Proteomic analysis of formalin-fixed paraffin embedded (FFPE) samples: pitfalls and potentials

Current Proteomics

Volumn 6, Issue 2, 2009, Pages 122-139

  Valera, Vladimir A ^a   Walter, Beatriz A ^a   Linehan, W Marston ^a   Roberts, David D ^a   Merino, Maria J ^a,b  

^a NATIONAL CANCER INSTITUTE   (United States)

^b NONE   (United States)

Author keywords

Antigen retrieval; Formalin fixed paraffin embedded tissues; Imaging mass spectrometry; Immunohistochemistry; Liquid chromatography; Mass spectrometry; Protein extraction; Proteomics

Indexed keywords

EID: 67650912065     PISSN: 15701646     EISSN: None     Source Type: Journal    
DOI: 10.2174/157016409788680938     Document Type: Article

References (81)

1. Ahram, M., Flaig, M.J., Gillespie, J.W., Duray, P.H., Linehan, W.M., Ornstein, D.K., Niu, S., Zhao, Y., et al. (2003). Evaluation of ethanol-fixed, paraffin-embedded tissues for proteomic applications. Proteomics 3 :413-21.
2. Altekar, M., Homon, C.A., Kashem, M.A., Mason, S.W., Nelson, R.M., Patnaude, L.A., Yingling, J. and Taylor, P.B. (2007). Assay optimization: a statistical design of experiments approach. Clin. Lab. Med. 27 :139-54.
3. Andreoletti, O., Berthon, P., Levavasseur, E., Marc, D., Lantier, F., Monks, E., Elsen, J.M. and Schelcher, F. (2002). Phenotyping of protein-prion (PrPsc)-accumulating cells in lymphoid and neural tissues of naturally scrapie-affected sheep by double-labeling immunohistochemistry. J. Histochem. Cytochem. 50 :1357-70.
4. Aoki, Y., Toyama, A., Shimada, T., Sugita, T., Aoki, C., Umino, Y., Suzuki, A., Aoki, D., et al. (2007). A novel method for analyzing formalin-fixed paraffin embedded (FFPE) tissue sections by mass spectrometry imaging. Proc. J. Acad. Ser. B 83 :205-14.
5. Balgley, B.M., Guo, T., Zhao, K., Fang, X., Tavassoli, F.A. and Lee, C.S. (2009). Evaluation of archival time on shotgun proteomics of formalin- fixed and paraffin-embedded tissues. J. Proteome Res. 8 :917-25.
6. Battifora, H. and Kopinski, M. (1986). The influence of protease digestion and duration of fixation on the immunostaining of keratins. A comparison of formalin and ethanol fixation. J. Histochem. Cytochem. 34 :1095-100.
7. Becker, K.F., Schott, C., Hipp, S., Metzger, V., Porschewski, P., Beck, R., Nahrig, J., Becker, I., et al. (2007). Quantitative protein analysis from formalin-fixed tissues: implications for translational clinical research and nanoscale molecular diagnosis. J. Pathol. 211 :370-8.
8. Belief, V., Boissiere, F., Bibeau, F., Desmetz, C., Berthe, M.L., Rochaix, P., Maudelonde, T., Mange, A., et al. (2008). Proteomic analysis of RCL2 paraffin-embedded tissues. J. Cell Mol. Med. 12 :2027-36.
9. Bratthauer, G.L. (1999). Processing of tissue specimens. Methods Mol. Biol.115 :77-84.
10. Brooks, S.A., Dwek, M.V. and Leathem, A.J. (1998). Release and analysis of polypeptides and glycopolypeptides from formalin-fixed, paraffin wax-embedded tissue. Histochem. J. 30 :609-15.
11. Chaurand, P., Sanders, M.E., Jensen, R.A. and Caprioli, R.M. (2004a). Proteomics in diagnostic pathology: profiling and imaging proteins directly in tissue sections. Am. J. Pathol. 165 :1057-68.
12. Chaurand, P., Schwartz, S.A., Billheimer, D., Xu, B.J., Crecelius, A. and Caprioli, R.M. (2004b). Integrating histology and imaging mass spec- trometry. Anal. Chem. 76 :1145-55.
13. Chu, W.-S., Liang, Q., Liu, J., Wei, M.Q., Winters, M., Liotta, L., Sandberg, G. and Gong, M. (2005). A nondestructive molecule extraction method allowing morphological and molecular analyses using a single tissue section. Lab Invest. 85 :1416-28.
14. Clark, R.K. and Damjanov, I. (1986). Immunoblotting of keratin polypep- tides extracted from tissues preserved in standard histologic fixatives. J. Histochem. Cytochem. 34 :679-82.
15. Conti, C.J., Larcher, F., Chesner, J. and Aldaz, C.M. (1988). Polyacrylamide gel electrophoresis and immunoblotting of proteins extracted from paraffin-embedded tissue sections. J. Histochem. Cytochem. 36 :547-50.
16. Costa, P.P., Jacobsson, B., Collins, V.P. and Biberfeld, P. (1986). Unmasking antigen determinants in amyloid. J. Histochem. Cytochem. 34 :1683-5.
17. Crockett, D.K., Lin, Z., Vaughn, C.P., Lim, M.S. and Elenitoba-Johnson, K.S. (2005). Identification of proteins from formalin-fixed paraffin- embedded cells by LC-MS/MS. Lab Invest. 85 :1405-15.
18. Curran, R.C. and Gregory, J. (1977). The unmasking of antigens in paraffin sections of tissue by trypsin. Experientia 33 :1400-1.
19. Dapson, R.W. (2007). Macromolecular changes caused by formalin fixation and antigen retrieval. Biotech. Histochem. Offic. Publ. Biol. Stain Commission 82 :133-40.
20. Denk, H., Radaszkiewicz, T. and Weirich, E. (1977). Pronase pretreatment of tissue sections enhances sensitivity of the unlabelled antibody- enzyme (PAP) technique. J. Immunol. Methods 15 :163-7.
21. Ellsworth, D.L., Russell, S., Deyarmin, B., Sullivan, A.G., Brzeski, H., Somiari, R.I. and Shriver, C.D. (2005). Laser-assisted microdissection in proteomic analyses. In: The proteomics protocols handbook, J. M. Walker (Ed.), Humana Press, Totowa, N.J., pp. 59-66.
22. Fowler, C.B., Cunningham, R.E., O'leary, T.J. and Mason, J.T. (2007). 'Tissue surrogates' as a model for archival formalin-fixed paraffin- embedded tissues. Lab Invest. 87 :836-46.
23. Fowler, C.B., Cunningham, R.E., Waybright, T.J., Blonder, J., Veenstra, T.D., O'leary, T.J. and Mason, J.T. (2008). Elevated hydrostatic pressure promotes protein recovery from formalin-fixed, paraffin-embedded tissue surrogates. Lab Invest. 88 :185-95.
24. Fraenkel-Conrat, H. and Mecham, D.K. (1949). The reaction of formaldehyde with proteins; demonstration of intermolecular cross-linking by means of osmotic pressure measurements. J. Biol. Chem. 177 :477-86.
25. French, D. and Edsall, J.T. (1945). The Reactions of Formaldehyde with Amino Acids and Proteins. In: Advances in Protein Chemistry, 1 M. L. Anson & Edsall, J. T. (Eds.), Academic Press, pp. 277-335.
26. Gorg, A., Drews, O. and Weiss, W. (2004). Separation of proteins using two-dimensional gel electrophoresis. In: Purifying proteins for pro- teomics: a laboratory manual, R. J. Simpson (Ed.), Cold Spring Harbor Laboratory Press, Cold Spring Harbor, N.Y., pp. 396.
27. Grizzle, W.E., Fredenburgh, J. and Myers, R.B. (2008). Fixation of tissues. In: Theory and Practice of Histological Techniques, 6th ed. J. D. Bancroft & Gamble, M. (Eds.), Churchill Livingstone/Elsevier, Philadelphia, PA, pp. 53-74.
28. Groseclose, M.R., Massion, P.P., Chaurand, P. and Caprioli, R.M. (2008). High-throughput proteomic analysis of formalin-fixed paraffin- embedded tissue microarrays using MALDI imaging mass spectrome-try. Proteomics 8 :3715-24.
29. Hamdan, M. and Righetti, P.G. (2005). Current Strategies for Protein Quantification. In: Proteomics Today: Protein Assessment and Biomarkers Using Mass Spectrometry, 2D Electrophoresis, and Microarray Technology, M. Hamdan & Righetti, P. G. (Eds.), John Wiley & Sons, Hoboken, N.J., pp. 127-83.
30. Haritani, M., Spencer, Y.I. and Wells, G.A. (1994). Hydrated autoclave pretreatment enhancement of prion protein immunoreactivity in formalin-fixed bovine spongiform encephalopathy-affected brain. Acta Neu-ropathol. 87 :86-90.
31. Hausen, P. and Dreyer, C. (1982). Urea Reactivates Antigens in Paraffin Sections for Immunofluorescent Staining. Biotech. Histochem. 57 :321-4.
32. Hayat, M.A. (2002a). Antigen Retrieval. In: Microscopy, immunohisto- chemistry, and antigen retrieval methods for light and electron microscopy, M. A. Hayat (Ed.), Kluwer Academic/Plenum Publishers, New York, pp. 117-54.
33. Hayat, M.A. (2002b). Factors Affecting Antigen Retrieval. In: Microscopy, immunohistochemistry, and antigen retrieval methods for light and electron microscopy, M. A. Hayat (Ed.), Kluwer Academic/Plenum Publishers: New York, pp. 71-93.
34. Hewitt, S.M., Lewis, F.A., Cao, Y., Conrad, R.C., Cronin, M., Danenberg, K.D., Goralski, T.J., Langmore, J.P., et al. (2008). Tissue handling and specimen preparation in surgical pathology: issues concerning the recovery of nucleic acids from formalin-fixed, paraffin-embedded tissue. Arch. Pathol. Lab Med. 132 :1929-35.
35. Hood, B.L., Darfler, M.M., Guiel, T.G., Furusato, B., Lucas, D.A., Ringeisen, B.R., Sesterhenn, I.A., Conrads, T.P., et al. (2005). Proteo- mic analysis of formalin-fixed prostate cancer tissue. Mol. Cell Pro- teomics 4 :1741-53.
36. Huang, S.N. (1975). Immunohistochemical demonstration of hepatitis B core and surface antigens in paraffin sections. Lab Invest. 33 :88-95.
37. Huang, S.N., Minassian, H. and More, J.D. (1976). Application of im- munofluorescent staining on paraffin sections improved by trypsin digestion. Lab Invest. 35 :383-90.
38. Ikeda, K., Monden, T., Kanoh, T., Tsujie, M., Izawa, H., Haba, A., Ohnishi, T., Sekimoto, M., et al. (1998). Extraction and analysis of diagnosti- cally useful proteins from formalin-fixed, paraffin-embedded tissue sections. J. Histochem. Cytochem. 46 :397-403.
39. Jiang, X., Feng, S., Tian, R., Ye, M. and Zou, H. (2007). Development of efficient protein extraction methods for shotgun proteome analysis of formalin-fixed tissues. J. Proteome Res. 6 :1038-47.
40. Kallen, R.G. and Jencks, W.P. (1966). Equilibria for the reaction of amines with formaldehyde and protons in aqueous solution. A re-examination of the formol titration. J. Biol. Chem. 241 :5864-78.
41. Kirkeby, S. and Moe, D. (1986). Studies on the actions of glutaraldehyde, formaldehyde, and mixtures of glutaraldehyde and formaldehyde on tissue proteins. Acta Histochem. 79 :115-21.
42. Kitamoto, T., Ogomori, K., Tateishi, J. and Prusiner, S.B. (1987). Formic acid pretreatment enhances immunostaining of cerebral and systemic amyloids. Lab Invest. 57 :230-6.
43. Kroll, J., Becker, K.F., Kuphal, S., Hein, R., Hofstadter, F. and Bosserhoff, A.K. (2008). Isolation of high quality protein samples from punches of formalin fixed and paraffin embedded tissue blocks. Histol. Histopa-thol. 23 :391-5.
44. Lemaire, R., Desmons, A., Tabet, J.C., Day, R., Salzet, M. and Fournier, I. (2007). Direct analysis and MALDI imaging of formalin-fixed, paraffin-embedded tissue sections. J. Proteome Res. 6 :1295-305.
45. Lewis, F., Maughan, N.J., Smith, V., Hillan, K. and Quirke, P. (2001). Unlocking the archive--gene expression in paraffin-embedded tissue. J.Pathol. 195 :66-71.
46. Mepham, B.L., Frater, W. and Mitchell, B.S. (1979). The use of proteolytic enzymes to improve immunoglobulin staining by the PAP technique. Histochem. J. 11 :345-57.
47. Metz, B., Kersten, G.F., Baart, G.J., De Jong, A., Meiring, H., Ten Hove, J., Van Steenbergen, M.J., Hennink, W.E., et al. (2006). Identification of formaldehyde-induced modifications in proteins: reactions with insulin. Bioconjug. Chem. 17 :815-22.
48. Metz, B., Kersten, G.F., Hoogerhout, P., Brugghe, H.F., Timmermans, H.A., De Jong, A., Meiring, H., Ten Hove, J., et al. (2004). Identification of formaldehyde-induced modifications in proteins: reactions with model peptides. J. Biol. Chem. 279 :6235-43.
49. Middlebrook, W.R. (1949). The irreversible combination of formaldehyde with proteins. Biochem. J. 44 :17-23.
50. Morgan, J.M., Navabi, H. and Jasani, B. (1997). Role of calcium chelation in high-temperature antigen retrieval at different pH values. J. Pathol. 182 :233-7.
51. Morgan, J.M., Navabi, H., Schmid, K.W. and Jasani, B. (1994). Possible role of tissue-bound calcium ions in citrate-mediated high-temperature antigen retrieval. J. Pathol. 174 :301-7.
52. Neubauer, A., Neubauer, B., He, M., Effert, P., Iglehart, D., Frye, R.A. and Liu, E. (1992). Analysis of gene amplification in archival tissue by differential polymerase chain reaction. Oncogene 7 :1019-25.
53. O'leary, T.J., Edmonds, P., Floyd, A.D., Mesa-Tejada, R., Robinowitz, M., Takes, P.A. and Taylor, C.R. (1999). Nat. Committee Clin. Lab. Standard. 19 :v.
54. Ono, A., Kumai, T., Koizumi, H., Nishikawa, H., Kobayashi, S. and Tado- koro, M. (2009). Overexpression of heat shock protein 27 in squamous cell carcinoma of the uterine cervix: a proteomic analysis using archival formalin-fixed, paraffin-embedded tissues. Human Pathol. 40 :41-9.
55. Palmer-Toy, D.E., Krastins, B., Sarracino, D.A., Nadol, J.B.Jr. and Merchant, S.N. (2005). Efficient method for the proteomic analysis of fixed and embedded tissues. J. Proteome Res. 4 :2404-11.
56. Peranen, J., Rikkonen, M. and Kaariainen, L. (1993). A method for exposing hidden antigenic sites in paraformaldehyde-fixed cultured cells, applied to initially unreactive antibodies. J. Histochem. Cytochem. 41 :447-54.
57. Pileri, S.A., Roncador, G., Ceccarelli, C., Piccioli, M., Briskomatis, A., Sabattini, E., Ascani, S., Santini, D., et al. (1997). Antigen retrieval techniques in immunohistochemistry: comparison of different methods. J. Pathol. 183 :116-23.
58. Prieto, D.A., Hood, B.L., Darfler, M.M., Guiel, T.G., Lucas, D.A., Conrads, T.P., Veenstra, T.D. and Krizman, D.B. (2005). Liquid Tissue: proteo- mic profiling of formalin-fixed tissues. Biotechniques Suppl :32-5. Qiagen (2008). Qproteome FFPE Tissue 2D-PAGE Kit Handbook, Online kitmanual/handbook. http://www1.qiagen.com/HB/Qproteome-FFPETissue2DPAGEKit-EN Accessed on: 01/19/2009
59. Rahimi, F., Shepherd, C.E., Halliday, G.M., Geczy, C.L. and Raftery, M.J. (2006). Antigen-epitope retrieval to facilitate proteomic analysis of formalin-fixed archival brain tissue. Anal. Chem. 78 :7216-21.
60. Rait, V.K., O'leary, T.J. and Mason, J.T. (2004a). Modeling formalin fixation and antigen retrieval with bovine pancreatic ribonuclease A: I- structural and functional alterations. Lab Invest. 84 :292-9.
61. Rait, V.K., Xu, L., O'leary, T.J. and Mason, J.T. (2004b). Modeling formalin fixation and antigen retrieval with bovine pancreatic RNase A II. Interrelationship of cross-linking, immunoreactivity, and heat treatment.Lab Invest. 84 :300-6.
62. Ronci, M., Bonanno, E., Colantoni, A., Pieroni, L., Di Ilio, C., Spagnoli, L.G., Federici, G. and Urbani, A. (2008). Protein unlocking procedures of formalin-fixed paraffin-embedded tissues: application to MALDI- TOF imaging ms investigations. Proteomics 8 :3702-14.
63. Shi, S.-R., Gu, J. and Taylor, C.R. (2000). Antigen Retrieval Techniques: Immunohistochemistry And Molecular Morphology, Eaton Pub., Natick, MA.
64. Shi, S.R., Cote, R.J., Wu, L., Liu, C., Datar, R., Shi, Y., Liu, D., Lim, H., et al. (2002). DNA extraction from archival formalin-fixed, paraffin- embedded tissue sections based on the antigen retrieval principle: heating under the influence of pH. J. Histochem. Cytochem. 50 :1005-11.
65. Shi, S.R., Cote, R.J., Yang, C., Chen, C., Xu, H.J., Benedict, W.F. and Taylor, C.R. (1996). Development of an optimal protocol for antigen retrieval: a 'test battery' approach exemplified with reference to the staining of retinoblastoma protein (pRB) in formalin-fixed paraffin sections. J. Pathol. 179 :347-52.
66. Shi, S.R., Key, M.E. and Kalra, K.L. (1991). Antigen retrieval in formalin- fixed, paraffin-embedded tissues: an enhancement method for immuno- histochemical staining based on microwave oven heating of tissue sections. J. Histochem. Cytochem. 39: 741-8.
67. Shi, S.R., Liu, C., Balgley, B.M., Lee, C. and Taylor, C.R. (2006). Protein extraction from formalin-fixed, paraffin-embedded tissue sections: quality evaluation by mass spectrometry. J. Histochem. Cytochem. 54 :739-43.
68. Shi, S.R., Liu, C. and Taylor, C.R. (2007). Standardization of immunohisto- chemistry for formalin-fixed, paraffin-embedded tissue sections based on the antigen-retrieval technique: from experiments to hypothesis. J. Histochem. Cytochem. 55 :105-9.
69. Simpson, R.J. (2007). Selected chemical and enzymic cleavage reagents for protein chains. Cold Spring Harbor Protocols http://cshprotocols.- cshlp.org/cgi/content/full/2007/8/pdb.tab1ip13?&text-only=true Accessed on: 01/19/2009 doi:10.1101/10.1101/-pdb.tab1ip13
70. Sompuram, S.R., Vani, K. and Bogen, S.A. (2006). A Molecular Model of Antigen Retrieval Using a Peptide Array. Am. J. Clin. Pathol. 125 :91-8.
71. Sompuram, S.R., Vani, K., Messana, E. and Bogen, S.A. (2004). A molecular mechanism of formalin fixation and antigen retrieval. Am. J. Clin. Pathol. 121 :190-9.
72. Stearns, V. (2006). Predictive Value of cerb B2 for Endocrine Therapy and Chemotherapy in Breast Cancer. In: Biomarkers in Breast Cancer, G. Gasparini & Hayes, D. (Eds.), Humana Press, pp. 129-57.
73. Stewart, N.A. and Veenstra, T.D. (2008). Sample Preparation for Mass Spectrometry Analysis of Formalin-Fixed Paraffin-Embedded Tissue. In: 2D PAGE: Sample Preparation and Fractionation, 1st ed. J. Walker (Ed.), Springer, Totowa, NJ., pp. 131-8.
74. Stoeckli, M., Chaurand, P., Hallahan, D.E. and Caprioli, R.M. (2001). Imaging mass spectrometry: a new technology for the analysis of protein expression in mammalian tissues. Nat. Med. 7 :493-6.
75. Toews, J., Rogalski, J.C., Clark, T.J. and Kast, J. (2008). Mass spectromet- ric identification of formaldehyde-induced peptide modifications under in vivo protein cross-linking conditions. Anal. Chim. Acta 618 :168-83.
76. Valera, V.A., Walter, B.A. and Merino, M.J. (2008). Optimal protein extraction from formalin-fixed paraffin-embedded tissues for expression profiling of tumors. Lab. Invest. 88 :373.
77. Werner, M., Von Wasielewski, R. and Komminoth, P. (1996). Antigen retrieval, signal amplification and intensification in immunohistochem-istry. Histochem. Cell Biol. 105 :253-60.
78. Wisztorski, M., Lemaire, R., Stauber, J., Menguelet, S.A., Croix, D., Mathe, O.J., Day, R., Salzet, M., et al. (2007). New developments in MALDI imaging for pathology proteomic studies. Curr. Pharm. Des. 13 :3317-24.
79. Xu, H., Yang, L., Wang, W., Shi, S.R., Liu, C., Liu, Y., Fang, X., Taylor, C.R., et al. (2008). Antigen retrieval for proteomic characterization of formalin-fixed and paraffin-embedded tissues. J. Proteome Res. 7 :1098-108.
80. Yamashita, S. and Okada, Y. (2005). Mechanisms of heat-induced antigen retrieval: analyses in vitro employing SDS-PAGE and immunohisto- chemistry. J. Histochem. Cytochem. 53 :13-21.
81. Yasuda, K., Yamashita, S., Aiso, S., Shiozawa, M. and Komatsu, T. (1986). Immunohistochemical study of gamma-glutamyl transpeptidase with monoclonal antibodies. I. preparation and characteristics of monoclonal antibodies to gamma-glutamyl transpeptidase. Acta Histochem. Cytochem. 19 :589-600.