The role of CC chemokine receptor 6 in host defense in a model of invasive pulmonary aspergillosis

American Journal of Respiratory and Critical Care Medicine

Volumn 175, Issue 11, 2007, Pages 1165-1172

  Phadke, Anagha P ^a   Akangire, Gangaram ^a   Park, Stacy J ^a,b   Lira, Sergio A ^c   Mehrad, Borna ^a,b,d  

^a UNIVERSITY OF TEXAS SOUTHWESTERN MEDICAL CENTER   (United States)

^b UNIVERSITY OF VIRGINIA   (United States)

^c MOUNT SINAI SCHOOL OF MEDICINE   (United States)

^d UNIVERSITY OF VIRGINIA   (United States)

Author keywords

CCR6 protein, mouse; Dendritic cells; Fungi, filamentous; Pneumonia

Indexed keywords

BETA CHEMOKINE RECEPTOR CCR6; CHEMOKINE RECEPTOR; UNCLASSIFIED DRUG;

ANIMAL CELL; ANIMAL EXPERIMENT; ANIMAL MODEL; ARTICLE; ASPERGILLUS FUMIGATUS; CONIDIUM; CONTROLLED STUDY; DENDRITIC CELL; HOST RESISTANCE; IMMUNE RESPONSE; IN VITRO STUDY; IN VIVO STUDY; LUNG ASPERGILLOSIS; MORTALITY; MOUSE; NONHUMAN; PHAGOCYTOSIS; POPULATION; PRIORITY JOURNAL; WILD TYPE;

ANIMALS; ASPERGILLOSIS, ALLERGIC BRONCHOPULMONARY; ASPERGILLUS FUMIGATUS; BONE MARROW; CELL MOVEMENT; CELLS, CULTURED; CHEMOKINES, CC; DENDRITIC CELLS; DISEASE MODELS, ANIMAL; FLOW CYTOMETRY; LEUKOCYTES; LUNG; MACROPHAGE INFLAMMATORY PROTEINS; MICE; MICE, INBRED C57BL; MYELOID CELLS; PHAGOCYTOSIS; RECEPTORS, CHEMOKINE; SEVERITY OF ILLNESS INDEX;

EID: 34249805431     PISSN: 1073449X     EISSN: 15354970     Source Type: Journal    
DOI: 10.1164/rccm.200602-256OC     Document Type: Article

References (69)

1. Patterson TF. Advances and challenges in management of invasive mycoses. Lancet 2005;366:1013-1025.
2. Bozza S, Gaziano R, Spreca A, Bacci A, Montagnoli C, di Francesco P, Romani L. Dendritic cells transport conidia and hyphae of Aspergillus fumigatus from the airways to the draining lymph nodes and initiate disparate Th responses to the fungus. J Immunol 2002;168:1362-1371.
3. Cenci E, Mencacci A, Bacci A, Bistoni F, Kurup VP, Romani L. T cell vaccination in mice with invasive pulmonary aspergillosis. J Immunol 2000;165:381-388.
4. Morrison BE, Park SJ, Mooney JM, Mehrad B. Chemokine-mediated recruitment of NK cells is a critical host defense mechanism in invasive aspergillosis. J Clin Invest 2003;112:1862-1870.
5. Perez-Canadillas JM, Zaballos A, Gutierrez J, Varona R, Roncal F, Albar JP, Marquez G, Bruix M. NMR solution structure of murine CCL20/MIP-3alpha, a chemokine that specifically chemoattracts immature dendritic cells and lymphocytes through its highly specific interaction with the beta-chemokine receptor CCR6. J Biol Chem 2001;276:28372-28379.
6. Yang D, Chertov O, Bykovskaia SN, Chen Q, Buffo MJ, Shogan J, Anderson M, Schroder JM, Wang JM, Howard OM, et al. Beta-defensins: linking innate and adaptive immunity through dendritic and T cell CCR6. Science 1999;286:525-528.
7. Power CA, Church DJ, Meyer A, Alouani S, Proudfoot AE, Clark-Lewis I, Sozzani S, Mantovani A, Wells TN. Cloning and characterization of a specific receptor for the novel CC chemokine MIP-3alpha from lung dendritic cells. J Exp Med 1997;186:825-835.
8. Greaves DR, Wang W, Dairaghi DJ, Dieu MC, Saint-Vis B, Franz-Bacon K, Rossi D, Caux C, McClanahan T, Gordon S, et al. CCR6, a CC chemokine receptor that interacts with macrophage inflammatory protein 3alpha and is highly expressed in human dendritic cells. J Exp Med 1997;186:837-844.
9. Krzysiek R, Lefevre EA, Bernard J, Foussat A, Galanaud P, Louache F, Richard Y. Regulation of CCR6 chemokine receptor expression and responsiveness to macrophage inflammatory protein-3alpha/CCL20 in human B cells. Blood 2000;96:2338-2345.
10. Fitzhugh DJ, Naik S, Caughman SW, Hwang ST. Cutting edge: CC chemokine receptor 6 is essential for arrest of a subset of memory T cells on activated dermal microvascular endothelial cells under physiologic flow conditions in vitro. J Immunol 2000;165:6677-6681.
11. Kleinewietfeld M, Puentes F, Borsellino G, Battistini L, Rotzschke O, Falk K. CCR6 expression defines regulatory effector/memory-like cells within the CD25+CD4+ T cell subset. Blood 2004.
12. Yang GX, Lian ZX, Kikuchi K, Liu YJ, Ansari AA, Ikehara S, Gershwin ME. CD4-plasmacytoid dendritic cells (pDCs) migrate in lymph nodes by CpG inoculation and represent a potent functional subset of pDCs. J Immunol 2005;174:3197-3203.
13. Penna G, Sozzani S, Adorini L. Cutting edge: selective usage of chemokine receptors by plasmacytoid dendritic cells. J Immunol 2001;167:1862-1866.
14. Kucharzik T, Hudson JT III, 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.
15. Dieu-Nosjean MC, Massacrier C, Homey B, Vanbervliet B, Pin JJ, Vicari A, Lebecque S, Dezutter-Dambuyant C, Schmitt D, Zlotnik A, et al. Macrophage inflammatory protein 3alpha is expressed at inflamed epithelial surfaces and is the most potent chemokine known in attracting Langerhans cell precursors. J Exp Med 2000;192:705-718.
16. Charbonnier AS, Kohrgruber N, Kriehuber E, Stingl G, Rot A, Maurer D. Macrophage inflammatory protein 3alpha is involved in the constitutive trafficking of epidermal Langerhans cells. J Exp Med 1999;190:1755-1768.
17. Osterholzer JJ, Ames T, Polak T, Sonstein J, Moore BB, Chensue SW, Toews GB, Curtis JL. CCR2 and CCR6, but not endothelial selectins, mediate the accumulation of immature dendritic cells within the lungs of mice in response to particulate antigen. J Immunol 2005;175:874-883.
18. Cook DN, Prosser DM, Forster R, Zhang J, Kuklin NA, Abbondanzo SJ, Niu XD, Chen SC, Manfra DJ, Wiekowski MT, et al. CCR6 mediates dendritic cell localization, lymphocyte homeostasis, and immune responses in mucosal tissue. Immunity 2000;12:495-503.
19. Lugering A, Floer M, Westphal S, Maaser C, Spahn TW, Schmidt MA, Domschke W, Williams IR, Kucharzik T. Absence of CCR6 inhibits CD4+ regulatory T-cell development and M-cell formation inside Peyer's patches. Am J Pathol 2005;166:1647-1654.
20. Varona R, Cadenas V, Flores J, Martinez AC, Marquez G. CCR6 has a non-redundant role in the development of inflammatory bowel disease. Eur J Immunol 2003;33:2937-2946.
21. Varona R, Cadenas V, Gomez L, Martinez AC, Marquez G. CCR6 regulates CD4+ T-cell-mediated acute graft-versus-host disease responses. Blood 2005;106:18-26.
22. Varona R, Villares R, Carramolino L, Goya I, Zaballos A, Gutierrez J, Torres M, Martinez AC, Marquez G. CCR6-deficient mice have impaired leukocyte homeostasis and altered contact hypersensitivity and delayed-type hypersensitivity responses. J Clin Invest 2001;107:R37-R45.
23. 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.
24. Lukacs NW, Prosser DM, Wiekowski M, Lira SA, Cook DN. Requirement for the chemokine receptor CCR6 in allergic pulmonary inflammation. J Exp Med 2001;194:551-555.
25. Brand S, Olszak T, Beigel F, Diebold J, Otte JM, Eichhorst ST, Goke B, Dambacher J. Cell differentiation dependent expressed CCR6 mediates ERK-1/2, SAPK/JNK, and Akt signaling resulting in proliferation and migration of colorectal cancer cells. J Cell Biochem 2006;97:709-723.
26. Dellacasagrande J, Schreurs OJ, Hofgaard PO, Omholt H, Steinsvoll S, Schenck K, Bogen B, Dembic Z. Liver metastasis of cancer facilitated by chemokine receptor CCR6. Scand J Immunol 2003;57:534-544.
27. Bozza S, Perruccio K, Montagnoli C, Gaziano R, Bellocchio S, Burchielli E, Nkwanyuo G, Pitzurra L, Velardi A, Romani L. A dendritic cell vaccine against invasive aspergillosis in allogeneic hematopoietic transplantation. Blood 2003;102:3807-3814.
28. Benjamim CF, Lundy SK, Lukacs NW, Hogaboam CM, Kunkel SL. Reversal of long-term sepsis-induced immunosuppression by dendritic cell. Blood 2004;16:16.
29. Cenci E, Mencacci A, Fe d'Ostiani C, Del Sero G, Mosci P, Montagnoli C, Bacci A, Romani L. Cytokine- and T helper-dependent lung mucosal immunity in mice with invasive pulmonary aspergillosis. J Infect Dis 1998;178:1750-1760.
30. Phadke AP, Park SJ, Mehrad B. The role of CCR6 in host defense in murine pulmonary invasive aspergillosis [abstract]. Presented at the FASEB Experimental Biology Conference, San Diego, California; 2005.
31. Mehrad B, Strieter RM, Moore TA, Tsai WC, Lira SA, Standiford TJ. CXC chemokine receptor-2 ligands are necessary components of neutrophil-mediated host defense in invasive pulmonary aspergillosis. J Immunol 1999;163:6086-6094.
32. Mehrad B, Moore TA, Standiford TJ. Macrophage inflammatory protein-1 alpha is a critical mediator of host defense against invasive pulmonary aspergillosis in neutropenic hosts. J Immunol 2000;165:962-968.
33. Mehrad B, Wiekowski M, Morrison BE, Chen SC, Coronel EC, Manfra DJ, Lira SA. Transient lung-specific expression of the chemokine KC improves outcome in invasive aspergillosis. Am J Respir Crit Care Med 2002;166:1263-1268.
34. Labeur MS, Roters B, Pers B, Mehling A, Luger TA, Schwarz T, Grabbe S. Generation of tumor immunity by bone marrow-derived dendritic cells correlates with dendritic cell maturation stage. J Immunol 1999;162:168-175.
35. Vermaelen KY, Carro-Muino I, Lambrecht BN, Pauwels RA. Specific migratory dendritic cells rapidly transport antigen from the airways to the thoracic lymph nodes. J Exp Med 2001;193:51-60.
36. Vermaelen K, Pauwels R. Accurate and simple discrimination of mouse pulmonary dendritic cell and macrophage populations by flow cytometry: methodology and new insights. Cytometry A 2004;61:170-177.
37. von Garnier C, Filgueira L, Wikstrom M, Smith M, Thomas JA, Strickland DH, Holt PG, Stumbles PA. Anatomical location determines the distribution and function of dendritic cells and other APCs in the respiratory tract. J Immunol 2005;175:1609-1618.
38. Wang J, Snider DP, Hewlett BR, Lukacs NW, Gauldie J, Liang H, Xing Z. Transgenic expression of granulocyte-macrophage colonystimulating factor induces the differentiation and activation of a novel dendritic cell population in the lung. Blood 2000;95:2337-2345.
39. Gonzalez-Juarrero M, Shim TS, Kipnis A, Junqueira-Kipnis AP, Orme IM. Dynamics of macrophage cell populations during murine pulmonary tuberculosis. J Immunol 2003;171:3128-3135.
40. van Rijt LS, Jung S, Kleinjan A, Vos N, Willart M, Duez C, Hoogsteden HC, Lambrecht BN. In vivo depletion of lung CD11c+ dendritic cells during allergen challenge abrogates the characteristic features of asthma. J Exp Med 2005;201:981-991.
41. Peters W, Cyster JG, Mack M, Schlondorff D, Wolf AJ, Ernst JD, Charo IF. CCR2-dependent trafficking of F4/80dim macrophages and CD11cdim/intermediate dendritic cells is crucial for T cell recruitment to lungs infected with Mycobacterium tuberculosis. J Immunol 2004;172:7647-7653.
42. Kaltreider HB, Curtis JL, Arraj SM. The mechanism of appearance of specific antibody-forming cells in lungs of inbred mice after immunization with sheep erythrocytes intratracheally. II. Dose-dependence and kinetics of appearance of antibody-forming cells in hilar lymph nodes and lungs of unprimed and primed mice. Am Rev Respir Dis 1987;135:87-92.
43. Milik AM, Buechner-Maxwell VA, Sonstein J, Kim S, Seitzman GD, Beals TF, Curtis JL. Lung lymphocyte elimination by apoptosis in the murine response to intratracheal particulate antigen. J Clin Invest 1997;99:1082-1091.
44. Jakubzick C, Tacke F, Llodra J, van Rooijen N, Randolph GJ. Modulation of dendritic cell trafficking to and from the airways. J Immunol 2006;176:3578-3584.
45. Mehrad B, Strieter RM, Standiford TJ. Role of TNF-alpha in pulmonary host defense in murine invasive aspergillosis. J Immunol 1999;162:1633-1640.
46. 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.
47. Hromas R, Gray PW, Chantry D, Godiska R, Krathwohl M, Fife K, Bell GI, Takeda J, Aronica S, Gordon M, et al. Cloning and characterization of exodus, a novel beta-chemokine. Blood 1997;89:3315-3322.
48. Hieshima K, Imai T, Opdenakker G, Van Damme J, Kusuda J, Tei H, Sakaki Y, Takatsuki K, Miura R, Yoshie O, et al. Molecular cloning of a novel human CC chemokine liver and activation-regulated chemokine (LARC) expressed in liver: chemotactic activity for lymphocytes and gene localization on chromosome 2. J Biol Chem 1997;272:5846-5853.
49. Huffnagle GB. Investigating invasive aspergillosis. Am J Respir Crit Care Med 2002;166:1159-1160.
50. Serrano-Gomez D, Dominguez-Soto A, Ancochea J, Jimenez-Heffernan JA, Leal JA, Corbi AL. Dendritic cell-specific intercellular adhesion molecule 3-grabbing nonintegrin mediates binding and internalization of Aspergillus fumigatus conidia by dendritic cells and macrophages. J Immunol 2004;173:5635-5643.
51. Hohl TM, Van Epps HL, Rivera A, Morgan LA, Chen PL, Feldmesser M, Pamer EG. Aspergillus fumigatus triggers inflammatory responses by stage-specific beta-glucan display. PLoS Pathog 2005;1:e30.
52. Steele C, Rapaka RR, Metz A, Pop SM, Williams DL, Gordon S, Kolls JK, Brown GD. The beta-glucan receptor dectin-1 recognizes specific morphologies of Aspergillus fumigatus. PLoS Pathog 2005;1:e42.
53. Bellocchio S, Montagnoli C, Bozza S, Gaziano R, Rossi G, Mambula SS, Vecchi A, Mantovani A, Levitz SM, Romani L. The contribution of the Toll-like/IL-1 receptor superfamily to innate and adaptive immunity to fungal pathogens in vivo. J Immunol 2004;172:3059-3069.
54. Braedel S, Radsak M, Einsele H, Latge JP, Michan A, Loeffler J, Haddad Z, Grigoleit U, Schild H, Hebart H. Aspergillus fumigatus antigens activate innate immune cells via Toll-like receptors 2 and 4. Br J Haematol 2004;125:392-399.
55. Gonzalez-Juarrero M, Orme IM. Characterization of murine lung dendritic cells infected with Mycobacterium tuberculosis. Infect Immun 2001;69:1127-1133.
56. de Heer HJ, Hammad H, Soullie T, Hijdra D, Vos N, Willart MA, Hoogsteden HC, Lambrecht BN. Essential role of lung plasmacytoid dendritic cells in preventing asthmatic reactions to harmless inhaled antigen. J Exp Med 2004;200:89-98.
57. Vermaelen K, Pauwels R. Accelerated airway dendritic cell maturation, trafficking, and elimination in a mouse model of asthma. Am J Respir Cell Mol Biol 2003;29:405-409.
58. Belz GT, Smith CM, Kleinert L, Reading P, Brooks A, Shortman K, Carbone FR, Heath WR. Distinct migrating and nonmigrating dendritic cell populations are involved in MHC class I-restricted antigen presentation after lung infection with virus. Proc Natl Acad Sci USA 2004;101:8670-8675.
59. Dahl ME, Dabbagh K, Liggitt D, Kim S, Lewis DB. Viral-induced T helper type 1 responses enhance allergic disease by effects on lung dendritic cells. Nat Immunol 2004;5:337-343.
60. O'Keeffe M, Hochrein H, Vremec D, Caminschi I, Miller JL, Anders EM, Wu L, Lahoud MH, Henri S, Scott B, et al. Mouse plasmacytoid cells: long-lived cells, heterogeneous in surface phenotype and function, that differentiate into CD8(+) dendritic cells only after microbial stimulus. J Exp Med 2002;196:1307-1319.
61. Vanbervliet B, Homey B, Durand I, Massacrier C, Ait-Yahia S, de Bouteiller O, Vicari A, Caux C. Sequential involvement of CCR2 and CCR6 ligands for immature dendritic cell recruitment: possible role at inflamed epithelial surfaces. Eur J Immunol 2002;32:231-242.
62. Fainaru O, Shseyov D, Hantisteanu S, Groner Y. Accelerated chemokine receptor 7-mediated dendritic cell migration in Runx3 knockout mice and the spontaneous development of asthma-like disease. Proc Natl Acad Sci USA 2005;102:10598-10603.
63. Legge KL, Braciale TJ. Accelerated migration of respiratory dendritic cells to the regional lymph nodes is limited to the early phase of pulmonary infection. Immunity 2003;18:265-277.
64. Colino J, Snapper CM. Two distinct mechanisms for induction of dendritic cell apoptosis in response to intact Streptococcus pneumoniae. J Immunol 2003;171:2354-2365.
65. Fugier-Vivier I, Servet-Delprat C, Rivailler P, Rissoan MC, Liu YJ, Rabourdin-Combe C. Measles virus suppresses cell-mediated immunity by interfering with the survival and functions of dendritic and T cells. J Exp Med 1997;186:813-823.
66. Fogg DK, Sibon C, Miled C, Jung S, Aucouturier P, Littman DR, Cumano A, Geissmann F. A clonogenic bone marrow progenitor specific for macrophages and dendritic cells. Science 2006;311:83-87.
67. Geissmann F, Jung S, Littman DR. Blood monocytes consist of two principal subsets with distinct migratory properties. Immunity 2003;19:71-82.
68. Xu H, Manivannan A, Dawson R, Crane IJ, Mack M, Sharp P, Liversidge J. Differentiation to the CCR2+ inflammatory phenotype in vivo is a constitutive, time-limited property of blood monocytes and is independent of local inflammatory mediators. J Immunol 2005;175:6915-6923.
69. Leon B, Martinez del Hoyo G, Parrillas V, Vargas HH, Sanchez-Mateos P, Longo N, Lopez-Bravo M, Ardavin C. Dendritic cell differentiation potential of mouse monocytes: monocytes represent immediate precursors of CD8- and CD8+ splenic dendritic cells. Blood 2004;103:2668-2676.