Lipoarabinomannan-responsive polycytotoxic T cells are associated with protection in human tuberculosis

American Journal of Respiratory and Critical Care Medicine

Volumn 194, Issue 3, 2016, Pages 345-355

  Busch, Martin ^a   Herzmann, Christian ^b   Kallert, Stephanie ^a   Zimmermann, Andreas ^a   Hofer, Christoph ^a   Mayer, Daniel ^a   Zenk, Sebastian F ^a   Muche, Rainer ^c   Lange, Christoph ^b   Bloom, Barry R ^d   Modlin, Robert L ^e   Stenger, Steffen ^a  

^a UNIVERSITY HOSPITAL ULM   (Germany)

^b German Center for Infection Research   (Germany)

^c UNIVERSITY OF ULM   (Germany)

^d HARVARD SCHOOL OF PUBLIC HEALTH   (United States)

^e UNIVERSITY OF CALIFORNIA   (United States)

Author keywords

Cytotoxicity; Glycolipid antigens; Infectious immunology; Unconventional T cells

Indexed keywords

CD1 ANTIGEN; CD1B ANTIGEN; CD1C ANTIGEN; GAMMA INTERFERON; GRANULYSIN; GRANZYME B; LIPOARABINOMANNAN; MAJOR HISTOCOMPATIBILITY ANTIGEN CLASS 1; PERFORIN; T6 ANTIGEN; LIPOPOLYSACCHARIDE;

ANTIGEN PRESENTING CELL; ANTIGEN SPECIFICITY; ARTICLE; BACTERIAL GROWTH; BACTERIAL LOAD; BACTERIAL VIRULENCE; CELL SELECTION; CONTROLLED STUDY; CYTOKINE PRODUCTION; CYTOTOXIC T LYMPHOCYTE; FLOW CYTOMETRY; GROWTH INHIBITION; HUMAN; HUMAN CELL; IMMUNOGENICITY; INFECTION CONTROL; INFECTION PREVENTION; LATENT TUBERCULOSIS; LUNG LAVAGE; LUNG TUBERCULOSIS; LYMPHOCYTE COUNT; MULTICENTER STUDY (TOPIC); MYCOBACTERIUM TUBERCULOSIS; PERIPHERAL BLOOD MONONUCLEAR CELL; POLYCYTOTOXIC T LYMPHOCYTE; PRIORITY JOURNAL; PROSPECTIVE STUDY; T LYMPHOCYTE ACTIVATION; IMMUNOLOGY; T LYMPHOCYTE SUBPOPULATION; TUBERCULOSIS;

FLOW CYTOMETRY; HUMANS; LIPOPOLYSACCHARIDES; MYCOBACTERIUM TUBERCULOSIS; T-LYMPHOCYTE SUBSETS; TUBERCULOSIS;

EID: 84988985715     PISSN: 1073449X     EISSN: 15354970     Source Type: Journal    
DOI: 10.1164/rccm.201509-1746OC     Document Type: Article

References (39)

1. Salgame P, Geadas C, Collins L, Jones-Ló pez E, Ellner JJ. Latent tuberculosis infection-revisiting and revising concepts. Tuberculosis (Edinb) 2015;95:373-384.
2. Mack U, Migliori GB, Sester M, Rieder HL, Ehlers S, Goletti D, Bossink A, Magdorf K, Hö lscher C, Kampmann B, et al.; C. Lange; TBNET. LTBI: latent tuberculosis infection or lasting immune responses to M. tuberculosis? A TBNET consensus statement. Eur Respir J 2009;33: 956-973.
3. Heimbeck J. Incidence of tuberculosis in young adult women, with special reference to employment. Br J Tuberc 1938;32:154-166.
4. Andrews JR, Noubary F, Walensky RP, Cerda R, Losina E, Horsburgh CR. Risk of progression to active tuberculosis following reinfection with Mycobacterium tuberculosis. Clin Infect Dis 2012;54:784-791.
5. Zellweger JP, Sotgiu G, Block M, Dore S, Altet N, Blunschi R, Bogyi M, Bothamley G, Bothe C, Codecasa L, et al.; TBNET. Risk assessment of tuberculosis in contacts by IFN-g release assays: a Tuberculosis Network European Trials Group Study. Am J Respir Crit Care Med 2015;191:1176-1184.
6. 1 T cells. J Exp Med 2002;196:1473-1481.
7. Joosten SA, van Meijgaarden KE, van Weeren PC, Kazi F, Geluk A, Savage ND, Drijfhout JW, Flower DR, Hanekom WA, Klein MR, et al. Mycobacterium tuberculosis peptides presented by HLA-E molecules are targets for human CD8 T-cells with cytotoxic as well as regulatory activity. PLoS Pathog 2010;6:e1000782.
8. 1 T-cells recognizing peptides from Mycobacterium tuberculosis (Mtb) presented by HLA-E have an unorthodox Th2-like, multifunctional, Mtb inhibitory phenotype and represent a novel human T-cell subset. PLoS Pathog 2015;11:e1004671.
9. Gold MC, Napier RJ, Lewinsohn DM. MR1-restricted mucosal associated invariant T (MAIT) cells in the immune response to Mycobacterium tuberculosis. Immunol Rev 2015;264:154-166.
10. Van Rhijn I, Moody DB. CD1 and mycobacterial lipids activate human T cells. Immunol Rev 2015;264:138-153.
11. 1 T cells. Nature 1994;372:691-694.
12. Sieling PA, Chatterjee D, Porcelli SA, Prigozy TI, Mazzaccaro RJ, Soriano T, Bloom BR, Brenner MB, Kronenberg M, Brennan PJ, et al. CD1-restricted T cell recognition of microbial lipoglycan antigens. Science 1995;269:227-230.
13. Moody DB, Reinhold BB, Guy MR, Beckman EM, Frederique DE, Furlong ST, Ye S, Reinhold VN, Sieling PA, Modlin RL, et al. Structural requirements for glycolipid antigen recognition by CD1b-restricted T cells. Science 1997;278:283-286.
14. Gilleron M, Stenger S, Mazorra Z, Wittke F, Mariotti S, Bö hmer G, Prandi J, Mori L, Puzo G, De Libero G. Diacylated sulfoglycolipids are novel mycobacterial antigens stimulating CD1-restricted T cells during infection with Mycobacterium tuberculosis. J Exp Med 2004;199:649-659.
15. Moody DB, Young DC, Cheng TY, Rosat JP, Roura-Mir C, O'Connor PB, Zajonc DM, Walz A, Miller MJ, Levery SB, et al. T cell activation by lipopeptide antigens. Science 2004;303:527-531.
16. Layre E, Collmann A, Bastian M, Mariotti S, Czaplicki J, Prandi J, Mori L, Stenger S, De Libero G, Puzo G, et al. Mycolic acids constitute a scaffold for mycobacterial lipid antigens stimulating CD1-restricted T cells. Chem Biol 2009;16:82-92.
17. Stenger S, Hanson DA, Teitelbaum R, Dewan P, Niazi KR, Froelich CJ, Ganz T, Thoma-Uszynski S, Melián A, Bogdan C, et al. An antimicrobial activity of cytolytic T cells mediated by granulysin. Science 1998;282:121-125.
18. Stenger S, Mazzaccaro RJ, Uyemura K, Cho S, Barnes PF, Rosat JP, Sette A, Brenner MB, Porcelli SA, Bloom BR, et al. Differential effects of cytolytic T cell subsets on intracellular infection. Science 1997; 276:1684-1687.
19. Montamat-Sicotte DJ, Millington KA, Willcox CR, Hingley-Wilson S, Hackforth S, Innes J, Kon OM, Lammas DA, Minnikin DE, Besra GS, et al. A mycolic acid-specific CD1-restricted T cell population contributes to acute and memory immune responses in human tuberculosis infection. J Clin Invest 2011;121:2493-2503.
20. Herzmann C, Sotgiu G, Schaberg T, Ernst M, Stenger S, Lange C; German TB or Not TB Consortium. Early BCG vaccination is unrelated to pulmonary immunity against Mycobacterium tuberculosis in adults. Eur Respir J 2014;44:1087-1090.
21. Hä ussinger K, Ballin A, Becker HD, Bö lcskei P, Dierkesmann R, Dittrich I, Frank W, Freitag L, Gottschall R, Guschall WR, et al.; Working party on Recommendations for Quality Stanards in Endoscopy of the German Society of Pulmonology (Section Endoscopy). [Recommendations for quality standards in bronchoscopy] [in German]. Pneumologie 2004;58:344-356.
22. Walch M, Dotiwala F, Mulik S, Thiery J, Kirchhausen T, Clayberger C, Krensky AM, Martinvalet D, Lieberman J. Cytotoxic cells kill intracellular bacteria through granulysin-mediated delivery of granzymes. Cell 2014;157:1309-1323.
23. 1 T cell-mediated antimicrobial activity against Mycobacterium tuberculosis in humans. J Clin Invest 2009;119:1167-1177.
24. 1 T cells are functionally and phenotypically different between latent infection and active disease. Eur J Immunol 2013;43:1568-1577.
25. Ernst WA, Thoma-Uszynski S, Teitelbaum R, Ko C, Hanson DA, Clayberger C, Krensky AM, Leippe M, Bloom BR, Ganz T, et al. Granulysin, a T cell product, kills bacteria by altering membrane permeability. J Immunol 2000;165:7102-7108.
26. Di Liberto D, Buccheri S, Caccamo N, Meraviglia S, Romano A, Di Carlo P, Titone L, Dieli F, Krensky AM, Salerno A. Decreased serum granulysin levels in childhood tuberculosis which reverse after therapy. Tuberculosis (Edinb) 2007;87:322-328.
27. 1 T cells as candidate immune marker for tuberculosis during childhood and adolescence. PLoS One 2011;6:e29367.
28. Ochoa MT, Stenger S, Sieling PA, Thoma-Uszynski S, Sabet S, Cho S, Krensky AM, Rollinghoff M, Nunes Sarno E, Burdick AE, et al. T-cell release of granulysin contributes to host defense in leprosy. Nat Med 2001;7:174-179.
29. 1 regulatory T cells in the granulomatous lesions. Am J Pathol 2009;174:2211-2224.
30. Rahman S, Magalhaes I, Rahman J, Ahmed RK, Sizemore DR, Scanga CA, Weichold F, Verreck F, Kondova I, Sadoff J, et al. Prime-boost vaccination with rBCG/rAd35 enhances CD8? cytolytic T-cell responses in lesions from Mycobacterium tuberculosis-infected primates. Mol Med 2012;18:647-658.
31. Ma J, Lu J, Huang H, Teng X, Tian M, Yu Q, Yuan X, Jing Y, Shi C, Li J, et al. Inhalation of recombinant adenovirus expressing granulysin protects mice infected with Mycobacterium tuberculosis. Gene Ther 2015;22:968-976.
32. 2T lymphocytes to a microbial antigen. Nature 1992; 360:593-597.
33. 1 ab T cell pool. J Immunol 1999;162:366-371.
34. Van Rhijn I, Kasmar A, de Jong A, Gras S, Bhati M, Doorenspleet ME, de Vries N, Godfrey DI, Altman JD, de Jager W, et al. A conserved human T cell population targets mycobacterial antigens presented by CD1b. Nat Immunol 2013;14:706-713.
35. Kasmar AG, van Rhijn I, Cheng TY, Turner M, Seshadri C, Schiefner A, Kalathur RC, Annand JW, de Jong A, Shires J, et al. CD1b tetramers bind ab T cell receptors to identify a mycobacterial glycolipid-reactive T cell repertoire in humans. J Exp Med 2011;208:1741-1747.
36. Solovic I, Sester M, Gomez-Reino JJ, Rieder HL, Ehlers S, Milburn HJ, Kampmann B, Hellmich B, Groves R, Schreiber S, et al. The risk of tuberculosis related to tumour necrosis factor antagonist therapies: a TBNET consensus statement. Eur Respir J 2010;36:1185-1206.
37. Bloom CI, Graham CM, Berry MP, Wilkinson KA, Oni T, Rozakeas F, Xu Z, Rossello-Urgell J, Chaussabel D, Banchereau J, et al. Detectable changes in the blood transcriptome are present after two weeks of antituberculosis therapy. PLoS One 2012;7:e46191.
38. 1 T cells in human tuberculosis. Proc Natl Acad Sci USA 2000;97:12210-12215.
39. Le Bourhis L, Dusseaux M, Bohineust A, Bessoles S, Martin E, Premel V, Coré M, Sleurs D, Serriari NE, Treiner E, et al. MAIT cells detect and efficiently lyse bacterially-infected epithelial cells. PLoS Pathog 2013;9:e1003681.