Data analysis as a source of variability of the HLA-peptide multimer assay: From manual gating to automated recognition of cell clusters

Cancer Immunology, Immunotherapy

Volumn 64, Issue 5, 2015, Pages 585-598

  Gouttefangeas, Cécile ^a   Chan, Cliburn ^b   Attig, Sebastian ^a,g   Køllgaard, Tania T ^c,h   Rammensee, Hans Georg ^a   Stevanović, Stefan ^a   Wernet, Dorothee ^d   thor Straten, Per ^c   Welters, Marij J P ^e   Ottensmeier, Christian ^f   van der Burg, Sjoerd H ^e   Britten, Cedrik M ^g  

^a UNIVERSITY OF TÜBINGEN   (Germany)

^b DUKE UNIVERSITY MEDICAL CENTER   (United States)

^c Mental Health Services CPH   (Denmark)

^d UNIVERSITY HOSPITAL TÜBINGEN   (Germany)

^e LEIDEN UNIVERSITY MEDICAL CENTER   (Netherlands)

^f UNIVERSITY HOSPITAL SOUTHAMPTON NHS FOUNDATION TRUST   (United Kingdom)

^g JOHANNES GUTENBERG UNIVERSITY   (Germany)

^h Rigshospitalet   (Denmark)

Author keywords

Automated analysis; Data analysis; Flow cytometry gating; HLA peptide multimer; Proficiency panel

Indexed keywords

HLA A ANTIGEN; PEPTIDE; POLYMER; REAGENT; HLA ANTIGEN;

ANTIGEN SPECIFICITY; ARTICLE; AUTOMATION; CELL VIABILITY; CONTROLLED STUDY; DATA ANALYSIS; FLOW CYTOMETRY; HLA SYSTEM; HUMAN; HUMAN CELL; IMMUNOASSAY; MOLECULAR RECOGNITION; NORMAL HUMAN; OUTCOME ASSESSMENT; PERIPHERAL BLOOD MONONUCLEAR CELL; PRIORITY JOURNAL; STAINING; T LYMPHOCYTE; THAWING; CD8+ T LYMPHOCYTE; CYTOLOGY; IMMUNOLOGICAL MONITORING; IMMUNOLOGY; INFORMATION PROCESSING; OBSERVER VARIATION; PROCEDURES; REPRODUCIBILITY; STANDARDS; STATISTICAL ANALYSIS; STATISTICS AND NUMERICAL DATA;

AUTOMATIC DATA PROCESSING; CD8-POSITIVE T-LYMPHOCYTES; DATA INTERPRETATION, STATISTICAL; FLOW CYTOMETRY; HEALTHY VOLUNTEERS; HLA ANTIGENS; HUMANS; MONITORING, IMMUNOLOGIC; OBSERVER VARIATION; REPRODUCIBILITY OF RESULTS;

EID: 84938414151     PISSN: 03407004     EISSN: 14320851     Source Type: Journal    
DOI: 10.1007/s00262-014-1649-1     Document Type: Article

References (44)

1. Davis MM, Altman JD, Newell EW (2011) Interrogating the repertoire: broadening the scope of peptide–MHC multimer analysis. Nat Rev Immunol 11:551–558
2. Altman JD, Moss PA, Goulder PJ, Barouch DH, McHeyzer-Williams MG, Bell JI, McMichael AJ, Davis MM (1996) Phenotypic analysis of antigen-specific T lymphocytes. Science 274:94–96
3. + T cells vary in differentiation phenotype in different persistent virus infections. Nat Med 8:379–385
4. + T cells is reflected by their avidity, polyfunctionality, and clonal turnover. J Exp Med 204:2473–2485
5. + T cells in metastases from melanoma patients. J Clin Invest 121:2350–2360
6. Andersen RS, Kvistborg P, Frosig TM, Pedersen NW, Lyngaa R, Bakker AH, Shu CJ, Straten P, Schumacher TN, Hadrup SR (2012) Parallel detection of antigen-specific T cell responses by combinatorial encoding of MHC multimers. Nat Protoc 7:891–902
7. + T-cell responses to a multipeptide melanoma vaccine: outcome of a multicenter randomized trial. Clin Cancer Res 15:7036–7044
8. Coulie PG, Karanikas V, Colau D, Lurquin C, Landry C, Marchand M, Dorval T, Brichard V, Boon T (2001) A monoclonal cytolytic T-lymphocyte response observed in a melanoma patient vaccinated with a tumor-specific antigenic peptide encoded by gene MAGE-3. Proc Natl Acad Sci USA 98:10290–10295
9. Filipazzi P, Pilla L, Mariani L, Patuzzo R, Castelli C, Camisaschi C, Maurichi A, Cova A, Rigamonti G, Giardino F, Di Florio A, Asioli M, Frati P, Sovena G, Squarcina P, Maio M, Danielli R, Chiarion-Sileni V, Villa A, Lombardo C, Tragni G, Santinami M, Parmiani G, Rivoltini L (2012) Limited induction of tumor cross-reactive T cells without a measurable clinical benefit in early melanoma patients vaccinated with human leukocyte antigen class I-modified peptides. Clin Cancer Res 18:6485–6496
10. Walter S, Weinschenk T, Stenzl A, Zdrojowy R, Pluzanska A, Szczylik C, Staehler M, Brugger W, Dietrich PY, Mendrzyk R, Hilf N, Schoor O, Fritsche J, Mahr A, Maurer D, Vass V, Trautwein C, Lewandrowski P, Flohr C, Pohla H, Stanczak JJ, Bronte V, Mandruzzato S, Biedermann T, Pawelec G, Derhovanessian E, Yamagishi H, Miki T, Hongo F, Takaha N, Hirakawa K, Tanaka H, Stevanovic S, Frisch J, Mayer-Mokler A, Kirner A, Rammensee HG, Reinhardt C, Singh-Jasuja H (2012) Multipeptide immune response to cancer vaccine IMA901 after single-dose cyclophosphamide associates with longer patient survival. Nat Med 18:1254–1261
11. De Vries IJ, Bernsen MR, Lesterhuis WJ, Scharenborg NM, Strijk SP, Gerritsen MJ, Ruiter DJ, Figdor CG, Punt CJ, Adema GJ (2005) Immunomonitoring tumor-specific T cells in delayed-type hypersensitivity skin biopsies after dendritic cell vaccination correlates with clinical outcome. J Clin Oncol 23:5779–5787
12. Van Tendeloo VF, Van de Velde A, Van Driessche A, Cools N, Anguille S, Ladell K, Gostick E, Vermeulen K, Pieters K, Nijs G, Stein B, Smits EL, Schroyens WA, Gadisseur AP, Vrelust I, Jorens PG, Goossens H, De Vries IJ, Price DA, Oji Y, Oka Y, Sugiyama H, Berneman ZN (2010) Induction of complete and molecular remissions in acute myeloid leukemia by Wilms’ tumor 1 antigen-targeted dendritic cell vaccination. Proc Natl Acad Sci USA 107:13824–13829
13. Wooldridge L, Lissina A, Cole DK, van den Berg HA, Price DA, Sewell AK (2009) Tricks with tetramers: how to get the most from multimeric peptide-MHC. Immunology 126:147–164
14. Herzenberg LA, Tung J, Moore WA, Herzenberg LA, Parks DR (2006) Interpreting flow cytometry data: a guide for the perplexed. Nat Immunol 7:681–685
15. Mahnke Y, Chattopadhyay P, Roederer M (2010) Publication of optimized multicolor immunofluorescence panels. Cytometry A 77:814–818
16. Lee JA, Spidlen J, Boyce K, Cai J, Crosbie N, Dalphin M, Furlong J, Gasparetto M, Goldberg M, Goralczyk EM, Hyun B, Jansen K, Kollmann T, Kong M, Leif R, McWeeney S, Moloshok TD, Moore W, Nolan G, Nolan J, Nikolich-Zugich J, Parrish D, Purcell B, Qian Y, Selvaraj B, Smith C, Tchuvatkina O, Wertheimer A, Wilkinson P, Wilson C, Wood J, Zigon R, Scheuermann RH, Brinkman RR (2008) MIFlowCyt: the minimum information about a Flow Cytometry Experiment. Cytom A 73:926–930
17. + T cells with peptide-major histocompatibility complex class I tetramers. Cytom A 73:1001–1009
18. Perfetto SP, Ambrozak D, Nguyen R, Chattopadhyay PK, Roederer M (2012) Quality assurance for polychromatic flow cytometry using a suite of calibration beads. Nat Protoc 7:2067–2079
19. Horton H, Thomas EP, Stucky JA, Frank I, Moodie Z, Huang Y, Chiu YL, McElrath MJ, De Rosa SC (2007) Optimization and validation of an 8-color intracellular cytokine staining (ICS) assay to quantify antigen-specific T cells induced by vaccination. J Immunol Methods 323:39–54
20. Maecker HT, McCoy JP, Nussenblatt R (2012) Standardizing immunophenotyping for the human immunology project. Nat Rev Immunol 12:191–200
21. Maecker HT, McCoy JP Jr, Amos M, Elliott J, Gaigalas A, Wang L, Aranda R, Banchereau J, Boshoff C, Braun J, Korin Y, Reed E, Cho J, Hafler D, Davis M, Fathman CG, Robinson W, Denny T, Weinhold K, Desai B, Diamond B, Gregersen P, Di Meglio P, Nestle FO, Peakman M, Villanova F, Ferbas J, Field E, Kantor A, Kawabata T, Komocsar W, Lotze M, Nepom J, Ochs H, O’Lone R, Phippard D, Plevy S, Rich S, Roederer M, Rotrosen D, Yeh JH (2010) A model for harmonizing flow cytometry in clinical trials. Nat Immunol 11:975–978
22. van der Burg SH, Kalos M, Gouttefangeas C, Janetzki S, Ottensmeier C, Welters MJ, Romero P, Britten CM, Hoos A (2011) Harmonization of immune biomarker assays for clinical studies. Sci Transl Med 3:108ps44
23. + T lymphocytes by structural and functional assays. Cancer Immunol Immunother 57:289–302
24. Mander A, Gouttefangeas C, Ottensmeier C, Welters MJ, Low L, van der Burg SH, Britten CM (2010) Serum is not required for ex vivo IFN-gamma ELISPOT: a collaborative study of different protocols from the European CIMT Immunoguiding Program. Cancer Immunol Immunother 59:619–627
25. Filbert H, Attig S, Bidmon N, Renard BY, Janetzki S, Sahin U, Welters MJ, Ottensmeier C, van der Burg SH, Gouttefangeas C, Britten CM (2013) Serum-free freezing media support high cell quality and excellent ELISPOT assay performance across a wide variety of different assay protocols. Cancer Immunol Immunother 62:615–627
26. Welters MJ, Gouttefangeas C, Ramwadhdoebe TH, Letsch A, Ottensmeier CH, Britten CM, van der Burg SH (2012) Harmonization of the intracellular cytokine staining assay. Cancer Immunol Immunother 61:967–978
27. Janetzki S, Panageas KS, Ben Porat L, Boyer J, Britten CM, Clay TM, Kalos M, Maecker HT, Romero P, Yuan J, Kast WM, Hoos A (2008) Results and harmonization guidelines from two large-scale international Elispot proficiency panels conducted by the Cancer Vaccine Consortium (CVC/SVI). Cancer Immunol Immunother 57:303–315
28. Attig S, Price L, Janetzki S, Kalos M, Pride M, McNeil L, Clay T, Yuan J, Odunsi K, Hoos A, Romero P, Britten CM (2011) A critical assessment for the value of markers to gate-out undesired events in HLA-peptide multimer staining protocols. J Transl Med 9:108
29. Jaimes MC, Maecker HT, Yan M, Maino VC, Hanley MB, Greer A, Darden JM, D’Souza MP (2011) Quality assurance of intracellular cytokine staining assays: analysis of multiple rounds of proficiency testing. J Immunol Methods 363:143–157
30. McNeil LK, Price L, Britten CM, Jaimes M, Maecker H, Odunsi K, Matsuzaki J, Staats JS, Thorpe J, Yuan J, Janetzki S (2013) A harmonized approach to intracellular cytokine staining gating: results from an international multiconsortia proficiency panel conducted by the Cancer Immunotherapy Consortium (CIC/CRI). Cytom A 83:728–738
31. Maecker HT, Rinfret A, D’Souza P, Darden J, Roig E, Landry C, Hayes P, Birungi J, Anzala O, Garcia M, Harari A, Frank I, Baydo R, Baker M, Holbrook J, Ottinger J, Lamoreaux L, Epling CL, Sinclair E, Suni MA, Punt K, Calarota S, El-Bahi S, Alter G, Maila H, Kuta E, Cox J, Gray C, Altfeld M, Nougarede N, Boyer J, Tussey L, Tobery T, Bredt B, Roederer M, Koup R, Maino VC, Weinhold K, Pantaleo G, Gilmour J, Horton H, Sekaly RP (2005) Standardization of cytokine flow cytometry assays. BMC Immunol 6:13
32. Chan C, Feng F, Ottinger J, Foster D, West M, Kepler TB (2008) Statistical mixture modeling for cell subtype identification in flow cytometry. Cytom A 73:693–701
33. Frelinger J, Ottinger J, Gouttefangeas C, Chan C (2010) Modeling flow cytometry data for cancer vaccine immune monitoring. Cancer Immunol Immunother 59:1435–1441
34. Aghaeepour N, Finak G, Dougall D, Khodabakhshi AH, Mah P, Obermoser G, Spidlen J, Taylor I, Wuensch SA, Bramson J, Eaves C, Weng AP, Iii ES, Ho K, Kollmann T, Rogers W, De Rosa S, Dalal B, Azad A, Pothen A, Brandes A, Bretschneider H, Bruggner R, Finck R, Jia R, Zimmerman N, Linderman M, Dill D, Nolan G, Chan C, Khettabi FE, O’Neill K, Chikina M, Ge Y, Sealfon S, Sugar I, Gupta A, Shooshtari P, Zare H, De Jager PL, Jiang M, Keilwagen J, Maisog JM, Luta G, Barbo AA, Majek P, Vilcek J, Manninen T, Huttunen H, Ruusuvuori P, Nykter M, McLachlan GJ, Wang K, Naim I, Sharma G, Nikolic R, Pyne S, Qian Y, Qiu P, Quinn J, Roth A, Meyer P, Stolovitzky G, Saez-Rodriguez J, Norel R, Bhattacharjee M, Biehl M, Bucher P, Bunte K, Di Camillo B, Sambo F, Sanavia T, Trifoglio E, Toffolo G, Dimitrieva S, Dreos R, Ambrosini G, Grau J, Grosse I, Posch S, Guex N, Keilwagen J, Kursa M, Rudnicki W, Liu B, Maienschein-Cline M, Manninen T, Huttunen H, Ruusuvuori P, Nykter M, Schneider P, Seifert M, Strickert M, Vilar JM, Hoos H, Mosmann TR, Brinkman R, Gottardo R, Scheuermann RH (2013) Critical assessment of automated flow cytometry data analysis techniques. Nat Methods 10:228–238
35. Cron A, Gouttefangeas C, Frelinger J, Lin L, Singh SK, Britten CM, Welters MJ, van der Burg SH, West M, Chan C (2013) Hierarchical modeling for rare event detection and cell subset alignment across flow cytometry samples. PLoS Comput Biol 9:e1003130
36. Britten CM, Janetzki S, Butterfield LH, Ferrari G, Gouttefangeas C, Huber C, Kalos M, Levitsky HI, Maecker HT, Melief CJ, O’Donnell-Tormey J, Odunsi K, Old LJ, Ottenhoff TH, Ottensmeier C, Pawelec G, Roederer M, Roep BO, Romero P, van der Burg SH, Walter S, Hoos A, Davis MM (2012) T cell assays and MIATA: the essential minimum for maximum impact. Immunity 37:1–2
37. Britten CM, Janetzki S, Ben Porat L, Clay TM, Kalos M, Maecker H, Odunsi K, Pride M, Old L, Hoos A, Romero P (2009) Harmonization guidelines for HLA-peptide multimer assays derived from results of a large scale international proficiency panel of the Cancer Vaccine Consortium. Cancer Immunol Immunother 58:1701–1713
38. Speiser DE, Pittet MJ, Guillaume P, Lubenow N, Hoffman E, Cerottini JC, Romero P (2004) Ex vivo analysis of human antigen-specific CD8 + T-cell responses: quality assessment of fluorescent HLA-A2 multimer and interferon-gamma ELISPOT assays for patient immune monitoring. J Immunother 27:298–308
39. + T lymphocytes by single-platform, HLA tetramer-based flow cytometry: a European multicenter evaluation. Cytom B Clin Cytom 62:1–13
40. Mosmann TR, Naim I, Rebhahn J, Datta S, Cavenaugh JS, Weaver JM, Sharma G (2014) SWIFT-scalable clustering for automated identification of rare cell populations in large, high-dimensional flow cytometry datasets, part 2: biological evaluation. Cytom A 85:422–433
41. Knabel M, Franz TJ, Schiemann M, Wulf A, Villmow B, Schmidt B, Bernhard H, Wagner H, Busch DH (2002) Reversible MHC multimer staining for functional isolation of T-cell populations and effective adoptive transfer. Nat Med 8:631–637
42. Whelan JA, Dunbar PR, Price DA, Purbhoo MA, Lechner F, Ogg GS, Griffiths G, Phillips RE, Cerundolo V, Sewell AK (1999) Specificity of CTL interactions with peptide-MHC class I tetrameric complexes is temperature dependent. J Immunol 163:4342–4348
43. Bergeron M, Nicholson JK, Phaneuf S, Ding T, Soucy N, Badley AD, Hawley Foss NC, Mandy F (2002) Selection of lymphocyte gating protocol has an impact on the level of reliability of T-cell subsets in aging specimens. Cytometry 50:53–61
44. White S, Laske K, Welters MJP, Bidmon N, van der Burg SJ, Britten CM, Enzor J, Staats J, Weinhold KJ, Gouttefangeas C, Chan C (2014) Managing multi-center flow cytometry data for immune monitoring. Cancer Inform (in press)