CCR2 plays a critical role in dendritic cell maturation: Possible role of CCL2 and NF-κB

Journal of Immunology

Volumn 184, Issue 10, 2010, Pages 5571-5581

  Jimenez, Fabio ^a,b   Quinones, Marlon P ^a,b   Martinez, Hernan G ^a,b   Estrada, Carlos A ^b   Clark, Kassandra ^a,b   Garavito, Edgar ^b   Ibarra, Jessica ^b   Melby, Peter C ^a,b   Ahuja, Seema S ^a,b  

^a VETERANS AFFAIRS MEDICAL CENTER   (United States)

^b UNIVERSITY OF TEXAS HEALTH SCIENCE CENTER AT SAN ANTONIO   (United States)

Author keywords

[No Author keywords available]

Indexed keywords

B7 ANTIGEN; CD40 ANTIGEN; CD86 ANTIGEN; CHEMOKINE RECEPTOR CCR2; GAMMA INTERFERON; IMMUNOGLOBULIN ENHANCER BINDING PROTEIN; INTERLEUKIN 12P70; LIPOPOLYSACCHARIDE; MACROPHAGE INFLAMMATORY PROTEIN 3BETA; MONOCYTE CHEMOTACTIC PROTEIN 1; CCL2 PROTEIN, MOUSE; CCR2 PROTEIN, MOUSE; INTERLEUKIN 12;

ANIMAL CELL; ANIMAL EXPERIMENT; ANIMAL MODEL; ARTICLE; CELL MIGRATION; CONTROLLED STUDY; CYTOKINE PRODUCTION; DENDRITIC CELL; INFECTION SENSITIVITY; LANGERHANS CELL; LEISHMANIA MAJOR; LYMPH NODE CELL; MOUSE; NONHUMAN; PRIORITY JOURNAL; RADIOSENSITIVITY; SPLEEN CELL; ANIMAL; BIOLOGICAL MODEL; BIOSYNTHESIS; C57BL MOUSE; CELL CULTURE; CELL DIFFERENTIATION; CELL MOTION; GENETICS; IMMUNOLOGY; METABOLISM; MOUSE MUTANT; PATHOLOGY; PHYSIOLOGY; SKIN LEISHMANIASIS; TRANSCRIPTION INITIATION; UPREGULATION;

ANIMALS; CELL DIFFERENTIATION; CELL MOVEMENT; CELLS, CULTURED; CHEMOKINE CCL2; DENDRITIC CELLS; INTERLEUKIN-12; LANGERHANS CELLS; LEISHMANIA MAJOR; LEISHMANIASIS, CUTANEOUS; MICE; MICE, INBRED C57BL; MICE, KNOCKOUT; MICE, SCID; MODELS, IMMUNOLOGICAL; NF-KAPPA B; RECEPTORS, CCR2; TRANSCRIPTIONAL ACTIVATION; UP-REGULATION;

EID: 77954752407     PISSN: 00221767     EISSN: 15506606     Source Type: Journal    
DOI: 10.4049/jimmunol.0803494     Document Type: Article

References (76)

1. Blanco, P., A. K. Palucka, V. Pascual, and J. Banchereau. 2008. Dendritic cells and cytokines in human inflammatory and autoimmune diseases. Cytokine Growth Factor Rev. 19: 41-52.
2. Banchereau, J., and R. M. Steinman. 1998. Dendritic cells and the control of immunity. Nature 392: 245-252.
3. Quah, B. J., and H. C. O'Neill. 2005. Maturation of function in dendritic cells for tolerance and immunity. J. Cell. Mol. Med. 9: 643-654.
4. Cools, N., P. Ponsaerts, V. F. Van Tendeloo, and Z. N. Berneman. 2007. Balancing between immunity and tolerance: an interplay between dendritic cells, regulatory T cells, and effector T cells. J. Leukoc. Biol. 82: 1365-1374.
5. Randolph, G. J., V. Angeli, and M. A. Swartz. 2005. Dendritic-cell trafficking to lymph nodes through lymphatic vessels. Nat. Rev. Immunol. 5: 617-628.
6. Randolph, G. J., G. Sanchez-Schmitz, and V. Angeli. 2005. Factors and signals that govern the migration of dendritic cells via lymphatics: recent advances. Springer Semin. Immunopathol. 26: 273-287.
7. Wang, J., X. Wang, S. Hussain, Y. Zheng, S. Sanjabi, F. Ouaaz, and A. A. Beg. 2007. Distinct roles of different NF-κB subunits in regulating inflammatory and T cell stimulatory gene expression in dendritic cells. J. Immunol. 178: 6777-6788. (Pubitemid 46847402)
8. Pietilä, T. E., V. Veckman, A. Lehtonen, R. Lin, J. Hiscott, and I. Julkunen. 2007. Multiple NF-κB and IFN regulatory factor family transcription factors regulate CCL19 gene expression in human monocyte-derived dendritic cells. J. Immunol. 178: 253-261.
9. Moore, F., S. Buonocore, E. Aksoy, N. Ouled-Haddou, S. Goriely, E. Lazarova, F. Paulart, C. Heirman, E. Vaeremans, K. Thielemans, et al. 2007. An alternative pathway of NF-κB activation results in maturation and T cell priming activity of dendritic cells overexpressing a mutated IkBα. J. Immunol. 178: 1301-1311.
10. Bharadwaj, A. S., and D. K. Agrawal. 2007. Transcription factors in the control of dendritic cell life cycle. Immunol. Res. 37: 79-96.
11. Steinman, R. M. 2007. Dendritic cells: understanding immunogenicity. Eur. J. Immunol. 37(Suppl. 1): S53-S60.
12. Schuler, G., and R. M. Steinman. 1985. Murine epidermal Langerhans cells mature into potent immunostimulatory dendritic cells in vitro. J. Exp. Med. 161: 526-546.
13. Fujii, S., K. Liu, C. Smith, A. J. Bonito, and R. M. Steinman. 2004. The linkage of innate to adaptive immunity via maturing dendritic cells in vivo requires CD40 ligation in addition to antigen presentation and CD80/86 costimulation. J. Exp. Med. 199: 1607-1618.
14. Sozzani, S., P. Allavena, A. Vecchi, and A. Mantovani. 2000. Chemokines and dendritic cell traffic. J. Clin. Immunol. 20: 151-160.
15. 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.
16. 4 transporter MRP1 regulates CCL19 (MIP-3β, ELC)-dependent mobilization of dendritic cells to lymph nodes. Cell 103: 757-768.
17. Cyster, J. G. 1999. Chemokines and cell migration in secondary lymphoid organs. Science 286: 2098-2102. (Pubitemid 129516279)
18. Gunn, M. D. 2003. Chemokine mediated control of dendritic cell migration and function. Semin. Immunol. 15: 271-276.
19. Larsen, C. P., R. M. Steinman, M. Witmer-Pack, D. F. Hankins, P. J. Morris, and J. M. Austyn. 1990. Migration and maturation of Langerhans cells in skin transplants and explants. J. Exp. Med. 172: 1483-1493.
20. Macatonia, S. E., S. C. Knight, A. J. Edwards, S. Griffiths, and P. Fryer. 1987. Localization of antigen on lymph node dendritic cells after exposure to the contact sensitizer fluorescein isothiocyanate: functional and morphological studies. J. Exp. Med. 166: 1654-1667.
21. Sato, N., S. K. Ahuja, M. Quinones, V. Kostecki, R. L. Reddick, P. C. Melby, W. A. Kuziel, and S. S. Ahuja. 2000. CC chemokine receptor (CCR)2 is required for Langerhans cell migration and localization of T helper cell type 1 (Th1)-inducing dendritic cells: absence of CCR2 shifts the Leishmania major-resistant phenotype to a susceptible state dominated by Th2 cytokines, B cell outgrowth, and sustained neutrophilic inflammation. J. Exp. Med. 192: 205-218.
22. -/- dendritic cells: implications for islet transplantation. Transplantation 85: 1030-1038.
23. Rao, A. R., M. P. Quinones, E. Garavito, Y. Kalkonde, F. Jimenez, C. Gibbons, J. Perez, P. Melby, W. Kuziel, R. L. Reddick, et al. 2003. CC chemokine receptor 2 expression in donor cells serves an essential role in graft-versus-host-disease. J. Immunol. 171: 4875-4885.
24. Quinones, M., S. K. Ahuja, P. C. Melby, L. Pate, R. L. Reddick, and S. S. Ahuja. 2000. Preformed membrane-associated stores of interleukin (IL)-12 are a previously unrecognized source of bioactive IL-12 that is mobilized within minutes of contact with an intracellular parasite. J. Exp. Med. 192: 507-516.
25. Ahuja, S. S., R. L. Reddick, N. Sato, E. Montalbo, V. Kostecki, W. Zhao, M. J. Dolan, P. C. Melby, and S. K. Ahuja. 1999. Dendritic cell (DC)-based anti-infective strategies: DCs engineered to secrete IL-12 are a potent vaccine in a murine model of an intracellular infection. J. Immunol. 163: 3890-3897.
26. Pulendran, B., J. L. Smith, G. Caspary, K. Brasel, D. Pettit, E. Maraskovsky, and C. R. Maliszewski. 1999. Distinct dendritic cell subsets differentially regulate the class of immune response in vivo. Proc. Natl. Acad. Sci. USA 96: 1036-1041.
27. Shurin, M. R., P. P. Pandharipande, T. D. Zorina, C. Haluszczak, V. M. Subbotin, O. Hunter, A. Brumfield, W. J. Storkus, E. Maraskovsky, and M. T. Lotze. 1997. FLT3 ligand induces the generation of functionally active dendritic cells in mice. Cell. Immunol. 179: 174-184.
28. Heinzel, F. P., D. S. Schoenhaut, R. M. Rerko, L. E. Rosser, and M. K. Gately. 1993. Recombinant interleukin 12 cures mice infected with Leishmania major. J. Exp. Med. 177: 1505-1509.
29. Quinones, M. P., Y. Kalkonde, C. A. Estrada, F. Jimenez, R. Ramirez, L. Mahimainathan, S. Mummidi, G. G. Choudhury, H. Martinez, L. Adams, et al. 2008. Role of astrocytes and chemokine systems in acute TNFα induced demyelinating syndrome: CCR2-dependent signals promote astrocyte activation and survival via NF-κB and Akt. Mol. Cell. Neurosci. 37: 96-109.
30. 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.
31. -/- mice: the role of mast cells. J. Immunol. 163: 2160-2167.
32. Liu, S. F., X. Ye, and A. B. Malik. 1999. Inhibition of NF-κB activation by pyrrolidine dithiocarbamate prevents In vivo expression of proinflammatory genes. Circulation 100: 1330-1337.
33. Nathens, A. B., R. Bitar, C. Davreux, M. Bujard, J. C. Marshall, A. P. Dackiw, R. W. Watson, and O. D. Rotstein. 1997. Pyrrolidine dithiocarbamate attenuates endotoxin-induced acute lung injury. Am. J. Respir. Cell Mol. Biol. 17: 608-616.
34. Cuzzocrea, S., P. K. Chatterjee, E. Mazzon, L. Dugo, I. Serraino, D. Britti, G. Mazzullo, A. P. Caputi, and C. Thiemermann. 2002. Pyrrolidine dithiocarbamate attenuates the development of acute and chronic inflammation. Br. J. Pharmacol. 135: 496-510.
35. Yang, J., Y. Park, H. Zhang, X. Xu, G. A. Laine, K. C. Dellsperger, and C. Zhang. 2009. Feed-forward signaling of TNF-α and NF-κB via IKK-β pathway contributes to insulin resistance and coronary arteriolar dysfunction in type 2 diabetic mice. Am. J. Physiol. Heart Circ. Physiol. 296: H1850-H1858.
36. Domingo-Domènech, J., R. Pippa, M. Tápia, P. Gascón, O. Bachs, and M. Bosch. 2008. Inactivation of NF-κB by proteasome inhibition contributes to increased apoptosis induced by histone deacetylase inhibitors in human breast cancer cells. Breast Cancer Res. Treat. 112: 53-62.
37. Granata, F., A. Frattini, S. Loffredo, A. Del Prete, S. Sozzani, G. Marone, and M. Triggiani. 2006. Signaling events involved in cytokine and chemokine production induced by secretory phospholipase A2 in human lung macrophages. Eur. J. Immunol. 36: 1938-1950.
38. Secchiero, P., D. Milani, A. Gonelli, E. Melloni, D. Campioni, D. Gibellini, S. Capitani, and G. Zauli. 2003. Tumor necrosis factor (TNF)-related apoptosisinducing ligand (TRAIL) and TNF-α promote the NF-κB-dependent maturation of normal and leukemic myeloid cells. J. Leukoc. Biol. 74: 223-232.
39. Wang, X. C., C. Jobin, J. B. Allen, W. L. Roberts, and G. J. Jaffe. 1999. Suppression of NF-κB-dependent proinflammatory gene expression in human RPE cells by a proteasome inhibitor. Invest. Ophthalmol. Vis. Sci. 40: 477-486.
40. Lawrence, T., D. W. Gilroy, P. R. Colville-Nash, and D. A. Willoughby. 2001. Possible new role for NF-κB in the resolution of inflammation. Nat. Med. 7: 1291-1297.
41. Bonizzi, G., M. Bebien, D. C. Otero, K. E. Johnson-Vroom, Y. Cao, D. Vu, A. G. Jegga, B. J. Aronow, G. Ghosh, R. C. Rickert, and M. Karin. 2004. Activation of IKKα target genes depends on recognition of specific κB binding sites by RelB:p52 dimers. EMBO J. 23: 4202-4210.
42. Konecny, P., A. J. Stagg, H. Jebbari, N. English, R. N. Davidson, and S. C. Knight. 1999. Murine dendritic cells internalize Leishmania major promastigotes, produce IL-12 p40 and stimulate primary T cell proliferation in vitro. Eur. J. Immunol. 29: 1803-1811.
43. von Stebut, E., Y. Belkaid, T. Jakob, D. L. Sacks, and M. C. Udey. 1998. Uptake of Leishmania major amastigotes results in activation and interleukin 12 release from murine skin-derived dendritic cells: implications for the initiation of anti-Leishmania immunity. J. Exp. Med. 188: 1547-1552.
44. Gorak, P. M., C. R. Engwerda, and P. M. Kaye. 1998. Dendritic cells, but not macrophages, produce IL-12 immediately following Leishmania donovani infection. Eur. J. Immunol. 28: 687-695.
45. Reis e Sousa, C., S. Hieny, T. Scharton-Kersten, D. Jankovic, H. Charest, R. N. Germain, and A. Sher. 1997. In vivo microbial stimulation induces rapid CD40 ligand-independent production of interleukin 12 by dendritic cells and their redistribution to T cell areas. J. Exp. Med. 186: 1819-1829.
46. Al-Wabel, M. A., W. K. Tonui, L. Cui, S. K. Martin, and R. G. Titus. 2007. Protection of susceptible BALB/c mice from challenge with Leishmania major by nucleoside hydrolase, a soluble exo-antigen of Leishmania. Am. J. Trop. Med. Hyg. 77: 1060-1065.
47. Merad, M., M. G. Manz, H. Karsunky, A. Wagers, W. Peters, I. Charo, I. L. Weissman, J. G. Cyster, and E. G. Engleman. 2002. Langerhans cells renew in the skin throughout life under steady-state conditions. Nat. Immunol. 3: 1135-1141.
48. Quinones, M. P., S. K. Ahuja, F. Jimenez, J. Schaefer, E. Garavito, A. Rao, G. Chenaux, R. L. Reddick, W. A. Kuziel, and S. S. Ahuja. 2004. Experimental arthritis in CC chemokine receptor 2-null mice closely mimics severe human rheumatoid arthritis. J. Clin. Invest. 113: 856-866.
49. Esche, C., V. M. Subbotin, O. Hunter, J. M. Peron, C. Maliszewski, M. T. Lotze, and M. R. Shurin. 1999. Differential regulation of epidermal and dermal dendritic cells by IL-12 and Flt3 ligand. J. Invest. Dermatol. 113: 1028-1032.
50. Sánchez-Sánchez, N., L. Riol-Blanco, and J. L. Rodríguez-Fernández. 2006. The multiple personalities of the chemokine receptor CCR7 in dendritic cells. J. Immunol. 176: 5153-5159.
51. Sato, K., H. Kawasaki, H. Nagayama, R. Serizawa, J. Ikeda, C. Morimoto, K. Yasunaga, N. Yamaji, K. Tadokoro, T. Juji, and T. A. Takahashi. 1999. CC chemokine receptors, CCR-1 and CCR-3, are potentially involved in antigen-presenting cell function of human peripheral blood monocyte-derived dendritic cells. Blood 93: 34-42.
52. Marsland, B. J., P. Bättig, M. Bauer, C. Ruedl, U. Lässing, R. R. Beerli, K. Dietmeier, L. Ivanova, T. Pfister, L. Vogt, et al. 2005. CCL19 and CCL21 induce a potent proinflammatory differentiation program in licensed dendritic cells. Immunity 22: 493-505.
53. Mizumoto, N., K. Iwabichi, H. Nakamura, M. Ato, A. Shibaki, T. Kawashima, H. Kobayashi, C. Iwabuchi, A. Ohkawara, and K. Onoé. 2001. Enhanced contact hypersensitivity in human monocyte chemoattractant protein-1 transgenic mouse. Immunobiology 204: 477-493.
54. Yamazaki, S., H. Yokozeki, T. Satoh, I. Katayama, and K. Nishioka. 1998. TNF-α, RANTES, and MCP-1 are major chemoattractants of murine Langerhans cells to the regional lymph nodes. Exp. Dermatol. 7: 35-41.
55. Vecchi, A., L. Massimiliano, S. Ramponi, W. Luini, S. Bernasconi, R. Bonecchi, P. Allavena, M. Parmentier, A. Mantovani, and S. Sozzani. 1999. Differential responsiveness to constitutive vs. inducible chemokines of immature and mature mouse dendritic cells. J. Leukoc. Biol. 66: 489-494.
56. Kriehuber, E., W. Bauer, A. S. Charbonnier, D. Winter, S. Amatschek, D. Tamandl, N. Schweifer, G. Stingl, and D. Maurer. 2005. Balance between NF-κB and JNK/AP-1 activity controls dendritic cell life and death. Blood 106: 175-183. (Pubitemid 40967190)
57. O'Sullivan, B. J., and R. Thomas. 2002. CD40 ligation conditions dendritic cell antigen-presenting function through sustained activation of NF-κB. J. Immunol. 168: 5491-5498.
58. Rescigno, M., M. Martino, C. L. Sutherland, M. R. Gold, and P. Ricciardi-Castagnoli. 1998. Dendritic cell survival and maturation are regulated by different signaling pathways. J. Exp. Med. 188: 2175-2180.
59. Yoshimura, S., J. Bondeson, F. M. Brennan, B. M. Foxwell, and M. Feldmann. 2001. Role of NF-κB in antigen presentation and development of regulatory T cells elucidated by treatment of dendritic cells with the proteasome inhibitor PSI. Eur. J. Immunol. 31: 1883-1893.
60. Isomura, I., K. Tsujimura, and A. Morita. 2006. Antigen-specific peripheral tolerance induced by topical application of NF-κB decoy oligodeoxynucleotide. J. Invest. Dermatol. 126: 97-104.
61. Brodmerkel, C. M., R. Huber, M. Covington, S. Diamond, L. Hall, R. Collins, L. Leffet, K. Gallagher, P. Feldman, P. Collier, et al. 2005. Discovery and pharmacological characterization of a novel rodent-active CCR2 antagonist, INCB3344. J. Immunol. 175: 5370-5378.
62. Laderach, D., D. Compagno, O. Danos, W. Vainchenker, and A. Galy. 2003. RNA interference shows critical requirement for NF-κB p50 in the production of IL-12 by human dendritic cells. J. Immunol. 171: 1750-1757.
63. Ouaaz, F., J. Arron, Y. Zheng, Y. Choi, and A. A. Beg. 2002. Dendritic cell development and survival require distinct NF-κB subunits. Immunity 16: 257-270. (Pubitemid 34211965)
64. Traynor, T. R., A. C. Herring, M. E. Dorf, W. A. Kuziel, G. B. Toews, and G. B. Huffnagle. 2002. Differential roles of CC chemokine ligand 2/monocyte chemotactic protein-1 and CCR2 in the development of T1 immunity. J. Immunol. 168: 4659-4666.
65. + dendritic cells. Nat. Immunol. 1: 83-87.
66. De Smedt, T., B. Pajak, E. Muraille, L. Lespagnard, E. Heinen, P. De Baetselier, J. Urbain, O. Leo, and M. Moser. 1996. Regulation of dendritic cell numbers and maturation by lipopolysaccharide in vivo. J. Exp. Med. 184: 1413-1424.
67. Quinones, M. P., C. A. Estrada, F. Jimenez, H. Martinez, O. Willmon, W. A. Kuziel, S. K. Ahuja, and S. S. Ahuja. 2007. CCL2-independent role of CCR2 in immune responses against Leishmania major. Parasite Immunol. 29: 211-217.
68. Suzue, K., S. Kobayashi, T. Takeuchi, M. Suzuki, and S. Koyasu. 2008. Critical role of dendritic cells in determining the Th1/Th2 balance upon Leishmania major infection. Int. Immunol. 20: 337-343.
69. von Stebut, E., Y. Belkaid, B. V. Nguyen, M. Cushing, D. L. Sacks, and M. C. Udey. 2000. Leishmania major-infected murine Langerhans cell-like dendritic cells from susceptible mice release IL-12 after infection and vaccinate against experimental cutaneous Leishmaniasis. Eur. J. Immunol. 30: 3498-3506.
70. Berberich, C., J. R. Ramírez-Pineda, C. Hambrecht, G. Alber, Y. A. Skeiky, and H. Moll. 2003. Dendritic cell (DC)-based protection against an intracellular pathogen is dependent upon DC-derived IL-12 and can be induced by molecularly defined antigens. J. Immunol. 170: 3171-3179.
71. Wiethe, C., A. Debus, M. Mohrs, A. Steinkasserer, M. Lutz, and A. Gessner. 2008. Dendritic cell differentiation state and their interaction with NKT cells determine Th1/Th2 differentiation in the murine model of Leishmania major infection. J. Immunol. 180: 4371-4381.
72. Ritter, U., and A. Osterloh. 2007. A new view on cutaneous dendritic cell subsets in experimental leishmaniasis. Med. Microbiol. Immunol. (Berl.) 196: 51-59.
73. Iezzi, G., A. Fröhlich, B. Ernst, F. Ampenberger, S. Saeland, N. Glaichenhaus, and M. Kopf. 2006. Lymph node resident rather than skin-derived dendritic cells initiate specific T cell responses after Leishmania major infection. J. Immunol. 177: 1250-1256. (Pubitemid 44036630)
74. Misslitz, A. C., K. Bonhagen, D. Harbecke, C. Lippuner, T. Kamradt, and T. Aebischer. 2004. Two waves of antigen-containing dendritic cells in vivo in experimental Leishmania major infection. Eur. J. Immunol. 34: 715-725.
75. Tabbara, K. S., N. C. Peters, F. Afrin, S. Mendez, S. Bertholet, Y. Belkaid, and D. L. Sacks. 2005. Conditions influencing the efficacy of vaccination with live organisms against Leishmania major infection. Infect. Immun. 73: 4714-4722.
76. Wang, L., L. S. Bursch, A. Kissenpfennig, B. Malissen, S. C. Jameson, and K. A. Hogquist. 2008. Langerin expressing cells promote skin immune responses under defined conditions. J. Immunol. 180: 4722-4727.