Cysteine-cysteinyl chemokine receptor 6 mediates invariant natural killer T cell airway recruitment and innate stage resistance during mycobacterial infection

Journal of Innate Immunity

Volumn 3, Issue 1, 2011, Pages 99-108

  Stolberg, Valerie R ^a,b   Chiu, Bo Chin ^a   Martin, Brian E ^a   Shah, Samir A ^b   Sandor, Matyas ^c   Chensue, Stephen W ^a,b  

^a UNIVERSITY OF MICHIGAN MEDICAL SCHOOL   (United States)

^b Pathology and Laboratory Medicine   (United States)

^c UNIVERSITY OF WISCONSIN MADISON   (United States)

Author keywords

Chemokine receptors; Cysteine cysteinyl chemokine receptor 6; Lung; Mycobacteria; Natural killer T cells

Indexed keywords

CD1D ANTIGEN; CHEMOKINE RECEPTOR CCR6; MACROPHAGE INFLAMMATORY PROTEIN 3ALPHA; OVALBUMIN; T LYMPHOCYTE RECEPTOR ALPHA CHAIN; T LYMPHOCYTE RECEPTOR BETA CHAIN;

ADAPTIVE IMMUNITY; ANIMAL MODEL; ANTIBIOTIC RESISTANCE; ARTICLE; BACTERIAL CLEARANCE; BOVINE TUBERCULOSIS; CD8+ T LYMPHOCYTE; CONTROLLED STUDY; FEMALE; FLOW CYTOMETRY; INNATE IMMUNITY; KNOCKOUT MOUSE; LUNG ALVEOLUS CELL; LUNG LAVAGE; LYMPHOCYTE TRANSFER; MALE; MOUSE; MYCOBACTERIUM BOVIS; NONHUMAN; PRIORITY JOURNAL; PROTEIN RESTRICTION;

ANIMALS; CHEMOKINE CCL20; HUMANS; IMMUNITY, INNATE; LUNG; LYMPHOCYTE ACTIVATION; MICE; MICE, INBRED C57BL; MICE, KNOCKOUT; MYCOBACTERIUM BOVIS; NATURAL KILLER T-CELLS; RECEPTORS, ANTIGEN, T-CELL, ALPHA-BETA; RECEPTORS, CCR6; T-LYMPHOCYTES; TUBERCULOSIS, PULMONARY;

EID: 78650516204     PISSN: 1662811X     EISSN: 16628128     Source Type: Journal    
DOI: 10.1159/000321156     Document Type: Article

References (45)

1. Baba M, Imai T, Nishimura M, Kakizaki M, Takagi S, Hieshima K, Nomiyama H, Yoshie O: Identification of CCR6, the specific receptor for a novel lymphocyte-directed CC chemokine larc. J Biol Chem 1997;272:14893-14898.
2. Varona R, Zaballos A, Gutierrez J, Martin P, Roncal F, Albar JP, Ardavin C, Marquez G: Molecular cloning, functional characterization and mRNA expression analysis of the murine chemokine receptor CCR6 and its specific ligand mip-3 alpha. FEBS Lett 1998;440:188-194.
3. Schutyser E, Struyf S, Van Damme J: The CC chemokine CCL20 and its receptor CCR6. Cytokine Growth Factor Rev 2003;14:409-426.
4. Kucharzik T, Hudson JT, 3rd, Waikel RL, Martin WD, Williams IR: CCR6 expression distinguishes mouse myeloid and lymphoid dendritic cell subsets: demonstration using a CCR6 EGFP knock-in mouse. Eur J Immunol 2002;32:104-112.
5. Caux C, Ait-Yahia S, Chemin K, de Bouteiller O, Dieu-Nosjean MC, Homey B, Massacrier C, Vanbervliet B, Zlotnik A, Vicari A: Dendritic cell biology and regulation of dendritic cell trafficking by chemokines. Springer Semin Immunopathol 2000;22:345-369.
6. Homey B, Dieu-Nosjean MC, Wiesenborn A, Massacrier C, Pin JJ, Oldham E, Catron D, Buchanan ME, Muller A, deWaal Malefyt R, Deng G, Orozco R, Ruzicka T, Lehmann P, Lebecque S, Caux C, Zlotnik A: Up-regulation of macrophage inflammatory protein-3 β/CCL20 and CC chemokine receptor 6 in psoriasis. J Immunol 2000;164:6621-6632.
7. Kobayashi H, Miura S, Nagata H, Tsuzuki Y, Hokari R, Ogino T, Watanabe C, Azuma T, Ishii H: In situ demonstration of dendritic cell migration from rat intestine to mesenteric lymph nodes: relationships to maturation and role of chemokines. J Leukoc Biol 2004;75:434-442.
8. Le Borgne M, Etchart N, Goubier A, Lira SA, Sirard JC, van Rooijen N, Caux C, Ait-Yahia S, Vicari A, Kaiserlian D, Dubois B: Dendritic cells rapidly recruited into epithelial tissues via CCR6/CCL20 are responsible for CD8+ T cell crosspriming in vivo. Immunity 2006;24:191-201.
9. Salazar-Gonzalez RM, Niess JH, Zammit DJ, Ravindran R, Srinivasan A, Maxwell JR, Stoklasek T, Yadav R, Williams IR, Gu X, McCormick BA, Pazos MA, Vella AT, Lefrancois L, Reinecker HC, McSorley SJ: CCR6-mediated dendritic cell activation of pathogen-specific T cells in Peyer's patches. Immunity 2006;24:623-632.
10. Kim CH: Migration and function of Th17 cells. Inflamm Allergy Drug Targets 2009;8:221-228.
11. Villares R, Cadenas V, Lozano M, Almonacid L, Zaballos A, Martinez AC, Varona R: CCR6 regulates EAE pathogenesis by controlling regulatory CD4+ T-cell recruitment to target tissues. Eur J Immunol 2009;39:1671-1681.
12. Reibman J, Hsu Y, Chen LC, Bleck B, Gordon T: Airway epithelial cells release mip-3 β/CCL20 in response to cytokines and ambient particulate matter. Am J Respir Cell Mol Biol 2003;28:648-654.
13. Starner TD, Barker CK, Jia HP, Kang Y, Mc-Cray PB Jr: Ccl20 is an inducible product of human airway epithelia with innate immune properties. Am J Respir Cell Mol Biol 2003;29:627-633.
14. Facco M, Baesso I, Miorin M, Bortoli M, Cabrelle A, Boscaro E, Gurrieri C, Trentin L, Zambello R, Calabrese F, Cassatella MA, Semenzato G, Agostini C: Expression and role of CCR6/CCL20 chemokine axis in pulmonary sarcoidosis. J Leukoc Biol 2007;82:946-955.
15. Francis JN, Sabroe I, Lloyd CM, Durham SR, Till SJ: Elevated CCR6+ CD4+ t lymphocytes in tissue compared with blood and induction of CCL20 during the asthmatic late response. Clin Exp Immunol 2008;152:440-447.
16. Korbel DS, Schneider BE, Schaible UE: Innate immunity in tuberculosis: myths and truth. Microbes Infect 2008;10:995-1004.
17. Junqueira-Kipnis AP, Kipnis A, Jamieson A, Juarrero MG, Diefenbach A, Raulet DH, Turner J, Orme IM: NK cells respond to pulmonary infection with mycobacterium tuberculosis, but play a minimal role in protection. J Immunol 2003;171:6039-6045.
18. Kawamura I: Protective immunity against mycobacterium tuberculosis. Kekkaku 2006;81:687-691.
19. Emoto M, Emoto Y, Buchwalow IB, Kaufmann SH: Induction of IFN-γ-producing CD4+ natural killer T cells by Mycobacterium bovis bacillus Calmette Guerin. Eur J Immunol 1999;29:650-659.
20. Dieli F, Ivanyi J, Marsh P, Williams A, Naylor I, Sireci G, Caccamo N, Di Sano C, Salerno A: Characterization of lung γδ T cells following intranasal infection with mycobacterium bovis bacillus calmette-guerin. J Immunol 2003;170:463-469.
21. Venkataswamy MM, Porcelli SA: Lipid and glycolipid antigens of CD1d-restricted natural killer T cells. Semin Immunol 2009;22:68-78.
22. Cook DN, Prosser DM, Forster R, Zhang J, Kuklin NA, Abbondanzo SJ, Niu XD, Chen SC, Manfra DJ, Wiekowski MT, Sullivan LM, Smith SR, Greenberg HB, Narula SK, Lipp M, Lira SA: CCR6 mediates dendritic cell localization, lymphocyte homeostasis, and immune responses in mucosal tissue. Immunity 2000;12:495-503.
23. Chiu BC, Shang XZ, Stolberg VR, Komuniecki E, Chensue SW: Population analysis of CD4+T cell chemokine receptor transcript expression during in vivo type-1 (mycobacterial) and type-2 (schistosomal) immune responses. J Leukoc Biol 2002;72:363-372.
24. Chiu BC, Stolberg VR, Chensue SW: Mononuclear phagocyte-derived IL-10 suppresses the innate IL-12/IFN-γaxis in lung-challenged aged mice. J Immunol 2008;181:3156-3166.
25. Chiu BC, Freeman CM, Stolberg VR, Hu JS, Zeibecoglou K, Lu B, Gerard C, Charo IF, Lira SA, Chensue SW: Impaired lung dendritic cell activation in CCR2 knockout mice. Am J Pathol 2004;165:1199-1209.
26. Qiu B, Frait KA, Reich F, Komuniecki E, Chensue SW: Chemokine expression dynamics in mycobacterial (type-1) and schistosomal (type-2) antigen-elicited pulmonary granuloma formation. Am J Pathol 2001;158:1503-1515.
27. Chiu BC, Freeman CM, Stolberg VR, Komuniecki E, Lincoln PM, Kunkel SL, Chensue SW: Cytokine-chemokine networks in experimental mycobacterial and schistosomal lung granuloma formation. Am J Respir Cell Mol Biol 2003;10:106-116.
28. Wolf AJ, Desvignes L, Linas B, Banaiee N, Tamura T, Takatsu K, Ernst JD: Initiation of the adaptive immune response to mycobacterium tuberculosis depends on antigen production in the local lymph node, not the lungs. J Exp Med 2008;205:105-115.
29. Im JS, Kang TJ, Lee SB, Kim CH, Lee SH, Venkataswamy MM, Serfass ER, Chen B, Illarionov PA, Besra GS, Jacobs WR Jr, Chae GT, Porcelli SA: Alteration of the relative levels of iNKT cell subsets is associated with chronic mycobacterial infections. Clin Immunol 2008;127:214-224.
30. Sada-Ovalle I, Chiba A, Gonzales A, Brenner MB, Behar SM: Innate invariant NKT cells recognize mycobacterium tuberculosis-infected macrophages, produce interferon-γ, and kill intracellular bacteria. PLoS Pathog 2008;4: e1000239.
31. Thomas SY, Hou R, Boyson JE, Means TK, Hess C, Olson DP, Strominger JL, Brenner MB, Gumperz JE, Wilson SB, Luster AD: CD1d-restricted NKT cells express a chemokine receptor profile indicative of Th1-type inflammatory homing cells. J Immunol 2003;171:2571-2580.
32. Doisne JM, Becourt C, Amniai L, Duarte N, Le Luduec JB, Eberl G, Benlagha K: Skin and peripheral lymph node invariant NKT cells are mainly retinoic acid receptor-related orphan receptor (γ) t+ and respond preferentially under inflammatory conditions. J Immunol 2009;183:2142-2149.
33. Thomas SY, Banerji A, Medoff BD, Lilly CM, Luster AD: Multiple chemokine receptors, including CCR6 and CXCR3, regulate antigeninduced T cell homing to the human asthmatic airway. J Immunol 2007;179:1901-1912.
34. Sugawara I: Why does tuberculosis lead to specific inflammation? Nihon Hansenbyo Gakkai Zasshi 2009;78:263-269.
35. Lee JS, Lee JY, Son JW, Oh JH, Shin DM, Yuk JM, Song CH, Paik TH, Jo EK: Expression and regulation of the CC-chemokine ligand 20 during human tuberculosis. Scand J Immunol 2008;67:77-85.
36. Chackerian A, Alt J, Perera V, Behar SM: Activation of NKT cells protects mice from tuberculosis. Infect Immun 2002;70:6302-6309.
37. Behar SM, Porcelli SA: Cd1-restricted T cells in host defense to infectious diseases. Curr Top Microbiol Immunol 2007;314:215-250.
38. Snyder-Cappione JE, Nixon DF, Loo CP, Chapman JM, Meiklejohn DA, Melo FF, Costa PR, Sandberg JK, Rodrigues DS, Kallas EG: Individuals with pulmonary tuberculosis have lower levels of circulating CD1 drestricted NKT cells. J Infect Dis 2007;195:1361-1364.
39. Inoue T, Yoshikai Y, Matsuzaki G, Nomoto K: Early appearing γ/δ-bearing T cells during infection with Calmette Guerin bacillus. J Immunol 1991;146:2754-2762.
40. Ladel CH, Blum C, Dreher A, Reifenberg K, Kaufmann SH: Protective role of γ/δ T cells and α/β T cells in tuberculosis. Eur J Immunol 1995;25:2877-2881.
41. Paradis TJ, Cole SH, Nelson RT, Gladue RP: Essential role of CCR6 in directing activated T cells to the skin during contact hypersensitivity. J Invest Dermatol 2008;128:628-633.
42. Williams IR: CCR6 and CCL20: partners in intestinal immunity and lymphorganogenesis. Ann NY Acad Sci 2006;1072:52-61.
43. Harrison OJ, Foley J, Bolognese BJ, Long E, 3rd, Podolin PL, Walsh PT: Airway infiltration of CD4+ CCR6+ Th17 type cells associated with chronic cigarette smoke induced airspace enlargement. Immunol Lett 2008;121:13-21.
44. Lundy SK, Lira SA, Smit JJ, Cook DN, Berlin AA, Lukacs NW: Attenuation of allergen-induced responses in CCR6-/-mice is dependent upon altered pulmonary t lymphocyte activation. J Immunol 2005;174:2054-2060.
45. Brand S: Crohn's disease: Th1, Th17 or both? The change of a paradigm: new immunological and genetic insights implicate Th17 cells in the pathogenesis of Crohn's disease. Gut 2009;58:1152-1167.