{"status":"ok","message-type":"work","message-version":"1.0.0","message":{"indexed":{"date-parts":[[2026,10,21]],"date-time":"2026-10-21T03:39:15Z","timestamp":1792553955675,"version":"4.5.0"},"reference-count":43,"publisher":"MDPI AG","issue":"3","license":[{"start":{"date-parts":[[2012,7,30]],"date-time":"2012-07-30T00:00:00Z","timestamp":1343606400000},"content-version":"vor","delay-in-days":0,"URL":"https:\/\/creativecommons.org\/licenses\/by\/3.0\/"}],"content-domain":{"domain":[],"crossmark-restriction":false},"short-container-title":["Cells"],"abstract":"<jats:p>T cell monitoring is increasingly performed using cryopreserved PBMC. It has been suggested that resting of PBMC after thawing, that is, culturing them overnight in test medium, produces higher antigen-induced spot counts in ELISPOT assays. To evaluate the importance of overnight resting, we systematically tested cryopreserved PBMC from 25 healthy donors. CEF peptides (comprising CMV, EBV and flu antigens) were used to stimulate CD8 cells and mumps antigen to stimulate CD4 cells. The data show that resting significantly increased antigen-elicited T cell responses only for CEF high responder PBMC. The maximal gain observed was doubling of spot counts. For CEF low responders, and for mumps responders of either low- or high reactivity levels, resting had no statistically significant effect on the observed spot counts. Therefore, resting is not a generally applicable approach to improve ELISPOT assay performance, but can be recommended only for clinical subject cohorts and antigens for which it has a proven benefit. Because resting invariably leads to losing about half of the PBMC available for testing, and because doubling the PBMC numbers plated into the assay reliably doubles the antigen-induced spot counts, we suggest the latter approach as a simple and reliable alternative to resting for enhancing the performance of ELISPOT assays. Our data imply that resting is not required if PBMC were cryopreserved and thawed under conditions that minimize apoptosis of the cells. Therefore, this study should draw attention to the need to optimize freezing and thawing conditions for successful T cell work.<\/jats:p>","DOI":"10.3390\/cells1030409","type":"journal-article","created":{"date-parts":[[2012,7,30]],"date-time":"2012-07-30T10:51:50Z","timestamp":1343645510000},"page":"409-427","update-policy":"https:\/\/doi.org\/10.3390\/mdpi_crossmark_policy","source":"Crossref","is-referenced-by-count":30,"title":["Resting of Cryopreserved PBMC Does Not Generally Benefit the Performance of Antigen-Specific T Cell ELISPOT Assays"],"prefix":"10.3390","volume":"1","author":[{"given":"Stefanie","family":"Kuerten","sequence":"first","affiliation":[{"name":"Department of Anatomy I, University of Cologne, Joseph-Stelzmann-Str. 9, 50931 Cologne, Germany"}],"role":[{"vocabulary":"crossref","role":"author"}]},{"given":"Helena","family":"Batoulis","sequence":"additional","affiliation":[{"name":"Department of Anatomy I, University of Cologne, Joseph-Stelzmann-Str. 9, 50931 Cologne, Germany"}],"role":[{"vocabulary":"crossref","role":"author"}]},{"given":"Mascha S.","family":"Recks","sequence":"additional","affiliation":[{"name":"Department of Anatomy I, University of Cologne, Joseph-Stelzmann-Str. 9, 50931 Cologne, Germany"}],"role":[{"vocabulary":"crossref","role":"author"}]},{"given":"Edith","family":"Karacsony","sequence":"additional","affiliation":[{"name":"Cellular Technology Ltd. (C.T.L), Shaker Heights, OH 44122, USA"}],"role":[{"vocabulary":"crossref","role":"author"}]},{"given":"Wenji","family":"Zhang","sequence":"additional","affiliation":[{"name":"Cellular Technology Ltd. (C.T.L), Shaker Heights, OH 44122, USA"}],"role":[{"vocabulary":"crossref","role":"author"}]},{"given":"Ramu A.","family":"Subbramanian","sequence":"additional","affiliation":[{"name":"Cellular Technology Ltd. (C.T.L), Shaker Heights, OH 44122, USA"}],"role":[{"vocabulary":"crossref","role":"author"}]},{"given":"Paul V.","family":"Lehmann","sequence":"additional","affiliation":[{"name":"Cellular Technology Ltd. (C.T.L), Shaker Heights, OH 44122, USA"}],"role":[{"vocabulary":"crossref","role":"author"}]}],"member":"1968","published-online":{"date-parts":[[2012,7,30]]},"reference":[{"key":"ref_1","doi-asserted-by":"crossref","first-page":"463","DOI":"10.1016\/j.humimm.2011.03.001","article-title":"Comparison of antibody and T-cell responses elicited by licensed inactivated- and live-attenuated influenza vaccines against H3N2 hemagglutinin","volume":"72","author":"Basha","year":"2011","journal-title":"Hum. Immunol."},{"key":"ref_2","doi-asserted-by":"crossref","first-page":"232","DOI":"10.4161\/hv.1.6.2342","article-title":"Randomized, placebo-controlled, phase I\/IIa evaluation of the safety and immunogenicity of fowlpox virus expressing HIV gag-pol and interferon-gamma in HIV-1 infected subjects","volume":"1","author":"Emery","year":"2005","journal-title":"Hum. Vaccin."},{"key":"ref_3","doi-asserted-by":"crossref","first-page":"4905","DOI":"10.1016\/j.vaccine.2006.03.058","article-title":"Immunization with SARS-CoV S DNA vaccine generates memory CD4+ and CD8+ T cell immune responses","volume":"24","author":"Huang","year":"2006","journal-title":"Vaccine"},{"key":"ref_4","doi-asserted-by":"crossref","first-page":"5771","DOI":"10.4049\/jimmunol.164.11.5771","article-title":"Revisiting tolerance induced by autoantigen in incomplete Freund's adjuvant","volume":"164","author":"Heeger","year":"2000","journal-title":"J. Immunol."},{"key":"ref_5","doi-asserted-by":"crossref","first-page":"36","DOI":"10.1186\/1471-2474-6-36","article-title":"Immunologic testing of xeno-derived osteochondral grafts using peripheral blood mononuclear cells from healthy human donors","volume":"6","author":"Hetherington","year":"2005","journal-title":"BMC Musculoskelet. Disord."},{"key":"ref_6","doi-asserted-by":"crossref","first-page":"534","DOI":"10.1111\/j.1398-9995.2008.01674.x","article-title":"Detection and quantification of drug-specific T cells in penicillin allergy","volume":"64","author":"Rozieres","year":"2009","journal-title":"Allergy"},{"key":"ref_7","doi-asserted-by":"crossref","first-page":"4598","DOI":"10.4049\/jimmunol.174.8.4598","article-title":"Does the frequency and avidity spectrum of the neuroantigen-specific T cells in the blood mirror the autoimmune process in the central nervous system of mice undergoing experimental allergic encephalomyelitis?","volume":"174","author":"Hofstetter","year":"2005","journal-title":"J. Immunol."},{"key":"ref_8","doi-asserted-by":"crossref","first-page":"365","DOI":"10.1016\/S0896-8411(03)00111-2","article-title":"Comparison of cytokine ELISpot assay formats for the detection of islet antigen autoreactive T cells. Report of the third immunology of diabetes society T-cell workshop","volume":"21","author":"Schloot","year":"2003","journal-title":"J. Autoimmun."},{"key":"ref_9","doi-asserted-by":"crossref","first-page":"5654","DOI":"10.4049\/jimmunol.0900645","article-title":"Encephalitogenicity of complete Freund's adjuvant relative to CpG is linked to induction of Th17 cells","volume":"183","author":"Jaini","year":"2009","journal-title":"J. Immunol."},{"key":"ref_10","doi-asserted-by":"crossref","first-page":"289","DOI":"10.1097\/00002371-200005000-00001","article-title":"Quantification of tumor-specific T lymphocytes with the ELISPOT assay","volume":"23","author":"Schmittel","year":"2000","journal-title":"J. Immunother."},{"key":"ref_11","doi-asserted-by":"crossref","first-page":"97","DOI":"10.1097\/00002371-200203000-00001","article-title":"Immunologic monitoring of cancer vaccine therapy: Results of a workshop sponsored by the Society for Biological Therapy","volume":"25","author":"Keilholz","year":"2002","journal-title":"J. Immunother."},{"key":"ref_12","doi-asserted-by":"crossref","first-page":"149","DOI":"10.3109\/08820130009062299","article-title":"Immunologic monitoring of clinical trials in patients with cancer: Technology versus common sense","volume":"29","author":"Whiteside","year":"2000","journal-title":"Immunol. Invest."},{"key":"ref_13","doi-asserted-by":"crossref","first-page":"3","DOI":"10.1007\/978-1-61779-325-7_1","article-title":"Unique strengths of ELISPOT for T cell diagnostics","volume":"792","author":"Lehmann","year":"2012","journal-title":"Methods Mol. Biol."},{"key":"ref_14","doi-asserted-by":"crossref","first-page":"3723","DOI":"10.4049\/jimmunol.164.7.3723","article-title":"Direct visualization of cytokine-producing recall antigen-specific CD4 memory T cells in healthy individuals and HIV patients","volume":"164","author":"Helms","year":"2000","journal-title":"J. Immunol."},{"key":"ref_15","doi-asserted-by":"crossref","first-page":"79","DOI":"10.1016\/S0022-1759(03)00226-6","article-title":"CD4+ and CD8+ cells in cryopreserved human PBMC maintain full functionality in cytokine ELISPOT assays","volume":"278","author":"Kreher","year":"2003","journal-title":"J. Immunol. Methods"},{"key":"ref_16","doi-asserted-by":"crossref","first-page":"28","DOI":"10.1016\/j.cellimm.2005.09.002","article-title":"IL-2 absorption affects IFN-gamma and IL-5, but not IL-4 producing memory T cells in double color cytokine ELISPOT assays","volume":"237","author":"Quast","year":"2005","journal-title":"Cell Immunol."},{"key":"ref_17","doi-asserted-by":"crossref","first-page":"1372","DOI":"10.4049\/jimmunol.178.3.1372","article-title":"Kinetics and organ distribution of IL-17-producing CD4 cells in proteolipid protein 139\u2013151 peptide-induced experimental autoimmune encephalomyelitis of SJL mice","volume":"178","author":"Hofstetter","year":"2007","journal-title":"J. Immunol."},{"key":"ref_18","doi-asserted-by":"crossref","first-page":"36","DOI":"10.1016\/j.cellimm.2007.07.004","article-title":"Granzyme B production distinguishes recently activated CD8(+) memory cells from resting memory cells","volume":"247","author":"Nowacki","year":"2007","journal-title":"Cell Immunol."},{"key":"ref_19","doi-asserted-by":"crossref","first-page":"143","DOI":"10.1016\/S0022-1759(00)00191-5","article-title":"Granzyme B ELISPOT assay for ex vivo measurements of T cell immunity","volume":"240","author":"Rininsland","year":"2000","journal-title":"J. Immunol. Methods"},{"key":"ref_20","doi-asserted-by":"crossref","first-page":"62","DOI":"10.1089\/aid.2007.0125","article-title":"Dissociated production of perforin, granzyme B, and IFN-gamma by HIV-specific CD8(+) cells in HIV infection","volume":"24","author":"Kuerten","year":"2008","journal-title":"AIDS Res. Hum. Retroviruses"},{"key":"ref_21","doi-asserted-by":"crossref","first-page":"111","DOI":"10.1016\/S0022-1759(03)00240-0","article-title":"Detection of low-frequency antigen-specific IL-10-producing CD4(+) T cells via ELISPOT in PBMC: Cognate vs. nonspecific production of the cytokine","volume":"279","author":"Guerkov","year":"2003","journal-title":"J. Immunol. Methods"},{"key":"ref_22","doi-asserted-by":"crossref","first-page":"1862","DOI":"10.4049\/jimmunol.164.4.1862","article-title":"Single-cytokine-producing CD4 memory cells predominate in type 1 and type 2 immunity","volume":"164","author":"Karulin","year":"2000","journal-title":"J. Immunol."},{"key":"ref_23","doi-asserted-by":"crossref","unstructured":"Prabhakar, U., and Kelley, M. (2008). Validation of Cell-Based Assays in the GLP Setting, Wiley.","DOI":"10.1002\/9780470987810"},{"key":"ref_24","doi-asserted-by":"crossref","first-page":"9","DOI":"10.1186\/1479-5876-2-9","article-title":"A modified human ELISPOT assay to detect specific responses to primary tumor cell targets","volume":"2","author":"Malyguine","year":"2004","journal-title":"J. Transl. Med."},{"key":"ref_25","doi-asserted-by":"crossref","first-page":"303","DOI":"10.1007\/s00262-007-0380-6","article-title":"Results and harmonization guidelines from two large-scale international Elispot proficiency panels conducted by the Cancer Vaccine Consortium (CVC\/SVI)","volume":"57","author":"Janetzki","year":"2008","journal-title":"Cancer Immunol. Immunother."},{"key":"ref_26","doi-asserted-by":"crossref","first-page":"289","DOI":"10.1007\/s00262-007-0378-0","article-title":"The CIMT-monitoring panel: A two-step approach to harmonize the enumeration of antigen-specific CD8+ T lymphocytes by structural and functional assays","volume":"57","author":"Britten","year":"2008","journal-title":"Cancer Immunol. Immunother."},{"key":"ref_27","first-page":"51","article-title":"Standardization and validation issues of the ELISPOT assay","volume":"302","author":"Janetzki","year":"2005","journal-title":"Methods Mol. Biol."},{"key":"ref_28","doi-asserted-by":"crossref","first-page":"e14330","DOI":"10.1371\/journal.pone.0014330","article-title":"Equivalence of ELISpot assays demonstrated between major HIV network laboratories","volume":"5","author":"Gill","year":"2010","journal-title":"PLoS One"},{"key":"ref_29","doi-asserted-by":"crossref","first-page":"1","DOI":"10.1016\/j.jim.2009.02.007","article-title":"Automation of the ELISpot assay for high-throughput detection of antigen-specific T-cell responses","volume":"344","author":"Almeida","year":"2009","journal-title":"J. Immunol. Methods"},{"key":"ref_30","unstructured":"Moldovan, I. Cellular Technology Limited, Shaker Heights, OH, USA, Personal communication, 2012."},{"key":"ref_31","unstructured":"ePBMC data base. Available online:http:\/\/www.immunospot.com."},{"key":"ref_32","doi-asserted-by":"crossref","first-page":"86","DOI":"10.1089\/aid.2006.0129","article-title":"Enhanced rates and magnitude of immune responses detected against an HIV vaccine: Effect of using an optimized process for isolating PBMC","volume":"23","author":"Kierstead","year":"2007","journal-title":"AIDS Res. Hum. Retroviruses"},{"key":"ref_33","doi-asserted-by":"crossref","first-page":"244","DOI":"10.1016\/j.it.2006.03.005","article-title":"Apoptotic cell removal in development and tissue homeostasis","volume":"27","author":"Henson","year":"2006","journal-title":"Trends Immunol."},{"key":"ref_34","doi-asserted-by":"crossref","first-page":"551","DOI":"10.1038\/sj.cdd.4400404","article-title":"The role of phosphatidylserine in recognition of apoptotic cells by phagocytes","volume":"5","author":"Fadok","year":"1998","journal-title":"Cell Death Differ."},{"key":"ref_35","doi-asserted-by":"crossref","first-page":"350","DOI":"10.1038\/37022","article-title":"Immunosuppressive effects of apoptotic cells","volume":"390","author":"Voll","year":"1997","journal-title":"Nature"},{"key":"ref_36","first-page":"20","article-title":"Apoptotic human cells inhibit migration of granulocytes via release of lactoferrin","volume":"119","author":"Bournazou","year":"2009","journal-title":"J. Clin. Invest."},{"key":"ref_37","doi-asserted-by":"crossref","first-page":"83","DOI":"10.1016\/S0008-8749(03)00006-6","article-title":"Lactoferrin down-regulates the LPS-induced cytokine production in monocytic cells via NF-kappa B","volume":"220","author":"Haversen","year":"2002","journal-title":"Cell Immunol."},{"key":"ref_38","doi-asserted-by":"crossref","first-page":"235","DOI":"10.1182\/blood.V80.1.235.235","article-title":"Regulation of cytokine release from mononuclear cells by the iron-binding protein lactoferrin","volume":"80","author":"Crouch","year":"1992","journal-title":"Blood"},{"key":"ref_39","doi-asserted-by":"crossref","first-page":"1291","DOI":"10.1046\/j.1440-1746.2002.02868.x","article-title":"Oral administration of lactoferrin reduces colitis in rats via modulation of the immune system and correction of cytokine imbalance","volume":"17","author":"Togawa","year":"2002","journal-title":"J. Gastroenterol. Hepatol."},{"key":"ref_40","first-page":"811","article-title":"Effects of lactoferrin on the immune response modified by the immobilization stress","volume":"57","author":"Zimecki","year":"2005","journal-title":"Pharmacol. Rep."},{"key":"ref_41","doi-asserted-by":"crossref","first-page":"313","DOI":"10.3390\/cells1030313","article-title":"Optimal thawing of cryopreserved peripheral blood mononuclear cells for use in high-throughput human immune monitoring studies","volume":"1","author":"Ramachandran","year":"2012","journal-title":"Cells"},{"key":"ref_42","first-page":"117","article-title":"Image analysis and data management of ELISPOT assay results","volume":"302","author":"Lehmann","year":"2005","journal-title":"Methods Mol. Biol."},{"key":"ref_43","unstructured":"FACSDivaTM, version 4; flow cytometry analysis software, BD Biosciences."}],"container-title":["Cells"],"original-title":[],"language":"en","link":[{"URL":"https:\/\/www.mdpi.com\/2073-4409\/1\/3\/409\/pdf","content-type":"unspecified","content-version":"vor","intended-application":"similarity-checking"}],"deposited":{"date-parts":[[2025,10,11]],"date-time":"2025-10-11T21:51:31Z","timestamp":1760219491000},"score":1,"resource":{"primary":{"URL":"https:\/\/www.mdpi.com\/2073-4409\/1\/3\/409"}},"subtitle":[],"short-title":[],"issued":{"date-parts":[[2012,7,30]]},"references-count":43,"journal-issue":{"issue":"3","published-online":{"date-parts":[[2012,9]]}},"alternative-id":["cells1030409"],"URL":"https:\/\/doi.org\/10.3390\/cells1030409","relation":{},"ISSN":["2073-4409"],"issn-type":[{"value":"2073-4409","type":"electronic"}],"subject":[],"published":{"date-parts":[[2012,7,30]]}}}