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Review

Toward improving the proteomic analysis of formalin-fixed, paraffin-embedded tissue

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Pages 389-400 | Published online: 09 Jan 2014

References

  • Mallick P, Kuster B. Proteomics: a pragmatic perspective. Nat. Biotechnol. 28(7), 695–709 (2010).
  • Shi S-R, Liu C, Balgley BM, Lee C, Taylor CR. Protein extraction from formalin-fixed, paraffin-embedded tissue sections: quality evaluation by mass spectrometry. J. Histochem. Cytochem. 54(6), 739–743 (2006).
  • Patel V, Hood BL, Molinolo AA et al. Proteomic analysis of laser-captured paraffin-embedded tissues: a molecular portrait of head and neck cancer progression. Clin. Cancer Res. 14(4), 1002–1014 (2008).
  • Ostasiewicz P, Zielinska DF, Mann M, Wiśniewski JR. Proteome, phosphoproteome, and N-glycoproteome are quantitatively preserved in formalin-fixed paraffin-embedded tissue and analyzable by high-resolution mass spectrometry. J. Proteome Res. 9(7), 3688–3700 (2010).
  • Azimzadeh O, Barjaktarovic Z, Aubele M et al. Formalin-fixed paraffin-embedded (FFPE) proteome analysis using gel-free and gel-based proteomics. J. Proteome Res. 9(9), 4710–4720 (2010).
  • Blonder J, Veenstra TD. Clinical proteomic applications of formalin-fixed paraffin-embedded tissues. Clin. Lab. Med. 29(1), 101–113 (2009).
  • Fowler CB, O'Leary TJ, Mason JT. Modeling formalin fixation and histological processing with bovine ribonuclease A: Effects of ethanol dehydration on reversal of formaldehyde-induced cross-links. Lab. Invest. 88(7), 785–791 (2008).
  • Shi SR, Taylor CR, Fowler CB, Mason JT. Complete solubilization of formalin-fixed, paraffin-embedded tissue may improve proteomic studies. Proteomics Clin. Appl. 7(3–4), 264–272 (2013).
  • Ikeda K, Monden T, Kanoh T et al. Extraction and analysis of diagnostically useful proteins from formalin-fixed, paraffin-embedded tissue sections. J. Histochem. Cytochem. 46(3), 397–403 (1998).
  • DeSouza LV, Krakovska O, Darfler MM et al. mTRAQ-based quantification of potential endometrial carcinoma biomarkers from archived formalin-fixed paraffin-embedded tissues. Proteomics 10(17), 3108–3116 (2010).
  • Azimzadeh O, Scherthan H, Yentrapalli R et al. Label-free protein profiling of formalin-fixed paraffin-embedded (FFPE) heart tissue reveals immediate mitochondrial impairment after ionising radiation. J. Proteomics 75(8), 2384–2395 (2012).
  • Gemoll T, Roblick UJ, Habermann JK. MALDI mass spectrometry imaging in oncology (review). Mol. Med. Rep. 4(6), 1045–1051 (2011).
  • Blum F. Der formaldehyd als hartungsmittel. Z. Wiss. Mikrosc. 10, 314–315 (1893).
  • Fox CH, Johnson FB, Whiting J, Roller PP. Formaldehyde fixation. J. Histochem. Cytochem. 33(8), 845–853 (1985).
  • Nielsen GD, Larsen ST, Wolkoff P. Recent trend in risk assessment of formaldehyde exposures from indoor air. Arch. Toxicol. 87(1), 73–98 (2013).
  • Metz B, Kersten GFA, Hoogerhout P et al. Identification of formaldehyde-induced modifications in proteins: reactions with model peptides. J. Biol. Chem. 279(8), 6235–6243 (2004).
  • Metz B, Kersten GFA, Baart GJ et al. Identification of formaldehyde-induced modifications in proteins: reactions with insulin. Bioconjug. Chem. 17(3), 815–822 (2006).
  • Toews J, Rogalski JC, Kast J. Accessibility governs the relative reactivity of basic residues in formaldehyde-induced protein modifications. Anal. Chim. Acta. 676(1–2), 60–67 (2010).
  • Sompuram SR. A molecular mechanism of formalin fixation and antigen retrieval. Am. J. Clin. Pathol. 121(2), 190–199 (2004).
  • Thompson SM, Craven RA, Nirmalan NJ et al. Impact of pre-analytical factors on the proteomic analysis of formalin-fixed paraffin-embedded tissue. Proteomics Clin. Appl. 7(3–4), 241–251 (2013).
  • Sarto C, Valsecchi C, Mocarelli P. Renal cell carcinoma: handling and treatment. Proteomics 2(11), 1627–1629 (2002).
  • Skold K, Svensson M, Norrman M et al. The significance of biochemical and molecular sample integrity in brain proteomics and peptidomics: stathmin 2-20 and peptides as sample quality indicators. Proteomics 7(24), 4445–4456 (2007).
  • Espina V, Mueller C, Liotta LA. Phosphoprotein stability in clinical tissue and its relevance for reverse phase protein microarray technology. Methods Mol. Biol. 785, 23–43 (2011).
  • Pinhel IF, Macneill FA, Hills MJ et al. Extreme loss of immunoreactive p-Akt and p-Erk1/2 during routine fixation of primary breast cancer. Breast Cancer Res. 12(5), R76 (2010).
  • Wolff C, Schott C, Porschewski P, Reischauer B, Becker KF. Successful protein extraction from over-fixed and long-term stored formalin-fixed tissues. PLoS One 6(1), e16353 (2011).
  • Tanca A, Pagnozzi D, Falchi G et al. Impact of fixation time on GeLC-MS/MS proteomic profiling of formalin-fixed, paraffin-embedded tissues. J. Proteomics 74(7), 1015–1021 (2011).
  • Xie R, Chung JY, Ylaya K et al. Factors influencing the degradation of archival formalin-fixed paraffin-embedded tissue sections. J. Histochem. Cytochem. 59(4), 356–365 (2011).
  • Sprung RW, Brock JW, Tanksley JP et al. Equivalence of protein inventories obtained from formalin-fixed paraffin-embedded and frozen tissue in multidimensional liquid chromatography-tandem mass spectrometry shotgun proteomic analysis. Mol. Cell Proteomics 8(8), 1988–1998 (2009).
  • Scicchitano MS. Protein extraction from formalin-fixed, paraffin-embedded tissue enables robust proteomic profiles by mass spectrometry. J. Histochem. Cytochem. 57(9), 849–860 (2009).
  • Fowler CB, Waybright TJ, Veenstra TD, O'Leary TJ, Mason JT. Pressure-assisted protein extraction: a novel method for recovering proteins from archival tissue for proteomic analysis. J. Proteome Res. 11(4), 2602–2608 (2012).
  • Balgley BM, Guo T, Zhao K et al. Evaluation of archival time on shotgun proteomics of formalin-fixed and paraffin-embedded tissues. J. Proteome Res. 8(2), 917–925 (2009).
  • Fowler CB, Cunningham RE, O'Leary TJ, Mason JT. ‘Tissue surrogates’ as a model for archival formalin-fixed paraffin-embedded tissues. Lab. Invest. 87(8), 836–846 (2007).
  • Fowler CB, Cunningham RE, Waybright TJ et al. Elevated hydrostatic pressure promotes protein recovery from formalin-fixed, paraffin-embedded tissue surrogates. Lab. Invest. 88(2), 185–195 (2008).
  • Fowler CB, Chesnick IE, Moore CD, O'Leary TJ, Mason JT. Elevated pressure improves the extraction and identification of proteins recovered from formalin-fixed, paraffin-embedded tissue surrogates. PLoS One 5(12), e14253 (2010).
  • Magdeldin S, Yamamoto T. Toward deciphering proteomes of formalin-fixed paraffin-embedded (FFPE) tissues. Proteomics 12(7), 1045–1058 (2012).
  • Jiang X, Jiang X, Feng S et al. Development of efficient protein extraction methods for shotgun proteome analysis of formalin-fixed tissues. J. Proteome Res. 6(3), 1038–1047 (2007).
  • Chung JY, Lee SJ, Kris Y et al. A well-based reverse-phase protein array applicable to extracts from formalin-fixed paraffin-embedded tissue. Proteomics Clin. Appl. 2(10–11), 1539–1547 (2008).
  • Tanca A, Pagnozzi D, Addis MF. Setting proteins free: progresses and achievements in proteomics of formalin-fixed, paraffin-embedded tissues. Proteomics Clin. Appl. 6(1–2), 7–21 (2011).
  • Zhang H, Lin Q, Ponnusamy S et al. Differential recovery of membrane proteins after extraction by aqueous methanol and trifluoroethanol. Proteomics 7(10), 1654–1663 (2007).
  • Kajiya H, Takekoshi S, Takei M et al. Selection of buffer pH by the isoelectric point of the antigen for the efficient heat-induced epitope retrieval: re-appraisal for nuclear protein pathobiology. Histochem. Cell Biol. 132(6), 659–667 (2009).
  • Zale SE, Klibanov AM. Why does ribonuclease irreversibly inactivate at high temperatures? Biochemistry 25(19), 5432–5444 (1986).
  • Volkin DB. Thermal destruction processes in proteins involving cystine residues. J. Biol. Chem. 262(7), 2945–2950 (1987).
  • Bogen S, Vani K, Sompuram S. Molecular mechanisms of antigen retrieval: antigen retrieval reverses steric interference caused by formalin-induced cross-links. Biotech. Histochem. 84(5), 207–215 (2009).
  • Fowler CB, Evers DL, O'Leary TJ, Mason JT. Antigen retrieval causes protein unfolding: evidence for a linear epitope model of recovered immunoreactivity. J. Histochem. Cytochem. 59(4), 366–381 (2011).
  • Shi SR, Key ME, Kalra KL. Antigen retrieval in formalin-fixed, paraffin-embedded tissues: an enhancement method for immunohistochemical staining based on microwave oven heating of tissue sections. J. Histochem. Cytochem. 39(6), 741–748 (1991).
  • Prieto DA, Hood BL, Darfler MM et al. Liquid Tissue: proteomic profiling of formalin-fixed tissues. Biotechniques (Suppl.), 32–35 (2005).
  • Xu H, Yang L, Wang W et al. Antigen retrieval for proteomic characterization of formalin-fixed and paraffin-embedded tissues. J. Proteome Res. 7(3), 1098–1108 (2008).
  • Addis MF, Tanca A, Pagnozzi D et al. Generation of high-quality protein extracts from formalin-fixed, paraffin-embedded tissues. Proteomics 9(15), 3815–3823 (2009).
  • Tanca A, Pagnozzi D, Burrai GP et al. Comparability of differential proteomics data generated from paired archival fresh-frozen and formalin-fixed samples by GeLC-MS/MS and spectral counting. J. Proteomics 77, 561–576 (2012).
  • Wiśniewski JR, Zougman A, Nagaraj N, Mann M. Universal sample preparation method for proteome analysis. Nat. Methods 6(5), 359–362 (2009).
  • Wiśniewski JR, Dus K, Mann M. Proteomic workflow for analysis of archival formalin fixed and paraffin embedded clinical samples to a depth of 10,000 proteins. Proteomics Clin. Appl. 7(3–4), 225–233 (2013).
  • Wiśniewski JR, Mann M. Consecutive proteolytic digestion in an enzyme reactor increases depth of proteomic and phosphoproteomic analysis. Anal. Chem. 84(6), 2631–2637 (2012).
  • Fu Z, Yan K, Rosenberg A et al. Improved protein extractionand protein identification from archival formalin-fixed paraffin-embedded human aortas. Proteomics Clin. Appl. 7(3–4), 217–224 (2013).
  • Naidoo K, Jones R, Dmitrovic B et al. Proteome of formalin-fixed paraffin-embedded pancreatic ductal adenocarcinoma and lymph node metastases. J. Pathol. 226(5), 756–763 (2012).
  • Kawamura T, Nomura M, Tojo H et al. Proteomic analysis of laser-microdissected paraffin-embedded tissues: (1) Stage-related protein candidates upon non-metastatic lung adenocarcinoma. J. Proteomics 73(6), 1089–1099 (2010).
  • 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. 132(6), 1368–1382 (2013).
  • 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 41(2), 175–185 (2012).
  • Alkhas A, Hood BL, Oliver K et al. Standardization of a sample preparation and analytical workflow for proteomics of archival endometrial cancer tissue. J. Proteome Res. 10(11), 5264–5271 (2011).
  • Wisztorski M, Fatou B, Franck J et al. Microproteomics by Liquid Extraction Surface Analysis: Application to FFPE tissue to study the Fimbria region of tubo-ovarian cancer. Proteomics Clin. Appl. 7(3–4), 234–240 (2013).
  • Hatakeyama K, Wakabayashi-Nakao K, Aoki Y et al. Novel protein extraction approach using micro-sized chamber for evaluation of proteins eluted from formalin-fixed paraffin-embedded tissue sections. Proteome Sci. 10, 19 (2012).
  • Gygi SP, Rist B, Gerber SA et al. Quantitative analysis of complex protein mixtures using isotope-coded affinity tags. Nat. Biotechnol. 17(10), 994–999 (1999).
  • Ross PL, Huang YN, Marchese JN et al. Multiplexed protein quantitation in Saccharomyces cerevisiae using amine-reactive isobaric tagging reagents. Mol. Cell Proteomics 3(12), 1154–1169 (2004).
  • Jain MR, Liu T, Hu J et al. Quantitative Proteomic Analysis of Formalin Fixed Paraffin Embedded Oral HPV Lesions from HIV Patients. Open Proteomics J. 1, 40–45 (2008).
  • Xiao Z, Li G, Chen Y et al. Quantitative proteomic analysis of formalin-fixed and paraffin-embedded nasopharyngeal carcinoma using iTRAQ labeling, two-dimensional liquid chromatography, and tandem mass spectrometry. J. Histochem. Cytochem. 58(6), 517–527 (2010).
  • Jain MR, Li Q, Liu T et al. Proteomic identification of immunoproteasome accumulation in formalin-fixed rodent spinal cords with experimental autoimmune encephalomyelitis. J. Proteome Res. 11(3), 1791–1803 (2012).
  • Byrum S, Avaritt NL, Mackintosh SG et al. A quantitative proteomic analysis of FFPE melanoma. J. Cutan. Pathol. 38(11), 933–936 (2011).
  • Hauck SM, Dietter J, Kramer RL et al. Deciphering membrane-associated molecular processes in target tissue of autoimmune uveitis by label-free quantitative mass spectrometry. Mol. Cell Proteomics 9(10), 2292–2305 (2010).
  • Guzel C, Ursem NT, Dekker LJ et al. Multiple reaction monitoring assay for pre-eclampsia related calcyclin peptides in formalin fixed paraffin embedded placenta. J. Proteome Res. 10(7), 3274–3282 (2011).
  • Nishimura T, Nomura M, Tojo H et al. Proteomic analysis of laser-microdissected paraffin-embedded tissues: (2) MRM assay for stage-related proteins upon non-metastatic lung adenocarcinoma. J. Proteomics 73(6), 1100–1110 (2010).
  • Gamez-Pozo A, Sanchez-Navarro I, Calvo E et al. Protein phosphorylation analysis in archival clinical cancer samples by shotgun and targeted proteomics approaches. Mol. Biosyst. 7(8), 2368–2374 (2011).
  • Becker KF, Schott C, Hipp S et al. Quantitative protein analysis from formalin-fixed tissues: implications for translational clinical research and nanoscale molecular diagnosis. J. Pathol. 211(3), 370–378 (2007).
  • Addis MF, Tanca A, Pagnozzi D, Rocca S, Uzzau S. 2-D PAGE and MS analysis of proteins from formalin-fixed, paraffin-embedded tissues. Proteomics 9(18), 4329–4339 (2009).
  • Tanca A, Pagnozzi D, Falchi G et al. Application of 2-D DIGE to formalin-fixed, paraffin-embedded tissues. Proteomics 11(5), 1005–1011 (2011).
  • Guo H, Liu W, Ju Z et al. An efficient procedure for protein extraction from formalin-fixed, paraffin-embedded tissues for reverse phase protein arrays. Proteome Sci. 10(1), 56 (2012).
  • Berg D, Hipp S, Malinowsky K, Bollner C, Becker KF. Molecular profiling of signalling pathways in formalin-fixed and paraffin-embedded cancer tissues. Eur. J. Cancer 46(1), 47–55 (2010).
  • Berg D, Wolff C, Langer R et al. Discovery of new molecular subtypes in oesophageal adenocarcinoma. PLoS One 6(9), e23985 (2011).
  • Berg D, Malinowsky K, Reischauer B, Wolff C, Becker KF. Use of formalin-fixed and paraffin-embedded tissues for diagnosis and therapy in routine clinical settings. Methods Mol. Biol. 785, 109–122 (2011).
  • Berg D, Wolff C, Malinowsky K et al. Profiling signalling pathways in formalin-fixed and paraffin-embedded breast cancer tissues reveals cross-talk between EGFR, HER2, HER3 and uPAR. J. Cell Physiol. 227(1), 204–212 (2012).
  • Berg D, Langer R, Tran K et al. Protein microarray-based comparison of HER2, estrogen receptor, and progesterone receptor status in core biopsies and surgical specimens from FFPE breast cancer tissues. Appl. Immunohistochem. Mol. Morphol. 19(4), 300–305 (2011).
  • Wulfkuhle JD, Berg D, Wolff C et al. Molecular Analysis of HER2 Signaling in Human Breast Cancer by Functional Protein Pathway Activation Mapping. Clin. Cancer Res. 18(23), 6426–6435 (2012).
  • Assadi M, Lamerz J, Jarutat T et al. Multiple protein analysis of FFPE tissue samples with reverse-phase protein arrays. Mol. Cell Proteomics. doi:10.1074/mcp.M112.023051 (2013) (Epub ahead of print).
  • Malinowsky K, Wolff C, Gundisch S, Berg D, Becker K. Targeted therapies in cancer - challenges and chances offered by newly developed techniques for protein analysis in clinical tissues. J. Cancer 2, 26–35 (2011).
  • Minerva L, Ceulemans A, Baggerman G, Arckens L. MALDI MS imaging as a tool for biomarker discovery: Methodological challenges in a clinical setting. Proteomics Clin. Appl. 6(11–12), 581–595 (2012).
  • Lemaire R, Desmons A, Tabet JC et al. Direct analysis and MALDI imaging of formalin-fixed, paraffin-embedded tissue sections. J. Proteome Res. 6(4), 1295–1305 (2007).
  • Morita Y, Ikegami K, Goto-Inoue N et al. Imaging mass spectrometry of gastric carcinoma in formalin-fixed paraffin-embedded tissue microarray. Cancer Sci. 101(1), 267–273 (2010).
  • Ronci M, Bonanno E, Colantoni A et al. Protein unlocking procedures of formalin-fixed paraffin-embedded tissues: application to MALDI-TOF imaging MS investigations. Proteomics 8(18), 3702–3714 (2008).
  • Gustafsson JO, Oehler MK, McColl SR, Hoffmann P. Citric acid antigen retrieval (CAAR) for tryptic peptide imaging directly on archived formalin-fixed paraffin-embedded tissue. J. Proteome Res. 9(9), 4315–4328 (2010).
  • Groseclose MR, Massion PP, Chaurand P, Caprioli RM. High-Throughput proteomic analysis of formalin-fixed paraffin-embedded tissue microarrays using MALDI imaging mass spectrometry. Proteomics 8(18), 3715–3724 (2008).
  • Casadonte R, Caprioli RM. Proteomic analysis of formalin-fixed paraffin-embedded tissue by MALDI imaging mass spectrometry. Nat. Protoc. 6(11), 1695–1709 (2011).
  • Alexandrow T. MALDI imaging mass spectrometry: statistical data analysis and current computational challenges. BMC Bioinformatics 13(Suppl. 16), S11 (2012).
  • Stauber J, MacAleese L, Franck J et al. On-tissue protein identification and imaging by MALDI-ion mobility mass spectrometry. J. Am. Soc. Mass Spectrom. 21(3), 338–347 (2010).
  • Gustafsson JO, Eddes JS, Meding S et al. Internal calibrants allow high accuracy peptide matching between MALDI imaging MS and LC-MS/MS. J. Proteomics 75(16), 5093–5105 (2012).
  • Rait VK, O'Leary TJ, Mason JT. Modeling formalin fixation and antigen retrieval with bovine pancreatic ribonuclease A: I-structural and functional alterations. Lab. Invest. 84(3), 292–299 (2004).
  • Rait VK, Xu L, O'Leary TJ, Mason JT. Modeling formalin fixation and antigen retrieval with bovine pancreatic RNase A II. Interrelationship of cross-linking, immunoreactivity, and heat treatment. Lab. Invest. 84(3), 300–306 (2004).
  • Chu WS, Liang Q, Liu J et al. A nondestructive molecule extraction method allowing morphological and molecular analyses using a single tissue section. Lab. Invest. 85(11), 1416–1428 (2005).

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