Garbage in, garbage out: A critical evaluation of strategies used for validation of immunohistochemical biomarkers

Molecular Oncology

Volumn 8, Issue 4, 2014, Pages 783-798

  O'Hurley, Gillian ^a,b,c   Sjöstedt, Evelina ^b   Rahman, Arman ^c   Li, Bo ^a   Kampf, Caroline ^b   Pontén, Fredrik ^b   Gallagher, William M ^a,c   Lindskog, Cecilia ^b  

^a UNIVERSITY COLLEGE DUBLIN   (Ireland)

^b UPPSALA UNIVERSITY   (Sweden)

^c ONCOMARK LIMITED   (Ireland)

Author keywords

Antibody reliability; Antibody validation; Biomarker discovery; Immunohistochemistry; Workflow

Indexed keywords

BIOLOGICAL MARKER; EPIDERMAL GROWTH FACTOR RECEPTOR 2; ESTROGEN RECEPTOR; PROGESTERONE RECEPTOR; ANTIBODY; TUMOR MARKER;

ANTIBODY BLOOD LEVEL; ANTIBODY SPECIFICITY; ANTIGEN ANTIBODY REACTION; ANTIGEN BINDING; FOOD AND DRUG ADMINISTRATION; HUMAN; IMMUNOHISTOCHEMISTRY; IN SITU HYBRIDIZATION; MASS SPECTROMETRY; NONHUMAN; PROTEIN ANALYSIS; PROTEIN EXPRESSION; PROTEIN PHOSPHORYLATION; REVIEW; RNA SEQUENCE; SENSITIVITY AND SPECIFICITY; TISSUE SECTION; WESTERN BLOTTING; DIAGNOSTIC USE; EVALUATION STUDY; LABORATORY DIAGNOSIS; METABOLISM; NEOPLASMS; PROCEDURES; STANDARD; STANDARDS; UNITED STATES; VALIDATION STUDY;

ANTIBODIES; HUMANS; IMMUNOHISTOCHEMISTRY; NEOPLASMS; REFERENCE STANDARDS; SPECIMEN HANDLING; TUMOR MARKERS, BIOLOGICAL; UNITED STATES; UNITED STATES FOOD AND DRUG ADMINISTRATION; VALIDATION STUDIES AS TOPIC;

EID: 84919345654     PISSN: 15747891     EISSN: 18780261     Source Type: Journal    
DOI: 10.1016/j.molonc.2014.03.008     Document Type: Review

References (123)

1. Algenas C., Agaton C., Fagerberg L., Asplund A., Bjorling L., Bjorling E., Kampf C., Lundberg E., Nilsson P., Persson A., Wester K., Ponten F., Wernerus H., Uhlen M., Ottosson Takanen J., Hober S. Antibody performance in western blot applications is context-dependent. Biotechnol. J. 2014, 9(3):435-445.
2. Anderson L., Hunter C.L. Quantitative mass spectrometric multiple reaction monitoring assays for major plasma proteins. Mol. Cell Proteomics 2006, 5(4):573-588.
3. Asplund A., Edqvist P.H., Schwenk J.M., Ponten F. Antibodies for profiling the human proteome - the human protein atlas as a resource for cancer research. Proteomics 2012, 12(13):2067-2077.
4. Baker A.F., Dragovich T., Ihle N.T., Williams R., Fenoglio-Preiser C., Powis G. Stability of phosphoprotein as a biological marker of tumor signaling. Clin. Cancer Res. 2005, 11(12):4338-4340.
5. Bartlett J.M., Thomas J., Ross D.T., Seitz R.S., Ring B.Z., Beck R.A., Pedersen H.C., Munro A., Kunkler I.H., Campbell F.M., Jack W., Kerr G.R., Johnstone L., Cameron D.A., Chetty U. Mammostrat as a tool to stratify breast cancer patients at risk of recurrence during endocrine therapy. Breast Cancer Res.: BCR 2010, 12(4):R47.
6. Bartlett J.M., Bloom K.J., Piper T., Lawton T.J., van de Velde C.J., Ross D.T., Ring B.Z., Seitz R.S., Beck R.A., Hasenburg A., Kieback D., Putter H., Markopoulos C., Dirix L., Seynaeve C., Rea D. Mammostrat as an immunohistochemical multigene assay for prediction of early relapse risk in the tamoxifen versus exemestane adjuvant multicenter trial pathology study. J.Clin. Oncol. : Off. J. Am. Soc. Clin. Oncol. 2012, 30(36):4477-4484.
7. Bataille F., Troppmann S., Klebl F., Rogler G., Stoelcker B., Hofstadter F., Bosserhoff A.K., Rummele P. Multiparameter immunofluorescence on paraffin-embedded tissue sections. Appl. Immunohistochem. Mol. Morphol.: AIMM/Off. Publ. Soc. Appl. Immunohistochem. 2006, 14(2):225-228.
8. Battifora H. The multitumor (sausage) tissue block: novel method for immunohistochemical antibody testing. Lab Invest. 1986, 55(2):244-248.
9. Biomarkers and surrogate endpoints: preferred definitions and conceptual framework. Clin. Pharmacol. Ther. 2001, 69(3):89-95. Biomarkers-Definitions-Working-Group.
10. Bjorling E., Uhlen M. Antibodypedia, a portal for sharing antibody and antigen validation data. Mol Cell Proteom. 2008, 7(10):2028-2037.
11. Blind C., Koepenik A., Pacyna-Gengelbach M., Fernahl G., Deutschmann N., Dietel M., Krenn V., Petersen I. Antigenicity testing by immunohistochemistry after tissue oxidation. J.Clin. Pathol. 2008, 61(1):79-83.
12. Blokzijl A., Friedman M., Ponten F., Landegren U. Profiling protein expression and interactions: proximity ligation as a tool for personalized medicine. J.Intern. Med. 2010, 268(3):232-245.
13. Blow N. Tissue preparation: tissue issues. Nature 2007, 448(7156):959-963.
14. Bodo J., Hsi E.D. Phosphoproteins and the dawn of functional phenotyping. Pathobiol.: J. Immunopathol. Mol. Cell. Biol. 2011, 78(2):115-121.
15. Bordeaux J., Welsh A., Agarwal S., Killiam E., Baquero M., Hanna J., Anagnostou V., Rimm D. Antibody validation. Biotechniques 2003, 48(3):197-209.
16. Bossard C., Jarry A., Colombeix C., Bach-Ngohou K., Moreau A., Loussouarn D., Mosnier J.F., Laboisse C.L. Phosphohistone H3 labelling for histoprognostic grading of breast adenocarcinomas and computer-assisted determination of mitotic index. J.Clin. Pathol. 2006, 59(7):706-710.
17. Brawand D., Soumillon M., Necsulea A., Julien P., Csardi G., Harrigan P., Weier M., Liechti A., Aximu-Petri A., Kircher M., Albert F.W., Zeller U., Khaitovich P., Grutzner F., Bergmann S., Nielsen R., Paabo S., Kaessmann H. The evolution of gene expression levels in mammalian organs. Nature 2011, 478(7369):343-348.
18. Carson J.P., Thaller C., Eichele G. A transcriptome atlas of the mouse brain at cellular resolution. Curr. Opin. Neurobiol. 2002, 12(5):562-565.
19. Cattoretti G., Pileri S., Parravicini C., Becker M.H., Poggi S., Bifulco C., Key G., D'Amato L., Sabattini E., Feudale E., et al. Antigen unmasking on formalin-fixed, paraffin-embedded tissue sections. J.Pathol. 1993, 171(2):83-98.
20. Chang T.W. Binding of cells to matrixes of distinct antibodies coated on solid surface. J.Immunol. Methods 1983, 65(1-2):217-223.
21. Cho S.W., Kim S., Kim J.M., Kim J.S. Targeted genome engineering in human cells with the Cas9 RNA-guided endonuclease. Nat. Biotechnol. 2013, 31(3):230-232.
22. Christensen N.K., Winthers L. Multi-staining immunohistochemistry. IHC Stain. Meth. 2009, 103-108.
23. Comanescu M., Arsene D., Ardeleanu C., Bussolati G. The mandate for a proper preservation in histopathological tissues. Rom. J. Morphol. Embryol.=Revue roumaine de morphologie embryologie 2012, 53(2):233-242.
24. Conway C., Dobson L., O'Grady A., Kay E., Costello S., O'Shea D. Virtual microscopy as an enabler of automated/quantitative assessment of protein expression in TMAs. Histochem. Cell Biol. 2008, 130(3):447-463.
25. Coons A.H., Creech H.J., Jones R.N. Immunological properties of an antibody containing a fluorescent group. Proc. Soc. Exp. Biol. Med. 1941, 47:200-202.
26. Couchman J.R. Commercial antibodies: the good, bad, and really ugly. J.Histochem. Cytochem.: Off. J. Histochem. Soc. 2009, 57(1):7-8.
27. Cuzick J., Dowsett M., Pineda S., Wale C., Salter J., Quinn E., Zabaglo L., Mallon E., Green A.R., Ellis I.O., Howell A., Buzdar A.U., Forbes J.F. Prognostic value of a combined estrogen receptor, progesterone receptor, Ki-67, and human epidermal growth factor receptor 2 immunohistochemical score and comparison with the Genomic Health recurrence score in early breast cancer. J.Clin. Oncol. : Off. J. Am. Soc. Clin. Oncol. 2011, 29(32):4273-4278.
28. D'Amico F., Skarmoutsou E., Stivala F. State of the art in antigen retrieval for immunohistochemistry. J.Immunol. Methods 2009, 341(1-2):1-18.
29. Dabbs D.J. Diagnostic Immunohistochemistry 2006, Elsevier, Pittsburgh.
30. Debiec-Rychter M., Wasag B., Stul M., De Wever I., Van Oosterom A., Hagemeijer A., Sciot R. Gastrointestinal stromal tumours (GISTs) negative for KIT (CD117 antigen) immunoreactivity. J.Pathol. 2004, 202(4):430-438.
31. Emoto K., Yamashita S., Okada Y. Mechanisms of heat-induced antigen retrieval: does pH or ionic strength of the solution play a role for refolding antigens?. J.Histochem. Cytochem.: Off. J. Histochem. Soc. 2005, 53(11):1311-1321.
32. Fagerberg L., Jonasson K., von Heijne G., Uhlen M., Berglund L. Prediction of the human membrane proteome. Proteomics 2010, 10(6):1141-1149.
33. Fagerberg L., Hallstrom B.M., Oksvold P., Kampf C., Djureinovic D., Odeberg J., Habuka M., Tahmasebpoor S., Danielsson A., Edlund K., Asplund A., Sjostedt E., Lundberg E., Al-Khalili Szigyarto C., Skogs M., Ottosson Takanen J., Berling H., Tegel H., Mulder J., Nilsson P., Schwenk J.M., Lindskog C., Danielsson F., Mardinoglu A., Sivertsson A., von Felitzen K., Forsberg M., Zwahlen M., Olsson I., Navani S., Huss M., Nielsen J., Ponten F., Uhlen M. Analysis of the human tissue-specific expression by genome-wide integration of transcriptomics and antibody-based proteomics. Mol Cell Proteom. 2013, 13(2):397-406.
34. Ferri G.L., Gaudio R.M., Castello I.F., Berger P., Giro G. Quadruple immunofluorescence: a direct visualization method. J.Histochem. Cytochem.: Off. J. Histochem. Soc. 1997, 45(2):155-158.
35. Fetsch P.A., Abati A. Overview of the clinical immunohistochemistry laboratory: regulations and troubleshooting guidelines. Methods Mol. Biol. 1999, 115:405-414.
36. Fiore C., Bailey D., Conlon N., Wu X., Martin N., Fiorentino M., Finn S., Fall K., Andersson S.O., Andren O., Loda M., Flavin R. Utility of multispectral imaging in automated quantitative scoring of immunohistochemistry. J.Clin. Pathol. 2012, 65(6):496-502.
37. Fowler C.B., Evers D.L., O'Leary T.J., Mason J.T. Antigen retrieval causes protein unfolding: evidence for a linear epitope model of recovered immunoreactivity. J.Histochem. Cytochem.: Off. J. Histochem. Soc. 2011, 59(4):366-381.
38. Fuzery A.K., Levin J., Chan M.M., Chan D.W. Translation of proteomic biomarkers into FDA approved cancer diagnostics: issues and challenges. Clin. Proteomics 2013, 10(1):13.
39. Gall J.G., Pardue M.L. Formation and detection of RNA-DNA hybrid molecules in cytological preparations. Proc. Natl. Acad. Sci. U S A 1969, 63(2):378-383.
40. Gerdes M.J., Sevinsky C.J., Sood A., Adak S., Bello M.O., Bordwell A., Can A., Corwin A., Dinn S., Filkins R.J., Hollman D., Kamath V., Kaanumalle S., Kenny K., Larsen M., Lazare M., Li Q., Lowes C., McCulloch C.C., McDonough E., Montalto M.C., Pang Z., Rittscher J., Santamaria-Pang A., Sarachan B.D., Seel M.L., Seppo A., Shaikh K., Sui Y., Zhang J., Ginty F. Highly multiplexed single-cell analysis of formalin-fixed, paraffin-embedded cancer tissue. Proc. Natl. Acad. Sci. U S A 2013, 110(29):11982-11987.
41. Ghaemmaghami S., Huh W.K., Bower K., Howson R.W., Belle A., Dephoure N., O'Shea E.K., Weissman J.S. Global analysis of protein expression in yeast. Nature 2003, 425(6959):737-741.
42. Greenbaum D., Jansen R., Gerstein M. Analysis of mRNA expression and protein abundance data: an approach for the comparison of the enrichment of features in the cellular population of proteins and transcripts. Bioinformatics 2002, 18(4):585-596.
43. Greenwell A., Foley J.F., Maronpot R.R. An enhancement method for immunohistochemical staining of proliferating cell nuclear antigen in archival rodent tissues. Cancer Lett. 1991, 59(3):251-256.
44. Greenwell A., Foley J.F., Maronpot R.R. Detecting proliferating cell nuclear antigen in archival rodent tissues. Environ. Health Perspect. 1993, 101(Suppl. 5):207-209.
45. Gremel G., Bergman J., Djureinovic D., Edqvist P.H., Maindad V., Bharambe B.M., Khan W.A., Navani S., Elebro J., Jirstrom K., Hellberg D., Uhlen M., Micke P., Ponten F. A systematic analysis of commonly used antibodies in cancer diagnostics. Histopathology 2014, 64(2):293-305.
46. Gustashaw K.M., Najmabadi P., Potts S. Measuring protein expression in Tissue: the complemenatary roles of brightfield and fluoescence in whole slide scanning. LABMEDICINE 2010, 41(3):135-142.
47. Hack C.J. Integrated transcriptome and proteome data: the challenges ahead. Brief Funct. Genomic Proteomic 2004, 3(3):212-219.
48. Hammond M.E., Hayes D.F., Dowsett M., Allred D.C., Hagerty K.L., Badve S., Fitzgibbons P.L., Francis G., Goldstein N.S., Hayes M., Hicks D.G., Lester S., Love R., Mangu P.B., McShane L., Miller K., Osborne C.K., Paik S., Perlmutter J., Rhodes A., Sasano H., Schwartz J.N., Sweep F.C., Taube S., Torlakovic E.E., Valenstein P., Viale G., Visscher D., Wheeler T., Williams R.B., Wittliff J.L., Wolff A.C. American Society of Clinical Oncology/College of American Pathologists guideline recommendations for immunohistochemical testing of estrogen and progesterone receptors in breast cancer. J.Clin. Oncol. 2010, 28(16):2784-2795.
49. Hawkes R., Niday E., Gordon J. A dot-immunobinding assay for monoclonal and other antibodies. Anal. Biochem. 1982, 119(1):142-147.
50. Hoover K.B., Liao S.Y., Bryant P.J. Loss of the tight junction MAGUK ZO-1 in breast cancer: relationship to glandular differentiation and loss of heterozygosity. Am. J. Pathol. 1998, 153(6):1767-1773.
51. Howat W.J., Lewis A., Jones P., Kampf C., Ponten F., van der Loos C.M., Gray N., Womack C., Warford A. Antibody validation of immunohistochemistry for biomarker discovery: recommendations of a consortium of academic and pharmaceutical based histopathology researchers. Methods 2014 Feb 11, pii: S1046-2023(14)00028-0 [Epub ahead of print]. 10.1016/j.ymeth.2014.01.018.
52. Jin L., Lloyd R.V. In situ hybridization: methods and applications. J.Clin. Lab. Anal. 1997, 11(1):2-9.
53. Jones R.J., Boyce T., Fennell M., Jacobs V., Pinto F., Duffield E., Clack G., Green T., Kelly J., Robertson J. The impact of delay in cryo-fixation on biomarkers of Src tyrosine kinase activity in human breast and bladder cancers. Cancer Chemother. Pharmacol. 2008, 61(1):23-32.
54. Jordan R.C., Daniels T.E., Greenspan J.S., Regezi J.A. Advanced diagnostic methods in oral and maxillofacial pathology. Part II: immunohistochemical and immunofluorescent methods. Oral. Surg. Oral. Med. Oral. Pathol. Oral. Radiol. Endod. 2002, 93(1):56-74.
55. Kakimoto K., Takekoshi S., Miyajima K., Osamura R.Y. Hypothesis for the mechanism for heat-induced antigen retrieval occurring on fresh frozen sections without formalin-fixation in immunohistochemistry. J.Mol. Histol. 2008, 39(4):389-399.
56. Kall L., Krogh A., Sonnhammer E.L. A combined transmembrane topology and signal peptide prediction method. J.Mol. Biol. 2004, 338(5):1027-1036.
57. Kampf C., Mardinoglu A., Fagerberg L., Hallström B.M., Edlund K., Lundberg E., Pontén F., Nielsen J., Uhlen M. The human liver-specific proteome defined by transcriptomics and antibody-based profiling. FASEB J. 2014 Mar 19, [Epub ahead of print].
58. Kampf C., Olsson I., Ryberg U., Sjostedt E., Ponten F. Production of tissue microarrays, immunohistochemistry staining and digitalization within the human protein atlas. J.Vis. Exp. 2012, 63.
59. Kay E.W., Walsh C.J., Cassidy M., Curran B., Leader M. C-erbB-2 immunostaining: problems with interpretation. J.Clin. Pathol. 1994, 47(9):816-822.
60. Kiflemariam S., Andersson S., Asplund A., Ponten F., Sjoblom T. Scalable in situ hybridization on tissue arrays for validation of novel cancer and tissue-specific biomarkers. PLoS One 2012, 7(3):e32927.
61. Kohler G., Milstein C. Continuous cultures of fused cells secreting antibody of predefined specificity. Nature 1975, 256(5517):495-497.
62. Kononen J., Bubendorf L., Kallioniemi A., Barlund M., Schraml P., Leighton S., Torhorst J., Mihatsch M.J., Sauter G., Kallioniemi O.P. Tissue microarrays for high-throughput molecular profiling of tumor specimens. Nat. Med. 1998, 4(7):844-847.
63. Krupp M., Marquardt J.U., Sahin U., Galle P.R., Castle J., Teufel A. RNA-Seq Atlas - a reference database for gene expression profiling in normal tissue by next-generation sequencing. Bioinformatics 2012, 28(8):1184-1185.
64. Kumar V.A., Fausto A.K. Robbins and Cotran Pathologic Basis of Disease 2005, Elsevier Inc.
65. Lange V., Picotti P., Domon B., Aebersold R. Selected reaction monitoring for quantitative proteomics: a tutorial. Mol. Syst. Biol. 2008, 4:222.
66. Lein E.S., Hawrylycz M.J., Ao N., Ayres M., Bensinger A., Bernard A., Boe A.F., Boguski M.S., Brockway K.S., Byrnes E.J., Chen L., Chen L., Chen T.M., Chin M.C., Chong J., Crook B.E., Czaplinska A., Dang C.N., Datta S., Dee N.R., Desaki A.L., Desta T., Diep E., Dolbeare T.A., Donelan M.J., Dong H.W., Dougherty J.G., Duncan B.J., Ebbert A.J., Eichele G., Estin L.K., Faber C., Facer B.A., Fields R., Fischer S.R., Fliss T.P., Frensley C., Gates S.N., Glattfelder K.J., Halverson K.R., Hart M.R., Hohmann J.G., Howell M.P., Jeung D.P., Johnson R.A., Karr P.T., Kawal R., Kidney J.M., Knapik R.H., Kuan C.L., Lake J.H., Laramee A.R., Larsen K.D., Lau C., Lemon T.A., Liang A.J., Liu Y., Luong L.T., Michaels J., Morgan J.J., Morgan R.J., Mortrud M.T., Mosqueda N.F., Ng L.L., Ng R., Orta G.J., Overly C.C., Pak T.H., Parry S.E., Pathak S.D., Pearson O.C., Puchalski R.B., Riley Z.L., Rockett H.R., Rowland S.A., Royall J.J., Ruiz M.J., Sarno N.R., Schaffnit K., Shapovalova N.V., Sivisay T., Slaughterbeck C.R., Smith S.C., Smith K.A., Smith B.I., Sodt A.J., Stewart N.N., Stumpf K.R., Sunkin S.M., Sutram M., Tam A., Teemer C.D., Thaller C., Thompson C.L., Varnam L.R., Visel A., Whitlock R.M., Wohnoutka P.E., Wolkey C.K., Wong V.Y., Wood M., Yaylaoglu M.B., Young R.C., Youngstrom B.L., Yuan X.F., Zhang B., A.Zwingman T., Jones A.R. Genome-wide atlas of gene expression in the adult mouse brain. Nature 2007, 445(7124):168-176.
67. Leong A.S. Diagnostic immunohistochemistry - problems and solutions. Pathology 1992, 24(1):1-4.
68. Leong T.Y., Leong A.S. How does antigen retrieval work?. Adv. Anat. Pathol. 2007, 14(2):129-131.
69. Lindskog M., Rockberg J., Uhlen M., Sterky F. Selection of protein epitopes for antibody production. Biotechniques 2005, 38(5):723-727.
70. Lindskog C., Korsgren O., Ponten F., Eriksson J.W., Johansson L., Danielsson A. Novel pancreatic beta cell-specific proteins: antibody-based proteomics for identification of new biomarker candidates. J.Proteomics 2012, 75(9):2611-2620.
71. Lizardi P.M., Huang X., Zhu Z., Bray-Ward P., Thomas D.C., Ward D.C. Mutation detection and single-molecule counting using isothermal rolling-circle amplification. Nat. Genet. 1998, 19(3):225-232.
72. Lu P., Vogel C., Wang R., Yao X., Marcotte E.M. Absolute protein expression profiling estimates the relative contributions of transcriptional and translational regulation. Nat. Biotechnol. 2007, 25(1):117-124.
73. Mali P., Yang L., Esvelt K.M., Aach J., Guell M., DiCarlo J.E., Norville J.E., Church G.M. RNA-guided human genome engineering via Cas9. Science 2013, 339(6121):823-826.
74. Mansfield J.R., Gossage K.W., Hoyt C.C., Levenson R.M. Autofluorescence removal, multiplexing, and automated analysis methods for in-vivo fluorescence imaging. J.Biomed. Opt. 2005, 10(4):41207.
75. Mason T.E., Phifer R.F., Spicer S.S., Swallow R.A., Dreskin R.B. An immunoglobulin-enzyme bridge method for localizing tissue antigens. J.Histochem. Cytochem. 1969, 17(9):563-569.
76. Mason D.Y., Micklem K., Jones M. Double immunofluorescence labelling of routinely processed paraffin sections. J.Pathol. 2000, 191(4):452-461.
77. Moreau A., Le Neel T., Joubert M., Truchaud A., Laboisse C. Approach to automation in immunohistochemistry. Clin. Chim. Acta 1998, 278(2):177-184.
78. Nakane P.K. Simultaneous localization of multiple tissue antigens using the peroxidase-labeled antibody method: a study on pituitary glands of the rat. J.Histochem. Cytochem. 1968, 16(9):557-560.
79. Niki H., Hosokawa S., Nagaike K., Tagawa T. A new immunofluorostaining method using red fluorescence of PerCP on formalin-fixed paraffin-embedded tissues. J.Immunol. Methods 2004, 293(1-2):143-151.
80. Nilsson P., Paavilainen L., Larsson K., Odling J., Sundberg M., Andersson A.C., Kampf C., Persson A., Al-Khalili Szigyarto C., Ottosson J., Bjorling E., Hober S., Wernerus H., Wester K., Ponten F., Uhlen M. Towards a human proteome atlas: high-throughput generation of mono-specific antibodies for tissue profiling. Proteomics 2005, 5(17):4327-4337.
81. Nurnberger J., Kavapurackal R., Zhang S.J., Opazo Saez A., Heusch G., Philipp T., Pietruck F., Kribben A. Differential tissue distribution of the Invs gene product inversin. Cell Tissue Res. 2006, 323(1):147-155.
82. Papaxoinis K., Patsouris E., Kittas C., Nicolopoulou-Stamati P. Insulinlike growth factor I receptor and estrogen receptor beta expressions are inversely correlated in colorectal neoplasms and affected by the insulin resistance syndrome. Hum. Pathol. 2007, 38(7):1037-1046.
83. Pekmezci M., Szpaderska A., Osipo C., Ersahin C. The effect of cold ischemia time and/or formalin fixation on estrogen receptor, progesterone receptor, and human epidermal growth factor Receptor-2 results in breast carcinoma. Pathol, Res. Int. 2012, 2012:947041.
84. Picotti P., Aebersold R., Domon B. The implications of proteolytic background for shotgun proteomics. Mol. Cell Proteom. 2007, 6(9):1589-1598.
85. Ponten F., Gry M., Fagerberg L., Lundberg E., Asplund A., Berglund L., Oksvold P., Bjorling E., Hober S., Kampf C., Navani S., Nilsson P., Ottosson J., Persson A., Wernerus H., Wester K., Uhlen M. A global view of protein expression in human cells, tissues, and organs. Mol. Syst. Biol. 2009, 5:337.
86. Ponten F., Schwenk J.M., Asplund A., Edqvist P.H. The Human Protein Atlas as a proteomic resource for biomarker discovery. J.Intern. Med. 2011, 270(5):428-446.
87. Prichard J., Bitting A., Meyers J. Handbook of Practical Immunohistochemistry 2011, Springer, New York.
88. Prioleau J., Schnitt S.J. p53 antigen loss in stored paraffin slides. N.Engl. J. Med. 1995, 332(22):1521-1522.
89. Qian X., Lloyd R.V. Recent developments in signal amplification methods for in situ hybridization. Diagn. Mol. Pathol. 2003, 12(1):1-13.
90. Rakha E.A., Patel A., Powe D.G., Benhasouna A., Green A.R., Lambros M.B., Reis-Filho J.S., Ellis I.O. Clinical and biological significance of E-cadherin protein expression in invasive lobular carcinoma of the breast. Am. J. Surg. Pathol. 2010, 34(10):1472-1479.
91. Rao D.D., Vorhies J.S., Senzer N., Nemunaitis J. siRNA vs. shRNA: similarities and differences. Adv. Drug. Deliv. Rev. 2009, 61(9):746-759.
92. Robertson D., Savage K., Reis-Filho J.S., Isacke C.M. Multiple immunofluorescence labelling of formalin-fixed paraffin-embedded (FFPE) tissue. BMC Cell Biol. 2008, 9:13.
93. Saper C.B. An open letter to our readers on the use of antibodies. J.Comp. Neurol. 2005, 493(4):477-478.
94. Saper C.B. A guide to the perplexed on the specificity of antibodies. J.Histochem. Cytochem. 2009, 57(1):1-5.
95. Sauter G., Mirlacher M. Tissue microarrays for predictive molecular pathology. J.Clin. Pathol. 2002, 55(8):575-576.
96. Schwanhausser B., Busse D., Li N., Dittmar G., Schuchhardt J., Wolf J., Chen W., Selbach M. Global quantification of mammalian gene expression control. Nature 2011, 473(7347):337-342.
97. Scott I.S., Heath T.M., Morris L.S., Rushbrook S.M., Bird K., Vowler S.L., J.Arends M., Coleman N. A novel immunohistochemical method for estimating cell cycle phase distribution in ovarian serous neoplasms: implications for the histopathological assessment of paraffin-embedded specimens. Br. J. Cancer 2004, 90(8):1583-1590.
98. Seth P. Vector-mediated cancer gene therapy: an overview. Cancer Biol. Ther. 2005, 4(5):512-517.
99. Shah R.B., Zhou M., LeBlanc M., Snyder M., Rubin M.A. Comparison of the basal cell-specific markers, 34betaE12 and p63, in the diagnosis of prostate cancer. Am. J. Surg. Pathol. 2002, 26(9):1161-1168.
100. Shi S.R., Taylor C.R. Antigen Retrieval Immunohistochemistry Based Research and Diagnostics 2011, John Wiley & Sons.
101. Shi S.R., Key M.E., Kalra K.L. 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.: Off. J. Histochem. Soc. 1991, 39(6):741-748.
102. Shi S.R., Liu C., Taylor C.R. Standardization of immunohistochemistry for formalin-fixed, paraffin-embedded tissue sections based on the antigen-retrieval technique: from experiments to hypothesis. J.Histochem. Cytochem.: Off. J. Histochem. Soc. 2007, 55(2):105-109.
103. Smith N.R., Womack C. A matrix approach to guide IHC-based tissue biomarker development in oncology drug discovery. J.Pathol. 2014, 232(2):190-198.
104. Soderberg O., Gullberg M., Jarvius M., Ridderstrale K., Leuchowius K.J., Jarvius J., Wester K., Hydbring P., Bahram F., Larsson L.G., Landegren U. Direct observation of individual endogenous protein complexes in situ by proximity ligation. Nat Methods 2006, 3(12):995-1000.
105. Soderberg O., Leuchowius K.J., Gullberg M., Jarvius M., Weibrecht I., Larsson L.G., Landegren U. Characterizing proteins and their interactions in cells and tissues using the in situ proximity ligation assay. Methods 2008, 45(3):227-232.
106. Suetterlin R., Baschong W., Laeng R.H. Immunofluorescence and confocal laser scanning microscopy of chronic myeloproliferative disorders on archival formaldehyde-fixed bone marrow. J.Histochem. Cytochem.: Off. J. Histochem. Soc. 2004, 52(3):347-354.
107. Suurmeijer A.J., Boon M.E. Notes on the application of microwaves for antigen retrieval in paraffin and plastic tissue sections. Euro. J. Morphol. 1993, 31(1-2):144-150.
108. Taylor C.R. An exaltation of experts: concerted efforts in the standardization of immunohistochemistry. Hum Pathol. 1994, 25(1):2-11.
109. Taylor C.R. Standardization in immunohistochemistry: the role of antigen retrieval in molecular morphology. Biotech. Histochem.: Off. Publ. Biol. Stain Comm. 2006, 81(1):3-12.
110. Taylor C.R., Levenson R.M. Quantification of immunohistochemistry-issues concerning methods, utility and semiquantitative assessment II. Histopathology 2006, 49(4):411-424.
111. Towbin H., Staehelin T., Gordon J. Electrophoretic transfer of proteins from polyacrylamide gels to nitrocellulose sheets: procedure and some applications. Proc. Natl. Acad Sci. U S A 1979, 76(9):4350-4354.
112. Uhlen M., Bjorling E., Agaton C., Szigyarto C.A., Amini B., Andersen E., Andersson A.C., Angelidou P., Asplund A., Asplund C., Berglund L., Bergstrom K., Brumer H., Cerjan D., Ekstrom M., Elobeid A., Eriksson C., Fagerberg L., Falk R., Fall J., Forsberg M., Bjorklund M.G., Gumbel K., Halimi A., Hallin I., Hamsten C., Hansson M., Hedhammar M., Hercules G., Kampf C., Larsson K., Lindskog M., Lodewyckx W., Lund J., Lundeberg J., Magnusson K., Malm E., Nilsson P., Odling J., Oksvold P., Olsson I., Oster E., Ottosson J., Paavilainen L., Persson A., Rimini R., Rockberg J., Runeson M., Sivertsson A., Skollermo A., Steen J., Stenvall M., Sterky F., Stromberg S., Sundberg M., Tegel H., Tourle S., Wahlund E., Walden A., Wan J., Wernerus H., Westberg J., Wester K., Wrethagen U., Xu L.L., Hober S., Ponten F. A human protein atlas for normal and cancer tissues based on antibody proteomics. Mol Cell Proteomics 2005, 4(12):1920-1932.
113. Uhlen M., Oksvold P., Fagerberg L., Lundberg E., Jonasson K., Forsberg M., Zwahlen M., Kampf C., Wester K., Hober S., Wernerus H., Bjorling L., Ponten F. Towards a knowledge-based human protein atlas. Nat. Biotechnol. 2010, 28(12):1248-1250.
114. Viklund H., Bernsel A., Skwark M., Elofsson A. SPOCTOPUS: a combined predictor of signal peptides and membrane protein topology. Bioinformatics 2008, 24(24):2928-2929.
115. von Boguslawsky K. Immunohistochemical detection of progesterone receptors in paraffin sections. A novel method using microwave oven pretreatment. APMIS 1994, 102(9):641-646.
116. Wang Z., Gerstein M., Snyder M. RNA-Seq: a revolutionary tool for transcriptomics. Nat. Rev. Genet. 2009, 10(1):57-63.
117. Warford A., Howat W., McCafferty J. Expression profiling by high-throughput immunohistochemistry. J Immunol. Methods 2004, 290(1-2):81-92.
118. Weinstein M.H., Signoretti S., Loda M. Diagnostic utility of immunohistochemical staining for p63, a sensitive marker of prostatic basal cells. Mod Pathol. 2002, 15(12):1302-1308.
119. Wester K., Wahlund E., Sundstrom C., Ranefall P., Bengtsson E., Russell P.J., Ow K.T., Malmstrom P.U., Busch C. Paraffin section storage and immunohistochemistry. Effects of time, temperature, fixation, and retrieval protocol with emphasis on p53 protein and MIB1 antigen. Appl. Immunohistochem. Mol. Morphol. 2000, 8(1):61-70.
120. Williams J.H., Mepham B.L., Wright D.H. Tissue preparation for immunocytochemistry. J.Clin. Pathol. 1997, 50(5):422-428.
121. Wu C., Orozco C., Boyer J., Leglise M., Goodale J., Batalov S., Hodge C.L., Haase J., Janes J., Huss J.W., Su A.I. BioGPS: an extensible and customizable portal for querying and organizing gene annotation resources. Genome Biol. 2009, 10(11):R130.
122. Xie R., Chung J.Y., Ylaya K., Williams R.L., Guerrero N., Nakatsuka N., Badie C., Hewitt S.M. Factors influencing the degradation of archival formalin-fixed paraffin-embedded tissue sections. J.Histochem. Cytochem. : Off. J. Histochem. Soc. 2011, 59(4):356-365.
123. Zieba A., Wahlby C., Hjelm F., Jordan L., Berg J., Landegren U., Pardali K. Bright-field microscopy visualization of proteins and protein complexes by in situ proximity ligation with peroxidase detection. Clin. Chem. 2010, 56(1):99-110.