Specific CD8 T cells in IgE-mediated allergy correlate with allergen dose and allergic phenotype

American Journal of Respiratory and Critical Care Medicine

Volumn 181, Issue 1, 2010, Pages 7-16

  Aguilar Pimentel, Juan A ^a   Alessandrini, Francesca ^b   Huster, Katharina M ^a   Jakob, Thilo ^c   Schulz, Holger ^b   Behrendt, Heidrun ^b   Ring, Johannes ^a,b   De Angelis, Martin Hrabé ^b   Busch, Dirk H ^a   Mempel, Martin ^a,b   Ollert, Markus ^a  

^a TECHNICAL UNIVERSITY OF MUNICH   (Germany)

^b INSTITUTE OF EPIDEMIOLOGY   (Germany)

^c UNIVERSITY OF FREIBURG   (Germany)

Author keywords

Airway inflammation; Asthma; Cytotoxicity; Immunotherapy; Tolerance

Indexed keywords

IMMUNOGLOBULIN E; INTERLEUKIN 4; MAJOR HISTOCOMPATIBILITY ANTIGEN CLASS 1; OVALBUMIN;

ADOPTIVE TRANSFER; AEROSOL; AIRWAY; ALLERGIC ASTHMA; ANIMAL CELL; ANIMAL EXPERIMENT; ANIMAL MODEL; ARTICLE; CD8+ T LYMPHOCYTE; CONTROLLED STUDY; CYTOTOXICITY; DISEASE EXACERBATION; FLOW CYTOMETRY; IMMUNOTHERAPY; INFLAMMATION; LUNG FUNCTION TEST; MOUSE; NONHUMAN; PHENOTYPE; PRIORITY JOURNAL; SENSITIZATION; SYMPTOM;

ALLERGENS; ANIMALS; ATP-BINDING CASSETTE TRANSPORTERS; BRONCHIAL PROVOCATION TESTS; BRONCHOALVEOLAR LAVAGE FLUID; CD8-POSITIVE T-LYMPHOCYTES; FEMALE; FLOW CYTOMETRY; HYPERSENSITIVITY; IMMUNOGLOBULIN E; IMMUNOLOGIC MEMORY; MICE; MICE, INBRED BALB C; MICE, KNOCKOUT; OVALBUMIN; PEPTIDE FRAGMENTS;

EID: 73849149166     PISSN: 1073449X     EISSN: 15354970     Source Type: Journal    
DOI: 10.1164/rccm.200902-0190OC     Document Type: Article

References (52)

1. Kay AB. Allergy and allergic diseases: first of two parts. N Engl J Med 2001;344:30-37.
2. Nakajima H, Iwamoto I, Tomoe S, Matsumura R, Tomioka H, Takatsu K, Yoshida S. CD4+ T-lymphocytes and interleukin-5 mediate antigen-induced eosinophil infiltration into the mouse trachea. Am Rev Respir Dis 1992;146:374-377.
3. Gavett SH, Chen X, Finkelman F, Wills-Karp M. Depletion of murine CD4+ T lymphocytes prevents antigen-induced airway hyperreactivity and pulmonary eosinophilia.AmJRespir CellMol Biol 1994;10:587-593.
4. Miyahara N, Swanson BJ, Takeda K, Taube C, Miyahara S, Kodama T, Dakhama A, Ott VL, Gelfand EW. Effector CD8+ T cells mediate inflammation and airway hyper-responsiveness. NatMed 2004;10:865-869.
5. Stock P, Kallinich T, Akbari O, Quarcoo D, Gerhold K, Wahn U, Umetsu DT, Hamelmann E. CD8(+) T cells regulate immune responses in a murine model of allergen-induced sensitization and airway inflammation. Eur J Immunol 2004;34:1817-1827.
6. Wells JW, Cowled CJ, Giorgini A, Kemeny DM, Noble A. Regulation of allergic airway inflammation by class I-restricted allergen presentation and CD8 T-cell infiltration. J Allergy Clin Immunol 2007;119:226-234.
7. Tsuchiya K, Isogai S, Tamaoka M, Inase N, Akashi T, Martin JG, Yoshizawa Y. Depletion of CD8+ T cells enhances airway remodelling in a rodent model of asthma. Immunology 2009;126:45-54.
8. Gardner LM, Spyroglou L, O'Hehir RE, Rolland JM. Increased allergen concentration enhances IFN-gamma production by allergic donor T cells expressing a peripheral tissue trafficking phenotype. Allergy 2004;59:1308-1317.
9. Pooley JL,HeathWR,Shortman K.Cutting edge: intravenous soluble antigen is presented to CD4 T cells by CD8- dendritic cells, but cross-presented to CD8 T cells by CD8+ dendritic cells. J Immunol 2001;166:5327-5330.
10. Pozzi LA, Maciaszek JW, Rock KL. Both dendritic cells and macrophages can stimulate naive CD8 T cells in vivo to proliferate, develop effector function, and differentiate into memory cells. J Immunol 2005;175:2071-2081.
11. Staerz UD, Karasuyama H, Garner AM. Cytotoxic T lymphocytes against a soluble protein. Nature 1987;329:449-451.
12. Thomas MJ, Noble A, Sawicka E, Askenase PW, Kemeny DM. CD8 T cells inhibit IgE via dendritic cell IL-12 induction that promotes Th1 T cell counter-regulation. J Immunol 2002;168:216-223.
13. Kemeny DM. CD8+ T cells in atopic disease. Curr Opin Immunol 1998;10:628-633.
14. Holmes BJ, MacAry PA, Kemeny DM. Depletion of CD8+ T cells following primary immunization with ovalbumin results in a high and persistent IgE response. Int Arch Allergy Immunol 1997;113:160-162.
15. Allakhverdi Z, Lamkhioued B, Olivenstein R, Hamid Q, Renzi PM. CD8 depletion-induced late airway response is characterized by eosinophilia, increased eotaxin, and decreased IFN-gamma expression in rats. Am J Respir Crit Care Med 2000;162:1123-1131.
16. Seymour BW, Gershwin LJ, Coffman RL. Aerosol-induced immunoglobulin (Ig)-E unresponsiveness to ovalbumin does not require CD8+ or T cell receptor (TCR)-gamma/delta+ T cells or interferon (IFN)-gamma in a murine model of allergen sensitization. J Exp Med 1998;187:721-731.
17. Miyahara N, Takeda K, Kodama T, Joetham A, Taube C, Park JW, Miyahara S, Balhorn A, Dakhama A, Gelfand EW. Contribution of antigen-primed CD8+ T cells to the development of airway hyperresponsiveness and inflammation is associated with IL-13. J Immunol 2004;172:2549-2558.
18. O'Sullivan S, Cormican L, Faul JL, Ichinohe S, Johnston SL, Burke CM, PoulterLW.Activated, cytotoxicCD8(+)Tlymphocytes contribute to the pathology of asthma death. Am J Respir Crit CareMed 2001;164:560-564.
19. Akdis CA, Blaser K, Akdis M. Mechanisms of allergen-specific immunotherapy. Chem Immunol Allergy 2006;91:195-203.
20. Gabrielsson S, Soderlund A, Paulie S, van der Pouw Kraan TC, Troye-Blomberg M, Rak S. Specific immunotherapy prevents increased levels of allergen-specific IL-4- and IL-13-producing cells during pollen season. Allergy 2001;56:293-300.
21. Blaser K, Carballido J, Faith A, Crameri R, Akdis C. Determinants and mechanisms of human immune responses to bee venom phospholipase A2. Int Arch Allergy Immunol 1998;117:1-10.
22. Platts-Mills TA, Vaughan JW, Blumenthal K, Pollart Squillace S, Sporik RB. Serum IgG and IgG4 antibodies to Fel d 1 among children exposed to 20 microg Fel d 1 at home: relevance of a nonallergic modified Th2 response. Int Arch Allergy Immunol 2001;124:126-129.
23. Bousquet J, Lockey R, Malling HJ. Allergen immunotherapy: therapeutic vaccines for allergic diseases. A WHO position paper. J Allergy Clin Immunol 1998;102:558-562.
24. Moffitt JE, Golden DB, Reisman RE, Lee R, Nicklas R, Freeman T, deshazo R, Tracy J, Bernstein IL, Blessing-Moore J, et al. Stinging insect hypersensitivity: a practice parameter update. J Allergy Clin Immunol 2004;114:869-886.
25. Secrist H, DeKruyff RH, Umetsu DT. Interleukin 4 production by CD4+ T cells from allergic individuals is modulated by antigen concentration and antigen-presenting cell type. J Exp Med 1995;181:1081-1089.
26. Sakai K, Yokoyama A, Kohno N, Hiwada K. Effect of different sensitizing doses of antigen in a murine model of atopic asthma. Clin Exp Immunol 1999;118:9-15.
27. Morokata T, Ishikawa J, Yamada T. Antigen dose defines T helper 1 and T helper 2 responses in the lungs of C57BL/6 and BALB/c mice independently of splenic responses. Immunol Lett 2000;72:119-126.
28. Klenerman P, Cerundolo V, Dunbar PR. Tracking T cells with tetramers: new tales from new tools. Nat Rev Immunol 2002;2:263-272.
29. Aguilar-Pimentel A, Huster K, Alessandrini F, Jakob T, Behrendt H, Ring J, Busch DH, Mempel M, Ollert M. Modulation of the antigen dose during allergic sensitization reveals a key role for CD8+ T cells in reducing allergic airway inflammation. Allergy 2008;63:s88.
30. Aguilar-Pimentel JA, Huster K, Alessandrini F, Gutermuth J, Jakob T, Behrendt H, Ring J, Busch D, Mempel M, Ollert M. De novo induction and recruitment of allergen-specific effector CD8+ T cells in a mouse model of IgE-mediated allergy and airway inflammation. J Allergy Clin Immunol 2005;115:S274.
31. Alessandrini F, Schulz H, Takenaka S, Lentner B, Karg E, Behrendt H, Jakob T. Effects of ultrafine carbon particle inhalation on allergic inflammation of the lung. J Allergy Clin Immunol 2006;117:824-830.
32. Frentsch M, Arbach O, Kirchhoff D, Moewes B, Worm M, Rothe M, Scheffold A, Thiel A. Direct access to CD4+ T cells specific for defined antigens according to CD154 expression. Nat Med 2005;11:1118-1124.
33. Wherry EJ, Teichgraber V, Becker TC, Masopust D, Kaech SM, Antia R, von Andrian UH, Ahmed R. Lineage relationship and protective immunity of memory CD8 T cell subsets. Nat Immunol 2003;4:225-234.
34. Huster KM, Busch V, Schiemann M, Linkemann K, Kerksiek KM, Wagner H, Busch DH. Selective expression of IL-7 receptor on memory T cells identifies early CD40l-dependent generation of distinct CD8+ memory T cell subsets. Proc Natl Acad Sci USA 2004;101:5610-5615.
35. Jaakkola I, Merinen M, Jalkanen S, Hanninen A. Ly6C induces clustering of LFA-1 (CD11a/CD18) and is involved in subtypespecific adhesion of CD8 T cells. J Immunol 2003;170:1283-1290.
36. Curtsinger JM, Lins DC, Mescher MF. CD8+ memory T cells (CD44high, Ly-6C+) are more sensitive than naive cells to (CD44low, Ly-6C-) to TCR/CD8 signaling in response to antigen. J Immunol 1998;160:3236-3243.
37. Ashton-Rickardta PG, Opferman JT. Memory T lymphocytes. Cell Mol Life Sci 1999;56:69-77.
38. Schaller MA, Lundy SK, Huffnagle GB, Lukacs NW. CD8+ T cell contributions to allergen induced pulmonary inflammation and airway hyperreactivity. Eur J Immunol 2005;35:2061-2070.
39. Knabel M, Franz TJ, Schiemann M, Wulf A, Villmow B, Schmidt B, Bernhard H, Wagner H, Busch DH. Reversible MHC multimer staining for functional isolation of T-cell populations and effective adoptive transfer. Nat Med 2002;8:631-637.
40. Koelle DM, Liu Z, McClurkan CM, Topp MS, Riddell SR, Pamer EG, Johnson AS, Wald A, Corey L. Expression of cutaneous lymphocyteassociated antigen by CD8(+) T cells specific for a skin-tropic virus. J Clin Invest 2002;110:537-548.
41. Masopust D, Vezys V, Usherwood EJ, Cauley LS, Olson S, Marzo AL, Ward RL, Woodland DL, Lefrancois L. Activated primary and memory CD8 T cells migrate to nonlymphoid tissues regardless of site of activation or tissue of origin. J Immunol 2004;172:4875-4882.
42. Dikopoulos N, Jomantaite I, Schirmbeck R, Reimann J. Specific, functional effector/memory CD81 T cells are found in the liver post-vaccination. J Hepatol 2003;39:910-917.
43. Yoshida A, Ohba M, Wu X, Sasano T, Nakamura M, Endo Y. Accumulation of platelets in the lung and liver and their degranulation following antigen-challenge in sensitized mice. Br J Pharmacol 2002;137:146-152.
44. Ackerman AL, Kyritsis C, Tampe R, Cresswell P. Early phagosomes in dendritic cells form a cellular compartment sufficient for cross presentation of exogenous antigens. Proc Natl Acad Sci USA 2003;100:12889-12894.
45. Zinkernagel RM. On cross-priming of MHC class I-specific CTL: rule or exception? Eur J Immunol 2002;32:2385-2392.
46. Drachenberg KJ, Wheeler AW, Stuebner P, Horak F. A well-tolerated grass pollen-specific allergy vaccine containing a novel adjuvant, monophosphoryl lipid a, reduces allergic symptoms after only four preseasonal injections. Allergy 2001;56:498-505.
47. Delayre-Orthez C, de Blay F, Frossard N, Pons F. Dose-dependent effects of endotoxins on allergen sensitization and challenge in the mouse. Clin Exp Allergy 2004;34:1789-1795.
48. Yoshida M, Leigh R, Matsumoto K, Wattie J, Ellis R, O'Byrne PM, Inman MD. Effect of interferon-gamma on allergic airway responses in interferon-gamma- deficient mice. Am J Respir Crit Care Med 2002;166:451-456.
49. Dakhama A, Park JW, Taube C, Joetham A, Balhorn A, Miyahara N, Takeda K, Gelfand EW. The enhancement or prevention of airway hyperresponsiveness during reinfection with respiratory syncytial virus is critically dependent on the age at first infection and IL-13 production. J Immunol 2005;175:1876-1883.
50. Van Kaer L, Ashton-Rickardt PG, Ploegh HL, Tonegawa S. TAP1 mutant mice are deficient in antigen presentation, surface class I molecules, and CD4-8+ T cells. Cell 1992;71:1205-1214.
51. Huang TJ, MacAry PA, Kemeny DM, Chung KF. Effect of CD81 T-cell depletion on bronchial hyper-responsiveness and inflammation in sensitized and allergen-exposed Brown-Norway rats. Immunology 1999;96:416-423.
52. Seneviratne SL, Jones L, King AS, Black A, Powell S, McMichael AJ, Ogg GS. Allergen-specific CD8(+) T cells and atopic disease. J Clin Invest 2002;110:1283-1291.