Neuroantigen-specific CD4 cells expressing interferon-γ (IFN-γ), Interleukin (IL)-2 and IL-3 in a mutually exclusive manner prevail in experimental allergic encephalomyelitis (EAE)

Cells

Volumn 1, Issue 3, 2012, Pages 576-596

  Karulin, Alexey Y ^a   Quast, Stefan ^b   Hesse, Maike D ^b   Lehmann, Paul V ^a  

^a Cellular Technology Ltd   (United States)

^b FORSCHUNGSZENTRUM JÜLICH   (Germany)

Author keywords

Cytokine co expression; Dual color ELISPOT Memory T cells; EAE MS; Neuroimmunology; Polyfunctional T cells; Th1 cells; Two color ELISPOT

Indexed keywords

CYTOKINE; GAMMA INTERFERON; INTERLEUKIN 2; INTERLEUKIN 3; MYELIN BASIC PROTEIN; PROTEOLIPID PROTEIN;

ALLERGIC ENCEPHALOMYELITIS; ANIMAL CELL; ANIMAL TISSUE; ANTIGEN EXPRESSION; ANTIGEN PRESENTING CELL; ARTICLE; BINDING AFFINITY; BYSTANDER EFFECT; CD4+ T LYMPHOCYTE; CELL MIGRATION; CONTROLLED STUDY; ENZYME LINKED IMMUNOSPOT ASSAY; FEMALE; IMMUNIZATION; MOUSE; NONHUMAN; PROTEIN EXPRESSION;

EID: 85011532094     PISSN: None     EISSN: 20734409     Source Type: Journal    
DOI: 10.3390/cells1030576     Document Type: Article

References (58)

1. Murphy, K.; Ouyang, W.; Farrar, J.; Yang, J.; Ranganath, S.; Asnagli, H.; Afkarian, M.; Murphy, T. Signaling and transcription in T helper development. Annu. Rev. Immunol. 2000, 18, 451-494.
2. Han, Q.; Bagheri, N.; Bradshaw, E.; Hafler, D.; Lauffenburger, D.; Love, J. Polyfunctional responses by human T cells result from sequential release of cytokines. Proc. Natl. Acad. Sci. USA 2012, 109, 1607-1612.
3. Kryczek, I.; Banerjee, M.; Cheng, P.; Vatan, L.; Szeliga, W.; Wei, S.; Huang, E.; Finlayson, E.; Simeone, D.; Welling, T.; et al. Phenotype, distribution, generation, and functional and clinical relevance of Th17 cells in the human tumor environments. Blood 2009, 114, 1141-1149.
4. Bucy, R.; Karr, L.; Huang, G.; Li, J.; Carter, D.; Honjo, K.; Lemons, J.; Murphy, K.; Weaver, C. Single cell analysis of cytokine gene coexpression during CD4+ T-cell phenotype development. Proc. Natl. Acad. Sci. USA 1995, 92, 7565-7569.
5. Saparov, A.; Elson, C.; Devore-Carter, D.; Bucy, R.; Weaver, C. Single-cell analyses of CD4+ T cells from alpha beta T cell receptor-transgenic mice: A distinct mucosal cytokine phenotype in the absence of transgene-specific antigen. Eur. J. Immunol. 1997, 27, 1774-1781.
6. Karulin, A.; Hesse, M.; Tary-Lehmann, M.; Lehmann, P. Single-cytokine-producing CD4 memory cells predominate in type 1 and type 2 immunity. J. Immunol. 2000, 164, 1862-1872.
7. Veiga-Fernandes, H.; Walter, U.; Bourgeois, A.; McLean, A.; Rocha, B. Response of naive and memory CD8+ T cells to antigen stimulation in vivo. Nat. Immunol. 2000, 1, 47-53.
8. Effros, R.; Pawelec, G. Replicative senescence of T cells: Does the Hayflick Limit lead to immune exhaustion? Immunol. Today 1997, 18, 450-454.
9. Bradl, M.; Schmid, M.; Wekerle, H. Clonotypic chromosomal aberrations in long-term lines of myelin-specific rat T lymphocytes. J. Neuroimmunol. 1989, 24, 95-104.
10. Betts, M.; Nason, M.; West, S.; de Rosa, S.; Migueles, S.; Abraham, J.; Lederman, M.; Benito, J.; Goepfert, P.; Connors, M.; et al. HIV nonprogressors preferentially maintain highly functional HIV-specific CD8+ T cells. Blood 2006, 107, 4781-4789.
11. Duvall, M.; Precopio, M.; Ambrozak, D.; Jaye, A.; McMichael, A.; Whittle, H.; Roederer, M.; Rowland-Jones, S.; Koup, R. Polyfunctional T cell responses are a hallmark of HIV-2 infection. Eur. J. Immunol. 2008, 38, 350-363.
12. Krol, L.; Stuchly, J.; Hubacek, P.; Keslova, P.; Sedlacek, P.; Stary, J.; Hrusak, O.; Kalina, T. Signature profiles of CMV-specific T-cells in patients with CMV reactivation after hematopoietic SCT. Bone Marrow Transplant. 2011, 46, 1089-1098.
13. Lachmann, R.; Bajwa, M.; Vita, S.; Smith, H.; Cheek, E.; Akbar, A.; Kern, F. Polyfunctional T cells accumulate in large human cytomegalovirus-specific T cell responses. J. Virol. 2012, 86, 1001-1009.
14. Caccamo, N.; Guggino, G.; Joosten, S.; Gelsomino, G.; di Carlo, P.; Titone, L.; Galati, D.; Bocchino, M.; Matarese, A.; Salerno, A.; et al. Multifunctional CD4(+) T cells correlate with active Mycobacterium tuberculosis infection. Eur. J. Immunol. 2010, 40, 2211-2220.
15. El Fenniri, L.; Toossi, Z.; Aung, H.; El Iraki, G.; Bourkkadi, J.; Benamor, J.; Laskri, A.; Berrada, N.; Benjouad, A.; Mayanja-Kizza, H.; et al. Polyfunctional Mycobacterium tuberculosis-specific effector memory CD4+ T cells at sites of pleural TB. Tuberculosis (Edinb) 2011, 91, 224-230.
16. Wilkinson, K.; Wilkinson, R. Polyfunctional T cells in human tuberculosis. Eur. J. Immunol. 2010, 40, 2139-2142.
17. Hilchey, S.; Rosenberg, A.; Hyrien, O.; Secor-Socha, S.; Cochran, M.; Brady, M.; Wang, J.; Sanz, I.; Burack, W.; Quataert, S.; et al. Follicular lymphoma tumor-infiltrating T-helper (T(H) cells have the same polyfunctional potential as normal nodal T(H) cells despite skewed differentiation. Blood 2011, 118, 3591-3602.
18. Darrah, P.; Patel, D.; de Luca, P.; Lindsay, R.; Davey, D.; Flynn, B.; Hoff, S.; Andersen, P.; Reed, S.; Morris, S.; et al. Multifunctional TH1 cells define a correlate of vaccine-mediated protection against Leishmania major. Nat. Med. 2007, 13, 843-850.
19. Gomez, C.; Najera, J.; Perdiguero, B.; Garcia-Arriaza, J.; Sorzano, C.; Jimenez, V.; Gonzalez-Sanz, R.; Jimenez, J.; Munoz-Fernandez, M.; Lopez Bernaldo de Quiros, J.C.; et al. The HIV/AIDS vaccine candidate MVA-B administered as a single immunogen in humans triggers robust, polyfunctional, and selective effector memory T cell responses to HIV-1 antigens. J. Virol. 2011, 85, 11468-11478.
20. Lindenstrom, T.; Agger, E.; Korsholm, K.; Darrah, P.; Aagaard, C.; Seder, R.; Rosenkrands, I.; Andersen, P. Tuberculosis subunit vaccination provides long-term protective immunity characterized by multifunctional CD4 memory T cells. J. Immunol. 2009, 182, 8047-8055.
21. Makedonas, G.; Betts, M. Polyfunctional analysis of human t cell responses: Importance in vaccine immunogenicity and natural infection. Springer Semin. Immunopathol. 2006, 28, 209-219.
22. Precopio, M.; Betts, M.; Parrino, J.; Price, D.; Gostick, E.; Ambrozak, D.; Asher, T.; Douek, D.; Harari, A.; Pantaleo, G.; et al. Immunization with vaccinia virus induces polyfunctional and phenotypically distinctive CD8(+) T cell responses. J. Exp. Med. 2007, 204, 1405-1416.
23. Rosa, D.; Ribeiro, S.; Almeida, R.; Mairena, E.; Postol, E.; Kalil, J.; Cunha-Neto, E. A DNA vaccine encoding multiple HIV CD4 epitopes elicits vigorous polyfunctional, long-lived CD4+ and CD8+ T cell responses. PLoS One 2011, 6, e16921.
24. Hofstetter, H.; Toyka, K.; Tary-Lehmann, M.; Lehmann, P. Kinetics and organ distribution of IL-17-producing CD4 cells in proteolipid protein 139-151 peptide-induced experimental autoimmune encephalomyelitis of SJL mice. J. Immunol. 2007, 178, 1372-1378.
25. Jager, A.; Dardalhon, V.; Sobel, R.; Bettelli, E.; Kuchroo, V. Th1, Th17, and Th9 effector cells induce experimental autoimmune encephalomyelitis with different pathological phenotypes. J. Immunol. 2009, 183, 7169-7177.
26. Komiyama, Y.; Nakae, S.; Matsuki, T.; Nambu, A.; Ishigame, H.; Kakuta, S.; Sudo, K.; Iwakura, Y. IL-17 plays an important role in the development of experimental autoimmune encephalomyelitis. J. Immunol. 2006, 177, 566-573.
27. Kroenke, M.; Segal, B. IL-23 modulated myelin-specific T cells induce EAE via an IFNgamma driven, IL-17 independent pathway. Brain Behav. Immunol. 2011, 25, 932-937.
28. Lovett-Racke, A.; Yang, Y.; Racke, M. Th1 versus Th17: Are T cell cytokines relevant in multiple sclerosis? Biochim. Biophys. Acta 2011, 1812, 246-251.
29. Pollinger, B. IL-17 producing T cells in mouse models of multiple sclerosis and rheumatoid arthritis. J. Mol. Med. (Berl) 2012, 90, 613-624.
30. Harrington, L.; Hatton, R.; Mangan, P.; Turner, H.; Murphy, T.; Murphy, K.; Weaver, C. Interleukin 17-producing CD4+ effector T cells develop via a lineage distinct from the T helper type 1 and 2 lineages. Nat. Immunol. 2005, 6, 1123-1132.
31. Park, H.; Li, Z.; Yang, X.; Chang, S.; Nurieva, R.; Wang, Y.; Wang, Y.; Hood, L.; Zhu, Z.; Tian, Q.; et al. A distinct lineage of CD4 T cells regulates tissue inflammation by producing interleukin 17. Nat. Immunol. 2005, 6, 1133-1141.
32. Tuohy, V.; Lu, Z.; Sobel, R.; Laursen, R.; Lees, M. Identification of an encephalitogenic determinant of myelin proteolipid protein for SJL mice. J. Immunol. 1989, 142, 1523-1527.
33. Kuerten, S.; Rottlaender, A.; Rodi, M.; Velasco, V., Jr.; Schroeter, M.; Kaiser, C.; Addicks, K.; Tary-Lehmann, M.; Lehmann, P. The clinical course of EAE is reflected by the dynamics of the neuroantigen-specific T cell compartment in the blood. Clin. Immunol. 2010, 137, 422-432.
34. Mosmann, T.; Cherwinski, H.; Bond, M.; Giedlin, M.; Coffman, R. Two types of murine helper T cell clone. I. Definition according to profiles of lymphokine activities and secreted proteins. J. Immunol. 1986, 136, 2348-2357.
35. Pelfrey, C.; Rudick, R.; Cotleur, A.; Lee, J.; Tary-Lehmann, M.; Lehmann, P. Quantification of self-recognition in multiple sclerosis by single-cell analysis of cytokine production. J. Immunol. 2000, 165, 1641-1651.
36. Heeger, P.; Forsthuber, T.; Shive, C.; Biekert, E.; Genain, C.; Hofstetter, H.; Karulin, A.; Lehmann, P. Revisiting tolerance induced by autoantigen in incomplete Freund's adjuvant. J. Immunol. 2000, 164, 5771-5781.
37. Karulin, A.; Hesse, M.; Yip, H.; Lehmann, P. Indirect IL-4 pathway in type 1 immunity. J. Immunol. 2002, 168, 545-553.
38. Kersh, E.; Shaw, A.; Allen, P. Fidelity of T cell activation through multistep T cell receptor zeta phosphorylation. Science 1998, 281, 572-575.
39. Cai, Z.; Sprent, J. Influence of antigen dose and costimulation on the primary response of CD8+ T cells in vitro. J. Exp. Med. 1996, 183, 2247-2257.
40. Itoh, Y.; Germain, R. Single cell analysis reveals regulated hierarchical T cell antigen receptor signaling thresholds and intraclonal heterogeneity for individual cytokine responses of CD4+ T cells. J. Exp. Med. 1997, 186, 757-766.
41. Targoni, O.; Lehmann, P. Endogenous myelin basic protein inactivates the high avidity T cell repertoire. J. Exp. Med. 1998, 187, 2055-2063.
42. Busch, D.; Pamer, E. T cell affinity maturation by selective expansion during infection. J. Exp. Med. 1999, 189, 701-710.
43. Savage, P.; Boniface, J.; Davis, M. A kinetic basis for T cell receptor repertoire selection during an immune response. Immunity. 1999, 10, 485-492.
44. Padovan, E.; Giachino, C.; Cella, M.; Valitutti, S.; Acuto, O.; Lanzavecchia, A. Normal T lymphocytes can express two different T cell receptor beta chains: Implications for the mechanism of allelic exclusion. J. Exp. Med. 1995, 181, 1587-1591.
45. Roman, E.; Miller, E.; Harmsen, A.; Wiley, J.; von Andrian, U.; Huston, G.; Swain, S. CD4 effector T cell subsets in the response to influenza: Heterogeneity, migration, and function. J. Exp. Med. 2002, 196, 957-968.
46. Glickstein, L.; Huber, B. Karoushi--death by overwork in the immune system. J. Immunol. 1995, 155, 522-524.
47. Renno, T.; Attinger, A.; Locatelli, S.; Bakker, T.; Vacheron, S.; MacDonald, H. Cutting edge: Apoptosis of superantigen-activated T cells occurs preferentially after a discrete number of cell divisions in vivo. J. Immunol. 1999, 162, 6312-6315.
48. Lehmann, P. The fate of T cells in the brain: Veni, vidi, vici and veni, mori. Am. J. Pathol. 1998, 153, 677-680.
49. McKnight, A.; Perez, V.; Shea, C.; Gray, G.; Abbas, A. Costimulator dependence of lymphokine secretion by naive and activated CD4+ T lymphocytes from TCR transgenic mice. J. Immunol. 1994, 152, 5220-5225.
50. Ahmadzadeh, M.; Hussain, S.; Farber, D. Heterogeneity of the memory CD4 T cell response: Persisting effectors and resting memory T cells. J. Immunol. 2001, 166, 926-935.
51. Tuohy, V.; Lu, Z.; Sobel, R.; Laursen, R.; Lees, M. A synthetic peptide from myelin proteolipid protein induces experimental allergic encephalomyelitis. J. Immunol. 1988, 141, 1126-1130.
52. Hofstetter, H.; Targoni, O.; Karulin, A.; Forsthuber, T.; Tary-Lehmann, M.; Lehmann, P. 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? J. Immunol. 2005, 174, 4598-4605.
53. Targoni, O.; Baus, J.; Hofstetter, H.; Hesse, M.; Karulin, A.; Boehm, B.; Forsthuber, T.; Lehmann, P. Frequencies of neuroantigen-specific T cells in the central nervous system versus the immune periphery during the course of experimental allergic encephalomyelitis. J. Immunol. 2001, 166, 4757-4764.
54. Ishikawa, E.; Imagawa, M.; Hashida, S.; Yoshitake, S.; Hamaguchi, Y.; Ueno, T. Enzyme-labeling of antibodies and their fragments for enzyme immunoassay and immunohistochemical staining. J. Immunoass. 1983, 4, 209-327.
55. Hesse, M.; Karulin, A.; Boehm, B.; Lehmann, P.; Tary-function of its activation state. J. Immunol. 2001, 167, 1353-1361.
56. McKenzie, G.; Fallon, P.; Emson, C.; Grencis, R.; McKenzie, A. Simultaneous disruption of interleukin (IL)-4 and IL-13 defines individual roles in T helper cell type 2-mediated responses. J. Exp. Med. 1999, 189, 1565-1572.
57. Zhang, D.; Yang, L.; Ray, A. Differential responsiveness of the IL-5 and IL-4 genes to transcription factor GATA-3. J. Immunol. 1998, 161, 3817-3821.
58. Zhang, D.; Cohn, L.; Ray, P.; Bottomly, K.; Ray, A. Transcription factor GATA-3 is differentially expressed in murine Th1 and Th2 cells and controls Th2-specific expression of the interleukin-5 gene. J. Biol. Chem. 1997, 272, 21597-21603.