Functional heterogeneity and antimycobacterial effects of mouse mucosal-associated invariant T cells specific for riboflavin metabolites

Journal of Immunology

Volumn 195, Issue 2, 2015, Pages 587-601

  Sakala, Isaac G ^a,b   Kjer Nielsen, Lars ^c   Eickhoff, Christopher S ^a   Wang, Xiaoli ^b   Blazevic, Azra ^a   Liu, Ligong ^d   Fairlie, David P ^d   Rossjohn, Jamie ^e,f   McCluskey, James ^c   Fremont, Daved H ^b   Hansen, Ted H ^b   Hoft, Daniel F ^a  

^a SAINT LOUIS UNIVERSITY SCHOOL OF MEDICINE   (United States)

^b WASHINGTON UNIVERSITY SCHOOL OF MEDICINE   (United States)

^c UNIVERSITY OF MELBOURNE   (Australia)

^d UNIVERSITY OF QUEENSLAND   (Australia)

^e MONASH UNIVERSITY   (Australia)

^f CARDIFF UNIVERSITY SCHOOL OF MEDICINE   (United Kingdom)

Author keywords

[No Author keywords available]

Indexed keywords

CD4 ANTIGEN; CD69 ANTIGEN; CD8 ANTIGEN; CHEMOKINE RECEPTOR CXCR3; CYTOKINE; HERMES ANTIGEN; INTERLEUKIN 12; INTERLEUKIN 18; MAJOR HISTOCOMPATIBILITY ANTIGEN CLASS 1; PROTEIN MR1; PROTEIN NK1.1; RIBITYLLUMAZINE; RIBOFLAVIN DERIVATIVE; T LYMPHOCYTE RECEPTOR; TETRAMER; UNCLASSIFIED DRUG; VERY LATE ACTIVATION ANTIGEN 4; CD44 PROTEIN, MOUSE; CXCR3 PROTEIN, MOUSE; HLA ANTIGEN CLASS 1; KLRB1C PROTEIN, MOUSE; LECTIN; LEUKOCYTE ANTIGEN; LY ANTIGEN; LYMPHOCYTE ANTIGEN RECEPTOR; MR1 PROTEIN, MOUSE; NATURAL KILLER CELL LECTIN LIKE RECEPTOR SUBFAMILY B; RIBOFLAVIN; T LYMPHOCYTE ANTIGEN;

ANIMAL CELL; ANIMAL EXPERIMENT; ANIMAL MODEL; ANIMAL TISSUE; ARTICLE; CELL HETEROGENEITY; CELL SPECIFICITY; CONTROLLED STUDY; EFFECTOR CELL; IN VITRO STUDY; LUNG INFECTION; MEMORY T LYMPHOCYTE; MOUSE; MUCOSA CELL; MUCOSAL ASSOCIATED INVARIANT T CELL; MYCOBACTERIOSIS; NONHUMAN; PRIORITY JOURNAL; PROTEIN EXPRESSION; PROTEIN FUNCTION; T LYMPHOCYTE; TRANSGENIC MOUSE; TUBERCULOSIS; WILD TYPE; ANALOGS AND DERIVATIVES; ANIMAL; C57BL MOUSE; CD4+ T LYMPHOCYTE; CD8+ T LYMPHOCYTE; CELL CULTURE; DRUG EFFECTS; GENE EXPRESSION REGULATION; GENETIC HETEROGENEITY; GENETICS; IMMUNOLOGICAL MEMORY; IMMUNOLOGY; KNOCKOUT MOUSE; LUNG; MICROBIOLOGY; MUCOSAL IMMUNITY; MYCOBACTERIUM BOVIS; PATHOLOGY; PROTEIN MULTIMERIZATION; SIGNAL TRANSDUCTION; VETERINARY;

ANIMALS; ANTIGENS, CD; ANTIGENS, CD44; ANTIGENS, DIFFERENTIATION, T-LYMPHOCYTE; ANTIGENS, LY; CD4-POSITIVE T-LYMPHOCYTES; CD8-POSITIVE T-LYMPHOCYTES; CELLS, CULTURED; GENE EXPRESSION REGULATION, DEVELOPMENTAL; GENETIC HETEROGENEITY; HISTOCOMPATIBILITY ANTIGENS CLASS I; IMMUNITY, MUCOSAL; IMMUNOLOGIC MEMORY; INTEGRIN ALPHA4BETA1; INTERLEUKIN-12; INTERLEUKIN-18; LECTINS, C-TYPE; LUNG; MICE; MICE, INBRED C57BL; MICE, KNOCKOUT; MYCOBACTERIUM BOVIS; NK CELL LECTIN-LIKE RECEPTOR SUBFAMILY B; PROTEIN MULTIMERIZATION; RECEPTORS, ANTIGEN, T-CELL, ALPHA-BETA; RECEPTORS, CXCR3; RIBOFLAVIN; SIGNAL TRANSDUCTION; TUBERCULOSIS;

EID: 84936817615     PISSN: 00221767     EISSN: 15506606     Source Type: Journal    
DOI: 10.4049/jimmunol.1402545     Document Type: Article

References (83)

1. Hashimoto, K., M. Hirai, and Y. Kurosawa. 1995. A gene outside the human MHC related to classical HLA class I genes. Science 269: 693-695.
2. Kjer-Nielsen, L., O. Patel, A. J. Corbett, J. Le Nours, B. Meehan, L. Liu, M. Bhati, Z. Chen, L. Kostenko, R. Reantragoon, et al. 2012. MR1 presents microbial vitamin B metabolites to MAIT cells. Nature 491: 717-723.
3. Patel, O., L. Kjer-Nielsen, J. Le Nours, S. B. Eckle, R. Birkinshaw, T. Beddoe, A. J. Corbett, L. Liu, J. J. Miles, B. Meehan, et al. 2013. Recognition of vitamin B metabolites by mucosal-associated invariant T cells. Nat. Commun. 4: 2142.
4. Reantragoon, R., A. J. Corbett, I. G. Sakala, N. A. Gherardin, J. B. Furness, Z. Chen, S. B. Eckle, A. P. Uldrich, R. W. Birkinshaw, O. Patel, et al. 2013. Antigen-loaded MR1 tetramers define T cell receptor heterogeneity in mucosal-associated invariant T cells. J. Exp. Med. 210: 2305-2320.
5. Birkinshaw, R. W., L. Kjer-Nielsen, S. B. Eckle, J. McCluskey, and J. Rossjohn. 2014. MAITs, MR1 and vitamin B metabolites. Curr. Opin. Immunol. 26: 7-13.
6. Corbett, A. J., S. B. Eckle, R. W. Birkinshaw, L. Liu, O. Patel, J. Mahony, Z. Chen, R. Reantragoon, B. Meehan, H. Cao, et al. 2014. T-cell activation by transitory neo-antigens derived from distinct microbial pathways. Nature 509: 361-365.
7. McWilliam, H. E., R. W. Birkinshaw, J. A. Villadangos, J. McCluskey, and J. Rossjohn. 2015. MR1 presentation of vitamin B-based metabolite ligands. Curr. Opin. Immunol. 34C: 28-34.
8. Tilloy, F., E. Treiner, S. H. Park, C. Garcia, F. Lemonnier, H. de la Salle, A. Bendelac, M. Bonneville, and O. Lantz. 1999. An invariant T cell receptor alpha chain defines a novel TAP-independent major histocompatibility complex class Ib-restricted alpha/beta T cell subpopulation in mammals. J. Exp. Med. 189: 1907-1921.
9. Rossjohn, J., S. Gras, J. J. Miles, S. J. Turner, D. I. Godfrey, and J. McCluskey. 2015. T cell antigen receptor recognition of antigen-presenting molecules. Annu. Rev. Immunol. 33: 169-200.
10. Gold, M. C., and D. M. Lewinsohn. 2013. Co-dependents: MR1-restricted MAIT cells and their antimicrobial function. Nat. Rev. Microbiol. 11: 14-19.
11. Reantragoon, R., L. Kjer-Nielsen, O. Patel, Z. Chen, P. T. Illing, M. Bhati, L. Kostenko, M. Bharadwaj, B. Meehan, T. H. Hansen, et al. 2012. Structural insight into MR1-mediated recognition of the mucosal associated invariant T cell receptor. J. Exp. Med. 209: 761-774.
12. Eckle, S. B., R. W. Birkinshaw, L. Kostenko, A. J. Corbett, H. E. McWilliam, R. Reantragoon, Z. Chen, N. A. Gherardin, T. Beddoe, L. Liu, et al. 2014. A molecular basis underpinning the T cell receptor heterogeneity of mucosal-associated invariant T cells. J. Exp. Med. 211: 1585-1600.
13. Martin, E., E. Treiner, L. Duban, L. Guerri, H. Laude, C. Toly, V. Premel, A. Devys, I. C. Moura, F. Tilloy, et al. 2009. Stepwise development of MAIT cells in mouse and human. PLoS Biol. 7: e54.
14. Okamoto, N., O. Kanie, Y. Y. Huang, R. Fujii, H. Watanabe, and M. Shimamura. 2005. Synthetic alpha-mannosyl ceramide as a potent stimulant for an NKT cell repertoire bearing the invariant Valpha19-Jalpha26 TCR alpha chain. Chem. Biol. 12: 677-683.
15. Gold, M. C., J. E. McLaren, J. A. Reistetter, S. Smyk-Pearson, K. Ladell, G. M. Swarbrick, Y. Y. Yu, T. H. Hansen, O. Lund, M. Nielsen, et al. 2014. MR1-restricted MAIT cells display ligand discrimination and pathogen selectivity through distinct T cell receptor usage. J. Exp. Med. 211: 1601-1610.
16. Greenaway, H. Y., B. Ng, D. A. Price, D. C. Douek, M. P. Davenport, and V. Venturi. 2013. NKT and MAIT invariant TCRa sequences can be produced efficiently by VJ gene recombination. Immunobiology 218: 213-224.
17. Riegert, P., V. Wanner, and S. Bahram. 1998. Genomics, isoforms, expression, and phylogeny of the MHC class I-related MR1 gene. J. Immunol. 161: 4066-4077.
18. Huang, S., E. Martin, S. Kim, L. Yu, C. Soudais, D. H. Fremont, O. Lantz, and T. H. Hansen. 2009. MR1 antigen presentation to mucosal-associated invariant T cells was highly conserved in evolution. Proc. Natl. Acad. Sci. USA 106: 8290-8295.
19. Gold, M. C., S. Cerri, S. Smyk-Pearson, M. E. Cansler, T. M. Vogt, J. Delepine, E. Winata, G. M. Swarbrick, W. J. Chua, Y. Y. Yu, et al. 2010. Human mucosal associated invariant T cells detect bacterially infected cells. PLoS Biol. 8: e1000407.
20. Le Bourhis, L., E. Martin, I. Péguillet, A. Guihot, N. Froux, M. Coré, E. Lévy, M. Dusseaux, V. Meyssonnier, V. Premel, et al. 2010. Antimicrobial activity of mucosal-associated invariant T cells. Nat. Immunol. 11: 701-708.
21. Billerbeck, E., Y. H. Kang, L. Walker, H. Lockstone, S. Grafmueller, V. Fleming, J. Flint, C. B. Willberg, B. Bengsch, B. Seigel, et al. 2010. Analysis of CD161 expression on human CD8+ T cells defines a distinct functional subset with tissue-homing properties. Proc. Natl. Acad. Sci. USA 107: 3006-3011.
22. Dusseaux, M., E. Martin, N. Serriari, I. Péguillet, V. Premel, D. Louis, M. Milder, L. Le Bourhis, C. Soudais, E. Treiner, and O. Lantz. 2011. Human MAIT cells are xenobiotic-resistant, tissue-targeted, CD161hi IL-17-secreting T cells. Blood 117: 1250-1259.
23. Northfield, J. W., V. Kasprowicz, M. Lucas, N. Kersting, B. Bengsch, A. Kim, R. E. Phillips, B. D. Walker, R. Thimme, G. Lauer, and P. Klenerman. 2008. CD161 expression on hepatitis C virus-specific CD8+ T cells suggests a distinct pathway of T cell differentiation. Hepatology 47: 396-406.
24. Chua, W. J., S. M. Truscott, C. S. Eickhoff, A. Blazevic, D. F. Hoft, and T. H. Hansen. 2012. Polyclonal mucosa-associated invariant T cells have unique innate functions in bacterial infection. Infect. Immun. 80: 3256-3267.
25. Kawachi, I., J. Maldonado, C. Strader, and S. Gilfillan. 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: 1618-1627.
26. Gold, M. C., R. J. Napier, and D. M. Lewinsohn. 2015. MR1-restricted mucosal associated invariant T (MAIT) cells in the immune response to Mycobacterium tuberculosis. Immunol. Rev. 264: 154-166.
27. Cosgrove, C., J. E. Ussher, A. Rauch, K. Gärtner, A. Kurioka, M. H. Hühn, K. Adelmann, Y. H. Kang, J. R. Fergusson, P. Simmonds, et al. 2013. Early and nonreversible decrease of CD161++/MAIT cells in HIV infection. Blood 121: 951-961.
28. Leeansyah, E., A. Ganesh, M. F. Quigley, A. Sönnerborg, J. Andersson, P. W. Hunt, M. Somsouk, S. G. Deeks, J. N. Martin, M. Moll, et al. 2013. Activation, exhaustion, and persistent decline of the antimicrobial MR1-restricted MAIT-cell population in chronic HIV-1 infection. Blood 121: 1124-1135.
29. Wong, E. B., N. A. Akilimali, P. Govender, Z. A. Sullivan, C. Cosgrove, M. Pillay, D. M. Lewinsohn, W. R. Bishai, B. D. Walker, T. Ndung'u, et al. 2013. Low levels of peripheral CD161++CD8+ mucosal associated invariant T (MAIT) cells are found in HIV and HIV/TB co-infection. PLoS ONE 8: e83474.
30. Fernandez, C. S., T. Amarasena, A. D. Kelleher, J. Rossjohn, J. McCluskey, D. I. Godfrey, and S. J. Kent. 2015. MAIT cells are depleted early but retain functional cytokine expression in HIV infection. Immunol. Cell Biol. 93: 177-188.
31. Miyazaki, Y., S. Miyake, A. Chiba, O. Lantz, and T. Yamamura. 2011. Mucosal-associated invariant T cells regulate Th1 response in multiple sclerosis. Int. Immunol. 23: 529-535.
32. Annibali, V., G. Ristori, D. F. Angelini, B. Serafini, R. Mechelli, S. Cannoni, S. Romano, A. Paolillo, H. Abderrahim, A. Diamantini, et al. 2011. CD161(high) CD8+T cells bear pathogenetic potential in multiple sclerosis. Brain 134: 542-554.
33. Serriari, N. E., M. Eoche, L. Lamotte, J. Lion, M. Fumery, P. Marcelo, D. Chatelain, A. Barre, E. Nguyen-Khac, O. Lantz, et al. 2014. Innate mucosal-associated invariant T (MAIT) cells are activated in inflammatory bowel diseases. Clin. Exp. Immunol. 176: 266-274.
34. Magalhaes, I., K. Pingris, C. Poitou, S. Bessoles, N. Venteclef, B. Kiaf, L. Beaudoin, J. Da Silva, O. Allatif, J. Rossjohn, et al. 2015. Mucosal-associated invariant T cell alterations in obese and type 2 diabetic patients. J. Clin. Invest. 125: 1752-1762.
35. Treiner, E., L. Duban, S. Bahram, M. Radosavljevic, V. Wanner, F. Tilloy, P. Affaticati, S. Gilfillan, and O. Lantz. 2003. Selection of evolutionarily conserved mucosal-associated invariant T cells by MR1. Nature 422: 164-169.
36. Georgel, P., M. Radosavljevic, C. Macquin, and S. Bahram. 2011. The non-conventional MHC class I MR1 molecule controls infection by Klebsiella pneumoniae in mice. Mol. Immunol. 48: 769-775.
37. Meierovics, A., W. J. Yankelevich, and S. C. Cowley. 2013. MAIT cells are critical for optimal mucosal immune responses during in vivo pulmonary bacterial infection. Proc. Natl. Acad. Sci. USA 110: E3119-E3128.
38. Croxford, J. L., S. Miyake, Y. Y. Huang, M. Shimamura, and T. Yamamura. 2006. Invariant V(alpha)19i T cells regulate autoimmune inflammation. Nat. Immunol. 7: 987-994.
39. Walker, L. J., Y. H. Kang, M. O. Smith, H. Tharmalingham, N. Ramamurthy, V. M. Fleming, N. Sahgal, A. Leslie, Y. Oo, A. Geremia, et al. 2012. Human MAIT and CD8aa cells develop from a pool of type-17 precommitted CD8+ T cells. Blood 119: 422-433.
40. Pérarnau, B., M. F. Saron, B. Reina San Martin, N. Bervas, H. Ong, M. J. Soloski, A. G. Smith, J. M. Ure, J. E. Gairin, and F. A. Lemonnier. 1999. Single H2Kb, H2Db and double H2KbDb knockout mice: peripheral CD8+ T cell repertoire and anti-lymphocytic choriomeningitis virus cytolytic responses. Eur. J. Immunol. 29: 1243-1252.
41. Fang, X., P. Du, Y. Liu, and J. Tang. 2010. Efficient isolation of mouse liver NKT cells by perfusion. PLoS ONE 5: e10288.
42. Huang, S., S. Gilfillan, M. Cella, M. J. Miley, O. Lantz, L. Lybarger, D. H. Fremont, and T. H. Hansen. 2005. Evidence for MR1 antigen presentation to mucosal-associated invariant T cells. J. Biol. Chem. 280: 21183-21193.
43. Huang, S., S. Gilfillan, S. Kim, B. Thompson, X. Wang, A. J. Sant, D. H. Fremont, O. Lantz, and T. H. Hansen. 2008. MR1 uses an endocytic pathway to activate mucosal-associated invariant T cells. J. Exp. Med. 205: 1201-1211.
44. Miley, M. J., S. M. Truscott, Y. Y. Yu, S. Gilfillan, D. H. Fremont, T. H. Hansen, and L. Lybarger. 2003. Biochemical features of the MHC-related protein 1 consistent with an immunological function. J. Immunol. 170: 6090-6098.
45. Worku, S., and D. F. Hoft. 2003. Differential effects of control and antigen-specific T cells on intracellular mycobacterial growth. Infect. Immun. 71: 1763-1773.
46. Godfrey, D. I., M. Masciantonio, C. L. Tucek, M. A. Malin, R. L. Boyd, and P. Hugo. 1992. Thymic shared antigen-1. A novel thymocyte marker discriminating immature from mature thymocyte subsets. J. Immunol. 148: 2006-2011.
47. Lepore, M., A. Kalinichenko, A. Colone, B. Paleja, A. Singhal, A. Tschumi, B. Lee, M. Poidinger, F. Zolezzi, L. Quagliata, et al. 2014. Parallel T-cell cloning and deep sequencing of human MAIT cells reveal stable oligoclonal TCRb repertoire. Nat. Commun. 5: 3866.
48. Baldwin, T. A., M. M. Sandau, S. C. Jameson, and K. A. Hogquist. 2005. The timing of TCR alpha expression critically influences T cell development and selection. J. Exp. Med. 202: 111-121.
49. Huang, C. Y., and O. Kanagawa. 2004. Impact of early expression of TCR alpha chain on thymocyte development. Eur. J. Immunol. 34: 1532-1541.
50. Ussher, J. E., M. Bilton, E. Attwod, J. Shadwell, R. Richardson, C. de Lara, E. Mettke, A. Kurioka, T. H. Hansen, P. Klenerman, and C. B. Willberg. 2014. CD161++ CD8+ T cells, including the MAIT cell subset, are specifically acti vated by IL-12+IL-18 in a TCR-independent manner. Eur. J. Immunol. 44: 195-203.
51. Fehniger, T. A., M. H. Shah, M. J. Turner, J. B. VanDeusen, S. P. Whitman, M. A. Cooper, K. Suzuki, M. Wechser, F. Goodsaid, and M. A. Caligiuri. 1999. Differential cytokine and chemokine gene expression by human NK cells following activation with IL-18 or IL-15 in combination with IL-12: implications for the innate immune response. J. Immunol. 162: 4511-4520.
52. Velázquez, P., T. O. Cameron, Y. Kinjo, N. Nagarajan, M. Kronenberg, and M. L. Dustin. 2008. Cutting edge: activation by innate cytokines or microbial antigens can cause arrest of natural killer T cell patrolling of liver sinusoids. J. Immunol. 180: 2024-2028.
53. Tomura, M., S. Maruo, J. Mu, X. Y. Zhou, H. J. Ahn, T. Hamaoka, H. Okamura, K. Nakanishi, S. Clark, M. Kurimoto, and H. Fujiwara. 1998. Differential capacities of CD4+, CD8+, and CD4-CD8-T cell subsets to express IL-18 receptor and produce IFN-gamma in response to IL-18. J. Immunol. 160: 3759-3765.
54. Slight, S. R., and S. A. Khader. 2013. Chemokines shape the immune responses to tuberculosis. Cytokine Growth Factor Rev. 24: 105-113.
55. Feng, C. G., W. J. Britton, U. Palendira, N. L. Groat, H. Briscoe, and A. G. Bean. 2000. Up-regulation of VCAM-1 and differential expansion of beta integrin-expressing T lymphocytes are associated with immunity to pulmonary Myco-bacterium tuberculosis infection. J. Immunol. 164: 4853-4860.
56. Peters, W., and J. D. Ernst. 2003. Mechanisms of cell recruitment in the immune response to Mycobacterium tuberculosis. Microbes Infect. 5: 151-158.
57. Tang, X. Z., J. Jo, A. T. Tan, E. Sandalova, A. Chia, K. C. Tan, K. H. Lee, A. J. Gehring, G. De Libero, and A. Bertoletti. 2013. IL-7 licenses activation of human liver intrasinusoidal mucosal-associated invariant T cells. J. Immunol. 190: 3142-3152.
58. Seach, N., L. Guerri, L. Le Bourhis, Y. Mburu, Y. Cui, S. Bessoles, C. Soudais, and O. Lantz. 2013. Double-positive thymocytes select mucosal-associated invariant T cells. J. Immunol. 191: 6002-6009.
59. Leeansyah, E., L. Loh, D. F. Nixon, and J. K. Sandberg. 2014. Acquisition of innate-like microbial reactivity in mucosal tissues during human fetal MAIT-cell development. Nat. Commun. 5: 3143.
60. Le Bourhis, L., M. Dusseaux, A. Bohineust, S. Bessoles, E. Martin, V. Premel, M. Coré, D. Sleurs, N. E. Serriari, E. Treiner, et al. 2013. MAIT cells detect and efficiently lyse bacterially-infected epithelial cells. PLoS Pathog. 9: e1003681.
61. Wei, D. G., S. A. Curran, P. B. Savage, L. Teyton, and A. Bendelac. 2006. Mechanisms imposing the Vbeta bias of Valpha14 natural killer T cells and consequences for microbial glycolipid recognition. J. Exp. Med. 203: 1197-1207.
62. Rossjohn, J., D. G. Pellicci, O. Patel, L. Gapin, and D. I. Godfrey. 2012. Recognition of CD1d-restricted antigens by natural killer T cells. Nat. Rev. Immunol. 12: 845-857.
63. López-Sagaseta, J., C. L. Dulberger, J. E. Crooks, C. D. Parks, A. M. Luoma, A. McFedries, I. Van Rhijn, A. Saghatelian, and E. J. Adams. 2013. The molecular basis for Mucosal-Associated Invariant T cell recognition of MR1 proteins. Proc. Natl. Acad. Sci. USA 110: E1771-E1778.
64. Eckle, S. B., S. J. Turner, J. Rossjohn, and J. McCluskey. 2013. Predisposed ab T cell antigen receptor recognition of MHC and MHC-I like molecules? Curr. Opin. Immunol. 25: 653-659.
65. Shimamura, M., and Y. Y. Huang. 2002. Presence of a novel subset of NKT cells bearing an invariant V(alpha)19.1-J(alpha)26 TCR alpha chain. FEBS Lett. 516: 97-100.
66. Arase, H., N. Arase, and T. Saito. 1996. Interferon gamma production by natural killer (NK) cells and NK1.1+ T cells upon NKR-P1 cross-linking. J. Exp. Med. 183: 2391-2396.
67. Arase, N., H. Arase, S. Y. Park, H. Ohno, C. Ra, and T. Saito. 1997. Association with FcRgamma is essential for activation signal through NKR-P1 (CD161) in natural killer (NK) cells and NK1.1+ T cells. J. Exp. Med. 186: 1957-1963.
68. Chambers, W. H., N. L. Vujanovic, A. B. DeLeo, M. W. Olszowy, R. B. Herberman, and J. C. Hiserodt. 1989. Monoclonal antibody to a triggering structure expressed on rat natural killer cells and adherent lymphokine-activated killer cells. J. Exp. Med. 169: 1373-1389.
69. Giorda, R., W. A. Rudert, C. Vavassori, W. H. Chambers, J. C. Hiserodt, and M. Trucco. 1990. NKR-P1, a signal transduction molecule on natural killer cells. Science 249: 1298-1300.
70. Bartel, Y., B. Bauer, and A. Steinle. 2013. Modulation of NK cell function by genetically coupled C-type lectin-like receptor/ligand pairs encoded in the human natural killer gene complex. Front. Immunol. 4: 362.
71. Kadioglu, A., K. De Filippo, M. Bangert, V. E. Fernandes, L. Richards, K. Jones, P. W. Andrew, and N. Hogg. 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: 5907-5915.
72. Walrath, J. R., and R. F. Silver. 2011. The a4b1 integrin in localization of Mycobacterium tuberculosis-specific T helper type 1 cells to the human lung. Am. J. Respir. Cell Mol. Biol. 45: 24-30.
73. Rabin, R. L., M. K. Park, F. Liao, R. Swofford, D. Stephany, and J. M. Farber. 1999. Chemokine receptor responses on T cells are achieved through regulation of both receptor expression and signaling. J. Immunol. 162: 3840-3850.
74. Sallusto, F., A. Lanzavecchia, and C. R. Mackay. 1998. Chemokines and che-mokine receptors in T-cell priming and Th1/Th2-mediated responses. Immunol. Today 19: 568-574.
75. Kohlmeier, J. E., T. Cookenham, S. C. Miller, A. D. Roberts, J. P. Christensen, A. R. Thomsen, and D. L. Woodland. 2009. CXCR3 directs antigen-specific effector CD4+ T cell migration to the lung during parainfluenza virus infection. J. Immunol. 183: 4378-4384.
76. Farber, J. M. 1997. Mig and IP-10: CXC chemokines that target lymphocytes. J. Leukoc. Biol. 61: 246-257.
77. Lu, B., A. Humbles, D. Bota, C. Gerard, B. Moser, D. Soler, A. D. Luster, and N. P. Gerard. 1999. Structure and function of the murine chemokine receptor CXCR3. Eur. J. Immunol. 29: 3804-3812.
78. Groom, J. R., and A. D. Luster. 2011. CXCR3 ligands: redundant, collaborative and antagonistic functions. Immunol. Cell Biol. 89: 207-215.
79. Lim, J., S. C. Derrick, K. Kolibab, A. L. Yang, S. Porcelli, W. R. Jacobs, and S. L. Morris. 2009. Early pulmonary cytokine and chemokine responses in mice immunized with three different vaccines against Mycobacterium tuberculosis determined by PCR array. Clin. Vaccine Immunol. 16: 122-126.
80. Sauty, A., M. Dziejman, R. A. Taha, A. S. Iarossi, K. Neote, E. A. Garcia-Zepeda, Q. Hamid, and A. D. Luster. 1999. The T cell-specific CXC chemokines IP-10, Mig, and I-TAC are expressed by activated human bronchial epithelial cells. J. Immunol. 162: 3549-3558.
81. Barouch, D. H., S. Santra, J. E. Schmitz, M. J. Kuroda, T. M. Fu, W. Wagner, M. Bilska, A. Craiu, X. X. Zheng, G. R. Krivulka, et al. 2000. Control of viremia and prevention of clinical AIDS in rhesus monkeys by cytokine-augmented DNA vaccination. Science 290: 486-492.
82. Morrow, M. P., P. Pankhong, D. J. Laddy, K. A. Schoenly, J. Yan, N. Cisper, and D. B. Weiner. 2009. Comparative ability of IL-12 and IL-28B to regulate Treg populations and enhance adaptive cellular immunity. Blood 113: 5868-5877.
83. Kalams, S. A., S. Parker, X. Jin, M. Elizaga, B. Metch, M. Wang, J. Hural, M. Lubeck, J. Eldridge, M. Cardinali, et al; NIAID HIV Vaccine Trials Network. 2012. Safety and immunogenicity of an HIV-1 gag DNA vaccine with or without IL-12 and/or IL-15 plasmid cytokine adjuvant in healthy, HIV-1 uninfected adults. PLoS ONE 7: e29231.