Distribution of proteins among the AIP, CP, and PC cohorts

A Proteomic Comparison of Formalin-Fixed Paraffin-Embedded Pancreatic Tissue from Autoimmune Pancreatitis, Chronic Pancreatitis, and Pancreatic Cancer

Joao A Paulo, Vivek Kadiyala, Scott Brizard, Peter A Banks, Hanno Steen, Darwin L Conwell

Abstract


Content Formalin-fixed paraffin-embedded (FFPE) tissue is a standard for specimen preservation, and as such FFPE tissue banks are an untapped resource of histologically-characterized specimens for retrospective biomarker investigation for pancreatic disease. Objectives We use liquid chromatography coupled with tandem mass spectrometry (LC-MS/MS) to compare FFPE specimens from three different diseases of the exocrine pancreas. Design We investigated the proteomic profile of FFPE pancreatic tissue from 9 archived specimens that were histologically classified as: autoimmune pancreatitis (n=3), chronic pancreatitis (n=3), and pancreatic cancer (n=3), using LC-MS/MS. Setting This is a proteomic analysis experiment of FFPE pancreatic tissue in an academic center. Patients FFPE tissue specimens were provided by Dana-Farber/Harvard Cancer Center (Boston, MA, USA). Interventions FFPE tissue specimens were collected via routine surgical resection procedures. Main outcome measures We compared proteins identified from chronic pancreatitis, autoimmune pancreatitis, and pancreatic cancer FFPE pancreatic tissue. Results We identified 386 non-redundant proteins from 9 specimens. Following our filtering criteria, 73, 29, and 53 proteins were identified exclusively in autoimmune pancreatitis, chronic pancreatitis, and pancreatic cancer specimens, respectively. Conclusions We report that differentially-expressed proteins can be identified among FFPE tissues specimens originating from individuals with different histological diagnoses. These proteins merit further confirmation with a greater number of specimens and orthogonal validation, such as immunohistochemistry. The mass spectrometry-based methodology used herein has the potential to enhance diagnostic biomarker and therapeutic target discovery, further advancing pancreatic research.

Image: Distribution of proteins among the AIP, CP, and PC cohorts.


Keywords


Autoimmune Diseases; Biological Markers; Pancreas; Pancreatic Neoplasms; Pancreatitis, Chronic

References


NIH, Opportunities and Challenges in Digestive Diseases Research: Recommendations of the National Commission on Digestive Diseases, U.S. Department of Health and Human Services, National Institutes of Health, NIH publ. no. 08-6514 (2009) 159-167.

I. Nishimori, A. Tamakoshi, M. Otsuki, Prevalence of autoimmune pancreatitis in Japan from a nationwide survey in 2002, J Gastroenterol, 42 Suppl 18 (2007) 6-8.

R.K. Pearson, D.S. Longnecker, S.T. Chari, T.C. Smyrk, K. Okazaki, L. Frulloni, G. Cavallini, Controversies in clinical pancreatology: autoimmune pancreatitis: does it exist?, Pancreas, 27 (2003) 1-13.

I. Nishimori, A. Tamakoshi, S. Kawa, S. Tanaka, K. Takeuchi, T. Kamisawa, H. Saisho, K. Hirano, K. Okamura, N. Yanagawa, M. Otsuki, Influence of steroid therapy on the course of diabetes mellitus in patients with autoimmune pancreatitis: findings from a nationwide survey in Japan, Pancreas, 32 (2006) 244-248.

D.L. Finkelberg, D. Sahani, V. Deshpande, W.R. Brugge, Autoimmune pancreatitis, The New England journal of medicine, 355 (2006) 2670-2676.

R. Pannala, S.T. Chari, Autoimmune pancreatitis, Curr Opin Gastroenterol, 24 (2008) 591-596.

R. Law, M. Bronner, D. Vogt, T. Stevens, Autoimmune pancreatitis: a mimic of pancreatic cancer, Cleveland Clinic journal of medicine, 76 (2009) 607-615.

J.A. Paulo, L.S. Lee, P.A. Banks, H. Steen, D.L. Conwell, Proteomic analysis of formalin-fixed paraffin-embedded pancreatic tissue using liquid chromatography tandem mass spectrometry, Pancreas, 41 (2012) 175-185.

S.R. Shi, R.J. Cote, C.R. Taylor, Antigen retrieval techniques: current perspectives, J Histochem Cytochem, 49 (2001) 931-937.

H. Steen, M. Mann, The ABC's (and XYZ's) of peptide sequencing, Nature reviews, 5 (2004) 699-711.

B.A. Reimel, S. Pan, D.H. May, S.A. Shaffer, D.R. Goodlett, M.W. McIntosh, L.M. Yerian, M.P. Bronner, R. Chen, T.A. Brentnall, Proteomics on Fixed Tissue Specimens - A Review, Curr Proteomics, 6 (2009) 63-69.

B.M. Balgley, T. Guo, K. Zhao, X. Fang, F.A. Tavassoli, C.S. Lee, Evaluation of archival time on shotgun proteomics of formalin-fixed and paraffin-embedded tissues, Journal of proteome research, 8 (2009) 917-925.

X. Jiang, S. Feng, R. Tian, M. Ye, H. Zou, Development of efficient protein extraction methods for shotgun proteome analysis of formalin-fixed tissues, Journal of proteome research, 6 (2007) 1038-1047.

D.E. Palmer-Toy, B. Krastins, D.A. Sarracino, J.B. Nadol, Jr., S.N. Merchant, Efficient method for the proteomic analysis of fixed and embedded tissues, Journal of proteome research, 4 (2005) 2404-2411.

H. Xu, L. Yang, W. Wang, S.R. Shi, C. Liu, Y. Liu, X. Fang, C.R. Taylor, C.S. Lee, B.M. Balgley, Antigen retrieval for proteomic characterization of formalin-fixed and paraffin-embedded tissues, Journal of proteome research, 7 (2008) 1098-1108.

D. Kessner, M. Chambers, R. Burke, D. Agus, P. Mallick, ProteoWizard: open source software for rapid proteomics tools development, Bioinformatics, 24 (2008) 2534-2536.

I.V. Shilov, S.L. Seymour, A.A. Patel, A. Loboda, W.H. Tang, S.P. Keating, C.L. Hunter, L.M. Nuwaysir, D.A. Schaeffer, The Paragon Algorithm, a next generation search engine that uses sequence temperature values and feature probabilities to identify peptides from tandem mass spectra, Mol Cell Proteomics, 6 (2007) 1638-1655.

M.Q. Dong, J.D. Venable, N. Au, T. Xu, S.K. Park, D. Cociorva, J.R. Johnson, A. Dillin, J.R. Yates, 3rd, Quantitative mass spectrometry identifies insulin signaling targets in C. elegans, Science, 317 (2007) 660-663.

H. Liu, R.G. Sadygov, J.R. Yates, 3rd, A model for random sampling and estimation of relative protein abundance in shotgun proteomics, Anal Chem, 76 (2004) 4193-4201.

W. Cheung, M.M. Darfler, H. Alvarez, B.L. Hood, T.P. Conrads, N. Habbe, D.B. Krizman, J. Mollenhauer, G. Feldmann, A. Maitra, Application of a global proteomic approach to archival precursor lesions: deleted in malignant brain tumors 1 and tissue transglutaminase 2 are upregulated in pancreatic cancer precursors, Pancreatology : official journal of the International Association of Pancreatology, 8 (2008) 608-616.

B.L. Hood, M.M. Darfler, T.G. Guiel, B. Furusato, D.A. Lucas, B.R. Ringeisen, I.A. Sesterhenn, T.P. Conrads, T.D. Veenstra, D.B. Krizman, Proteomic analysis of formalin-fixed prostate cancer tissue, Mol Cell Proteomics, 4 (2005) 1741-1753.

P. Ostasiewicz, D.F. Zielinska, M. Mann, J.R. Wisniewski, Proteome, Phosphoproteome, and N-Glycoproteome Are Quantitatively Preserved in Formalin-Fixed Paraffin-Embedded Tissue and Analyzable by High-Resolution Mass Spectrometry, J Proteome Res, (2010).

T. Guo, W. Wang, P.A. Rudnick, T. Song, J. Li, Z. Zhuang, R.J. Weil, D.L. DeVoe, C.S. Lee, B.M. Balgley, Proteome analysis of microdissected formalin-fixed and paraffin-embedded tissue specimens, J Histochem Cytochem, 55 (2007) 763-772.

S.R. Shi, C. Liu, B.M. Balgley, C. Lee, C.R. Taylor, Protein extraction from formalin-fixed, paraffin-embedded tissue sections: quality evaluation by mass spectrometry, J Histochem Cytochem, 54 (2006) 739-743.

L.F. Waanders, K. Chwalek, M. Monetti, C. Kumar, E. Lammert, M. Mann, Quantitative proteomic analysis of single pancreatic islets, Proceedings of the National Academy of Sciences of the United States of America, 106 (2009) 18902-18907.

D.K. Crockett, Z. Lin, C.P. Vaughn, M.S. Lim, K.S. Elenitoba-Johnson, Identification of proteins from formalin-fixed paraffin-embedded cells by LC-MS/MS, Lab Invest, 85 (2005) 1405-1415.

G.M. Cavestro, L. Frulloni, T.M. Neri, P. Seghini, A. Nouvenne, A. Zanetti, P. Bovo, F. Di Mario, L. Okolicsanyi, G. Cavallini, Association of HLA-DRB1*0401 allele with chronic pancreatitis, Pancreas, 26 (2003) 388-391.

T.L. Freitag, C. Cham, H.H. Sung, G.F. Beilhack, I. Durinovic-Bello, S.D. Patel, R.T. Bronson, D. Schuppan, G. Sonderstrup, Human risk allele HLA-DRB1*0405 predisposes class II transgenic Ab0 NOD mice to autoimmune pancreatitis, Gastroenterology, 139 (2010) 281-291.

X. Li, R. Ni, J. Chen, Z. Liu, M. Xiao, F. Jiang, C. Lu, The presence of IGHG1 in human pancreatic carcinomas is associated with immune evasion mechanisms, Pancreas, 40 (2011) 753-761.

T. Yoshida, N. Shiraki, H. Baba, M. Goto, S. Fujiwara, K. Kume, S. Kume, Expression patterns of epiplakin1 in pancreas, pancreatic cancer and regenerating pancreas, Genes Cells, 13 (2008) 667-678.

E. Levi, D.S. Klimstra, A. Andea, O. Basturk, N.V. Adsay, MUC1 and MUC2 in pancreatic neoplasia, J Clin Pathol, 57 (2004) 456-462.

Z. Zhao, H. Liu, X. Wang, Z. Li, Separation and identification of HSP-associated protein complexes from pancreatic cancer cell lines using 2D CN/SDS-PAGE coupled with mass spectrometry, J Biomed Biotechnol, 2011 (2011) 193052.

C.H. Fox, F.B. Johnson, J. Whiting, P.P. Roller, Formaldehyde fixation, J Histochem Cytochem, 33 (1985) 845-853.

R.J. McKenna, Jr., W.V. Houck, New approaches to the minimally invasive treatment of lung cancer, Curr Opin Pulm Med, 11 (2005) 282-286.

K.F. Becker, C. Schott, S. Hipp, V. Metzger, P. Porschewski, R. Beck, J. Nährig, I. Becker, H. Höfler, Quantitative protein analysis from formalin-fixed tissues: implications for translational clinical research and nanoscale molecular diagnosis, The Journal of Pathology, 211 (2007) 370-378.

V. Thongboonkerd, Proteomics of human body fluids : principles, methods, and applications, Humana Press, Totowa, N.J., 2007.

S. Decramer, A. Gonzalez de Peredo, B. Breuil, H. Mischak, B. Monsarrat, J.L. Bascands, J.P. Schanstra, Urine in clinical proteomics, Mol Cell Proteomics, 7 (2008) 1850-1862.

D.M. Good, V. Thongboonkerd, J. Novak, J.L. Bascands, J.P. Schanstra, J.J. Coon, A. Dominiczak, H. Mischak, Body fluid proteomics for biomarker discovery: lessons from the past hold the key to success in the future, J Proteome Res, 6 (2007) 4549-4555.

Y.K. Paik, H. Kim, E.Y. Lee, M.S. Kwon, S.Y. Cho, Overview and introduction to clinical proteomics, Methods Mol Biol, 428 (2008) 1-31.

J. Barratt, P. Topham, Urine proteomics: the present and future of measuring urinary protein components in disease, Cmaj, 177 (2007) 361-368.

G.L. Hortin, D. Sviridov, Diagnostic potential for urinary proteomics, Pharmacogenomics, 8 (2007) 237-255.

H. Muller, H. Brenner, Urine markers as possible tools for prostate cancer screening: review of performance characteristics and practicality, Clinical chemistry, 52 (2006) 562-573.

N.P. Munro, D.A. Cairns, P. Clarke, M. Rogers, A.J. Stanley, J.H. Barrett, P. Harnden, D. Thompson, I. Eardley, R.E. Banks, M.A. Knowles, Urinary biomarker profiling in transitional cell carcinoma, International journal of cancer, 119 (2006) 2642-2650.

V. Thongboonkerd, Urinary proteomics: towards biomarker discovery, diagnostics and prognostics, Molecular bioSystems, 4 (2008) 810-815.

J.A. Paulo, L.S. Lee, B. Wu, K. Repas, P.A. Banks, H. Steen, D. Conwell, Cytokine protein microarray analysis of pancreatic fluid in tandem with the endoscopic pancreatic function test (ePFT), Pancreatology, Submitted (2010).

H. Tammen, Specimen collection and handling: standardization of blood sample collection, Methods Mol Biol, 428 (2008) 35-42.

L. Nonn, A. Vaishnav, L. Gallagher, P.H. Gann, mRNA and micro-RNA expression analysis in laser-capture microdissected prostate biopsies: valuable tool for risk assessment and prevention trials, Exp Mol Pathol, 88 (2010) 45-51.

N. Ikenaga, K. Ohuchida, K. Mizumoto, J. Yu, H. Fujita, K. Nakata, J. Ueda, N. Sato, E. Nagai, M. Tanaka, S100A4 mRNA is a diagnostic and prognostic marker in pancreatic carcinoma, J Gastrointest Surg, 13 (2009) 1852-1858.

A. Liu, M.T. Tetzlaff, P. Vanbelle, D. Elder, M. Feldman, J.W. Tobias, A.R. Sepulveda, X. Xu, MicroRNA expression profiling outperforms mRNA expression profiling in formalin-fixed paraffin-embedded tissues, Int J Clin Exp Pathol, 2 (2009) 519-527.

L.M. Gjerdrum, H.N. Abrahamsen, B. Villegas, B.S. Sorensen, H. Schmidt, S.J. Hamilton-Dutoit, The influence of immunohistochemistry on mRNA recovery from microdissected frozen and formalin-fixed, paraffin-embedded sections, Diagn Mol Pathol, 13 (2004) 224-233.

M. Ahram, M.J. Flaig, J.W. Gillespie, P.H. Duray, W.M. Linehan, D.K. Ornstein, S. Niu, Y. Zhao, E.F. Petricoin, 3rd, M.R. Emmert-Buck, Evaluation of ethanol-fixed, paraffin-embedded tissues for proteomic applications, Proteomics, 3 (2003) 413-421.

V.K. Rait, L. Xu, T.J. O'Leary, J.T. Mason, Modeling formalin fixation and antigen retrieval with bovine pancreatic RNase A II. Interrelationship of cross-linking, immunoreactivity, and heat treatment, Lab Invest, 84 (2004) 300-306.

V.K. Rait, T.J. O'Leary, J.T. Mason, Modeling formalin fixation and antigen retrieval with bovine pancreatic ribonuclease A: I-structural and functional alterations, Lab Invest, 84 (2004) 292-299.

M. Benchekroun, J. DeGraw, J. Gao, L. Sun, K. von Boguslawsky, A. Leminen, L.C. Andersson, M. Heiskala, Impact of fixative on recovery of mRNA from paraffin-embedded tissue, Diagn Mol Pathol, 13 (2004) 116-125.

R.L. Romero, A.C. Juston, J. Ballantyne, B.E. Henry, The applicability of formalin-fixed and formalin fixed paraffin embedded tissues in forensic DNA analysis, J Forensic Sci, 42 (1997) 708-714.

M.R. Emmert-Buck, R.F. Bonner, P.D. Smith, R.F. Chuaqui, Z. Zhuang, S.R. Goldstein, R.A. Weiss, L.A. Liotta, Laser capture microdissection, Science (New York, N.Y, 274 (1996) 998-1001.

V. Patel, B.L. Hood, A.A. Molinolo, N.H. Lee, T.P. Conrads, J.C. Braisted, D.B. Krizman, T.D. Veenstra, J.S. Gutkind, Proteomic analysis of laser-captured paraffin-embedded tissues: a molecular portrait of head and neck cancer progression, Clin Cancer Res, 14 (2008) 1002-1014.

A. Michalski, E. Damoc, O. Lange, E. Denisov, D. Nolting, M. Muller, R. Viner, J. Schwartz, P. Remes, M. Belford, J.J. Dunyach, J. Cox, S. Horning, M. Mann, A. Makarov, Ultra High Resolution Linear Ion Trap Orbitrap Mass Spectrometer (Orbitrap Elite) Facilitates Top Down LC MS/MS and Versatile Peptide Fragmentation Modes, Mol Cell Proteomics, 11 (2012) O111 013698.

A. Michalski, E. Damoc, J.P. Hauschild, O. Lange, A. Wieghaus, A. Makarov, N. Nagaraj, J. Cox, M. Mann, S. Horning, Mass spectrometry-based proteomics using Q Exactive, a high-performance benchtop quadrupole Orbitrap mass spectrometer, Mol Cell Proteomics, 10 (2011) M111 011015.




DOI: http://dx.doi.org/10.6092/1590-8577/1508

NBN: http://nbn.depositolegale.it/urn%3Anbn%3Ait%3Aunina-16139

Article Metrics

Metrics Loading ...

Metrics powered by PLOS ALM

Refbacks

  • There are currently no refbacks.




Creative Commons License
This work is licensed under a Creative Commons Attribution 4.0 International License.

ISSN 1590-8577 | JOP is published by CAB - Center for Libraries at "Federico II" University of Naples using Open Journal System