Immunotherapies and immune biomarkers in Type 1 diabetes: A partnership for success

Clinical Immunology

Volumn 161, Issue 1, 2015, Pages 37-43

  Rekers, Niels V ^a,b   von Herrath, Matthias G ^a   Wesley, Johnna D ^a  

^a NOVO NORDISK INC   (United States)

^b PACIFIC NORTHWEST RESEARCH INSTITUTE   (United States)

Author keywords

Biomarkers; Immunotherapy; Type 1 diabetes

Indexed keywords

AUTOANTIBODY; BIOLOGICAL MARKER; C PEPTIDE; HEMOGLOBIN A1C; PROTEIN;

ARTICLE; AUTOIMMUNITY; CYTOKINE RESPONSE; DIAGNOSTIC VALUE; DISEASE COURSE; ENZYME LINKED IMMUNOSPOT ASSAY; FLOW CYTOMETRY; FLUOROSPOT ASSAY; GENE LOCUS; GENETIC MARKER; GLYCEMIC CONTROL; HEALTH CARE QUALITY; HUMAN; IMMUNE RESPONSE; IMMUNOASSAY; IMMUNOTHERAPY; INSULIN DEPENDENT DIABETES MELLITUS; NONHUMAN; PRIORITY JOURNAL; SAFETY; SYMPTOM; T LYMPHOCYTE; TREATMENT RESPONSE; ANIMAL; DIABETES MELLITUS, TYPE 1; DISEASE MODEL; IMMUNOLOGY; METABOLISM; SENSITIVITY AND SPECIFICITY;

ANIMALS; AUTOANTIBODIES; BIOMARKERS; DIABETES MELLITUS, TYPE 1; DISEASE MODELS, ANIMAL; HUMANS; IMMUNOTHERAPY; SENSITIVITY AND SPECIFICITY; T-LYMPHOCYTES;

EID: 84949530853     PISSN: 15216616     EISSN: 15217035     Source Type: Journal    
DOI: 10.1016/j.clim.2015.05.021     Document Type: Article

References (104)

1. Eisenbarth G.S. Banting Lecture 2009: an unfinished journey: molecular pathogenesis to prevention of type 1A diabetes. Diabetes 2010, 59:759-774.
2. American Diabetes Association (2) Classification and diagnosis of diabetes. Diabetes Care 2015, 38(Suppl.):S8-S16.
3. The Diabetes Control and Complications Trial Research Group The effect of intensive treatment of diabetes on the development and progression of long-term complications in insulin-dependent diabetes mellitus. The Diabetes Control and Complications Trial Research Group. N. Engl. J. Med. 1993, 329:977-986.
4. Harjutsalo V., Sjoberg L., Tuomilehto J. Time trends in the incidence of type 1 diabetes in Finnish children: a cohort study. Lancet 2008, 371:1777-1782.
5. Greiner D.L., Rossini A.A., Mordes J.P. Translating data from animal models into methods for preventing human autoimmune diabetes mellitus: caveat emptor and primum non nocere. Clin. Immunol. 2001, 100:134-143.
6. van Belle T.L., Coppieters K.T., von Herrath M.G. Type 1 diabetes: etiology, immunology, and therapeutic strategies. Physiol. Rev. 2011, 91:79-118.
7. Wang L., Lovejoy N.F., Faustman D.L. Persistence of prolonged C-peptide production in type 1 diabetes as measured with an ultrasensitive C-peptide assay. Diabetes Care 2012, 35:465-470.
8. Akirav E., Kushner J.A., Herold K.C. Beta-cell mass and type 1 diabetes: going, going, gone?. Diabetes 2008, 57:2883-2888.
9. Atkinson M.A., Gianani R. The pancreas in human type 1 diabetes: providing new answers to age-old questions. Curr. Opin. Endocrinol. Diabetes Obes. 2009, 16:279-285.
10. Rowe P.A., Campbell-Thompson M.L., Schatz D.A., Atkinson M.A. The pancreas in human type 1 diabetes. Semin. Immunopathol. 2011, 33:29-43.
11. Atkinson M.A., Eisenbarth G.S., Michels A.W. Type 1 diabetes. Lancet 2014, 383:69-82.
12. Robertson R.P., Davis C., Larsen J., Stratta R., Sutherland D.E. Pancreas and islet transplantation in type 1 diabetes. Diabetes Care 2006, 29:935.
13. Garg S.K., Michels A.W., Shah V.N. Use of non-insulin therapies for type 1 diabetes. Diabetes Technol. Ther. 2013, 15:901-908.
14. Zhao L., Guo H., Chen H., Petersen R.B., Zheng L., Peng A., Huang K. Effect of Liraglutide on endoplasmic reticulum stress in diabetes. Biochem. Biophys. Res. Commun. 2013, 441:133-138.
15. Tao B.T., Taylor D.G. Economics of type 1 diabetes. Endocrinol. Metab. Clin. N. Am. 2010, 39:499-512.
16. Green J., Ariyan C. Update on immunotherapy in melanoma. Surg. Oncol. Clin. N. Am. 2015, 24:337-346.
17. Kundig T.M., Klimek L., Schendzielorz P., Renner W.A., Senti G., Bachmann M.F. Is the allergen really needed in allergy immunotherapy?. Curr. Treat. Options. Allergy 2015, 2:72-82.
18. Shoda L.K., Young D.L., Ramanujan S., Whiting C.C., Atkinson M.A., Bluestone J.A., Eisenbarth G.S., Mathis D., Rossini A.A., Campbell S.E., Kahn R., Kreuwel H.T. A comprehensive review of interventions in the NOD mouse and implications for translation. Immunity 2005, 23:115-126.
19. Bethel M.A., Sourij H. Impact of FDA guidance for developing diabetes drugs on trial design: from policy to practice. Curr. Cardiol. Rep. 2012, 14:59-69.
20. Kachapati K., Adams D., Bednar K., Ridgway W.M. The non-obese diabetic (NOD) mouse as a model of human type 1 diabetes. Methods Mol. Biol. 2012, 933:3-16.
21. Driver J.P., Serreze D.V., Chen Y.G. Mouse models for the study of autoimmune type 1 diabetes: a NOD to similarities and differences to human disease. Semin. Immunopathol. 2011, 33:67-87.
22. Thayer T.C., Wilson S.B., Mathews C.E. Use of nonobese diabetic mice to understand human type 1 diabetes. Endocrinol. Metab. Clin. N. Am. 2010, 39:541-561.
23. Maahs D.M., West N.A., Lawrence J.M., Mayer-Davis E.J. Epidemiology of type 1 diabetes. Endocrinol. Metab. Clin. N. Am. 2010, 39:481-497.
24. Zhang B., Kumar R.B., Dai H., Feldman B.J. A plasmonic chip for biomarker discovery and diagnosis of type 1 diabetes. Nat. Med. 2014, 20:948-953.
25. American Diabetes Association Standards of medical care in diabetes - 2015. Diabetes Care 2015, 38(Suppl. 1).
26. Herold K.C., Gitelman S.E., Ehlers M.R., Gottlieb P.A., Greenbaum C.J., Hagopian W., Boyle K.D., Keyes-Elstein L., Aggarwal S., Phippard D., Sayre P.H., McNamara J., Bluestone J.A. Teplizumab (anti-CD3 mAb) treatment preserves C-peptide responses in patients with new-onset type 1 diabetes in a randomized controlled trial: metabolic and immunologic features at baseline identify a subgroup of responders. Diabetes 2013, 62:3766-3774.
27. Hagopian W., Ferry R.J., Sherry N., Carlin D., Bonvini E., Johnson S., Stein K.E., Koenig S., Daifotis A.G., Herold K.C., Ludvigsson J. Teplizumab preserves C-peptide in recent-onset type 1 diabetes: two-year results from the randomized, placebo-controlled Protege trial. Diabetes 2013, 62:3901-3908.
28. Rigby M.R., Dimeglio L.A., Rendell M.S., Felner E.I., Dostou J.M., Gitelman S.E., Patel C.M., Griffin K.J., Tsalikian E., Gottlieb P.A., Greenbaum C.J., Sherry N.A., Moore W.V., Monzavi R., Willi S.M., Raskin P., Moran A., Russell W.E., Pinckney A., Keyes-Elstein L., Howell M., Aggarwal S., Lim N., Phippard D., Nepom G.T., McNamara J., Ehlers M.R. Targeting of memory T cells with alefacept in new-onset type 1 diabetes (T1DAL study): 12month results of a randomised, double-blind, placebo-controlled phase 2 trial. Lancet Diabetes Endocrinol. 2013, 1:284-294.
29. Orban T., Bundy B., Becker D.J., Dimeglio L.A., Gitelman S.E., Goland R., Gottlieb P.A., Greenbaum C.J., Marks J.B., Monzavi R., Moran A., Peakman M., Raskin P., Russell W.E., Schatz D., Wherrett D.K., Wilson D.M., Krischer J.P., Skyler J.S. Costimulation modulation with abatacept in patients with recent-onset type 1 diabetes: follow-up 1year after cessation of treatment. Diabetes Care 2014, 37:1069-1075.
30. Nowicka P., Santoro N., Liu H., Lartaud D., Shaw M.M., Goldberg R., Guandalini C., Savoye M., Rose P., Caprio S. Utility of hemoglobin A(1c) for diagnosing prediabetes and diabetes in obese children and adolescents. Diabetes Care 2011, 34:1306-1311.
31. Food and Drug Administration Guidance for industry diabetes mellitus: developing drugs and therapeutic biologics for treatment and prevention (Ref Type: Electronic Citation). http://www.fda.gov/downloads/Drugs/Guidances/ucm071624.pdf.
32. Culina S., Brezar V., Mallone R. Insulin and type 1 diabetes: immune connections. Eur. J. Endocrinol. 2013, 168:R19-R31.
33. Greenbaum C.J., Beam C.A., Boulware D., Gitelman S.E., Gottlieb P.A., Herold K.C., Lachin J.M., McGee P., Palmer J.P., Pescovitz M.D., Krause-Steinrauf H., Skyler J.S., Sosenko J.M. Fall in C-peptide during first 2years from diagnosis: evidence of at least two distinct phases from composite Type 1 Diabetes TrialNet data. Diabetes 2012, 61:2066-2073.
34. Ludvigsson J., Carlsson A., Deli A., Forsander G., Ivarsson S.A., Kockum I., Lindblad B., Marcus C., Lernmark A., Samuelsson U. Decline of C-peptide during the first year after diagnosis of Type 1 diabetes in children and adolescents. Diabetes Res. Clin. Pract. 2013, 100:203-209.
35. Barker A., Lauria A., Schloot N., Hosszufalusi N., Ludvigsson J., Mathieu C., Mauricio D., Nordwall M., Van der Schueren B., Mandrup-Poulsen T., Scherbaum W.A., Weets I., Gorus F.K., Wareham N., Leslie R.D., Pozzilli P. Age-dependent decline of beta-cell function in type 1 diabetes after diagnosis: a multi-centre longitudinal study. Diabetes Obes. Metab. 2014, 16:262-267.
36. Onengut-Gumuscu S., Chen W.M., Burren O., Cooper N.J., Quinlan A.R., Mychaleckyj J.C., Farber E., Bonnie J.K., Szpak M., Schofield E., Achuthan P., Guo H., Fortune M.D., Stevens H., Walker N.M., Ward L.D., Kundaje A., Kellis M., Daly M.J., Barrett J.C., Cooper J.D., Deloukas P., Todd J.A., Wallace C., Concannon P., Rich S.S. Fine mapping of type 1 diabetes susceptibility loci and evidence for colocalization of causal variants with lymphoid gene enhancers. Nat. Genet. 2015, 47:381-386.
37. Polychronakos C., Li Q. Understanding type 1 diabetes through genetics: advances and prospects. Nat. Rev. Genet. 2011, 12:781-792.
38. Noble J.A., Valdes A.M., Varney M.D., Carlson J.A., Moonsamy P., Fear A.L., Lane J.A., Lavant E., Rappner R., Louey A., Concannon P., Mychaleckyj J.C., Erlich H.A. HLA class I and genetic susceptibility to type 1 diabetes: results from the Type 1 Diabetes Genetics Consortium. Diabetes 2010, 59:2972-2979.
39. Baschal E.E., Eisenbarth G.S. Extreme genetic risk for type 1A diabetes in the post-genome era. J. Autoimmun. 2008, 31:1-6.
40. Erlich H.A., Valdes A.M., Noble J.A. Prediction of type 1 diabetes. Diabetes 2013, 62:1020-1021.
41. Decochez K., Truyen I., van der Auwera B., Weets I., Vandemeulebroucke E., de Leeuw I.H., Keymeulen B., Mathieu C., Rottiers R., Pipeleers D.G., Gorus F.K. Combined positivity for HLA DQ2/DQ8 and IA-2 antibodies defines population at high risk of developing type 1 diabetes. Diabetologia 2005, 48:687-694.
42. Mbunwe E., Van der Auwera B.J., Weets I., Van Crombrugge P., Crenier L., Coeckelberghs M., Seret N., Decochez K., Vandemeulebroucke E., Gillard P., Keymeulen B., vna Schravendijk C., Wenzlau J.M., Hutton J.C., Pipeleers D.G., Gorus F.K., Belgian Diabetes Registry In antibody-positive first-degree relatives of patients with type 1 diabetes, HLA-A * 24 and HLA-B * 18, but not HLA-B * 39, are predictors of impending diabetes with distinct HLA-DQ interactions. Diabetologia 2013, 56:1964-1970.
43. Erlich H., Valdes A.M., Noble J., Carlson J.A., Varney M., Concannon P., Mychaleckyj J.C., Todd J.A., Bonella P., Fear A.L., Lavant E., Louey A., Moonsamy P. HLA DR-DQ haplotypes and genotypes and type 1 diabetes risk: analysis of the type 1 diabetes genetics consortium families. Diabetes 2008, 57:1084-1092.
44. Nejentsev S., Howson J.M., Walker N.M., Szeszko J., Field S.F., Stevens H.E., Reynolds P., Hardy M., King E., Masters J., Hulme J., Maier L.M., Smyth D., Bailey R., Cooper J.D., Ribas G., Campbell R.D., Clayton D.G., Todd J.A. Localization of type 1 diabetes susceptibility to the MHC class I genes HLA-B and HLA-A. Nature 2007, 450:887-892.
45. Wang C., Krishnakumar S., Wilhelmy J., Babrzadeh F., Stepanyan L., Su L.F., Levinson D., Fernandez-Vina M.A., Davis R.W., Davis M.M., Mindrinos M. High-throughput, high-fidelity HLA genotyping with deep sequencing. Proc. Natl. Acad. Sci. U. S. A. 2012, 109:8676-8681.
46. Ehrenberg P.K., Geretz A., Baldwin K.M., Apps R., Polonis V.R., Robb M.L., Kim J.H., Michael N.L., Thomas R. High-throughput multiplex HLA genotyping by next-generation sequencing using multi-locus individual tagging. BMC Genomics 2014, 15:864.
47. Gorus F.K., Keymeulen B., Veld P.A., Pipeleers D.G. Predictors of progression to Type 1 diabetes: preparing for immune interventions in the preclinical disease phase. Expert. Rev. Clin. Immunol. 2013, 9:1173-1183.
48. Riches A.C., Sharp J.G., Thomas D.B., Smith S.V. Blood volume determination in the mouse. J. Physiol. 1973, 228:279-284.
49. Atkinson M.A. Pancreatic biopsies in type 1 diabetes: revisiting the myth of Pandora's box. Diabetologia 2014, 57:656-659.
50. Amrani A., Verdaguer J., Serra P., Tafuro S., Tan R., Santamaria P. Progression of autoimmune diabetes driven by avidity maturation of a T-cell population. Nature 2000, 406:739-742.
51. Savage P.A., Boniface J.J., Davis M.M. A kinetic basis for T cell receptor repertoire selection during an immune response. Immunity 1999, 10:485-492.
52. Lindsay R.S., Corbin K., Mahne A., Levitt B.E., Gebert M.J., Wigton E.J., Bradley B.J., Haskins K., Jacobelli J., Tang Q., Krummel M.F., Friedman R.S. Antigen recognition in the islets changes with progression of autoimmune islet infiltration. J. Immunol. 2015, 194:522-530.
53. van der Burg S.H., Kalos M., Gouttefangeas C., Janetzki S., Ottensmeier C., Welters M.J., Romero P., Britten C.M., Hoos A. Harmonization of immune biomarker assays for clinical studies. Sci. Transl. Med. 2011, 3. (108ps44).
54. LaGasse J.M., Brantley M.S., Leech N.J., Rowe R.E., Monks S., Palmer J.P., Nepom G.T., McCulloch D.K., Hagopian W.A. Successful prospective prediction of type 1 diabetes in schoolchildren through multiple defined autoantibodies: an 8-year follow-up of the Washington State Diabetes Prediction Study. Diabetes Care 2002, 25:505-511.
55. Palmer J.P., Asplin C.M., Clemons P., Lyen K., Tatpati O., Raghu P.K., Paquette T.L. Insulin antibodies in insulin-dependent diabetics before insulin treatment. Science 1983, 222:1337-1339.
56. Lan M.S., Wasserfall C., Maclaren N.K., Notkins A.L. IA-2, a transmembrane protein of the protein tyrosine phosphatase family, is a major autoantigen in insulin-dependent diabetes mellitus. Proc. Natl. Acad. Sci. U. S. A. 1996, 93:6367-6370.
57. Baekkeskov S., Aanstoot H.J., Christgau S., Reetz A., Solimena M., Cascalho M., Folli F., Richter-Olesen H., De C.P. Identification of the 64K autoantigen in insulin-dependent diabetes as the GABA-synthesizing enzyme glutamic acid decarboxylase. Nature 1990, 347:151-156.
58. Kaufman D.L., Erlander M.G., Clare-Salzler M., Atkinson M.A., Maclaren N.K., Tobin A.J. Autoimmunity to two forms of glutamate decarboxylase in insulin-dependent diabetes mellitus. J. Clin. Invest. 1992, 89:283-292.
59. Hagopian W.A., Michelsen B., Karlsen A.E., Larsen F., Moody A., Grubin C.E., Rowe R., Petersen J., McEvoy R., Lernmark A. Autoantibodies in IDDM primarily recognize the 65,000-M(r) rather than the 67,000-M(r) isoform of glutamic acid decarboxylase. Diabetes 1993, 42:631-636.
60. Wenzlau J.M., Juhl K., Yu L., Moua O., Sarkar S.A., Gottlieb P., Rewers M., Eisenbarth G.S., Jensen J., Davidson H.W., Hutton J.C. The cation efflux transporter ZnT8 (Slc30A8) is a major autoantigen in human type 1 diabetes. Proc. Natl. Acad. Sci. U. S. A. 2007, 104:17040-17045.
61. Bingley P.J., Bonifacio E., Mueller P.W. Diabetes Antibody Standardization Program: first assay proficiency evaluation. Diabetes 2003, 52:1128-1136.
62. Lampasona V., Schlosser M., Mueller P.W., Williams A.J., Wenzlau J.M., Hutton J.C., Achenbach P. Diabetes antibody standardization program: first proficiency evaluation of assays for autoantibodies to zinc transporter 8. Clin. Chem. 2011, 57:1693-1702.
63. Miao D., Steck A.K., Zhang L., Guyer K.M., Jiang L., Armstrong T., Muller S.M., Krischer J., Rewers M., Yu L. Electrochemiluminescence assays for insulin and glutamic acid decarboxylase autoantibodies improve prediction of type 1 diabetes risk. Diabetes Technol. Ther. 2015, 17:119-127.
64. Pihoker C., Gilliam L.K., Hampe C.S., Lernmark A. Autoantibodies in diabetes. Diabetes 2005, 54(Suppl. 2):S52-S61.
65. Hawa M.I., Fava D., Medici F., Deng Y.J., Notkins A.L., De M.G., Leslie R.D. Antibodies to IA-2 and GAD65 in type 1 and type 2 diabetes: isotype restriction and polyclonality. Diabetes Care 2000, 23:228-233.
66. Fuchtenbusch M., Kredel K., Bonifacio E., Schnell O., Ziegler A.G. Exposure to exogenous insulin promotes IgG1 and the T-helper 2-associated IgG4 responses to insulin but not to other islet autoantigens. Diabetes 2000, 49:918-925.
67. Hoppu S., Ronkainen M.S., Kimpimaki T., Simell S., Korhonen S., Ilonen J., Simell O., Knip M. Insulin autoantibody isotypes during the prediabetic process in young children with increased genetic risk of type 1 diabetes. Pediatr. Res. 2004, 55:236-242.
68. Chattopadhyay P.K., Melenhorst J.J., Ladell K., Gostick E., Scheinberg P., Barrett A.J., Wooldridge L., Roederer M., Sewell A.K., Price D.A. Techniques to improve the direct ex vivo detection of low frequency antigen-specific CD8+ T cells with peptide-major histocompatibility complex class I tetramers. Cytometry A 2008, 73:1001-1009.
69. Nepom G.T. MHC class II tetramers. J. Immunol. 2012, 188:2477-2482.
70. Hadrup S.R., Maurer D., Laske K., Frosig T.M., Andersen S.R., Britten C.M., van der Burg S.H., Walter S., Gouttefangeas C. Cryopreservation of MHC multimers: recommendations for quality assurance in detection of antigen specific T cells. Cytometry A 2015, 87:37-48.
71. Rountree W., Vandergrift N., Bainbridge J., Sanchez A.M., Denny T.N. Statistical methods for the assessment of EQAPOL proficiency testing: ELISpot, Luminex, and Flow Cytometry. J. Immunol. Methods 2014, 409:72-81.
72. Slota M., Lim J.B., Dang Y., Disis M.L. ELISpot for measuring human immune responses to vaccines. Expert Rev. Vaccines 2011, 10:299-306.
73. Alix-Panabieres C. EPISPOT assay: detection of viable DTCs/CTCs in solid tumor patients. Recent Results Cancer Res. 2012, 195:69-76.
74. Velthuis J.H., Unger W.W., Abreu J.R., Duinkerken G., Franken K., Peakman M., Bakker A.H., Reker-Hadrup S., Keymeulen B., Drijfhout J.W., Schumacher T.N., Roep B.O. Simultaneous detection of circulating autoreactive CD8+ T-cells specific for different islet cell-associated epitopes using combinatorial MHC multimers. Diabetes 2010, 59:1721-1730.
75. Pinkse G.G., Tysma O.H., Bergen C.A., Kester M.G., Ossendorp F., van Veelen P.A., Keymeulen B., Pipeleers D., Drijfhout J.W., Roep B.O. Autoreactive CD8 T cells associated with beta cell destruction in type 1 diabetes. Proc. Natl. Acad. Sci. U. S. A. 2005, 102:18425-18430.
76. Coppieters K.T., Dotta F., Amirian N., Campbell P.D., Kay T.W., Atkinson M.A., Roep B.O., von Herrath M.G. Demonstration of islet-autoreactive CD8 T cells in insulitic lesions from recent onset and long-term type 1 diabetes patients. J. Exp. Med. 2012, 209:51-60.
77. Rahier J., Guiot Y., Goebbels R.M., Sempoux C., Henquin J.C. Pancreatic beta-cell mass in European subjects with type 2 diabetes. Diabetes Obes. Metab. 2008, 10(Suppl. 4):32-42.
78. Saisho Y., Butler A.E., Meier J.J., Monchamp T., Allen-Auerbach M., Rizza R.A., Butler P.C. Pancreas volumes in humans from birth to age one hundred taking into account sex, obesity, and presence of type-2 diabetes. Clin. Anat. 2007, 20:933-942.
79. Pietropaolo M., Barinas-Mitchell E., Pietropaolo S.L., Kuller L.H., Trucco M. Evidence of islet cell autoimmunity in elderly patients with type 2 diabetes. Diabetes 2000, 49:32-38.
80. Sarikonda G., Pettus J., Phatak S., Sachithanantham S., Miller J.F., Wesley J.D., Cadag E., Chae J., Ganesan L., Mallios R., Edelman S., Peters B., von Herrath M. CD8 T-cell reactivity to islet antigens is unique to type 1 while CD4 T-cell reactivity exists in both type 1 and type 2 diabetes. J. Autoimmun. 2014, 50:77-82.
81. Altman J.D., Moss P.A., Goulder P.J., Barouch D.H., McHeyzer-Williams M.G., Bell J.I., McMichael A.J., Davis M.M. Phenotypic analysis of antigen-specific T lymphocytes. Science 1996, 274:94-96.
82. Novak E.J., Liu A.W., Nepom G.T., Kwok W.W. MHC class II tetramers identify peptide-specific human CD4(+) T cells proliferating in response to influenza A antigen. J. Clin. Invest. 1999, 104:R63-R67.
83. Hunsucker S.A., McGary C.S., Vincent B.G., Enyenihi A.A., Waugh J.P., McKinnon K.P., Bixby L.M., Ropp P.A., Coghill J.M., Wood W.A., Gabriel D.A., Sarantopoulos S., Shea T.C., Serody J.S., Alatrash G., Rodriguez-Cruz T., Lizee G., Buntzman A.S., Frelinger J.A., Glish G.L., Armistead P.M. Peptide/MHC tetramer-based sorting of CD8+ T cells to a leukemia antigen yields clonotypes drawn nonspecifically from an underlying restricted repertoire. Cancer Immunol. Res. 2015, 3:228-235.
84. Christophersen A., Raki M., Bergseng E., Lundin K.E., Jahnsen J., Sollid L.M., Qiao S.W. Tetramer-visualized gluten-specific CD4+ T cells in blood as a potential diagnostic marker for coeliac disease without oral gluten challenge. United Eur. Gastroenterol. J. 2014, 2:268-278.
85. Angin M., King M., Altfeld M., Walker B.D., Wucherpfennig K.W., Addo M.M. Identification of HIV-1-specific regulatory T-cells using HLA class II tetramers. AIDS 2012, 26:2112-2115.
86. Lissina A., Ladell K., Skowera A., Clement M., Edwards E., Seggewiss R., van den Berg H.A., Gostick E., Gallagher K., Jones E., Melenhorst J.J., Godkin A.J., Peakman M., Price D.A., Sewell A.K., Wooldridge L. Protein kinase inhibitors substantially improve the physical detection of T-cells with peptide-MHC tetramers. J. Immunol. Methods 2009, 340:11-24.
87. Roederer M., Tarnok A. OMIPs - orchestrating multiplexity in polychromatic science. Cytometry A 2010, 77:811-812.
88. Janetzki S., Hoos A., Melief C.J., Odunsi K., Romero P., Britten C.M. Structured reporting of T cell assay results. Cancer Immun. 2013, 13:13.
89. Meierhoff G., Ott P.A., Lehmann P.V., Schloot N.C. Cytokine detection by ELISPOT: relevance for immunological studies in type 1 diabetes. Diabetes Metab. Res. Rev. 2002, 18:367-380.
90. Smith J.G., Liu X., Kaufhold R.M., Clair J., Caulfield M.J. Development and validation of a gamma interferon ELISPOT assay for quantitation of cellular immune responses to varicella-zoster virus. Clin. Diagn. Lab. Immunol. 2001, 8:871-879.
91. Arif S., Moore F., Marks K., Bouckenooghe T., Dayan C.M., Planas R., Vives-Pi M., Powrie J., Tree T., Marchetti P., Huang G.C., Gurzov E.N., Pujol-Borrell R., Eizirik D.L., Peakman M. Peripheral and islet interleukin-17 pathway activation characterizes human autoimmune diabetes and promotes cytokine-mediated beta-cell death. Diabetes 2011, 60:2112-2119.
92. Alleva D.G., Crowe P.D., Jin L., Kwok W.W., Ling N., Gottschalk M., Conlon P.J., Gottlieb P.A., Putnam A.L., Gaur A. A disease-associated cellular immune response in type 1 diabetics to an immunodominant epitope of insulin. J. Clin. Invest. 2001, 107:173-180.
93. Arif S., Tree T.I., Astill T.P., Tremble J.M., Bishop A.J., Dayan C.M., Roep B.O., Peakman M. Autoreactive T cell responses show proinflammatory polarization in diabetes but a regulatory phenotype in health. J. Clin. Invest. 2004, 113:451-463.
94. Raz I., Elias D., Avron A., Tamir M., Metzger M., Cohen I.R. Beta-cell function in new-onset type 1 diabetes and immunomodulation with a heat-shock protein peptide (DiaPep277): a randomised, double-blind, phase II trial. Lancet 2001, 358:1749-1753.
95. Lebastchi J., Herold K.C. Immunologic and metabolic biomarkers of beta-cell destruction in the diagnosis of type 1 diabetes. Cold Spring Harb. Perspect. Med. 2012, 2:a007708.
96. Zhang W., Caspell R., Karulin A.Y., Ahmad M., Haicheur N., Abdelsalam A., Johannesen K., Vignard V., Dudzik P., Georgakopoulou K., Mihaylova A., Silina K., Aptsiauri N., Adams V., Lehmann P.V., McArdle S. ELISPOT assays provide reproducible results among different laboratories for T-cell immune monitoring - even in hands of ELISPOT-inexperienced investigators. J. Immunotoxicol. 2009, 6:227-234.
97. Labikova J., Vcelakova J., Ulmannova T., Petruzelkova L., Kolouskova S., Stechova K. The cytokine production of peripheral blood mononuclear cells reflects the autoantibody profile of patients suffering from type 1 diabetes. Cytokine 2014, 69:189-195.
98. Kreher C.R., Dittrich M.T., Guerkov R., Boehm B.O., Tary-Lehmann M. CD4+ and CD8+ cells in cryopreserved human PBMC maintain full functionality in cytokine ELISPOT assays. J. Immunol. Methods 2003, 278:79-93.
99. Schloot N.C., Meierhoff G., Karlsson F.M., Ott P., Putnam A., Lehmann P., Gottlieb P., Roep B.O., Peakman M., Tree T. 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. J. Autoimmun. 2003, 21:365-376.
100. Nagata M., Kotani R., Moriyama H., Yokono K., Roep B.O., Peakman M. Detection of autoreactive T cells in type 1 diabetes using coded autoantigens and an immunoglobulin-free cytokine ELISPOT assay: report from the fourth immunology of diabetes society T cell workshop. Ann. N. Y. Acad. Sci. 2004, 1037:10-15.
101. Okamoto Y., Abe T., Niwa T., Mizuhashi S., Nishida M. Development of a dual color enzyme-linked immunospot assay for simultaneous detection of murine T helper type 1- and T helper type 2-cells. Immunopharmacology 1998, 39:107-116.
102. Boulet S., Ndongala M.L., Peretz Y., Boisvert M.P., Boulassel M.R., Tremblay C., Routy J.P., Sekaly R.P., Bernard N.F. A dual color ELISPOT method for the simultaneous detection of IL-2 and IFN-gamma HIV-specific immune responses. J. Immunol. Methods 2007, 320:18-29.
103. Janetzki S., Rueger M., Dillenbeck T. Stepping up ELISpot: multi-level analysis in FluoroSpot assays. Cells 2014, 3:1102-1115.
104. Dillenbeck T., Gelius E., Fohlstedt J., Ahlborg N. Triple cytokine FluoroSpot analysis of human antigen-specific IFN-gamma, IL-17A and IL-22 responses. Cells 2014, 3:1116-1130.