ELISpot for measuring human immune responses to vaccines

Expert Review of Vaccines

Volumn 10, Issue 3, 2011, Pages 299-306

  Slota, Meredith ^a   Lim, Jong Baeck ^a   Dang, Yushe ^a   Disis, Mary L ^a  

^a UNIVERSITY OF WASHINGTON   (United States)

Author keywords

clinical trials; ELISpot; immune biomarker; quantitative; standardize

Indexed keywords

BCG VACCINE; CANCER VACCINE; CHEMOKINE; EPIDERMAL GROWTH FACTOR RECEPTOR 2; GAMMA INTERFERON; GRANZYME B; HUMAN IMMUNODEFICIENCY VIRUS VACCINE; INTERLEUKIN 10; INTERLEUKIN 12; INTERLEUKIN 17; INTERLEUKIN 1BETA; INTERLEUKIN 2; INTERLEUKIN 4; INTERLEUKIN 6; INTERLEUKIN 8; MALARIA VACCINE; MELANOMA ANTIGEN; PEPTIDE VACCINE; PROSTATE SPECIFIC ANTIGEN; TRANSFORMING GROWTH FACTOR BETA1; TUMOR NECROSIS FACTOR ALPHA;

ACQUIRED IMMUNE DEFICIENCY SYNDROME; ANTIBODY RESPONSE; ANTIGEN PRESENTING CELL; ANTIGEN SPECIFICITY; BREAST CANCER; CD4+ T LYMPHOCYTE; CD8+ T LYMPHOCYTE; CLINICAL TRIAL (TOPIC); CYTOKINE PRODUCTION; CYTOKINE RELEASE; CYTOTOXICITY; ENZYME LINKED IMMUNOSORBENT ASSAY; ENZYME LINKED IMMUNOSPOT ASSAY; FLUORESCENCE ANALYSIS; HUMAN; IMMUNE RESPONSE; IMMUNOLOGICAL MONITORING; MALARIA; MELANOMA; NATURAL KILLER CELL; PRIORITY JOURNAL; PROSTATE CANCER; REVIEW; T LYMPHOCYTE; TUBERCULOSIS; VACCINATION; VALIDATION STUDY;

ANTIGENS; CANCER VACCINES; CLINICAL TRIALS AS TOPIC; ENZYME-LINKED IMMUNOSPOT ASSAY; GRANZYMES; HUMANS; INTERFERON-GAMMA; T-LYMPHOCYTES; VACCINES;

EID: 79953238598     PISSN: 14760584     EISSN: 17448395     Source Type: Journal    
DOI: 10.1586/erv.10.169     Document Type: Review

References (57)

1. Czerkinsky CC, Nilsson LA, Nygren H, Ouchterlony O, Tarkowski A. A solid-phase enzyme-linked immunospot (ELISpot) assay for enumeration of specific antibody-secreting cells. J. Immunol. Methods 65(1-2), 109-121 (1983). Original paper describing enzyme-linked immunosorbent spot (ELISpot).
2. Jerne NK, Nordin AA. Plaque formation in agar by single antibody-producing cells. Science 140(3565), 405 (1963).
3. Gronowicz E, Coutinho A, Melchers F. A plaque assay for all cells secreting Ig of a given type or class. Eur. J. Immunol. 6(8), 588-590 (1976).
4. Czerkinsky C, Prince SJ, Michalek SM et al. Oral immunization with bacterial antigen induces IgA-secreting cells in peripheral blood in humans. Adv. Exp. Med. Biol. 216B, 1709-1719 (1987).
5. Czerkinsky CC, Tarkowski A, Nilsson LA et al. Reverse enzyme-linked immunospot assay (RELISpot) for the detection of cells secreting immunoreactive substances. J. Immunol. Methods 72(2), 489-496 (1984).
6. Taguchi T, McGhee JR, Coffman RL et al. Detection of individual mouse splenic T cells producing IFN-γ and IL-5 using the enzyme-linked immunospot (ELISpot) assay. J. Immunol. Methods 128(1), 65-73 (1990).
7. + T cells using an ELISpot assay. J. Immunol. Methods 181(1), 45-54 (1995).
8. + memory T cells. J. Exp. Med. 186(6), 859-865 (1997).
9. + T lymphocytes responsive to human immunodeficiency virus (HIV) peptide antigens in HIV-infected patients and seronegative persons at high risk for recent HIV exposure. J. Infect. Dis. 178(1), 260-265 (1998).
10. Letsch A, Scheibenbogen C. Quantification and characterization of specific T-cells by antigen-specific cytokine production using ELISpot assay or intracellular cytokine staining. Methods 31(2), 143-149 (2003).
11. Schmittel A, Keilholz U, Scheibenbogen C. Evaluation of the interferon-γ ELISpot-assay for quantification of peptide specific T lymphocytes from peripheral blood. J. Immunol. Methods 210(2), 167-174 (1997).
12. + T lymphocytes. Hum. Immunol. 65(11), 1307-1318 (2004).
13. Hill PC, Brookes RH, Fox A et al. Longitudinal assessment of an ELISpot test for Mycobacterium tuberculosis infection. PLoS Med. 4(6), e192 (2007).
14. Kester KE, Cummings JF, Ockenhouse CF et al. Phase 2a trial of 0, 1, and 3 month and 0, 7, and 28 day immunization schedules of malaria vaccine RTS,S/AS02 in malaria-naive adults at the Walter Reed Army Institute of Research. Vaccine 26(18), 2191-2202 (2008).
15. Lambotte O, Ferrari G, Moog C et al. Heterogeneous neutralizing antibody and antibody-dependent cell cytotoxicity responses in HIV-1 elite controllers. AIDS 23(8), 897-906 (2009).
16. Gray CM, Mlotshwa M, Riou C et al. Human immunodeficiency virus-specific γ interferon enzyme-linked immunospot assay responses targeting specific regions of the proteome during primary subtype C infection are poor predictors of the course of viremia and set point. J. Virol. 83(1), 470-478 (2009).
17. Calarota SA, Foli A, Maserati R et al. HIV-1-specific T cell precursors with high proliferative capacity correlate with low viremia and high CD4 counts in untreated individuals. J. Immunol. 180(9), 5907-5915 (2008).
18. Kenter GG, Welters MJ, Valentijn AR et al. Vaccination against HPV-16 oncoproteins for vulvar intraepithelial neoplasia. N. Engl. J. Med. 361(19), 1838-1847 (2009).
19. Kirkwood JM, Lee S, Moschos SJ et al. Immunogenicity and antitumor effects of vaccination with peptide vaccine+/- granulocyte-monocyte colony-stimulating factor and/or IFN-α2b in advanced metastatic melanoma: Eastern Cooperative Oncology Group Phase II Trial E1696. Clin. Cancer Res. 15(4), 1443-1451 (2009).
20. Gulley JL, Arlen PM, Madan RA et al. Immunologic and prognostic factors associated with overall survival employing a poxviral-based PSA vaccine in metastatic castrate-resistant prostate cancer. Cancer Immunol. Immunother. 59(5), 663-674 (2010).
21. Disis ML, Wallace DR, Gooley TA et al. Concurrent trastuzumab and HER2/neu-specific vaccination in patients with metastatic breast cancer. J. Clin. Oncol. 27(28), 4685-4692 (2009).
22. 51Cr-release assay for monitoring cell-mediated cytotoxicity. J. Transl. Med. 1(1), 14 (2003).
23. Trinchieri G, Perussia B. Human natural killer cells: biologic and pathologic aspects. Lab. Invest. 50(5), 489-513 (1984).
24. Smyth MJ, Trapani JA. Granzymes: exogenous proteinases that induce target cell apoptosis. Immunol. Today 16(4), 202-206 (1995).
25. Finn OJ, Lotze MT. A decade in the life of tumor immunology. Clin. Cancer Res. 7(Suppl. 3), 759S-760S (2001).
26. Bleackley RC, Lobe CG, Duggan B et al. The isolation and characterization of a family of serine protease genes expressed in activated cytotoxic T lymphocytes. Immunol. Rev. 103, 5-19 (1988).
27. Doherty PC, Christensen JP. Accessing complexity: the dynamics of virus-specific T cell responses. Annu. Rev. Immunol. 18, 561-592 (2000).
28. Russell JH, Ley TJ. Lymphocyte-mediated cytotoxicity. Annu. Rev. Immunol. 20, 323-370 (2002).
29. Assoian RK, Fleurdelys BE, Stevenson HC et al. Expression and secretion of type β transforming growth factor by activated human macrophages. Proc. Natl Acad. Sci. USA 84(17), 6020-6024 (1987).
30. Aung H, Sherman J, Tary-Lehman M, Toossi Z. Analysis of transforming growth factor-beta 1 (TGF-β1) expression in human monocytes infected with Mycobacterium avium at a single cell level by ELISpot assay. J. Immunol. Methods 259(1-2), 25-32 (2002).
31. Kabilan L, Andersson G, Lolli F et al. Detection of intracellular expression and secretion of interferon-γ at the single-cell level after activation of human T cells with tetanus toxoid in vitro. Eur. J. Immunol. 20(5), 1085-1089 (1990).
32. Hagiwara E, Abbasi F, Mor G, Ishigatsubo Y, Klinman DM. Phenotype and frequency of cells secreting IL-2, IL-4, IL-6, IL-10, IFN and TNF-α in human peripheral blood. Cytokine 7(8), 815-822 (1995).
33. Gazagne A, Claret E, Wijdenes J et al. A fluorospot assay to detect single T lymphocytes simultaneously producing multiple cytokines. J. Immunol. Methods 283(1-2), 91-98 (2003).
34. Kalogerakou F, Albanidou-Farmaki E, Markopoulos AK, Antoniades DZ. Detection of T cells secreting type 1 and type 2 cytokines in the peripheral blood of patients with oral lichen planus. Hippokratia 12(4), 230-235 (2008).
35. Smedman C, Gardlund B, Nihlmark K et al. ELISpot analysis of LPS-stimulated leukocytes: human granulocytes selectively secrete IL-8, MIP-1β and TNF-α. J. Immunol. Methods 346(1-2), 1-8 (2009).
36. Zheng X, de Paiva CS, Li DQ, Farley WJ, Pflugfelder SC. Desiccating stress promotion of Th17 differentiation by ocular surface tissues through a dendritic cell-mediated pathway. Invest. Ophthalmol. Vis. Sci. 51(6), 3083-3091 (2010).
37. Samaras V, Piperi C, Levidou G et al. Analysis of interleukin (IL)-8 expression in human astrocytomas: associations with IL-6, cyclooxygenase-2, vascular endothelial growth factor, and microvessel morphometry. Hum. Immunol. 70(6), 391-397 (2009).
38. Boulet S, Ndongala ML, Peretz Y et al. A dual color ELISpot method for the simultaneous detection of IL-2 and IFN-γ HIV-specific immune responses. J. Immunol. Methods 320(1-2), 18-29 (2007). Excellent methods covering the development of dual-color ELISpot.
39. + HIV-1-specific polyfunctional responses in patients with chronic HIV-1 infection receiving antiretroviral therapy. Vaccine 26(22), 2738-2745 (2008).
40. Darrah PA, Patel DT, De Luca PM et al. Multifunctional TH1 cells define a correlate of vaccine-mediated protection against Leishmania major. Nat. Med. 13(7), 843-850 (2007).
41. Weinberg A, Zhang L, Brown D et al. Viability and functional activity of cryopreserved mononuclear cells. Clin. Diagn. Lab. Immunol. 7(4), 714-716 (2000).
42. Disis ML, dela Rosa C, Goodell V et al. Maximizing the retention of antigen specific lymphocyte function after cryopreservation. J. Immunol. Methods 308(1-2), 13-18 (2006). Validated cryopreservation protocol for lymphocytes.
43. Mander A, Gouttefangeas C, Ottensmeier C et al. Serum is not required for ex vivo IFN-γ ELISpot: a collaborative study of different protocols from the European CIMT Immunoguiding Program. Cancer Immunol. Immunother. 59(4), 619-627 (2010). Protocol for the use of nonserum-containing media for ELISpot.
44. Janetzki S, Price L, Britten CM et al. Performance of serum-supplemented and serum-free media in IFNγ ELISpot assays for human T cells. Cancer Immunol. Immunother. 59(4), 609-618 (2010).
45. Maecker HT, Moon J, Bhatia S et al. Impact of cryopreservation on tetramer, cytokine flow cytometry, and ELISpot. BMC Immunol. 6, 17 (2005).
46. Maecker HT, Hassler J, Payne JK et al. Precision and linearity targets for validation of an IFNγ ELISpot, cytokine flow cytometry, and tetramer assay using CMV peptides. BMC Immunol. 9, 9 (2008). Comparison of the perfomance of ELISpot, tetramer and flow cytometry for detecting antigen-specific responses.
47. Zhang W, Caspell R, Karulin AY et al. ELISpot assays provide reproducible results among different laboratories for T-cell immune monitoring - even in hands of ELISpot-inexperienced investigators. J. Immunotoxicol. 6(4), 227-234 (2009).
48. Boaz MJ, Hayes P, Tarragona T et al. Concordant proficiency in measurement of T-cell immunity in human immunodeficiency virus vaccine clinical trials by peripheral blood mononuclear cell and enzyme-linked immunospot assays in laboratories from three continents. Clin. Vaccine Immunol. 16(2), 147-155 (2009).
49. Samri A, Durier C, Urrutia A et al. Evaluation of the interlaboratory concordance in quantification of human immunodeficiency virus-specific T cells with a γ interferon enzyme-linked immunospot assay. Clin. Vaccine Immunol. 13(6), 684-697 (2006).
50. Janetzki S, Panageas KS, Ben-Porat L et al. Results and harmonization guidelines from two large-scale international ELISpot proficiency panels conducted by the Cancer Vaccine Consortium (CVC/SVI). Cancer Immunol. Immunother. 57(3), 303-315 (2008). Assessment of the performance of ELISpot across multiple institutions.
51. Janetzki S, Cox JH, Oden N, Ferrari G. Standardization and validation issues of the ELISpot assay. Methods Mol. Biol. 302, 51-86 (2005).
52. Weinberg A, Song LY, Wilkening CL et al. Optimization of storage and shipment of cryopreserved peripheral blood mononuclear cells from HIV-infected and uninfected individuals for ELISpot assays. J. Immunol. Methods 363(1), 42-50 (2010).
53. Kalyuzhny A, Stark S. A simple method to reduce the background and improve well-to-well reproducibility of staining in ELISpot assays. J. Immunol. Methods 257(1-2), 93-97 (2001).
54. Moodie Z, Price L, Gouttefangeas C et al. Response definition criteria for ELISpot assays revisited. Cancer Immunol. Immunother. 59(10), 1489-1501 (2010). Thoughtful analysis on defining positive responses by ELISpot.
55. Dubey S, Clair J, Fu TM et al. Detection of HIV vaccine-induced cell-mediated immunity in HIV-seronegative clinical trial participants using an optimized and validated enzyme-linked immunospot assay. J. Acquir. Immune Defic. Syndr. 45(1), 20-27 (2007).
56. Pagano M, Gauvreau K. Principles of Biostatistics 2nd Edition. Duxbury Press, Pacific Grove, CA, USA (2000).
57. Hanekom WA, Dockrell HM, Ottenhoff TH et al. Immunological outcomes of new tuberculosis vaccine trials: WHO panel recommendations. PLoS Med. 5(7), e145 (2008).