MAIT cells are critical for optimal mucosal immune responses during in vivo pulmonary bacterial infection

Proceedings of the National Academy of Sciences of the United States of America

Volumn 110, Issue 33, 2013, Pages

  Meierovics, Anda ^a   Yankelevich, Wei Jen Chua ^a   Cowley, Siobhán C ^a  

^a CENTER FOR BIOLOGICS EVALUATION AND RESEARCH   (United States)

Author keywords

Respiratory infection; Tularemia

Indexed keywords

GAMMA INTERFERON; INTERLEUKIN 12; INTERLEUKIN 12P40; INTERLEUKIN 17; LIVE VACCINE; MAJOR HISTOCOMPATIBILITY ANTIGEN; T LYMPHOCYTE RECEPTOR ALPHA CHAIN; TUMOR NECROSIS FACTOR ALPHA;

ADAPTIVE IMMUNITY; ANIMAL CELL; ANIMAL EXPERIMENT; ANIMAL MODEL; ANTIGEN PRESENTING CELL; ARTICLE; BACTERIAL INFECTION; BACTERIAL LOAD; CELL SUSPENSION; CELLULAR IMMUNITY; CONTROLLED STUDY; CYTOKINE PRODUCTION; CYTOKINE RELEASE; FEMALE; FRANCISELLA TULARENSIS; IN VITRO STUDY; IN VIVO STUDY; INNATE IMMUNITY; LUNG INFECTION; MACROPHAGE ACTIVATION; MALE; MEDIASTINUM LYMPH NODE; MESENTERY LYMPH NODE; MOUSE; MUCOSA ASSOCIATED INVARIANT T LYMPHOCYTE; MUCOSAL IMMUNITY; NONHUMAN; PRIORITY JOURNAL; T LYMPHOCYTE; T LYMPHOCYTE ACTIVATION; T LYMPHOCYTE SUBPOPULATION;

RESPIRATORY INFECTION; TULAREMIA;

ANIMALS; FEMALE; FLOW CYTOMETRY; IMMUNITY, MUCOSAL; LUNG; MALE; MICE; MICE, INBRED C57BL; NATURAL KILLER T-CELLS; REAL-TIME POLYMERASE CHAIN REACTION; RESPIRATORY MUCOSA; TULAREMIA;

EID: 84882380657     PISSN: 00278424     EISSN: 10916490     Source Type: Journal    
DOI: 10.1073/pnas.1302799110     Document Type: Article

References (53)

1. Colmone A, Wang CR (2006) H2-M3-restricted T cell response to infection. Microbes Infect 8(8):2277-2283.
2. Kerksiek KM, Busch DH, Pilip IM, Allen SE, Pamer EG (1999) H2-M3-restricted T cells in bacterial infection: Rapid primary but diminished memory responses. J Exp Med 190(2):195-204.
3. Seaman MS, Wang CR, Forman J (2000) MHC class Ib-restricted CTL provide protection against primary and secondary Listeria monocytogenes infection. J Immunol 165(9): 5192-5201.
4. Chiba A, Dascher CC, Besra GS, Brenner MB (2008) Rapid NKT cell responses are selfterminating during the course of microbial infection. J Immunol 181(4):2292-2302.
5. Brigl M, et al. (2011) Innate and cytokine-driven signals, rather than microbial antigens, dominate in natural killer T cell activation during microbial infection. J Exp Med 208(6):1163-1177.
6. Brossay L, et al. (1998) CD1d-mediated recognition of an alpha-galactosylceramide by natural killer T cells is highly conserved through mammalian evolution. J Exp Med 188(8):1521-1528.
7. Treiner E, et al. (2003) Selection of evolutionarily conserved mucosal-associated invariant T cells by MR1. Nature 422(6928):164-169.
8. Martin E, et al. (2009) Stepwise development of MAIT cells in mouse and human. PLoS Biol 7(3):e54.
9. Porcelli S, Yockey CE, Brenner MB, Balk SP (1993) Analysis of T cell antigen receptor (TCR) expression by human peripheral blood CD4-8-alpha/beta T cells demonstrates preferential use of several V beta genes and an invariant TCR alpha chain. J Exp Med 178(1):1-16.
10. Tilloy F, et al. (1999) An invariant T cell receptor alpha chain defines a novel TAPindependent major histocompatibility complex class Ib-restricted alpha/beta T cell subpopulation in mammals. J Exp Med 189(12):1907-1921.
11. Gapin L (2009) Where do MAIT cells fit in the family of unconventional T cells? PLoS Biol 7(3):e70.
12. Young MH, et al. (2013) MAIT cell recognition of MR1 on bacterially infected and uninfected cells. PLoS ONE 8(1):e53789.
13. Huang S, et al. (2009) MR1 antigen presentation to mucosal-associated invariant T cells was highly conserved in evolution. Proc Natl Acad Sci USA 106(20):8290-8295.
14. Tsukamoto K, Deakin JE, Graves JA, Hashimoto K (2013) Exceptionally high conservation of the MHC class I-related gene, MR1, among mammals. Immunogenetics 65(2): 115-124.
15. Huang S, et al. (2005) Evidence for MR1 antigen presentation to mucosal-associated invariant T cells. J Biol Chem 280(22):21183-21193.
16. Kjer-Nielsen L, et al. (2012) MR1 presents microbial vitamin B metabolites to MAIT cells. Nature 491(7426):717-723.
17. Le Bourhis L, et al. (2010) Antimicrobial activity of mucosal-associated invariant T cells. Nat Immunol 11(8):701-708.
18. Gold MC, et al. (2010) Human mucosal associated invariant T cells detect bacterially infected cells. PLoS Biol 8(6):e1000407.
19. Chua WJ, et al. (2012) Polyclonal mucosa-associated invariant T cells have unique innate functions in bacterial infection. Infect Immun 80(9):3256-3267.
20. Georgel P, Radosavljevic M, Macquin C, Bahram S (2011) The non-conventional MHC class I MR1 molecule controls infection by Klebsiella pneumoniae in mice. Mol Immunol 48(5):769-775.
21. Gold MC, Lewinsohn DM (2013) Co-dependents: MR1-restricted MAIT cells and their antimicrobial function. Nat Rev Microbiol 11(1):14-19.
22. Ellis J, Oyston PC, Green M, Titball RW (2002) Tularemia. Clin Microbiol Rev 15(4): 631-646.
23. Dennis DT, et al.; Working Group on Civilian Biodefense (2001) Tularemia as a biological weapon: Medical and public health management. JAMA 285(21): 2763-2773.
24. Cowley SC, Meierovics AI, Frelinger JA, Iwakura Y, Elkins KL (2010) Lung CD4-CD8-double-negative T cells are prominent producers of IL-17A and IFN-gamma during primary respiratory murine infection with Francisella tularensis live vaccine strain. J Immunol 184(10):5791-5801.
25. Kawachi I, Maldonado J, Strader C, Gilfillan S (2006) MR1-restricted V alpha 19i mucosal-associated invariant T cells are innate T cells in the gut lamina propria that provide a rapid and diverse cytokine response. J Immunol 176(3):1618-1627.
26. Slight SR, Khader SA (2013) Chemokines shape the immune responses to tuberculosis. Cytokine Growth Factor Rev 24(2):105-113.
27. Kadioglu A, et al. (2011) The integrins Mac-1 and alpha4beta1 perform crucial roles in neutrophil and T cell recruitment to lungs during Streptococcus pneumoniae infection. J Immunol 186(10):5907-5915.
28. Elkins KL, Rhinehart-Jones TR, Culkin SJ, Yee D, Winegar RK (1996) Minimal requirements for murine resistance to infection with Francisella tularensis LVS. Infect Immun 64(8): 3288-3293.
29. Lin Y, et al. (2009) Interleukin-17 is required for T helper 1 cell immunity and host resistance to the intracellular pathogen Francisella tularensis. Immunity 31(5):799-810.
30. Lindgren H, Stenmark S, Chen W, Tärnvik A, Sjöstedt A (2004) Distinct roles of reactive nitrogen and oxygen species to control infection with the facultative intracellular bacterium Francisella tularensis. Infect Immun 72(12):7172-7182.
31. Cowley SC, Elkins KL (2003) Multiple T cell subsets control Francisella tularensis LVS intracellular growth without stimulation through macrophage interferon gamma receptors. J Exp Med 198(3):379-389.
32. Cowley SC, Sedgwick JD, Elkins KL (2007) Differential requirements by CD4+ and CD8+ T cells for soluble and membrane TNF in control of Francisella tularensis live vaccine strain intramacrophage growth. J Immunol 179:7709-7719.
33. Yee D, Rhinehart-Jones TR, Elkins KL (1996) Loss of either CD4+ or CD8+ T cells does not affect the magnitude of protective immunity to an intracellular pathogen, Francisella tularensis strain LVS. J Immunol 157(11):5042-5048.
34. Conlan JW, Sjöstedt A, North RJ (1994) CD4+ and CD8+ T-cell-dependent and-independent host defense mechanisms can operate to control and resolve primary and secondary Francisella tularensis LVS infection in mice. Infect Immun 62(12): 5603-5607.
35. Cowley SC, et al. (2005) CD4-CD8-T cells control intracellular bacterial infections both in vitro and in vivo. J Exp Med 202(2):309-319.
36. Matsuda JL, et al. (2002) Homeostasis of V alpha 14i NKT cells. Nat Immunol 3(10): 966-974.
37. Savage AK, et al. (2008) The transcription factor PLZF directs the effector program of the NKT cell lineage. Immunity 29(3):391-403.
38. Gold MC, et al. (2013) Human thymic MR1-restricted MAIT cells are innate pathogenreactive effectors that adapt following thymic egress. Mucosal Immunol 6(1):35-44.
39. Dusseaux M, et al. (2011) Human MAIT cells are xenobiotic-resistant, tissue-targeted, CD161hi IL-17-secreting T cells. Blood 117(4):1250-1259.
40. Olszak T, et al. (2012) Microbial exposure during early life has persistent effects on natural killer T cell function. Science 336(6080):489-493.
41. Gérart S, et al. (2013) Human iNKT and MAIT cells exhibit a PLZF-dependent proapoptotic propensity that is counterbalanced by XIAP. Blood 121(4):614-623.
42. Mempel M, et al. (2000) Comparison of the T cell patterns in leprous and cutaneous sarcoid granulomas. Presence of Valpha24-invariant natural killer T cells in T-cellreactive leprosy together with a highly biased T cell receptor Valpha repertoire. Am J Pathol 157(2):509-523.
43. Elkins KL, Rhinehart-Jones T, Nacy CA, Winegar RK, FortierAH(1993) T-cell-independent resistance to infection and generation of immunity to Francisella tularensis. Infect Immun 61(3):823-829.
44. Leeansyah E, et al. (2013) Activation, exhaustion, and persistent decline of the antimicrobial MR1-restricted MAIT-cell population in chronic HIV-1 infection. Blood 121(7):1124-1135.
45. Cosgrove C, et al. (2012) Early and non-reversible decrease of CD161++/MAIT cells in HIV infection. Blood 121:951-961.
46. Tupin E, Kinjo Y, Kronenberg M (2007) The unique role of natural killer T cells in the response to microorganisms. Nat Rev Microbiol 5(6):405-417.
47. Santic M, Molmeret M, Klose KE, Abu Kwaik Y (2006) Francisella tularensis travels a novel, twisted road within macrophages. Trends Microbiol 14(1):37-44.
48. Deretic V, Via LE, Fratti RA, Deretic D (1997) Mycobacterial phagosome maturation, rab proteins, and intracellular trafficking. Electrophoresis 18(14):2542-2547.
49. Brigl M, Brenner MB (2004) CD1: Antigen presentation and T cell function. Annu Rev Immunol 22:817-890.
50. Kronenberg M (2005) Toward an understanding of NKT cell biology: Progress and paradoxes. Annu Rev Immunol 23:877-900.
51. Bendelac A, Savage PB, Teyton L (2007) The biology of NKT cells. Annu Rev Immunol 25:297-336.
52. Gopal R, et al. (2012) IL-23-dependent IL-17 drives Th1-cell responses following Mycobacterium bovis BCG vaccination. Eur J Immunol 42(2):364-373.
53. Cowley SC, Elkins KL (2011) Immunity to francisella. Front Microbiol 2(26):26.