CD8+ T cells with an intraepithelial phenotype upregulate cytotoxic function upon influenza infection in human lung

Journal of Clinical Investigation

Volumn 121, Issue 6, 2011, Pages 2254-2263

  Piet, Berber ^a   De Bree, Godelieve J ^a   Smids Dierdorp, Barbara S ^a   Van Der Loos, Chris M ^a   Remmerswaal, Ester B M ^a   Von Der Thüsen, Jan H ^a,e   Van Haarst, Jan M W ^b   Eerenberg, Jan P ^b   Brinke, Anja Ten ^c   Van Der Bij, Wim ^d   Timens, Wim ^d   Van Lier, René A W ^a,f   Jonkers, René E ^a  

^a ACADEMIC MEDICAL CENTER   (Netherlands)

^b Tergooi Hospitals   (Netherlands)

^c SANQUIN RESEARCH   (Netherlands)

^d UNIVERSITY MEDICAL CENTER GRONINGEN   (Netherlands)

^e ROYAL BROMPTON AND HAREFIELD NHS FOUNDATION TRUST   (United Kingdom)

^f Sanquin Blood Supply   (Netherlands)

Author keywords

[No Author keywords available]

Indexed keywords

ALPHA INTEGRIN; CD103 ANTIGEN; GRANZYME B; INTERFERON; NATURAL KILLER CELL RECEPTOR NKG2A; PERFORIN; PREDNISOLONE; TOLL LIKE RECEPTOR; ALPHA E INTEGRINS; GRANZYME; GZMB PROTEIN, HUMAN; KLRC1 PROTEIN, HUMAN; LEUKOCYTE ANTIGEN; NATURAL KILLER CELL LECTIN LIKE RECEPTOR SUBFAMILY C; PORE FORMING CYTOTOXIC PROTEIN; PRF1 PROTEIN, HUMAN; T LYMPHOCYTE RECEPTOR; VERY LATE ACTIVATION ANTIGEN 1;

ADULT; AGED; ANTIGEN EXPRESSION; ANTIGEN SPECIFICITY; ARTICLE; CD8+ T LYMPHOCYTE; CELL ISOLATION; CHRONIC OBSTRUCTIVE LUNG DISEASE; CONTROLLED STUDY; CORTICOSTEROID THERAPY; CYTOKINE PRODUCTION; CYTOLYSIS; CYTOMEGALOVIRUS; CYTOTOXIC T LYMPHOCYTE; EPSTEIN BARR VIRUS; FEMALE; FIBROSING ALVEOLITIS; HUMAN; HUMAN CELL; HUMAN TISSUE; IMMUNOHISTOCHEMISTRY; IMMUNOSUPPRESSIVE TREATMENT; INFLUENZA; LOBECTOMY; LUNG ALVEOLUS CELL; LUNG ALVEOLUS EPITHELIUM; LUNG INFECTION; LUNG PARENCHYMA; LUNG RESECTION; LYMPHOCYTE COUNT; MALE; MONONUCLEAR CELL; PHENOTYPE; PRIORITY JOURNAL; PROTECTION; PROTEIN EXPRESSION; T LYMPHOCYTE SUBPOPULATION; UPREGULATION; BIOSYNTHESIS; BLOOD CELL; CHEMISTRY; CYTOTOXICITY; EPITHELIUM; GENE EXPRESSION REGULATION; GENETICS; HERPES VIRUS; IMMUNOLOGY; IMMUNOPHENOTYPING; INFLUENZA VIRUS A; LUNG; METABOLISM; MIDDLE AGED;

AGED; ANTIGENS, CD; BLOOD CELLS; CD8-POSITIVE T-LYMPHOCYTES; CYTOTOXICITY, IMMUNOLOGIC; EPITHELIUM; FEMALE; GENE EXPRESSION REGULATION; GRANZYMES; HERPESVIRIDAE; HUMANS; IMMUNOPHENOTYPING; INFLUENZA A VIRUS; INFLUENZA, HUMAN; INTEGRIN ALPHA CHAINS; INTEGRIN ALPHA1BETA1; LUNG; MALE; MIDDLE AGED; NK CELL LECTIN-LIKE RECEPTOR SUBFAMILY C; PORE FORMING CYTOTOXIC PROTEINS; T-CELL ANTIGEN RECEPTOR SPECIFICITY; T-LYMPHOCYTE SUBSETS; UP-REGULATION;

EID: 79957884875     PISSN: 00219738     EISSN: 15588238     Source Type: Journal    
DOI: 10.1172/JCI44675     Document Type: Article

References (56)

1. Hogg JC, et al. The nature of small-airway obstruction in chronic obstructive pulmonary disease. N Engl J Med. 2004;350(26):2645-2653. (Pubitemid 38787999)
2. Topham DJ, Tripp RA, Doherty PC. CD8+ T cells clear influenza virus by perforin or Fas-dependent processes. J Immunol. 1997;159(11):5197-5200. (Pubitemid 127470043)
3. Russell JH, Ley TJ. Lymphocyte-mediated cytotoxicity. Annu Rev Immunol. 2002;20:323-370. (Pubitemid 34293428)
4. Trapani JA, Sutton VR, Smyth MJ. CTL granules: evolution of vesicles essential for combating virus infections. Immunol Today. 1999;20(8):351-356. (Pubitemid 29356428)
5. Cerwenka A, Morgan TM, Dutton RW. Naive, effector, and memory CD8 T cells in protection against pulmonary influenza virus infection: homing properties rather than initial frequencies are crucial. J Immunol. 1999;163(10):5535-5543.
6. Hogan RJ, Zhong W, Usherwood EJ, Cookenham T, Roberts AD, Woodland DL. Protection from respiratory virus infections can be mediated by antigen-specific CD4(+) T cells that persist in the lungs. J Exp Med. 2001;193(8):981-986. (Pubitemid 32525871)
7. Liang S, Mozdzanowska K, Palladino G, Gerhard W. Heterosubtypic immunity to influenza type A virus in mice. Effector mechanisms and their longevity. J Immunol. 1994;152(4):1653-1661. (Pubitemid 24075695)
8. Ely KH, Roberts AD, Woodland DL. Cutting edge: effector memory CD8+ T cells in the lung airways retain the potential to mediate recall responses. J Immunol. 2003;171(7):3338-3342. (Pubitemid 37264925)
9. Kohlmeier JE, Woodland DL. Immunity to respiratory viruses. Annu Rev Immunol. 2009;27:61-82.
10. de Bree GJ, van Leeuwen EM, Out TA, Jansen HM, Jonkers RE, van Lier RA. Selective accumulation of differentiated CD8+ T cells specific for respiratory viruses in the human lung. J Exp Med. 2005; 202(10):1433-1442. (Pubitemid 41668745)
11. Cepek KL, et al. Adhesion between epithelial cells and T lymphocytes mediated by E-cadherin and the alpha E beta 7 integrin. Nature. 1994;372(6502):190-193.
12. Cerf-Bensussan N, Begue B, Gagnon J, Meo T. The human intraepithelial lymphocyte marker HML-1 is an integrin consisting of a beta 7 subunit associated with a distinctive alpha chain. Eur J Immunol. 1992; 22(1):273-277.
13. Goto E, et al. Human bronchial intraepithelial T lymphocytes as a distinct T-cell subset: their longterm survival in SCID-Hu chimeras. Am J Respir Cell Mol Biol. 2000;22(4):405-411. (Pubitemid 30343339)
14. Hirosako S, et al. Human bronchial intraepithelial T cells produce interferon-gamma and stimulate epithelial cells. Clin Exp Immunol. 2009;155(2):266-274.
15. Morgan AJ, Guillen C, Symon FA, Birring SS, Campbell JJ, Wardlaw AJ. CXCR6 identifies a putative population of retained human lung T cells characterised by co-expression of activation markers. Immunobiology. 2008;213(7):599-608.
16. Hirosako S, et al. CD8 and CD103 Are highly expressed in asthmatic bronchial intraepithelial lymphocytes. Int Arch Allergy Immunol. 2010;153(2):157-165.
17. El-Asady R, et al. TGF-{beta}-dependent CD103 expression by CD8(+) T cells promotes selective destruction of the host intestinal epithelium during graft-versushost disease. J Exp Med. 2005;201(10):1647-1657. (Pubitemid 40721008)
18. Johansson-Lindbom B, Agace WW. Generation of gut-homing T cells and their localization to the small intestinal mucosa. Immunol Rev. 2007;215:226-242. (Pubitemid 46212243)
19. Lefrancois L, et al. The role of beta7 integrins in CD8 T cell trafficking during an antiviral immune response. J Exp Med. 1999;189(10):1631- 1638. (Pubitemid 29240888)
20. Ray SJ, et al. The collagen binding alpha1beta1 integrin VLA-1 regulates CD8 T cell-mediated immune protection against heterologous influenza infection. Immunity. 2004;20(2):167-179. (Pubitemid 38258393)
21. Richter M, et al. Collagen distribution and expression of collagen-binding alpha1beta1 (VLA-1) and alpha2beta1 (VLA-2) integrins on CD4 and CD8 T cells during influenza infection. J Immunol. 2007; 178(7):4506-4516. (Pubitemid 46492403)
22. Chapman TJ, Topham DJ. Identification of a unique population of tissue-memory CD4+ T cells in the airways after influenza infection that is dependent on the integrin VLA-1. J Immunol. 2010; 184(7):3841-3849.
23. Jabri B, et al. Selective expansion of intraepithelial lymphocytes expressing the HLA-E-specific natural killer receptor CD94 in celiac disease. Gastroenterology. 2000;118(5):867-879. (Pubitemid 30243750)
24. Braud VM, et al. HLA-E binds to natural killer cell receptors CD94/NKG2A, B and C. Nature. 1998; 391(6669):795-799. (Pubitemid 28099678)
25. Figueiredo C, Seltsam A, Blasczyk R. Permanent silencing of NKG2A expression for cell-based therapeutics. J Mol Med. 2009;87(2):199-210.
26. Ikeda H, et al. Characterization of an antigen that is recognized on a melanoma showing partial HLA loss by CTL expressing an NK inhibitory receptor. Immunity. 1997;6(2):199-208. (Pubitemid 27145564)
27. Mingari MC, Ponte M, Vitale C, Bellomo R, Moretta L. Expression of HLA class I-specific inhibitory receptors in human cytolytic T lymphocytes: a regulated mechanism that controls T-cell activation and function. Hum Immunol. 2000;61(1):44-50. (Pubitemid 30058766)
28. Speiser DE, et al. In vivo expression of natural killer cell inhibitory receptors by human melanoma-specific cytolytic T lymphocytes. J Exp Med. 1999; 190(6):775-782. (Pubitemid 29451623)
29. Hamann D, et al. Phenotypic and functional separation of memory and effector human CD8+ T cells. J Exp Med. 1997;186(9):1407-1418. (Pubitemid 27479800)
30. Uss E, Rowshani AT, Hooibrink B, Lardy NM, van Lier RA, ten Berge IJ. CD103 is a marker for alloantigen-induced regulatory CD8+ T cells. J Immunol. 2006;177(5):2775-2783. (Pubitemid 44277792)
31. Smyth MJ, Trapani JA. Granzymes: exogenous proteinases that induce target cell apoptosis. Immunol Today. 1995;16(4):202-206.
32. Trapani JA, Davis J, Sutton VR, Smyth MJ. Proapoptotic functions of cytotoxic lymphocyte granule constituents in vitro and in vivo. Curr Opin Immunol. 2000;12(3):323-329. (Pubitemid 30240543)
33. McFarland RD, Douek DC, Koup RA, Picker LJ. Identification of a human recent thymic emigrant phenotype. Proc Natl Acad Sci U S A. 2000;97(8):4215- 4220.
34. Lanier LL, Corliss B, Wu J, Phillips JH. Association of DAP12 with activating CD94/NKG2C NK cell receptors. Immunity. 1998;8(6):693-701. (Pubitemid 28294516)
35. Kohlmeier JE, Cookenham T, Roberts AD, Miller SC, Woodland DL. Type I interferons regulate cytolytic activity of memory CD8+ T cells in the lung airways during respiratory virus challenge. Immunity. 2010;33(1):96-105.
36. Wakim LM, Waithman J, van Rooijen N, Heath WR, Carbone FR. Dendritic cell-induced memory T cell activation in nonlymphoid tissues. Science. 2008; 319(5860):198-202.
37. Woodland DL, Kohlmeier JE. Migration, maintenance and recall of memory T cells in peripheral tissues. Nat Rev Immunol. 2009;9(3):153-161.
38. Richter MV, Topham DJ. The alpha1beta1 integrin and TNF receptor II protect airway CD8+ effector T cells from apoptosis during influenza infection. J Immunol. 2007;179(8):5054-5063.
39. Wang XZ, Stepp SE, Brehm MA, Chen HD, Selin LK, Welsh RM. Virus-specific CD8 T cells in peripheral tissues are more resistant to apoptosis than those in lymphoid organs. Immunity. 2003;18(5):631-642. (Pubitemid 36588580)
40. Lawrence CW, Ream RM, Braciale TJ. Frequency, specificity, and sites of expansion of CD8(+) T cells during primary influenza virus infection. J Immunol. 2005;174(9):5332-5340. (Pubitemid 40593171)
41. Franciszkiewicz K, et al. Intratumoral induction of CD103 triggers tumor-specific CTL function and CCR5-dependent T-cell retention. Cancer Res. 2009;69(15):6249-6255.
42. French JJ, Cresswell J, Wong WK, Seymour K, Charnley RM, Kirby JA. T cell adhesion and cytolysis of pancreatic cancer cells: a role for E-cadherin in immunotherapy? Br J Cancer. 2002;87(9):1034-1041. (Pubitemid 35305658)
43. Le Floc'h A, et al. Alpha E beta 7 integrin interaction with E-cadherin promotes antitumor CTL activity by triggering lytic granule polarization and exocytosis. J Exp Med. 2007;204(3):559-570.
44. Smyth LJ, Kirby JA, Cunningham AC. Role of the mucosal integrin alpha(E)(CD103)beta(7) in tissue-restricted cytotoxicity. Clin Exp Immunol. 2007; 149(1):162-170. (Pubitemid 46897095)
45. Hadley GA, Charandee C, Weir MR, Wang D, Bartlett ST, Drachenberg CB. CD103+ CTL accumulate within the graft epithelium during clinical renal allograft rejection. Transplantation. 2001;72(9):1548-1555. (Pubitemid 33095514)
46. Taunk J, Roberts AI, Ebert EC. Spontaneous cytotoxicity of human intraepithelial lymphocytes against epithelial cell tumors. Gastroenterology. 1992; 102(1):69-75.
47. La Gruta NL, Kedzierska K, Stambas J, Doherty PC. A question of self-preservation: immunopathology in influenza virus infection. Immunol Cell Biol. 2007;85(2):85-92. (Pubitemid 46398724)
48. Zhou J, Matsuoka M, Cantor H, Homer R, Enelow RI. Cutting edge: engagement of NKG2A on CD8+ effector T cells limits immunopathology in influenza pneumonia. J Immunol. 2008;180(1):25-29.
49. Epling-Burnette PK, et al. Dysregulated NK receptor expression in patients with lymphoproliferative disease of granular lymphocytes. Blood. 2004; 103(9):3431-3439. (Pubitemid 38525675)
50. Sheu BC, et al. Up-regulation of inhibitory natural killer receptors CD94/NKG2A with suppressed intracellular perforin expression of tumor-infiltrating CD8+ T lymphocytes in human cervical carcinoma. Cancer Res. 2005;65(7):2921-2929.
51. Welsh RM, Stepp SE, Szomolanyi-Tsuda E, Peacock CD. Tumor viral escape from inhibited T cells. Nat Immunol. 2002;3(2):112-114. (Pubitemid 34141438)
52. Freeman CM, et al. Cytotoxic potential of lung CD8(+) T cells increases with chronic obstructive pulmonary disease severity and with in vitro stimulation by IL-18 or IL-15. J Immunol. 2010;184(11):6504-6513.
53. Holt PG, et al. Extraction of immune and inflammatory cells from human lung parenchyma: evaluation of an enzymatic digestion procedure. Clin Exp Immunol. 1986;66(1):188-200. (Pubitemid 16020156)
54. van der Loos CM. Multiple immunoenzyme staining: methods and visualizations for the observation with spectral imaging. J Histochem Cytochem. 2008; 56(4):313-328.
55. van der Loos CM. Chromogens in multiple immunohistochemical staining used for visual assessment and spectral imaging: the colourful future. J Histotechnol. 2010;33(1):31-40.
56. de Jong R, Brouwer M, Rebel VI, van Seventer GA, Miedema F, van Lier RA. Generation of alloreactive cytolytic T lymphocytes by immobilized anti-CD3 monoclonal antibodies. Analysis of requirements for human cytolytic T-lymphocyte differentiation. Immunology. 1990;70(3):357-364. (Pubitemid 20212248)