Protective effector memory CD4 T cells depend on ICOS for survival

PLoS ONE

Volumn 6, Issue 2, 2011, Pages

  Moore, Tamson V ^a   Clay, Bryan S ^a   Ferreira, Caroline M ^a   Williams, Jesse W ^a   Rogozinska, Magdalena ^b   Cannon, Judy L ^a   Shilling, Rebecca A ^a   Marzo, Amanda L ^b   Sperling, Anne I ^a  

^a UNIVERSITY OF CHICAGO   (United States)

^b RUSH UNIVERSITY MEDICAL CENTER   (United States)

Author keywords

[No Author keywords available]

Indexed keywords

CELL PROTEIN; INDUCIBLE COSTIMULATOR PROTEIN; INTERLEUKIN 4; UNCLASSIFIED DRUG; ICOSL PROTEIN, MOUSE; INDUCIBLE T CELL CO STIMULATOR; INDUCIBLE T-CELL CO-STIMULATOR; PROTEIN; T LYMPHOCYTE ANTIGEN;

ANIMAL CELL; ANIMAL EXPERIMENT; ANIMAL MODEL; ANIMAL TISSUE; ANTIGEN SPECIFICITY; ARTICLE; CD4+ T LYMPHOCYTE; CELL MATURATION; CELL STIMULATION; CELL SURVIVAL; CYTOKINE PRODUCTION; EFFECTOR CELL; IMMUNOREACTIVITY; INFECTION PREVENTION; INFECTION SENSITIVITY; INFLUENZA A; LYMPHOCYTE PROLIFERATION; MEMORY T LYMPHOCYTE; MOUSE; NONHUMAN; PHENOTYPIC VARIATION; REGULATORY MECHANISM; REINFECTION; T LYMPHOCYTE SUBPOPULATION; WILD TYPE; ANIMAL; BAGG ALBINO MOUSE; C57BL MOUSE; CELL PROTECTION; GENETIC PREDISPOSITION; GENETICS; IMMUNOLOGICAL MEMORY; IMMUNOLOGY; INFLUENZA VIRUS A; METABOLISM; MOUSE MUTANT; ORTHOMYXOVIRUS INFECTION; PHENOTYPE; PHYSIOLOGY;

MUS; ORTHOMYXOVIRIDAE; VERMES;

ANIMALS; ANTIGENS, DIFFERENTIATION, T-LYMPHOCYTE; CD4-POSITIVE T-LYMPHOCYTES; CELL SURVIVAL; CYTOPROTECTION; GENETIC PREDISPOSITION TO DISEASE; IMMUNOLOGIC MEMORY; INFLUENZA A VIRUS; INTERLEUKIN-4; MICE; MICE, INBRED BALB C; MICE, INBRED C57BL; MICE, KNOCKOUT; ORTHOMYXOVIRIDAE INFECTIONS; PHENOTYPE; PROTEINS;

EID: 79951996635     PISSN: None     EISSN: 19326203     Source Type: Journal    
DOI: 10.1371/journal.pone.0016529     Document Type: Article

References (64)

1. Swain SL, Dutton RW, Woodland DL, (2004) T cell responses to influenza virus infection: effector and memory cells. Viral Immunol 17: 197-209.
2. Xu R, Johnson AJ, Liggitt D, Bevan MJ, (2004) Cellular and humoral immunity against vaccinia virus infection of mice. J Immunol 172: 6265-6271.
3. Mountford AP, Coulson PS, Pemberton RM, Smythies LE, Wilson RA, (1992) The generation of interferon-gamma-producing T lymphocytes in skin-draining lymph nodes, and their recruitment to the lungs, is associated with protective immunity to Schistosoma mansoni. Immunology 75: 250-256.
4. Zaph C, Rook KA, Goldschmidt M, Mohrs M, Scott P, et al. (2006) Persistence and function of central and effector memory CD4+ T cells following infection with a gastrointestinal helminth. J Immunol 177: 511-518.
5. Palmer DR, Krzych U, (2002) Cellular and molecular requirements for the recall of IL-4-producing memory CD4(+)CD45RO(+)CD27(-) T cells during protection induced by attenuated Plasmodium falciparum sporozoites. Eur J Immunol 32: 652-661.
6. Rhee EG, Mendez S, Shah JA, Wu CY, Kirman JR, et al. (2002) Vaccination with heat-killed leishmania antigen or recombinant leishmanial protein and CpG oligodeoxynucleotides induces long-term memory CD4+ and CD8+ T cell responses and protection against leishmania major infection. J Exp Med 195: 1565-1573.
7. Mendez S, Belkaid Y, Seder RA, Sacks D, (2002) Optimization of DNA vaccination against cutaneous leishmaniasis. Vaccine 20: 3702-3708.
8. Claesson MH, Bregenholt S, Bonhagen K, Thoma S, Moller P, et al. (1999) Colitis-inducing potency of CD4+ T cells in immunodeficient, adoptive hosts depends on their state of activation, IL-12 responsiveness, and CD45RB surface phenotype. J Immunol 162: 3702-3710.
9. Bouwer HG, Hinrichs DJ, (1994) Adoptive transfer of experimental allergic encephalomyelitis: recipient response to myelin basic protein-reactive lymphocytes. J Neuroimmunol 54: 87-98.
10. Nakagome K, Dohi M, Okunishi K, To Y, Sato A, et al. (2005) Antigen-sensitized CD4+CD62Llow memory/effector T helper 2 cells can induce airway hyperresponsiveness in an antigen free setting. Respir Res 6: 46.
11. Bradley LM, Harbertson J, Freschi GC, Kondrack R, Linton PJ, (2000) Regulation of development and function of memory CD4 subsets. Immunol Res 21: 149-158.
12. Tang AL, Bingaman AW, Kadavil EA, Leeser DB, Farber DL, (2006) Generation and functional capacity of polyclonal alloantigen-specific memory CD4 T cells. Am J Transplant 6: 1275-1284.
13. Sallusto F, Lenig D, Forster R, Lipp M, Lanzavecchia A, (1999) Two subsets of memory T lymphocytes with distinct homing potentials and effector functions. Nature 401: 708-712.
14. Hengel RL, Thaker V, Pavlick MV, Metcalf JA, Dennis G Jr, et al. (2003) Cutting edge: L-selectin (CD62L) expression distinguishes small resting memory CD4+ T cells that preferentially respond to recall antigen. J Immunol 170: 28-32.
15. Bjorkdahl O, Barber KA, Brett SJ, Daly MG, Plumpton C, et al. (2003) Characterization of CC-chemokine receptor 7 expression on murine T cells in lymphoid tissues. Immunology 110: 170-179.
16. Messi M, Giacchetto I, Nagata K, Lanzavecchia A, Natoli G, et al. (2003) Memory and flexibility of cytokine gene expression as separable properties of human T(H)1 and T(H)2 lymphocytes. Nat Immunol 4: 78-86.
17. Ahmadzadeh M, Hussain SF, Farber DL, (2001) Heterogeneity of the memory CD4 T cell response: persisting effectors and resting memory T cells. J Immunol 166: 926-935.
18. Riou C, Yassine-Diab B, Van grevenynghe J, Somogyi R, Greller LD, et al. (2007) Convergence of TCR and cytokine signaling leads to FOXO3a phosphorylation and drives the survival of CD4+ central memory T cells. J Exp Med 204: 79-91.
19. Geginat J, Sallusto F, Lanzavecchia A, (2001) Cytokine-driven proliferation and differentiation of human naive, central memory, and effector memory CD4(+) T cells. J Exp Med 194: 1711-1719.
20. Dooms H, Abbas AK, (2006) Control of CD4+ T-cell memory by cytokines and costimulators. Immunol Rev 211: 23-38.
21. Soroosh P, Ine S, Sugamura K, Ishii N, (2007) Differential requirements for OX40 signals on generation of effector and central memory CD4+ T cells. J Immunol 179: 5014-5023.
22. Salek-Ardakani S, Croft M, (2006) Regulation of CD4 T cell memory by OX40 (CD134). Vaccine 24: 872-883.
23. Hutloff A, Dittrich AM, Beier KC, Eljaschewitsch B, Kraft R, et al. (1999) ICOS is an inducible T-cell co-stimulator structurally and functionally related to CD28. Nature 397: 263-266.
24. Sallusto F, Geginat J, Lanzavecchia A, (2004) Central memory and effector memory T cell subsets: function, generation, and maintenance. Annu Rev Immunol 22: 745-763.
25. Linton PJ, Haynes L, Klinman NR, Swain SL, (1996) Antigen-independent changes in naive CD4 T cells with aging. J Exp Med 184: 1891-1900.
26. Cossarizza A, Ortolani C, Paganelli R, Barbieri D, Monti D, et al. (1996) CD45 isoforms expression on CD4+ and CD8+ T cells throughout life, from newborns to centenarians: implications for T cell memory. Mech Ageing Dev 86: 173-195.
27. Linton PJ, Haynes L, Tsui L, Zhang X, Swain S, (1997) From naive to effector-alterations with aging. Immunol Rev 160: 9-18.
28. Moon JJ, Chu HH, Pepper M, McSorley SJ, Jameson SC, et al. (2007) Naive CD4(+) T cell frequency varies for different epitopes and predicts repertoire diversity and response magnitude. Immunity 27: 203-213.
29. Moon JJ, Chu HH, Hataye J, Pagan AJ, Pepper M, et al. (2009) Tracking epitope-specific T cells. Nat Protoc 4: 565-581.
30. Humphreys IR, Edwards L, Snelgrove RJ, Rae AJ, Coyle AJ, et al. (2006) A critical role for ICOS co-stimulation in immune containment of pulmonary influenza virus infection. Eur J Immunol 36: 2928-2938.
31. Kilbourne ED, (1969) Future influenza vaccines and the use of genetic recombinants. Bull World Health Organ 41: 643-645.
32. Flynn KJ, Belz GT, Altman JD, Ahmed R, Woodland DL, et al. (1998) Virus-specific CD8+ T cells in primary and secondary influenza pneumonia. Immunity 8: 683-691.
33. Burmeister Y, Lischke T, Dahler AC, Mages HW, Lam KP, et al. (2008) ICOS controls the pool size of effector-memory and regulatory T cells. J Immunol 180: 774-782.
34. Mahajan S, Cervera A, MacLeod M, Fillatreau S, Perona-Wright G, et al. (2007) The role of ICOS in the development of CD4 T cell help and the reactivation of memory T cells. Eur J Immunol 37: 1796-1808.
35. Watanabe M, Hara Y, Tanabe K, Toma H, Abe R, (2005) A distinct role for ICOS-mediated co-stimulatory signaling in CD4+ and CD8+ T cell subsets. Int Immunol.
36. Sporici RA, Beswick RL, von Allmen C, Rumbley CA, Hayden-Ledbetter M, et al. (2001) ICOS ligand costimulation is required for T-cell encephalitogenicity. Clin Immunol 100: 277-288.
37. Grimbacher B, Hutloff A, Schlesier M, Glocker E, Warnatz K, et al. (2003) Homozygous loss of ICOS is associated with adult-onset common variable immunodeficiency. Nat Immunol 4: 261-268.
38. Tafuri A, Shahinian A, Bladt F, Yoshinaga SK, Jordana M, et al. (2001) ICOS is essential for effective T-helper-cell responses. Nature 409: 105-109.
39. Takahashi N, Matsumoto K, Saito H, Nanki T, Miyasaka N, et al. (2009) Impaired CD4 and CD8 effector function and decreased memory T cell populations in ICOS-deficient patients. J Immunol 182: 5515-5527.
40. Bains I, Antia R, Callard R, Yates AJ, (2009) Quantifying the development of the peripheral naive CD4+ T-cell pool in humans. Blood 113: 5480-5487.
41. Hogan RJ, Zhong W, Usherwood EJ, Cookenham T, Roberts AD, et al. (2001) Protection from respiratory virus infections can be mediated by antigen- specific CD4(+) T cells that persist in the lungs. J Exp Med 193: 981-986.
42. Teijaro JR, Verhoeven D, Page CA, Turner D, Farber DL, (2010) Memory CD4 T cells direct protective responses to influenza virus in the lungs through helper-independent mechanisms. J Virol 84: 9217-9226.
43. Zhong W, Roberts AD, Woodland DL, (2001) Antibody-independent antiviral function of memory CD4+ T cells in vivo requires regulatory signals from CD8+ effector T cells. J Immunol 167: 1379-1386.
44. Hansen SG, Vieville C, Whizin N, Coyne-Johnson L, Siess DC, et al. (2009) Effector memory T cell responses are associated with protection of rhesus monkeys from mucosal simian immunodeficiency virus challenge. Nat Med 15: 293-299.
45. Kroczek R, Hamelmann E, (2005) T-cell costimulatory molecules: optimal targets for the treatment of allergic airway disease with monoclonal antibodies. J Allergy Clin Immunol 116: 906-909.
46. Paulos CM, Carpenito C, Plesa G, Suhoski MM, Varela-Rohena A, et al. The inducible costimulator (ICOS) is critical for the development of human T(H)17 cells. Sci Transl Med 2: 55ra78.
47. Lara-Marquez ML, Moan MJ, Cartwright S, Listman J, Israel E, et al. (2001) Atopic asthma: differential activation phenotypes among memory T helper cells. Clin Exp Allergy 31: 1232-1241.
48. Robinson DS, Bentley AM, Hartnell A, Kay AB, Durham SR, (1993) Activated memory T helper cells in bronchoalveolar lavage fluid from patients with atopic asthma: relation to asthma symptoms, lung function, and bronchial responsiveness. Thorax 48: 26-32.
49. Robinson DS, Hamid Q, Ying S, Tsicopoulos A, Barkans J, et al. (1992) Predominant TH2-like bronchoalveolar T-lymphocyte population in atopic asthma. N Engl J Med 326: 298-304.
50. Strickland DH, Stumbles PA, Zosky GR, Subrata LS, Thomas JA, et al. (2006) Reversal of airway hyperresponsiveness by induction of airway mucosal CD4+CD25+ regulatory T cells. J Exp Med 203: 2649-2660.
51. Busse WW, Coffman RL, Gelfand EW, Kay AB, Rosenwasser LJ, (1995) Mechanisms of persistent airway inflammation in asthma. A role for T cells and T-cell products. [Review] [21 refs]. American Journal of Respiratory & Critical Care Medicine 152: 388-393.
52. Cohn L, Elias JA, Chupp GL, (2004) Asthma: mechanisms of disease persistence and progression. Annu Rev Immunol 22: 789-815.
53. Dong C, Juedes AE, Temann UA, Shresta S, Allison JP, et al. (2001) ICOS co-stimulatory receptor is essential for T-cell activation and function. Nature 409: 97-101.
54. Julius MH, Simpson E, Herzenberg LA, (1973) A rapid method for the isolation of functional thymus-derived murine lymphocytes. Eur J Immunol 3: 645-649.
55. Lyons AB, Parish CR, (1994) Determination of lymphocyte division by flow cytometry. J Immunol Methods 171: 131-137.
56. Metwali A, Elliott D, Blum A, Weinstock JV, (1996) What Models of Granulomatous Inflammation Provide the Immunologist. Methods 9: 305-310.
57. Elliott D, (1996) Methods used to study immunoregulation of schistosome egg granulomas. Immunol Methods 9: 255-257.
58. Vella AT, Hulsebosch MD, Pearce EJ, (1992) Schistosoma mansoni eggs induce antigen-responsive CD44-hi T helper 2 cells and IL-4-secreting CD44-lo cells. Potential for T helper 2 subset differentiation is evident at the precursor level. J Immunol 149: 1714-1722.
59. Vella AT, Pearce EJ, (1992) CD4+ Th2 response induced by Schistosoma mansoni eggs develops rapidly, through an early, transient, Th0-like stage. J Immunol 148: 2283-2290.
60. Sabin EA, Kopf MA, Pearce EJ, (1996) Schistosoma mansoni egg-induced early IL-4 production is dependent upon IL-5 and eosinophils. J Exp Med 184: 1871-1878.
61. Sabin EA, Pearce EJ, (1995) Early IL-4 production by non-CD4+ cells at the site of antigen deposition predicts the development of a T helper 2 cell response to Schistosoma mansoni eggs. J Immunol 155: 4844-4853.
62. Grzych JM, Pearce E, Cheever A, Caulada ZA, Caspar P, et al. (1991) Egg deposition is the major stimulus for the production of Th2 cytokines in murine schistosomiasis mansoni. J Immunol 146: 1322-1327.
63. Hataye J, Moon JJ, Khoruts A, Reilly C, Jenkins MK, (2006) Naive and memory CD4+ T cell survival controlled by clonal abundance. Science 312: 114-116.
64. Barefoot BE, Sample CJ, Ramsburg EA, (2009) Recombinant vesicular stomatitis virus expressing influenza nucleoprotein induces CD8 T-cell responses that enhance antibody-mediated protection after lethal challenge with influenza virus. Clin Vaccine Immunol 16: 488-498.