov/books/NBK98930/
   Google Scholar
• Chen R, Eugene CY, Donohoe S, et al. Pancreatic cancer proteome: the proteins that underlie invasion, metastasis, and immunologic escape. Gastroenterology. 2005;129(4):1187–1197.
   PubMed Web of Science ®Google Scholar
• Pan S, Brentnall TA, Kelly K, et al. Tissue proteomics in pancreatic cancer study: discovery, emerging technologies, and challenges. Proteomics. 2013;13(3–4):710–721.
   PubMed Web of Science ®Google Scholar
• Berberat PO, Friess H, Wang L, et al. Comparative analysis of galectins in primary tumors and tumor metastasis in human pancreatic cancer. J Histochem Cytochem. 2001;49(4):539–549.
   PubMed Web of Science ®Google Scholar
• Chen J, Ni R, Xiao M, et al. Comparative proteomic analysis of differentially expressed proteins in human pancreatic cancer tissue. Hepatobiliary Pancreat Dis Int. 2009;8(2):193–200.
   Google Scholar
• Thompson CC, Ashcroft FJ, Patel S, et al. Pancreatic cancer cells overexpress gelsolin family-capping proteins, which contribute to their cell motility. Gut. 2007;56(1):95–106.
   PubMed Web of Science ®Google Scholar
• Bausch D, Thomas S, Mino-Kenudson M, et al. Plectin-1 as a novel biomarker for pancreatic cancer. Clin Cancer Res. 2011;17(2):302–309.
   PubMed Web of Science ®Google Scholar
• Martinez-Bosch N, Fernandez-Barrena MG, Moreno M, et al. Galectin-1 drives pancreatic carcinogenesis through stroma remodeling and Hedgehog signaling activation. Cancer Res. 2014;74(13):3512–3524.
   PubMed Web of Science ®Google Scholar
• Kelly KA, Bardeesy N, Anbazhagan R, et al. Targeted nanoparticles for imaging incipient pancreatic ductal adenocarcinoma. PLoS Med. 2008;5(4):e85.
   PubMed Web of Science ®Google Scholar
• Gronborg M, Kristiansen TZ, Iwahori A, et al. Biomarker discovery from pancreatic cancer secretome using a differential proteomic approach. Mol Cell Proteomics. 2006;5(1):157–171.
   PubMed Web of Science ®Google Scholar
• Jenkinson C, Elliott V, Evans A, et al. Decreased serum thrombospondin-1 levels in pancreatic cancer patients up to 24 months prior to clinical diagnosis: association with diabetes mellitus. Clin Cancer Res. 2015. doi:10.1158/1078-0432.CCR-15-0879. [Epub ahead of print] clincanres. 0879.2015.
   Google Scholar
• Hocker JR, Postier RG, Li M, et al. Discriminating patients with early-stage pancreatic cancer or chronic pancreatitis using serum electrospray mass profiling. Cancer Lett. 2015;359(2):314–324.
   PubMed Web of Science ®Google Scholar
• Brand RE, Nolen BM, Zeh HJ, et al. Serum biomarker panels for the detection of pancreatic cancer. Clin Cancer Res. 2011;17(4):805–816.
   PubMed Web of Science ®Google Scholar
• Tonack S, Jenkinson C, Cox T, et al. iTRAQ reveals candidate pancreatic cancer serum biomarkers: influence of obstructive jaundice on their performance. Br J Cancer. 2013;108(9):1846–1853.
   PubMed Web of Science ®Google Scholar
• Yue T, Goldstein IJ, Hollingsworth MA, et al. The prevalence and nature of glycan alterations on specific proteins in pancreatic cancer patients revealed using antibody-lectin sandwich arrays. Mol Cell Proteomics. 2009;8(7):1697–1707.
   PubMed Web of Science ®Google Scholar
• Remmers N, Anderson JM, Linde EM, et al. Aberrant expression of mucin core proteins and o-linked glycans associated with progression of pancreatic cancer. Clin Cancer Res. 2013;19(8):1981–1993.
   PubMed Web of Science ®Google Scholar
• Gerdtsson AS, Malats N, Säll A, et al. A multicenter trial defining a serum protein signature associated with pancreatic ductal adenocarcinoma. Int J Proteomics. 2015;2015:10. Article ID 587250. doi:10.1155/2015/587250.
   PubMedGoogle Scholar
• Makawita S, Smith C, Batruch I, et al. Integrated proteomic profiling of cell line conditioned media and pancreatic juice for the identification of pancreatic cancer biomarkers. Mol Cell Proteomics. 2011;10(10):M111.008599.
   PubMed Web of Science ®Google Scholar
• Costa-Silva B, Aiello NM, Ocean AJ, et al. Pancreatic cancer exosomes initiate pre-metastatic niche formation in the liver. Nat Cell Biol. 2015;17(6):816–826.
   PubMed Web of Science ®Google Scholar
• Melo SA, Luecke LB, Kahlert C, et al. Glypican-1 identifies cancer exosomes and detects early pancreatic cancer. Nature. 2015;523:177–182.
   PubMed Web of Science ®Google Scholar
• Foygel K, Wang H, Machtaler S, et al. Detection of pancreatic ductal adenocarcinoma in mice by ultrasound imaging of thymocyte differentiation antigen 1. Gastroenterology. 2013;145(4):885–894.e3.
   PubMed Web of Science ®Google Scholar
• Maes E, Mertens I, Valkenborg D, et al. Proteomics in cancer research: are we ready for clinical practice? Crit Rev Oncol. 2015;96(3):437–448.
   PubMed Web of Science ®Google Scholar
• Mullard A. Maturing antibody-drug conjugate pipeline hits 30. Nat Rev Drug Discov. 2013;12(5):329–332.
   PubMed Web of Science ®Google Scholar
• Sauerborn M, Van Dongen W. Practical considerations for the pharmacokinetic and immunogenic assessment of antibody–drug conjugates. BioDrugs. 2014;28(4):383–391.
   PubMed Web of Science ®Google Scholar