CCR7 deficiency leads to leukocyte activation and increased clearance in response to pulmonary Pseudomonas aeruginosa infection

Infection and Immunity

Volumn 78, Issue 5, 2010, Pages 2099-2107

  Eppert, Bryan L ^a   Motz, Gregory T ^a   Wortham, Brian W ^a   Flury, Jennifer L ^a   Borchers, Michael T ^a  

^a UNIVERSITY OF CINCINNATI COLLEGE OF MEDICINE   (United States)

Author keywords

[No Author keywords available]

Indexed keywords

B7 ANTIGEN; CD86 ANTIGEN; CHEMOKINE RECEPTOR CCR7; CYTOKINE; GAMMA INTERFERON; IL 23P40; INTERLEUKIN 12; INTERLEUKIN 1ALPHA; MACROPHAGE INFLAMMATORY PROTEIN 3BETA; SECONDARY LYMPHOID TISSUE CHEMOKINE; UNCLASSIFIED DRUG;

ANIMAL EXPERIMENT; ARTICLE; BACTERIUM CLEARANCE; BONE MARROW CELL; C57BL 6 MOUSE; CLEARANCE; CYTOKINE PRODUCTION; DENDRITIC CELL; HOST RESISTANCE; INFLAMMATION; INNATE IMMUNITY; LEUKOCYTE ACTIVATION; LUNG INFECTION; MOUSE; NONHUMAN; PRIORITY JOURNAL; PROTEIN DEFECT; PROTEIN EXPRESSION; PSEUDOMONAS INFECTION; RECEPTOR UPREGULATION; REGULATORY MECHANISM; RESPIRATORY BURST; T LYMPHOCYTE;

ANIMALS; CHEMOKINE CCL19; CHEMOKINE CCL21; COLONY COUNT, MICROBIAL; GENE EXPRESSION PROFILING; LEUKOCYTES; LUNG; MICE; MICE, INBRED C57BL; MICE, KNOCKOUT; PNEUMONIA, BACTERIAL; PSEUDOMONAS AERUGINOSA; PSEUDOMONAS INFECTIONS; RECEPTORS, CCR7;

EID: 77951228746     PISSN: 00199567     EISSN: 10985522     Source Type: Journal    
DOI: 10.1128/IAI.00962-09     Document Type: Article

References (46)

1. Ato, M., A. Maroof, S. Zubairi, H. Nakano, T. Kakiuchi, and P. M. Kaye. 2006. Loss of dendritic cell migration and impaired resistance to Leishmania donovani infection in mice deficient in CCL19 and CCL21. J. Immunol. 176:5486-5493.
2. Beaty, S. R., C. E. Rose, Jr., and S.-S. J. Sung. 2007. Diverse and potent chemokine production by lung CD11bhigh dendritic cells in homeostasis and in allergic lung inflammation. J. Immunol. 178:1882-1895.
3. Bromley, S. K., S. Y. Thomas, and A. D. Luster. 2005. Chemokine receptor CCR7 guides T cell exit from peripheral tissues and entry into afferent lymphatics. Nat. Immunol. 6:895-901.
4. Curtis, J. L. 2005. Cell-mediated adaptive immune defense of the lungs. Proc. Am. Thorac. Soc. 2:412-416.
5. Debes, G. F., C. N. Arnold, A. J. Young, S. Krautwald, M. Lipp, J. B. Hay, and E. C. Butcher. 2005. Chemokine receptor CCR7 required for T lymphocyte exit from peripheral tissues. Nat. Immunol. 6:889-894.
6. Debes, G. F., K. Bonhagen, T. Wolff, U. Kretschmer, S. Krautwald, T. Kamradt, and A. Hamann. 2004. CC Chemokine receptor 7 expression by effector/memory CD4+ T cells depends on antigen specificity and tissue localization during influenza A virus infection. J. Virol. 78:7528-7535.
7. del Rio, M.-L., J.-I. Rodriguez-Barbosa, J. Bolter, M. Ballmaier, O. Dittrich-Breiholz, M. Kracht, S. Jung, and R. Förster. 2008. CX3CR1+c-kit+ bone marrow cells give rise to CD103+ and CD103+ dendritic cells with distinct functional properties. J. Immunol. 181:6178-6188.
8. Ellis, T. N., and B. L. Beaman. 2004. Interferon-γ activation of polymorphonuclear neutrophil function. Immunology 112:2-12.
9. Förster, R., A. C. Davalos-Misslitz, and A. Rot. 2008. CCR7 and its ligands: balancing immunity and tolerance. Nat. Rev. Immunol. 8:362-371.
10. Förster, R., A. Schubel, D. Breitfeld, E. Kremmer, I. Renner-Müller, E. Wolf, and M. Lipp. 1999. CCR7 coordinates the primary immune response by establishing functional microenvironments in secondary lymphoid organs. Cell 99:23-33. (Pubitemid 29468627)
11. Giannoni, E., T. Sawa, L. Allen, J. Wiener-Kronish, and S. Hawgood. 2006. Surfactant proteins A and D enhance pulmonary clearance of Pseudomonas aeruginosa. Am. J. Respir. Cell Mol. Biol. 34:704-710.
12. Gunn, M. D., S. Kyuwa, C. Tam, T. Kakiuchi, A. Matsuzawa, L. T. Williams, and H. Nakano. 1999. Mice lacking expression of secondary lymphoid organ chemokine have defects in lymphocyte homing and dendritic cell localization. J. Exp. Med. 189:451-460.
13. Hartigan, A. J., J. Westwick, G. Jarai, and C. M. Hogaboam. 2009. CCR7 deficiency on dendritic cells enhances fungal clearance in a murine model of pulmonary invasive aspergillosis. J. Immunol. 183:5171-5179.
14. Hashimoto, S., J. F. Pittet, K. Hong, H. Folkesson, G. Bagby, L. Kobzik, C. Frevert, K. Watanabe, S. Tsurufuji, and J. Wiener-Kronish. 1996. Depletion of alveolar macrophages decreases neutrophil chemotaxis to Pseudomonas airspace infections. Am. J. Physiol. Lung Cell. Mol. Physiol. 270:L819-L828.
15. Heer, A. K., N. L. Harris, M. Kopf, and B. J. Marsland. 2008. CD4+ and CD8+ T cells exhibit differential requirements for CCR7-mediated antigen transport during influenza infection. J. Immunol. 181:6984-6994.
16. Holloway, B. W., V. Krishnapillai, and A. F. Morgan. 1979. Chromosomal genetics of Pseudomonas. Microbiol. Mol. Biol. Rev. 43:73-102.
17. Itakura, M., A. Tokuda, H. Kimura, S. Nagai, H. Yoneyama, N. Onai, S. Ishikawa, T. Kuriyama, and K. Matsushima. 2001. Blockade of secondary lymphoid tissue chemokine exacerbates Propionibacterium acnes-induced acute lung inflammation. J. Immunol. 166:2071-2079.
18. Junt, T., E. Scandella, R. Förster, P. Krebs, S. Krautwald, M. Lipp, H. Hengartner, and B. Ludewig. 2004. Impact of CCR7 on priming and distribution of antiviral effector and memory CTL. J. Immunol. 173:6684-6693. (Pubitemid 39541053)
19. Kocks, J. R., H. Adler, H. Danzer, K. Hoffmann, D. Jonigk, U. Lehmann, and R. Förster. 2009. Chemokine receptor CCR7 contributes to a rapid and efficient clearance of lytic murine {gamma}-herpes virus 68 from the lung, whereas bronchus-associated lymphoid tissue harbors virus during latency. J. Immunol. 182:6861-6869.
20. Kohout, T. A., S. L. Nicholas, S. J. Perry, G. Reinhart, S. Junger, and R. S. Struthers. 2004. Differential desensitization, receptor phosphorylation, {beta}-arrestin recruitment, and ERK1/2 activation by the two endogenous ligands for the CC chemokine receptor 7. J. Biol. Chem. 279:23214-23222.
21. Kooguchi, K., S. Hashimoto, A. Kobayashi, Y. Kitamura, I. Kudoh, J. Wiener-Kronish, and T. Sawa. 1998. Role of alveolar macrophages in initiation and regulation of inflammation in Pseudomonas aeruginosa pneumonia. Infect. Immun. 66:3164-3169.
22. Kursar, M., U. E. Höpken, M. Koch, A. Köhler, M. Lipp, S. H. E. Kaufmann, and H.-W. Mittrücker. 2005. Differential requirements for the chemokine receptor CCR7 in T cell activation during Listeria monocytogenes infection. J. Exp. Med. 201:1447-1457.
23. Mackay, C. R. 2001. Chemokines: immunology's high impact factors. Nat. Immunol. 2:95-101.
24. Marsland, B. J., P. Bättig, M. Bauer, C. Ruedl, U. Lässing, R. R. Beerli, K. Dietmeier, L. Ivanova, T. Pfister, L. Vogt, H. Nakano, C. Nembrini, P. Saudan, M. Kopf, and M. F. Bachmann. 2005. CCL19 and CCL21 induce a potent proinflammatory differentiation program in licensed dendritic cells. Immunity 22:493-505.
25. Martin, T. R., and C. W. Frevert. 2005. Innate immunity in the lungs. Proc. Am. Thorac. Soc. 2:403-411.
26. Martín-Fontecha, A., S. Sebastiani, U. E. Höpken, M. Uguccioni, M. Lipp, A. Lanzavecchia, and F. Sallusto. 2003. Regulation of dendritic cell migration to the draining lymph node: impact on T lymphocyte traffic and priming. J. Exp. Med. 198:615-621.
27. Nagira, M., T. Imai, K. Hieshima, J. Kusuda, M. Ridanpaa, S. Takagi, M. Nishimura, M. Kakizaki, H. Nomiyama, and O. Yoshie. 1997. Molecular cloning of a novel human CC chemokine secondary lymphoid-tissue chemokine that is a potent chemoattractant for lymphocytes and mapped to chromosome 9p13. J. Biol. Chem. 272:19518-19524.
28. Nieuwenhuis, E. E. S., T. Matsumoto, M. Exley, R. A. Schleipman, J. Glickman, D. T. Bailey, N. Corazza, S. P. Colgan, A. B. Onderdonk, and R. S. Blumberg. 2002. CD1d-dependent macrophage-mediated clearance of Pseudomonas aeruginosa from lung. Nat. Med. 8:588-593.
29. Ohl, L., M. Mohaupt, N. Czeloth, G. Hintzen, Z. Kiafard, J. Zwirner, T. Blankenstein, G. Henning, and R. Förster. 2004. CCR7 governs skin dendritic cell migration under inflammatory and steady-state conditions. Immunity 21:279-288. (Pubitemid 39094056)
30. Pene, F., B. Zuber, E. Courtine, C. Rousseau, F. Ouaaz, J. Toubiana, A. Tazi, J.-P. Mira, and J.-D. Chiche. 2008. Dendritic cells modulate lung response to Pseudomonas aeruginosa in a murine model of sepsis-induced immune dysfunction. J. Immunol. 181:8513-8520.
31. Rangel-Moreno, J., J. E. Moyron-Quiroz, L. Hartson, K. Kusser, and T. D. Randall. 2007. Pulmonary expression of CXC chemokine ligand 13, CC chemokine ligand 19, and CC chemokine ligand 21 is essential for local immunity to influenza. Proc. Natl. Acad. Sci. U. S. A. 104:10577-10582.
32. Riol-Blanco, L., N. Sanchez-Sanchez, A. Torres, A. Tejedor, S. Narumiya, A. L. Corbi, P. Sanchez-Mateos, and J. L. Rodriguez-Fernandez. 2005. The chemokine receptor CCR7 activates in dendritic cells two signaling modules that independently regulate chemotaxis and migratory speed. J. Immunol. 174:4070-4080. (Pubitemid 40395983)
33. Rot, A., and U. H. von Andrian. 2004. Chemokines in innate and adaptive host defense: basic chemokinese grammar for immune cells. Annu. Rev. Immunol. 22:891-928.
34. Sadikot, R. T., T. S. Blackwell, J. W. Christman, and A. S. Prince. 2005. Pathogen-host interactions in Pseudomonas aeruginosa pneumonia. Am. J. Respir. Crit. Care Med. 171:1209-1223.
35. Sullivan, S. K., D. A. McGrath, D. Grigoriadis, and K. B. Bacon. 1999. Pharmacological and signaling analysis of human chemokine receptor CCR-7 stably expressed in HEK-293 cells: high-affinity binding of recombinant ligands MIP-3beta and SLC stimulates multiple signaling cascades. Biochem. Biophys. Res. Commun. 263:685-690.
36. Sung, S.-S. J., S. M. Fu, C. E. Rose, Jr., F. Gaskin, S.-T. Ju, and S. R. Beaty. 2006. A major lung CD103 ({alpha}E)-beta7 integrin-positive epithelial dendritic cell population expressing langerin and tight junction proteins. J. Immunol. 176:2161-2172.
37. Trinchieri, G. 2003. Interleukin-12 and the regulation of innate resistance and adaptive immunity. Nat. Rev. Immunol. 3:133-146.
38. Tsai, W. C., R. M. Strieter, B. Mehrad, M. W. Newstead, X. Zeng, and T. J. Standiford. 2000. CXC chemokine receptor CXCR2 is essential for protective innate host response in murine Pseudomonas aeruginosa pneumonia. Infect. Immun. 68:4289-4296.
39. Vermaelen, K., and R. Pauwels. 2004. Accurate and simple discrimination of mouse pulmonary dendritic cell and macrophage populations by flow cytometry: methodology and new insights. Cytometry A 61:170-177. (Pubitemid 39362291)
40. Villablanca, E. J., D. Zhou, B. Valentinis, A. Negro, L. Raccosta, L. Mauri, A. Prinetti, S. Sonnino, C. Bordignon, C. Traversari, and V. Russo. 2008. Selected natural and synthetic retinoids impair CCR7- and CXCR4-dependent cell migration in vitro and in vivo. J. Leukoc. Biol. 84:871-879.
41. Walrand, S., S. Valeix, C. Rodriguez, R. Ligot, J. Chassagne, and M.-P. Vasson. 2003. Flow cytometry strudy of polymorphonuclear neutrophil oxidative burst: a comparison of three fluorescent probes. Clin. Chim. Acta 331:103-110.
42. Wesselkamper, S. C., B. L. Eppert, G. T. Motz, G. W. Lau, D. J. Hassett, and M. T. Borchers. 2008. NKG2D is critical for NK cell activation in host defense against Pseudomonas aeruginosa respiratory infection. J. Immunol. 181:5481-5489.
43. Yoshida, R., T. Imai, K. Hieshima, J. Kusuda, M. Baba, M. Kitaura, M. Nishimura, M. Kakizaki, H. Nomiyama, and O. Yoshie. 1997. Molecular cloning of a novel human CC chemokine EBI1-ligand chemokine that is a specific functional ligand for EBI1, CCR7. J. Biol. Chem. 272:13803-13809.
44. Young, H. A., and K. J. Hardy. 1995. Role of interferon-gamma in immune cell regulation. J. Leukoc. Biol. 58:373-381.
45. Zidar, D. A., J. D. Violin, E. J. Whalen, and R. J. Lefkowitz. 2009. Selective engagement of G protein coupled receptor kinases (GRKs) encodes distinct functions of biased ligands. Proc. Natl. Acad. Sci. U. S. A. 106:9649-9654.
46. Ziegler, E., M. Oberbarnscheidt, S. Bulfone-Paus, R. Förster, U. Kunzendorf, and S. Krautwald. 2007. CCR7 signaling inhibits T cell proliferation. J. Immunol. 179:6485-6493.