Resolvin E1 inhibits dendritic cell migration in the skin and attenuates contact hypersensitivity responses

Journal of Experimental Medicine

Volumn 212, Issue 11, 2015, Pages 1921-1930

  Sawada, Yu ^a,b   Honda, Tetsuya ^a   Hanakawa, Sho ^a   Nakamizo, Satoshi ^a   Murata, Teruasa ^a   Ueharaguchi Tanada, Yuri ^a   Ono, Sachiko ^a   Amano, Wataru ^a   Nakajima, Saeko ^a   Egawa, Gyohei ^a   Tanizaki, Hideaki ^a   Otsuka, Atsushi ^a   Kitoh, Akihiko ^a   Dainichi, Teruki ^a   Ogawa, Narihito ^c   Kobayashi, Yuichi ^c   Yokomizo, Takehiko ^d   Arita, Makoto ^e,f,g   Nakamura, Motonobu ^b   Miyachi, Yoshiki ^a   Kabashima, Kenji ^a,e   more..

^a KYOTO UNIVERSITY GRADUATE SCHOOL OF MEDICINE   (Japan)

^b UNIVERSITY OF OCCUPATIONAL AND ENVIRONMENTAL HEALTH   (Japan)

^c TOKYO INSTITUTE OF TECHNOLOGY   (Japan)

^d JUNTENDO UNIVERSITY SCHOOL OF MEDICINE   (Japan)

^e JAPAN SCIENCE AND TECHNOLOGY AGENCY   (Japan)

^f Institute of Physical and Chemical Research   (Japan)

^g YOKOHAMA CITY UNIVERSITY   (Japan)

Author keywords

[No Author keywords available]

Indexed keywords

2 (2,6 DIHYDROXYHEXYL) 6 (3 HYDROXY 1,5 UNDECADIENYL)PYRIDINE; LEUKOTRIENE B4; OMEGA 3 FATTY ACID; PROTEIN CDC42; RAC1 PROTEIN; RESOLVIN E1; UNCLASSIFIED DRUG; 5S,12R,18R-TRIHYDROXY-6Z,8E,10E,14Z,16E-EICOSAPENTAENOIC ACID; ACTIN; GAMMA INTERFERON; ICOSAPENTAENOIC ACID; LEUKOTRIENE B4 RECEPTOR; LTB4R1 PROTEIN, MOUSE;

ACTIN FILAMENT; ACTIN POLYMERIZATION; ADAPTIVE IMMUNITY; ANIMAL EXPERIMENT; ANIMAL MODEL; ANTIINFLAMMATORY ACTIVITY; ARTICLE; CELL MIGRATION; CONTACT ALLERGY; CONTROLLED STUDY; DENDRITIC CELL; DERMATITIS; FEMALE; IMMUNE RESPONSE; LYMPH NODE; MOUSE; MULTIPHOTON MICROSCOPY; NONHUMAN; PRIORITY JOURNAL; T LYMPHOCYTE ACTIVATION; ANALOGS AND DERIVATIVES; ANIMAL; BIOSYNTHESIS; C57BL MOUSE; CELL CULTURE; CELL MOTION; CHEMISTRY; DERMATITIS, CONTACT; DRUG EFFECTS; IMMUNOLOGY; PHYSIOLOGY; SKIN;

ACTINS; ANIMALS; CELL MOVEMENT; CELLS, CULTURED; DENDRITIC CELLS; DERMATITIS, CONTACT; EICOSAPENTAENOIC ACID; FEMALE; INTERFERON-GAMMA; LEUKOTRIENE B4; MICE; MICE, INBRED C57BL; RECEPTORS, LEUKOTRIENE B4; SKIN;

EID: 84959894543     PISSN: 00221007     EISSN: 15409538     Source Type: Journal    
DOI: 10.1084/jem.20150381     Document Type: Article

References (33)

1. Ando, R., H. Hama, M. Yamamoto-Hino, H. Mizuno, and A. Miyawaki. 2002. An optical marker based on the UV-induced green-to-red photoconversion of a fluorescent protein. Proc. Natl. Acad. Sci. USA. 99:12651-12656.http://dx.doi.org/10.1073/pnas.202320599
2. Arita, M., F. Bianchini, J. Aliberti, A. Sher, N. Chiang, S. Hong, R. Yang, N.A. Petasis, and C.N. Serhan. 2005a. Stereochemical assignment, antiinflammatory properties, and receptor for the omega-3 lipid mediator resolvin E1. J. Exp. Med. 201:713-722. http://dx.doi.org/10.1084/jem.20042031
3. Arita, M., M. Yoshida, S. Hong, E. Tjonahen, J.N. Glickman, N.A. Petasis, R.S. Blumberg, and C.N. Serhan. 2005b. Resolvin E1, an endogenous lipid mediator derived from omega-3 eicosapentaenoic acid, protects against 2,4,6-trinitrobenzene sulfonic acid-induced colitis. Proc. Natl. Acad. Sci. USA. 102:7671-7676. http://dx.doi.org/10.1073/pnas.0409271102
4. Arita, M., T. Ohira, Y.P. Sun, S. Elangovan, N. Chiang, and C.N. Serhan. 2007. Resolvin E1 selectively interacts with leukotriene B4 receptor BLT1 and ChemR23 to regulate inflammation. J. Immunol. 178:3912-3917. http://dx.doi.org/10.4049/jimmunol.178.6.3912
5. Benvenuti, F., S. Hugues, M. Walmsley, S. Ruf, L. Fetler, M. Popoff, V.L. Tybulewicz, and S. Amigorena. 2004. Requirement of Rac1 and Rac2 expression by mature dendritic cells for T cell priming. Science. 305:1150-1153. http://dx.doi.org/10.1126/science.1099159
6. Conti, P., M.R. Panara, R.C. Barbacane, F.C. Placido, M. Bongrazio, M. Reale, R.A. Dempsey, and S. Fiore. 1992. Blocking the interleukin-1 receptor inhibits leukotriene B4 and prostaglandin E2 generation in human monocyte cultures. Cell. Immunol. 145:199-209. http://dx.doi.org/10.1016/0008-8749(92)90323-H
7. Conti, P., M.R. Panara, R.C. Barbacane, M. Bongrazio, R.A. Dempsey, and M. Reale. 1993. Human recombinant IL-1 receptor antagonist (IL-1Ra) inhibits leukotriene B4 generation from human monocyte suspensions stimulated by lipopolysaccharide (LPS). Clin. Exp. Immunol. 91:526-531. http://dx.doi.org/10.1111/j.1365-2249.1993.tb05936.x
8. Dyerberg, J., H.O. Bang, E. Stoffersen, S. Moncada, and J.R. Vane. 1978. Eicosapentaenoic acid and prevention of thrombosis and atherosclerosis? Lancet. 312:117-119. http://dx.doi.org/10.1016/S0140-6736(78)91505-2
9. Edwards, D.C., L.C. Sanders, G.M. Bokoch, and G.N. Gill. 1999. Activation of LIM-kinase by Pak1 couples Rac/Cdc42 GTPase signalling to actin cytoskeletal dynamics. Nat. Cell Biol. 1:253-259. http://dx.doi.org/10.1038/12963
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. http://dx.doi.org/10.1016/S0092-8674(00)80059-8
11. Gaudreault, E., and J. Gosselin. 2007. Leukotriene B4-mediated release of antimicrobial peptides against cytomegalovirus is BLT1 dependent. Viral Immunol. 20:407-420. http://dx.doi.org/10.1089/vim.2006.0099
12. Haas-Stapleton, E.J., Y. Lu, S. Hong, M. Arita, S. Favoreto, S. Nigam, C.N. Serhan, and N. Agabian. 2007. Candida albicans modulates host defense by biosynthesizing the pro-resolving mediator resolvin E1. PLoS ONE. 2:e1316. http://dx.doi.org/10.1371/journal.pone.0001316
13. Haworth, O., M. Cernadas, R. Yang, C.N. Serhan, and B.D. Levy. 2008. Resolvin E1 regulates interleukin 23, interferon-γ and lipoxin A4 to promote the resolution of allergic airway inflammation. Nat. Immunol. 9:873-879. http://dx.doi.org/10.1038/ni.1627
14. Honda, T., and K. Kabashima. 2014. Leukotrienes as key mediators and amplifiers in allergic inflammation: insights from the bench and clinic. Exp. Dermatol. 23:95-96. http://dx.doi.org/10.1111/exd.12282
15. Honda, T., S. Nakajima, G. Egawa, K. Ogasawara, B. Malissen, Y. Miyachi, and K. Kabashima. 2010. Compensatory role of Langerhans cells and langerin-positive dermal dendritic cells in the sensitization phase of murine contact hypersensitivity. J. Allergy Clin. Immunol. 125:1154-1156.http://dx.doi.org/10.1016/j.jaci.2009.12.005
16. Honda, T., G. Egawa, S. Grabbe, and K. Kabashima. 2013. Update of immune events in the murine contact hypersensitivity model: toward the understanding of allergic contact dermatitis. J. Invest. Dermatol. 133:303-315. http://dx.doi.org/10.1038/jid.2012.284
17. Honda, T., J.G. Egen, T. Lämmermann, W. Kastenmüller, P. Torabi-Parizi, and R.N. Germain. 2014. Tuning of antigen sensitivity by T cell receptor-dependent negative feedback controls T cell effector function in inflamed tissues. Immunity. 40:235-247. http://dx.doi.org/10.1016/j.immuni.2013.11.017
18. Horrobin, D.F. 1987. Low prevalences of coronary heart disease (CHD), psoriasis, asthma and rheumatoid arthritis in Eskimos: are they caused by high dietary intake of eicosapentaenoic acid (EPA), a genetic variation of essential fatty acid (EFA) metabolism or a combination of both? Med. Hypotheses. 22:421-428. http://dx.doi.org/10.1016/0306-9877(87)90037-5
19. Lämmermann, T., and R.N. Germain. 2014. The multiple faces of leukocyte interstitial migration. Semin. Immunopathol. 36:227-251. http://dx.doi.org/10.1007/s00281-014-0418-8
20. Lämmermann, T., J. Renkawitz, X. Wu, K. Hirsch, C. Brakebusch, and M. Sixt. 2009. Cdc42-dependent leading edge coordination is essential for interstitial dendritic cell migration. Blood. 113:5703-5710. http://dx.doi.org/10.1182/blood-2008-11-191882
21. Lin, Y., X. Yang, W. Yue, X. Xu, B. Li, L. Zou, and R. He. 2014. Chemerin aggravates DSS-induced colitis by suppressing M2 macrophage polarization. Cell. Mol. Immunol. 11:355-366. http://dx.doi.org/10.1038/cmi.2014.15
22. Lindquist, R.L., G. Shakhar, D. Dudziak, H. Wardemann, T. Eisenreich, M.L. Dustin, and M.C. Nussenzweig. 2004. Visualizing dendritic cell networks in vivo. Nat. Immunol. 5:1243-1250. http://dx.doi.org/10.1038/ni1139
23. Luangsay, S., V. Wittamer, B. Bondue, O. De Henau, L. Rouger, M. Brait, J.D. Franssen, P. de Nadai, F. Huaux, and M. Parmentier. 2009. Mouse ChemR23 is expressed in dendritic cell subsets and macrophages, and mediates an anti-inflammatory activity of chemerin in a lung disease model. J. Immunol. 183:6489-6499. http://dx.doi.org/10.4049/jimmunol.0901037
24. Mori, T., K. Kabashima, R. Yoshiki, K. Sugita, N. Shiraishi, A. Onoue, E. Kuroda, M. Kobayashi, U. Yamashita, and Y. Tokura. 2008. Cutaneous hypersensitivities to hapten are controlled by IFN-γ-upregulated keratinocyte Th1 chemokines and IFN-γ-downregulated langerhans cell Th2 chemokines. J. Invest. Dermatol. 128:1719-1727. http://dx.doi.org/10.1038/jid.2008.5
25. Natsuaki, Y., G. Egawa, S. Nakamizo, S. Ono, S. Hanakawa, T. Okada, N. Kusuba, A. Otsuka, A. Kitoh, T. Honda, et al. 2014. Perivascular leukocyte clusters are essential for efficient activation of effector T cells in the skin. Nat. Immunol. 15:1064-1069. http://dx.doi.org/10.1038/ni.2992
26. Ogawa, N., and Y. Kobayashi. 2009. Total synthesis of resolving E1. Tetrahedron Lett. 50:6079-6082. http://dx.doi.org/10.1016/j.tetlet.2009.08.061
27. Secatto, A., E.M. Soares, G.A. Locachevic, P.A. Assis, F.W. Paula-Silva, C.H. Serezani, A.I. de Medeiros, and L.H. Faccioli. 2014. The leukotriene B/BLT axis is a key determinant in susceptibility and resistance to histoplasmosis. PLoS ONE. 9:e85083. http://dx.doi.org/10.1371/journal .pone.0085083
28. Serhan, C.N., N. Chiang, and T.E. Van Dyke. 2008. Resolving inflammation: dual anti-inflammatory and pro-resolution lipid mediators. Nat. Rev. Immunol. 8:349-361. http://dx.doi.org/10.1038/nri2294
29. Smith, R.J., D.E. Epps, J.M. Justen, L.M. Sam, M.A. Wynalda, F.A. Fitzpatrick, and F.S. Yein. 1987. Human neutrophil activation with interleukin-1. A role for intracellular calcium and arachidonic acid lipoxygenation. Biochem. Pharmacol. 36:3851-3858. http://dx.doi.org/10.1016/0006-2952(87)90449-7
30. Tanizaki, H., G. Egawa, K. Inaba, T. Honda, S. Nakajima, C.S. Moniaga, A. Otsuka, T. Ishizaki, M. Tomura, T. Watanabe, et al. 2010. Rho-mDia1 pathway is required for adhesion, migration, and T-cell stimulation in dendritic cells. Blood. 116:5875-5884. http://dx.doi.org/10.1182/blood-2010-01-264150
31. Terawaki, K., T. Yokomizo, T. Nagase, A. Toda, M. Taniguchi, K. Hashizume, T. Yagi, and T. Shimizu. 2005. Absence of leukotriene B4 receptor 1 confers resistance to airway hyperresponsiveness and Th2-type immune responses. J. Immunol. 175:4217-4225. http://dx.doi.org/10.4049/jimmunol.175.7.4217
32. Tomura, M., T. Honda, H. Tanizaki, A. Otsuka, G. Egawa, Y. Tokura, H. Waldmann, S. Hori, J.G. Cyster, T. Watanabe, et al. 2010. Activated regulatory T cells are the major T cell type emigrating from the skin during a cutaneous immune response in mice. J. Clin. Invest. 120:883-893. http://dx.doi.org/10.1172/JCI40926
33. Tull, S.P., C.M. Yates, B.H. Maskrey, V.B. O'Donnell, J. Madden, R.F. Grimble, P.C. Calder, G.B. Nash, and G.E. Rainger. 2009. Omega-3 Fatty acids and inflammation: novel interactions reveal a new step in neutrophil recruitment. PLoS Biol. 7:e1000177. http://dx.doi.org/10.1371/journal .pbio.1000177