The role of quantitative mass spectrometry in the discovery of pancreatic cancer biomarkers for translational science

Journal of Translational Medicine

Volumn 12, Issue 1, 2014, Pages

  Ansari, Daniel ^a   Aronsson, Linus ^a   Sasor, Agata ^a   Welinder, Charlotte ^a   Rezeli, Melinda ^b   Marko Varga, György ^b   Andersson, Roland ^a  

^a LUND UNIVERSITY   (Sweden)

^b LUND UNIVERSITY   (Sweden)

Author keywords

Biomarker; Diagnostics; Mass spectrometry; Pancreatic cancer; Proteomics

Indexed keywords

ASPORIN; CD9 ANTIGEN; FIBRONECTIN 1; GALECTIN 1; GELSOLIN; INTERCELLULAR ADHESION MOLECULE 1; METALLOPROTEINASE INHIBITOR 1; MONOCYTE CHEMOTACTIC PROTEIN 3; SOMATOMEDIN BINDING PROTEIN 2; STROMAL CELL DERIVED FACTOR 4; TRANSFORMING GROWTH FACTOR BETA; TUMOR MARKER; UNCLASSIFIED DRUG;

CANCER GROWTH; CANCER PROGNOSIS; CELL ADHESION; CELL INVASION; CELL PROLIFERATION; HUMAN; IMMUNE RESPONSE; ISOTOPE LABELING; LABEL FREE QUANTIFICATION; MASS SPECTROMETRY; METASTASIS; PANCREAS CANCER; PREDICTION; PROCESS DEVELOPMENT; PROTEIN ANALYSIS; PROTEIN DEEP MINING; PROTEIN DETERMINATION; PROTEIN TARGETING; PROTEOMICS; QUANTITATIVE ANALYSIS; REVIEW; METABOLISM; PANCREATIC NEOPLASMS; PROCEDURES; TRANSLATIONAL RESEARCH;

HUMANS; MASS SPECTROMETRY; PANCREATIC NEOPLASMS; TRANSLATIONAL MEDICAL RESEARCH; TUMOR MARKERS, BIOLOGICAL;

EID: 84899626810     PISSN: None     EISSN: 14795876     Source Type: Journal    
DOI: 10.1186/1479-5876-12-87     Document Type: Review

References (151)

1. Anderson NL. The roles of multiple proteomic platforms in a pipeline for new diagnostics. Mol Cell Proteomics 2005, 4:1441-1444.
2. Vegvari A, Marko-Varga G. Clinical protein science and bioanalytical mass spectrometry with an emphasis on lung cancer. Chem Rev 2010, 110:3278-3298.
3. Végvári T, Rezeli M, Döme B, Fehniger TE, Marko-Varga G. Translation Science for Targeted Personalized Medicine Treatments in "Selected Presentations from the 2011 Sino-American Symposium on Clinical and Translational Medicine" 2011, Washington, DC: Science/AAAS.
4. Zolg JW, Langen H. How industry is approaching the search for new diagnostic markers and biomarkers. Mol Cell Proteomics 2004, 3:345-354.
5. Siegel R, Naishadham D, Jemal A. Cancer statistics, 2013. CA Cancer J Clin 2013, 63:11-30.
6. Vincent A, Herman J, Schulick R, Hruban RH, Goggins M. Pancreatic cancer. Lancet 2011, 378:607-620.
7. Ferlay J, Shin HR, Bray F, Forman D, Mathers C, Parkin DM. Estimates of worldwide burden of cancer in 2008: GLOBOCAN 2008. Int J Cancer 2010, 127:2893-2917.
8. Tingstedt B, Andersson E, Flink A, Bolin K, Lindgren B, Andersson R. Pancreatic cancer, healthcare cost, and loss of productivity: a register-based approach. World J Surg 2011, 35:2298-2305.
9. Egawa S, Takeda K, Fukuyama S, Motoi F, Sunamura M, Matsuno S. Clinicopathological aspects of small pancreatic cancer. Pancreas 2004, 28:235-240.
10. Ariyama J, Suyama M, Satoh K, Sai J. Imaging of small pancreatic ductal adenocarcinoma. Pancreas 1998, 16:396-401.
11. Glenn JSW, Kurtzman SH, Steinberg SM, Sindelar WF. Evaluation of the utility of a radioimmunoassay for serum CA 19-9 levels in patients before and after treatment of carcinoma of the pancreas. J Clin Oncol 1988, 6:462-468.
12. Goonetilleke KSSA. Systematic review of carbohydrate antigen (CA 19-9) as a biochemical marker in the diagnosis of pancreatic cancer. Eur J Surg Oncol 2007, 33:266-270.
13. World Health Organization Classification of Tumours of the Digestive System 2010, Lyon: IARC Press, Bosman FT, Carneiro F, Hruban RH, Theise ND.
14. Klöppel G, Hruban RH, Longnecker DS, Adler G, Kern SE, Partanen TJ. Ductal adenocarcinoma of the pancreas. In: Hamilton SR, Aaltonen LA, eds. World Health Organization Classification of Tumours. Pathology and Genetics of Tumours of the Digestive System 2000, Lyon: IARC Press.
15. Kim JELK, Lee JK, Paik SW, Rhee JC, Choi KW. Clinical usefulness of carbohydrate antigen 19-9 as a screening test for pancreatic cancer in an asymptomatic population. J Gastroenterol Hepatol 2004, 19:182-186.
16. Kawai S, Suzuki K, Nishio K, Ishida Y, Okada R, Goto Y, Naito M, Wakai K, Ito Y, Hamajima N. Smoking and serum CA19-9 levels according to Lewis and secretor genotypes. Int J Cancer 2008, 123:2880-2884.
17. Duffy MJ, Sturgeon C, Lamerz R, Haglund C, Holubec VL, Klapdor R, Nicolini A, Topolcan O, Heinemann V. Tumor markers in pancreatic cancer: a European Group on Tumor Markers (EGTM) status report. Ann Oncol 2010, 21:441-447.
18. Wulfkuhle JD, Liotta LA, Petricoin EF. Proteomic applications for the early detection of cancer. Nat Rev Cancer 2003, 3:267-275.
19. Paik YK, Jeong SK, Omenn GS, Uhlen M, Hanash S, Cho SY, Lee HJ, Na K, Choi EY, Yan F, Zhang F, Zhang Y, Snyder M, Cheng Y, Chen R, Marko-Varga G, Deutsch EW, Kim H, Kwon JY, Aebersold R, Bairoch A, Taylor AD, Kim KY, Lee EY, Hochstrasser D, Legrain P, Hancock WS. The chromosome-centric human proteome project for cataloging proteins encoded in the genome. Nat Biotechnol 2012, 30:221-223.
20. Kondo T, Tasaka T, Sano F, Matsuda K, Kubo Y, Matsuhashi Y, Nakanishi H, Sadahira Y, Wada H, Sugihara T, Tohyama K. Philadelphia chromosome-positive acute myeloid leukemia (Ph+AML) treated with imatinib mesylate (IM): a report with IM plasma concentration and bcr-abl transcripts. Leuk Res 2009, 33:e137-e138.
21. Campbell PJ, Yachida S, Mudie LJ, Stephens PJ, Pleasance ED, Stebbings LA, Morsberger LA, Latimer C, McLaren S, Lin ML, McBride DJ, Varela I, Nik-Zainal SA, Leroy C, Jia M, Menzies A, Butler AP, Teague JW, Griffin CA, Burton J, Swerdlow H, Quail MA, Stratton MR, Iacobuzio-Donahue C, Futreal PA. The patterns and dynamics of genomic instability in metastatic pancreatic cancer. Nature 2010, 467:1109-1113.
22. Jones S, Zhang X, Parsons DW, Lin JC, Leary RJ, Angenendt P, Mankoo P, Carter H, Kamiyama H, Jimeno A, Hong SM, Fu B, Lin MT, Calhoun ES, Kamiyama M, Walter K, Nikolskaya T, Nikolsky Y, Hartigan J, Smith DR, Hidalgo M, Leach SD, Klein AP, Jaffee EM, Goggins M, Maitra A, Iacobuzio-Donahue C, Eshleman JR, Kern SE, Hruban RH, et al. Core signaling pathways in human pancreatic cancers revealed by global genomic analyses. Science 2008, 321:1801-1806.
23. Fenn JB, Mann M, Meng CK, Wong SF, Whitehouse CM. Electrospray ionization for mass spectrometry of large biomolecules. Science 1989, 246:64-71.
24. Karas M, Bahr U, Hillenkamp F. UV laser matrix desorption/ionization mass spectrometry of proteins in the 100 000 dalton range. Int J Mass Spectrom Ion Processes 1989, 92:231-242.
25. Tanaka K, Waki H, Ido Y, Akita S, Yoshida Y, Yoshida T, Matsuo T. Protein and polymer analyses up to m/z 100 000 by laser ionization time-of-flight mass spectrometry. Rapid Commun Mass Spectrom 1988, 2:151-153.
26. Biomarkers Definitions Working Group Biomarkers and surrogate endpoints: preferred definitions and conceptual framework. Clin Pharmacol Ther 2001, 69:89-95. Biomarkers Definitions Working Group.
27. Winter JM, Yeo CJ, Brody JR. Diagnostic, prognostic, and predictive biomarkers in pancreatic cancer. J Surg Oncol 2013, 107:15-22.
28. Baumgart S, Ellenrieder V, Fernandez-Zapico ME. Oncogenic transcription factors: cornerstones of inflammation-linked pancreatic carcinogenesis. Gut 2013, 62:310-316.
29. Donnarumma F, Végvári A, Rezeli M, Welinder C, Jansson B, Marko-Varga G. Accessing microenvironment compartments in FFPE-tissues by protein expression analysis. Bioanalysis 2013, In press.
30. Takadate T, Onogawa T, Fukuda T, Motoi F, Suzuki T, Fujii K, Kihara M, Mikami S, Bando Y, Maeda S, Ishida K, Minowa T, Hanagata N, Ohtsuka H, Katayose Y, Egawa S, Nishimura T, Unno M. 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, 132:1368-1382.
31. Marko-Varga GA, Fehniger TE. Microscale protein expression profiling during disease evolvement. J Chromatogr A 2004, 1053:279-290.
32. Honda K, Ono M, Shitashige M, Masuda M, Kamita M, Miura N, Yamada T. Proteomic approaches to the discovery of cancer biomarkers for early detection and personalized medicine. Jpn J Clin Oncol 2013, 43:103-109.
33. Anderson NL, Anderson NG. The human plasma proteome: history, character, and diagnostic prospects. Mol Cell Proteomics 2002, 1:845-867.
34. O'Farrell PH. High resolution two-dimensional electrophoresis of proteins. J Biol Chem 1975, 250:4007-4021.
35. Gronborg M, Bunkenborg J, Kristiansen TZ, Jensen ON, Yeo CJ, Hruban RH, Maitra A, Goggins MG, Pandey A. Comprehensive proteomic analysis of human pancreatic juice. J Proteome Res 2004, 3:1042-1055.
36. Zhou L, Lu Z, Yang A, Deng R, Mai C, Sang X, Faber KN, Lu X. Comparative proteomic analysis of human pancreatic juice: methodological study. Proteomics 2007, 7:1345-1355.
37. Abdallah CD-GE, Renaut J, Sergeant K. Gel-based and gel-free quantitative proteomics approaches at a glance. Int J Plant Genomics 2012, Article ID 494572.
38. Cox J, Mann M. Is proteomics the new genomics?. Cell 2007, 130:395-398.
39. Mann M. Comparative analysis to guide quality improvements in proteomics. Nat Methods 2009, 6:717-719.
40. Nilsson T, Mann M, Aebersold R, Yates JR, Bairoch A, Bergeron JJ. Mass spectrometry in high-throughput proteomics: ready for the big time. Nat Methods 2010, 7:681-685.
41. Rezeli M, Vegvari A, Fehniger TE, Laurell T, Marko-Varga G. Moving towards high density clinical signature studies with a human proteome catalogue developing multiplexing mass spectrometry assay panels. J Clin Bioinforma 2011, 1:7.
42. Choudhary C, Mann M. Decoding signalling networks by mass spectrometry-based proteomics. Nat Rev Mol Cell Biol 2010, 11:427-439.
43. Bondarenko PV, Chelius D, Shaler TA. Identification and relative quantitation of protein mixtures by enzymatic digestion followed by capillary reversed-phase liquid chromatography-tandem mass spectrometry. Anal Chem 2002, 74:4741-4749.
44. Wang W, Zhou H, Lin H, Roy S, Shaler TA, Hill LR, Norton S, Kumar P, Anderle M, Becker CH. Quantification of proteins and metabolites by mass spectrometry without isotopic labeling or spiked standards. Anal Chem 2003, 75:4818-4826.
45. Lundgren DH, Hwang SI, Wu L, Han DK. Role of spectral counting in quantitative proteomics. Expert Rev Proteomics 2010, 7:39-53.
46. Liu H, Sadygov RG, Yates JR. A model for random sampling and estimation of relative protein abundance in shotgun proteomics. Anal Chem 2004, 76:4193-4201.
47. Searle BC. Scaffold: a bioinformatic tool for validating MS/MS-based proteomic studies. Proteomics 2010, 10:1265-1269.
48. Richter R, Schulz-Knappe P, Schrader M, Standker L, Jurgens M, Tammen H, Forssmann WG. Composition of the peptide fraction in human blood plasma: database of circulating human peptides. J Chromatogr B Biomed Sci Appl 1999, 726:25-35.
49. Turtoi A, Musmeci D, Wang Y, Dumont B, Somja J, Bevilacqua G, De Pauw E, Delvenne P, Castronovo V. Identification of novel accessible proteins bearing diagnostic and therapeutic potential in human pancreatic ductal adenocarcinoma. J Proteome Res 2011, 10:4302-4313.
50. Golembieski WA, Rempel SA. cDNA array analysis of SPARC-modulated changes in glioma gene expression. J Neurooncol 2002, 60:213-226.
51. Ivanov SV, Ivanova AV, Salnikow K, Timofeeva O, Subramaniam M, Lerman MI. Two novel VHL targets, TGFBI (BIGH3) and its transactivator KLF10, are up-regulated in renal clear cell carcinoma and other tumors. Biochem Biophys Res Commun 2008, 370:536-540.
52. Ma C, Rong Y, Radiloff DR, Datto MB, Centeno B, Bao S, Cheng AW, Lin F, Jiang S, Yeatman TJ, Wang XF. Extracellular matrix protein betaig-h3/TGFBI promotes metastasis of colon cancer by enhancing cell extravasation. Genes Dev 2008, 22:308-321.
53. Yamanaka M, Kimura F, Kagata Y, Kondoh N, Asano T, Yamamoto M, Hayakawa M. BIGH3 is overexpressed in clear cell renal cell carcinoma. Oncol Rep 2008, 19:865-874.
54. Ahmed W, Kucich U, Abrams W, Bashir M, Rosenbloom J, Segade F, Mecham R, Rosenbloom J. Signaling pathway by which TGF-beta1 increases expression of latent TGF-beta binding protein-2 at the transcriptional level. Connect Tissue Res 1998, 37:263-276.
55. Vehvilainen P, Hyytiainen M, Keski-Oja J. Latent transforming growth factor-beta-binding protein 2 is an adhesion protein for melanoma cells. J Biol Chem 2003, 278:24705-24713.
56. Nakajima M, Kizawa H, Saitoh M, Kou I, Miyazono K, Ikegawa S. Mechanisms for asporin function and regulation in articular cartilage. J Biol Chem 2007, 282:32185-32192.
57. Zhang J, Song M, Wang J, Sun M, Wang B, Li R, Huang Y, Hou L, Jin Y, Wang M, Tang J. Enoyl coenzyme A hydratase 1 is an important factor in the lymphatic metastasis of tumors. Biomed Pharmacother 2011, 65:157-162.
58. Yu L, Wang L, Chen S. Olfactomedin 4, a novel marker for the differentiation and progression of gastrointestinal cancers. Neoplasma 2011, 58:9-13.
59. Zhang L, Ding F, Cao W, Liu Z, Liu W, Yu Z, Wu Y, Li W, Li Y, Liu Z. Stomatin-like protein 2 is overexpressed in cancer and involved in regulating cell growth and cell adhesion in human esophageal squamous cell carcinoma. Clin Cancer Res 2006, 12:1639-1646.
60. Cao W, Zhang B, Ding F, Zhang W, Sun B, Liu Z. Expression of SLP-2 was associated with invasion of esophageal squamous cell carcinoma. PLoS One 2013, 8:e63890.
61. Cui Z, Zhang L, Hua Z, Cao W, Feng W, Liu Z. Stomatin-like protein 2 is overexpressed and related to cell growth in human endometrial adenocarcinoma. Oncol Rep 2007, 17:829-833.
62. Chan DA, Sutphin PD, Nguyen P, Turcotte S, Lai EW, Banh A, Reynolds GE, Chi JT, Wu J, Solow-Cordero DE, Bonnet M, Flanagan JU, Bouley DM, Graves EE, Denny WA, Hay MP, Giaccia AJ. Targeting GLUT1 and the Warburg effect in renal cell carcinoma by chemical synthetic lethality. Sci Transl Med 2011, 3:94ra70.
63. Pizzi S, Porzionato A, Pasquali C, Guidolin D, Sperti C, Fogar P, Macchi V, De Caro R, Pedrazzoli S, Parenti A. Glucose transporter-1 expression and prognostic significance in pancreatic carcinogenesis. Histol Histopathol 2009, 24:175-185.
64. Ito H, Duxbury M, Zinner MJ, Ashley SW, Whang EE. Glucose transporter-1 gene expression is associated with pancreatic cancer invasiveness and MMP-2 activity. Surgery 2004, 136:548-556.
65. Paulo JA, Lee LS, Banks PA, Steen H, Conwell DL. Proteomic analysis of formalin-fixed paraffin-embedded pancreatic tissue using liquid chromatography tandem mass spectrometry. Pancreas 2012, 41:175-185.
66. Mogami T, Yokota N, Asai-Sato M, Yamada R, Koizume S, Sakuma Y, Yoshihara M, Nakamura Y, Takano Y, Hirahara F, Miyagi Y, Miyagi E. Annexin A4 is involved in proliferation, chemo-resistance and migration and invasion in ovarian clear cell adenocarcinoma cells. PLoS One 2013, 8:e80359.
67. Deng S, Wang J, Hou L, Li J, Chen G, Jing B, Zhang X, Yang Z. Annexin A1, A2, A4 and A5 play important roles in breast cancer, pancreatic cancer and laryngeal carcinoma, alone and/or synergistically. Oncol Lett 2013, 5:107-112.
68. Schwarz RE, Awasthi N, Konduri S, Caldwell L, Cafasso D, Schwarz MA. Antitumor effects of EMAP II against pancreatic cancer through inhibition of fibronectin-dependent proliferation. Cancer Biol Ther 2010, 9:632-639.
69. Matsubara J, Honda K, Ono M, Tanaka Y, Kobayashi M, Jung G, Yanagisawa K, Sakuma T, Nakamori S, Sata N, Nagai H, Ioka T, Okusaka T, Kosuge T, Tsuchida A, Shimahara M, Yasunami Y, Chiba T, Hirohashi S, Yamada T. Reduced plasma level of CXC chemokine ligand 7 in patients with pancreatic cancer. Cancer Epidemiol Biomarkers Prev 2011, 20:160-171.
70. Villanueva J, Shaffer DR, Philip J, Chaparro CA, Erdjument-Bromage H, Olshen AB, Fleisher M, Lilja H, Brogi E, Boyd J, Sanchez-Carbayo M, Holland EC, Cordon-Cardo C, Scher HI, Tempst P. Differential exoprotease activities confer tumor-specific serum peptidome patterns. J Clin Invest 2006, 116:271-284.
71. Van den Steen PE, Proost P, Wuyts A, Van Damme J, Opdenakker G. Neutrophil gelatinase B potentiates interleukin-8 tenfold by aminoterminal processing, whereas it degrades CTAP-III, PF-4, and GRO-alpha and leaves RANTES and MCP-2 intact. Blood 2000, 96:2673-2681.
72. Tian M, Cui YZ, Song GH, Zong MJ, Zhou XY, Chen Y, Han JX. Proteomic analysis identifies MMP-9, DJ-1 and A1BG as overexpressed proteins in pancreatic juice from pancreatic ductal adenocarcinoma patients. BMC Cancer 2008, 8:241.
73. Gevaert K, Impens F, Ghesquiere B, Van Damme P, Lambrechts A, Vandekerckhove J. Stable isotopic labeling in proteomics. Proteomics 2008, 8:4873-4885.
74. Picotti P, Aebersold R. Selected reaction monitoring-based proteomics: workflows, potential, pitfalls and future directions. Nat Methods 2012, 9:555-566.
75. Colzani M, Schutz F, Potts A, Waridel P, Quadroni M. Relative protein quantification by isobaric SILAC with immonium ion splitting (ISIS). Mol Cell Proteomics 2008, 7:927-937.
76. Pan S, Brentnall TA, Kelly K, Chen R. Tissue proteomics in pancreatic cancer study: discovery, emerging technologies, and challenges. Proteomics 2013, 13:710-721.
77. Amanchy R, Kalume DE, Pandey A. Stable isotope labeling with amino acids in cell culture (SILAC) for studying dynamics of protein abundance and posttranslational modifications. Sci STKE 2005 2005, 267:pl2.
78. Everley PA, Krijgsveld J, Zetter BR, Gygi SP. Quantitative cancer proteomics: stable isotope labeling with amino acids in cell culture (SILAC) as a tool for prostate cancer research. Mol Cell Proteomics 2004, 3:729-735.
79. Ong SEBB, Kratchmarova I, Kristensen DB, Steen H, Pandey A, Mann M. Stable isotope labeling by amino acids in cell culture, SILAC, as a simple and accurate approach to expression proteomics. Mol Cell Proteomics 2002, 1:376-386.
80. Geiger T, Cox J, Ostasiewicz P, Wisniewski JR, Mann M. Super-SILAC mix for quantitative proteomics of human tumor tissue. Nat Methods 2010, 7:383-385.
81. Gronborg M, Kristiansen TZ, Iwahori A, Chang R, Reddy R, Sato N, Molina H, Jensen ON, Hruban RH, Goggins MG, Maitra A, Pandey A. Biomarker discovery from pancreatic cancer secretome using a differential proteomic approach. Mol Cell Proteomics 2006, 5:157-171.
82. Wang HX, Li Q, Sharma C, Knoblich K, Hemler ME. Tetraspanin protein contributions to cancer. Biochem Soc Trans 2011, 39:547-552.
83. Sho M, Adachi M, Taki T, Hashida H, Konishi T, Huang CL, Ikeda N, Nakajima Y, Kanehiro H, Hisanaga M, Nakano H, Miyake M. Transmembrane 4 superfamily as a prognostic factor in pancreatic cancer. Int J Cancer 1998, 79:509-516.
84. Whitelock JM, Melrose J, Iozzo RV. Diverse cell signaling events modulated by perlecan. Biochemistry 2008, 47:11174-11183.
85. Jiang X, Multhaupt H, Chan E, Schaefer L, Schaefer RM, Couchman JR. Essential contribution of tumor-derived perlecan to epidermal tumor growth and angiogenesis. J Histochem Cytochem 2004, 52:1575-1590.
86. Mahley RW. Apolipoprotein E: cholesterol transport protein with expanding role in cell biology. Science 1988, 240:622-630.
87. Hui DY, Basford JE. Distinct signaling mechanisms for apoE inhibition of cell migration and proliferation. Neurobiol Aging 2005, 26:317-323.
88. Zhang H, Wu LM, Wu J. Cross-talk between apolipoprotein E and cytokines. Mediators Inflamm 2011, 2011:949072.
89. Chen J, Chen LJ, Yang RB, Xia YL, Zhou HC, Wu W, Lu Y, Hu LW, Zhao Y. Expression and clinical significance of apolipoprotein E in pancreatic ductal adenocarcinoma. Med Oncol 2013, 30:583.
90. Chen J, Wu W, Zhen C, Zhou H, Yang R, Chen L, Hu L. Expression and clinical significance of complement C3, complement C4b1 and apolipoprotein E in pancreatic cancer. Oncol Lett 2013, 6:43-48.
91. Martinez-Clemente M, Ferre N, Gonzalez-Periz A, Lopez-Parra M, Horrillo R, Titos E, Moran-Salvador E, Miquel R, Arroyo V, Funk CD, Claria J. 5-lipoxygenase deficiency reduces hepatic inflammation and tumor necrosis factor alpha-induced hepatocyte damage in hyperlipidemia-prone ApoE-null mice. Hepatology 2010, 51:817-827.
92. Liang JJ, Zhu S, Bruggeman R, Zaino RJ, Evans DB, Fleming JB, Gomez HF, Zander DS, Wang H. High levels of expression of human stromal cell-derived factor-1 are associated with worse prognosis in patients with stage II pancreatic ductal adenocarcinoma. Cancer Epidemiol Biomarkers Prev 2010, 19:2598-2604.
93. Walsh N, Clynes M, Crown J, O'Donovan N. Alterations in integrin expression modulates invasion of pancreatic cancer cells. J Exp Clin Cancer Res 2009, 28:140.
94. Yu KH, Barry CG, Austin D, Busch CM, Sangar V, Rustgi AK, Blair IA. Stable isotope dilution multidimensional liquid chromatography-tandem mass spectrometry for pancreatic cancer serum biomarker discovery. J Proteome Res 2009, 8:1565-1576.
95. Roland CL, Dineen SP, Toombs JE, Carbon JG, Smith CW, Brekken RA, Barnett CC. Tumor-derived intercellular adhesion molecule-1 mediates tumor-associated leukocyte infiltration in orthotopic pancreatic xenografts. Exp Biol Med (Maywood) 2010, 235:263-270.
96. Tempia-Caliera AA, Horvath LZ, Zimmermann A, Tihanyi TT, Korc M, Friess H, Buchler MW. Adhesion molecules in human pancreatic cancer. J Surg Oncol 2002, 79:93-100.
97. Kikkawa Y, Miner JH. Review: Lutheran/B-CAM: a laminin receptor on red blood cells and in various tissues. Connect Tissue Res 2005, 46:193-199.
98. Gygi SPRB, Gerber SA, Turecek F, Gelb MH, Aebersold R. Quantitative analysis of complex protein mixtures using isotope-coded affinity tags. Nat Biotechnol 1999, 17:994-999.
99. Yi ECLX, Cooke K, Lee H, Raught B, Page A, Aneliunas V, Hieter P, Goodlett DR, Aebersold R. Increased quantitative proteome coverage with (13)C/(12)C-based, acid-cleavable isotope-coded affinity tag reagent and modified data acquisition scheme. Proteomics 2005, 5:380-387.
100. Chen R, Yi EC, Donohoe S, Pan S, Eng J, Cooke K, Crispin DA, Lane Z, Goodlett DR, Bronner MP, Aebersold R, Brentnall TA. Pancreatic cancer proteome: the proteins that underlie invasion, metastasis, and immunologic escape. Gastroenterology 2005, 129:1187-1197.
101. Zheng L, Foley K, Huang L, Leubner A, Mo G, Olino K, Edil BH, Mizuma M, Sharma R, Le DT, Anders RA, Illei PB, Van Eyk JE, Maitra A, Laheru D, Jaffee EM. Tyrosine 23 phosphorylation-dependent cell-surface localization of annexin A2 is required for invasion and metastases of pancreatic cancer. PLoS One 2011, 6:e19390.
102. Zhang X, Liu S, Guo C, Zong J, Sun MZ. The association of annexin A2 and cancers. Clin Transl Oncol 2012, 14:634-640.
103. Chen R, Pan S, Yi EC, Donohoe S, Bronner MP, Potter JD, Goodlett DR, Aebersold R, Brentnall TA. Quantitative proteomic profiling of pancreatic cancer juice. Proteomics 2006, 6:3871-3879.
104. Busund LT, Richardsen E, Busund R, Ukkonen T, Bjornsen T, Busch C, Stalsberg H. Significant expression of IGFBP2 in breast cancer compared with benign lesions. J Clin Pathol 2005, 58:361-366.
105. Hsieh D, Hsieh A, Stea B, Ellsworth R. IGFBP2 promotes glioma tumor stem cell expansion and survival. Biochem Biophys Res Commun 2010, 397:367-372.
106. Pan S, Chen R, Crispin DA, May D, Stevens T, McIntosh MW, Bronner MP, Ziogas A, Anton-Culver H, Brentnall TA. Protein alterations associated with pancreatic cancer and chronic pancreatitis found in human plasma using global quantitative proteomics profiling. J Proteome Res 2011, 10:2359-2376.
107. Bloomston M, Shafii A, Zervos EE, Rosemurgy AS. TIMP-1 overexpression in pancreatic cancer attenuates tumor growth, decreases implantation and metastasis, and inhibits angiogenesis. J Surg Res 2002, 102:39-44.
108. Thompson ASJ, Kuhn K, Kienle S, Schwarz J, Schmidt G, Neumann T, Johnstone R, Mohammed AK, Hamon C. Tandem mass tags: a novel quantification strategy for comparative analysis of complex protein mixtures by MS/MS. Anal Chem 2003, 75:1895-1904.
109. Dayon LHA, Licker V, Turck N, Kuhn K, Hochstrasser DF, Burkhard PR, Sanchez JC. Relative quantification of proteins in human cerebrospinal fluids by MS/MS using 6-plex isobaric tags. Anal Chem 2008, 80:2921-2931.
110. Sinclair J, Timms JF. Quantitative profiling of serum samples using TMT protein labelling, fractionation and LC-MS/MS. Methods 2011, 54:361-369.
111. Ni XG, Zhou L, Wang GQ, Liu SM, Bai XF, Liu F, Peppelenbosch MP, Zhao P. The ubiquitin-proteasome pathway mediates gelsolin protein downregulation in pancreatic cancer. Mol Med 2008, 14:582-589.
112. Abulaizi M, Tomonaga T, Satoh M, Sogawa K, Matsushita K, Kodera Y, Obul J, Takano S, Yoshitomi H, Miyazaki M, Nomura F. The application of a three-step proteome analysis for identification of new biomarkers of pancreatic cancer. Int J Proteomics 2011, 2011:628787.
113. Wang R, Zhang T, Ma Z, Wang Y, Cheng Z, Xu H, Li W, Wang X. The interaction of coagulation factor XII and monocyte/macrophages mediating peritoneal metastasis of epithelial ovarian cancer. Gynecol Oncol 2010, 117:460-466.
114. Fedail SS, Harvey RF, Salmon PR, Brown P, Read AE. Trypsin and lactoferrin levels in pure pancreatic juice in patients with pancreatic disease. Gut 1979, 20:983-986.
115. Deng M, Zhang W, Tang H, Ye Q, Liao Q, Zhou Y, Wu M, Xiong W, Zheng Y, Guo X, Qin Z, He W, Zhou M, Xiang J, Li X, Ma J, Li G. Lactotransferrin acts as a tumor suppressor in nasopharyngeal carcinoma by repressing AKT through multiple mechanisms. Oncogene 2013, 32:4273-4283.
116. Beck F, Burkhart JM, Geiger J, Zahedi RP, Sickmann A. Robust workflow for iTRAQ-based peptide and protein quantification. Methods Mol Biol 2012, 893:101-113.
117. Ting L, Rad R, Gygi SP, Haas W. MS3 eliminates ratio distortion in isobaric multiplexed quantitative proteomics. Nat Methods 2011, 8:937-940.
118. Ow SY, Salim M, Noirel J, Evans C, Rehman I, Wright PC. iTRAQ underestimation in simple and complex mixtures: "the good, the bad and the ugly". J Proteome Res 2009, 8:5347-5355.
119. Pan S, Chen R, Reimel BA, Crispin DA, Mirzaei H, Cooke K, Coleman JF, Lane Z, Bronner MP, Goodlett DR, McIntosh MW, Traverso W, Aebersold R, Brentnall TA. Quantitative proteomics investigation of pancreatic intraepithelial neoplasia. Electrophoresis 2009, 30:1132-1144.
120. Sawai H, Okada Y, Funahashi H, Takahashi H, Matsuo Y, Yasuda A, Ochi N, Takeyama H, Manabe T. Basement membrane proteins play an important role in the invasive processes of human pancreatic cancer cells. J Surg Res 2008, 144:117-123.
121. Fitzner B, Walzel H, Sparmann G, Emmrich J, Liebe S, Jaster R. Galectin-1 is an inductor of pancreatic stellate cell activation. Cell Signal 2005, 17:1240-1247.
122. Masamune A, Satoh M, Hirabayashi J, Kasai K, Satoh K, Shimosegawa T. Galectin-1 induces chemokine production and proliferation in pancreatic stellate cells. Am J Physiol Gastrointest Liver Physiol 2006, 290:G729-G736.
123. Kikuchi S, Honda K, Tsuda H, Hiraoka N, Imoto I, Kosuge T, Umaki T, Onozato K, Shitashige M, Yamaguchi U, Ono M, Tsuchida A, Aoki T, Inazawa J, Hirohashi S, Yamada T. Expression and gene amplification of actinin-4 in invasive ductal carcinoma of the pancreas. Clin Cancer Res 2008, 14:5348-5356.
124. Welsch T, Keleg S, Bergmann F, Bauer S, Hinz U, Schmidt J. Actinin-4 expression in primary and metastasized pancreatic ductal adenocarcinoma. Pancreas 2009, 38:968-976.
125. Hayashida Y, Honda K, Idogawa M, Ino Y, Ono M, Tsuchida A, Aoki T, Hirohashi S, Yamada T. E-cadherin regulates the association between beta-catenin and actinin-4. Cancer Res 2005, 65:8836-8845.
126. Anderson L, Hunter CL. Quantitative mass spectrometric multiple reaction monitoring assays for major plasma proteins. Mol Cell Proteomics 2006, 5:573-588.
127. Whiteaker JR, Zhao L, Abbatiello SE, Burgess M, Kuhn E, Lin C, Pope ME, Razavi M, Anderson NL, Pearson TW, Carr SA, Paulovich AG. Evaluation of large scale quantitative proteomic assay development using peptide affinity-based mass spectrometry. Mol Cell Proteomics 2011, 10:M110 005645.
128. Whiteaker JR, Zhao L, Anderson L, Paulovich AG. An automated and multiplexed method for high throughput peptide immunoaffinity enrichment and multiple reaction monitoring mass spectrometry-based quantification of protein biomarkers. Mol Cell Proteomics 2010, 9:184-196.
129. Kamiie J, Ohtsuki S, Iwase R, Ohmine K, Katsukura Y, Yanai K, Sekine Y, Uchida Y, Ito S, Terasaki T. Quantitative atlas of membrane transporter proteins: development and application of a highly sensitive simultaneous LC/MS/MS method combined with novel in-silico peptide selection criteria. Pharm Res 2008, 25:1469-1483.
130. Scherl A, Shaffer SA, Taylor GK, Kulasekara HD, Miller SI, Goodlett DR. Genome-specific gas-phase fractionation strategy for improved shotgun proteomic profiling of proteotypic peptides. Anal Chem 2008, 80:1182-1191.
131. Lange V, Picotti P, Domon B, Aebersold R. Selected reaction monitoring for quantitative proteomics: a tutorial. Mol Syst Biol 2008, 4:222.
132. Unwin RD, Griffiths JR, Leverentz MK, Grallert A, Hagan IM, Whetton AD. Multiple reaction monitoring to identify sites of protein phosphorylation with high sensitivity. Mol Cell Proteomics 2005, 4:1134-1144.
133. Griffiths JR, Unwin RD, Evans CA, Leech SH, Corfe BM, Whetton AD. The application of a hypothesis-driven strategy to the sensitive detection and location of acetylated lysine residues. J Am Soc Mass Spectrom 2007, 18:1423-1428.
134. Duncan MWYA, Patterson SD. Quantifying proteins by mass spectrometry: the selectivity of SRM is only part of the problem. Proteomics 2009, 9:1124-1127.
135. MacLean B, Tomazela DM, Shulman N, Chambers M, Finney GL, Frewen B, Kern R, Tabb DL, Liebler DC, MacCoss MJ. Skyline: an open source document editor for creating and analyzing targeted proteomics experiments. Bioinformatics 2010, 26:966-968.
136. Martin DB, Holzman T, May D, Peterson A, Eastham A, Eng J, McIntosh M. MRMer, an interactive open source and cross-platform system for data extraction and visualization of multiple reaction monitoring experiments. Mol Cell Proteomics 2008, 7:2270-2278.
137. Sherwood CA, Eastham A, Lee LW, Risler J, Mirzaei H, Falkner JA, Martin DB. Rapid optimization of MRM-MS instrument parameters by subtle alteration of precursor and product m/z targets. J Proteome Res 2009, 8:3746-3751.
138. Abbatiello SE, Mani DR, Keshishian H, Carr SA. Automated detection of inaccurate and imprecise transitions in peptide quantification by multiple reaction monitoring mass spectrometry. Clin Chem 2010, 56:291-305.
139. Whiteaker JR, Lin C, Kennedy J, Hou L, Trute M, Sokal I, Yan P, Schoenherr RM, Zhao L, Voytovich UJ, Kelly-Spratt KS, Krasnoselsky A, Gafken PR, Hogan JM, Jones LA, Wang P, Amon L, Chodosh LA, Nelson PS, McIntosh MW, Kemp CJ, Paulovich AG. A targeted proteomics-based pipeline for verification of biomarkers in plasma. Nat Biotechnol 2011, 29:625-634.
140. Yoneyama T, Ohtsuki S, Ono M, Ohmine K, Uchida Y, Yamada T, Tachikawa M, Terasaki T. Quantitative targeted absolute proteomics-based large-scale quantification of proline-hydroxylated alpha-fibrinogen in plasma for pancreatic cancer diagnosis. J Proteome Res 2013, 12:753-762.
141. Baker M. Biorepositories: Building better biobanks. Nature 2012, 486:141-146.
142. Marko-Varga G, Omenn GS, Paik YK, Hancock WS. A first step toward completion of a genome-wide characterization of the human proteome. J Proteome Res 2013, 12:1-5.
143. Liang WS, Craig DW, Carpten J, Borad MJ, Demeure MJ, Weiss GJ, Izatt T, Sinari S, Christoforides A, Aldrich J, Kurdoglu A, Barrett M, Phillips L, Benson H, Tembe W, Braggio E, Kiefer JA, Legendre C, Posner R, Hostetter GH, Baker A, Egan JB, Han H, Lake D, Stites EC, Ramanathan RK, Fonseca R, Stewart AK, Von Hoff D. Genome-wide characterization of pancreatic adenocarcinoma patients using next generation sequencing. PLoS One 2012, 7:e43192.
144. Fagerberg L, Oksvold P, Skogs M, Algenas C, Lundberg E, Ponten F, Sivertsson A, Odeberg J, Klevebring D, Kampf C, Asplund A, Sjöstedt E, Al-Khalili Szigyarto C, Edqvist PH, Olsson I, Rydberg U, Hudson P, Ottosson Takanen J, Berling H, Björling L, Tegel H, Rockberg J, Nilsson P, Navani S, Jirström K, Mulder J, Schwenk JM, Zwahlen M, Hober S, Forsberg M, et al. Contribution of antibody-based protein profiling to the human Chromosome-centric Proteome Project (C-HPP). J Proteome Res 2013, 12:2439-2448.
145. Lane L, Argoud-Puy G, Britan A, Cusin I, Duek PD, Evalet O, Gateau A, Gaudet P, Gleizes A, Masselot A, Zwahlen C, Bairoch A. neXtProt: a knowledge platform for human proteins. Nucleic Acids Res 2012, 40:D76-D83.
146. Harsha HC, Jimeno A, Molina H, Mihalas AB, Goggins MG, Hruban RH, Schulick RD, Kamath U, Maitra A, Hidalgo M, Pandey A. Activated epidermal growth factor receptor as a novel target in pancreatic cancer therapy. J Proteome Res 2008, 7:4651-4658.
147. Ritchie SA, Akita H, Takemasa I, Eguchi H, Pastural E, Nagano H, Monden M, Doki Y, Mori M, Jin W, Sajobi TT, Jayasinghe D, Chitou B, Yamazaki Y, White T, Goodenowe DB. Metabolic system alterations in pancreatic cancer patient serum: potential for early detection. BMC Cancer 2013, 13:416.
148. Krastins B, Prakash A, Sarracino DA, Nedelkov D, Niederkofler EE, Kiernan UA, Nelson R, Vogelsang MS, Vadali G, Garces A, Sutton JN, Peterman S, Byram G, Darbouret B, Pérusse JR, Seidah NG, Coulombe B, Gobom J, Portelius E, Pannee J, Blennow K, Kulasingam V, Couchman L, Moniz C, Lopez MF. Rapid development of sensitive, high-throughput, quantitative and highly selective mass spectrometric targeted immunoassays for clinically important proteins in human plasma and serum. Clin Biochem 2013, 46:399-410.
149. Addona TA, Abbatiello SE, Schilling B, Skates SJ, Mani DR, Bunk DM, Spiegelman CH, Zimmerman LJ, Ham A-JL, Keshishian H, Hall SC, Allen S, Blackman RK, Borchers CH, Buck C, Cardasis HL, Cusack MP, Dodder NG, Gibson BW, Held JM, Hiltke T, Jackson A, Johansen EB, Kinsinger CR, Li J, Mesri M, Neubert TA, Niles RK, Pulsipher TC, Ransohoff D, et al. Multi-site assessment of the precision and reproducibility of multiple reaction monitoring-based measurements of proteins in plasma. Nat Biotech 2009, 27:633-641.
150. Paik YK, Hancock WS. Uniting ENCODE with genome-wide proteomics. Nat Biotechnol 2012, 30:1065-1067.
151. Lichti CF, Liu H, Shavkunov AS, Mostovenko E, Sulman EP, Ezhilarasan R, Wang Q, Kroes RA, Moskal JC, Fenyo D, Oksuz BA, Conrad CA, Lang FF, Berven FS, Végvári A, Rezeli M, Marko-Varga G, Hober S, Nilsson CL. Integrated chromosome 19 transcriptomic and proteomic data sets derived from glioma cancer stem-cell lines. J Proteome Res 2014, 13:191-199.