Nuclear receptor Nur77 attenuates airway inflammation in mice by suppressing NF-κB activity in lung epithelial cells

Journal of Immunology

Volumn 195, Issue 4, 2015, Pages 1388-1398

  Kurakula, Kondababu ^a   Vos, Mariska ^a   Logiantara, Adrian ^a   Roelofs, Joris J ^a   Nieuwenhuis, Maartje A ^b   Koppelman, Gerard H ^c   Postma, Dirkje S ^b   Van Rijt, Leonie S ^a   De Vries, Carlie J M ^a  

^a UNIVERSITY OF AMSTERDAM   (Netherlands)

^b UNIVERSITY MEDICAL CENTER GRONINGEN   (Netherlands)

^c UNIVERSITY OF GRONINGEN   (Netherlands)

Author keywords

[No Author keywords available]

Indexed keywords

I KAPPA B ALPHA; IMMUNOGLOBULIN ENHANCER BINDING PROTEIN; IMMUNOGLOBULIN G1; IMMUNOGLOBULIN G2A; MUCIN 5AC; NUCLEAR RECEPTOR NUR77; CYTOKINE; IMMUNOGLOBULIN G; MUC5AC PROTEIN, MOUSE;

ANIMAL EXPERIMENT; ANIMAL MODEL; ARTICLE; ASTHMA; CELL INFILTRATION; CONTROLLED STUDY; CYTOKINE PRODUCTION; DISEASE SEVERITY; EOSINOPHIL; EPITHELIUM CELL; FEMALE; GAIN OF FUNCTION MUTATION; GENE EXPRESSION REGULATION; GENE OVEREXPRESSION; GENE SILENCING; GENETIC ASSOCIATION; HUMAN; HUMAN CELL; IMMUNOGLOBULIN BLOOD LEVEL; LOSS OF FUNCTION MUTATION; LUNG ALVEOLUS EPITHELIUM; LUNG LAVAGE; LYMPH NODE; LYMPHOCYTE; MACROPHAGE; MOUSE; NONHUMAN; NUR77 GENE; NUR77 GENEPROTEIN TARGETING; PATHOGENESIS; PRIORITY JOURNAL; PROTEIN EXPRESSION; PROTEIN FUNCTION; PROTEIN PHOSPHORYLATION; PROTEIN PROTEIN INTERACTION; RESPIRATORY TRACT ALLERGY; RESPIRATORY TRACT INFLAMMATION; SINGLE NUCLEOTIDE POLYMORPHISM; TH2 CELL; UPREGULATION; WILD TYPE; ALLELE; ANIMAL; BLOOD; BRONCHOALVEOLAR LAVAGE FLUID; DEFICIENCY; DISEASE MODEL; ENZYME ACTIVATION; GENE EXPRESSION; GENETICS; IMMUNOLOGY; INFLAMMATION; KNOCKOUT MOUSE; LEUKOCYTE COUNT; LUNG ALVEOLUS CELL; METABOLISM; ODDS RATIO; PATHOLOGY; SIGNAL TRANSDUCTION;

ALLELES; ANIMALS; ASTHMA; BRONCHOALVEOLAR LAVAGE FLUID; CYTOKINES; DISEASE MODELS, ANIMAL; ENZYME ACTIVATION; EOSINOPHILS; GENE EXPRESSION; IMMUNOGLOBULIN G; INFLAMMATION; LEUKOCYTE COUNT; LYMPH NODES; MICE; MICE, KNOCKOUT; MUCIN 5AC; NF-KAPPA B; NUCLEAR RECEPTOR SUBFAMILY 4, GROUP A, MEMBER 1; ODDS RATIO; PNEUMOCYTES; POLYMORPHISM, SINGLE NUCLEOTIDE; RESPIRATORY HYPERSENSITIVITY; SIGNAL TRANSDUCTION;

EID: 84938915304     PISSN: 00221767     EISSN: 15506606     Source Type: Journal    
DOI: 10.4049/jimmunol.1401714     Document Type: Article

References (41)

1. Hamid, Q., and M. Tulic. 2009. Immunobiology of asthma. Annu. Rev. Physiol. 71: 489-507.
2. Renauld, J. C. 2001. New insights into the role of cytokines in asthma. J. Clin. Pathol. 54: 577-589.
3. Boyce, J. A., D. Broide, K. Matsumoto, and B. S. Bochner. 2009. Advances in mechanisms of asthma, allergy, and immunology in 2008. J. Allergy Clin. Immunol. 123: 569-574.
4. Lambrecht, B. N., and H. Hammad. 2009. Biology of lung dendritic cells at the origin of asthma. Immunity 31: 412-424.
5. Rothenberg, M. E., and S. P. Hogan. 2006. The eosinophil. Annu. Rev. Immunol. 24: 147-174.
6. Wills-Karp, M. 2004. Interleukin-13 in asthma pathogenesis. Immunol. Rev. 202: 175-190.
7. Herrick, C. A., and K. Bottomly. 2003. To respond or not to respond: T cells in allergic asthma. Nat. Rev. Immunol. 3: 405-412.
8. Ono, S. J., T. Nakamura, D. Miyazaki, M. Ohbayashi, M. Dawson, and M. Toda. 2003. Chemokines: roles in leukocyte development, trafficking, and effector function. J. Allergy Clin. Immunol. 111: 1185-1199, quiz 1200.
9. Pope, S. M., N. Zimmermann, K. F. Stringer, M. L. Karow, and M. E. Rothenberg. 2005. The eotaxin chemokines and CCR3 are fundamental regulators of allergen-induced pulmonary eosinophilia. J. Immunol. 175: 5341-5350.
10. Dowell,M. L., T. L. Lavoie, J. Solway, and R. Krishnan. 2014. Airway smooth muscle: a potential target for asthma therapy. Curr. Opin. Pulm. Med. 20: 66-72.
11. Rose, M. C., and J. A. Voynow. 2006. Respiratory tract mucin genes and mucin glycoproteins in health and disease. Physiol. Rev. 86: 245-278.
12. Evans, C. M., K. Kim, M. J. Tuvim, and B. F. Dickey. 2009. Mucus hypersecretion in asthma: causes and effects. Curr. Opin. Pulm. Med. 15: 4-11.
13. Hart, L. A., V. L. Krishnan, I. M. Adcock, P. J. Barnes, and K. F. Chung. 1998. Activation and localization of transcription factor, nuclear factor-kB, in asthma. Am. J. Respir. Crit. Care Med. 158: 1585-1592.
14. Poynter, M. E., R. Cloots, T. van Woerkom, K. J. Butnor, P. Vacek, D. J. Taatjes, C. G. Irvin, and Y. M. Janssen-Heininger. 2004. NF-kB activation in airways modulates allergic inflammation but not hyperresponsiveness. J. Immunol. 173: 7003-7009.
15. Fujisawa, T., S. Velichko, P. Thai, L. Y. Hung, F. Huang, and R. Wu. 2009. Regulation of airway MUC5AC expression by IL-1b and IL-17A; the NF-kB paradigm. J. Immunol. 183: 6236-6243.
16. Hamers, A. A., R. N. Hanna, H. Nowyhed, C. C. Hedrick, and C. J. de Vries. 2013. NR4A nuclear receptors in immunity and atherosclerosis. Curr. Opin. Lipidol. 24: 381-385.
17. van Tiel, C. M., and C. J. de Vries. 2012. NR4All in the vessel wall. J. Steroid Biochem. Mol. Biol. 130: 186-193.
18. Kurakula, K., A. A. Hamers, V. de Waard, and C. J. de Vries. 2013. Nuclear receptors in atherosclerosis: a superfamily with many "Goodfellas". Mol. Cell. Endocrinol. 368: 71-84.
19. Zhou, F., Y. Drabsch, T. J. Dekker, A. G. de Vinuesa, Y. Li, L. J. Hawinkels, K. A. Sheppard, M. J. Goumans, R. B. Luwor, C. J. de Vries, et al. 2014. Nuclear receptor NR4A1 promotes breast cancer invasion and metastasis by activating TGF-b signalling. Nat. Commun. 5: 3388.
20. Pires, N. M., T. W. Pols, M. R. de Vries, C. M. van Tiel, P. I. Bonta, M. Vos, E. K. Arkenbout, H. Pannekoek, J. W. Jukema, P. H. Quax, and C. J. de Vries. 2007. Activation of nuclear receptor Nur77 by 6-mercaptopurine protects against neointima formation. Circulation 115: 493-500.
21. Arkenbout, E. K., V. de Waard, M. van Bragt, T. A. van Achterberg, J. M. Grimbergen, B. Pichon, H. Pannekoek, and C. J. de Vries. 2002. Protective function of transcription factor TR3 orphan receptor in atherogenesis: decreased lesion formation in carotid artery ligation model in TR3 transgenic mice. Circulation 106: 1530-1535.
22. You, B., Y. Y. Jiang, S. Chen, G. Yan, and J. Sun. 2009. The orphan nuclear receptor Nur77 suppresses endothelial cell activation through induction of IkBa expression. Circ. Res. 104: 742-749.
23. Harant, H., and I. J. Lindley. 2004. Negative cross-talk between the human orphan nuclear receptor Nur77/NAK-1/TR3 and nuclear factor-kB. Nucleic Acids Res. 32: 5280-5290.
24. Hanna, R. N., I. Shaked, H. G. Hubbeling, J. A. Punt, R. Wu, E. Herrley, C. Zaugg, H. Pei, F. Geissmann, K. Ley, and C. C. Hedrick. 2012. NR4A1 (Nur77) deletion polarizes macrophages toward an inflammatory phenotype and increases atherosclerosis. Circ. Res. 110: 416-427.
25. Hamers, A. A., M. Vos, F. Rassam, G. Marinković, K. Kurakula, P. J. van Gorp, M. P. de Winther, M. J. Gijbels, V. de Waard, and C. J. de Vries. 2012. Bone marrow-specific deficiency of nuclear receptor Nur77 enhances atherosclerosis. Circ. Res. 110: 428-438.
26. Kagaya, S., R. Hashida, N. Ohkura, T. Tsukada, Y. Sugita, M. Terakawa, G. Tsujimoto, T. Katsunuma, A. Akasawa, K. Matsumoto, and H. Saito. 2005. NR4A orphan nuclear receptor family in peripheral blood eosinophils from patients with atopic dermatitis and apoptotic eosinophils in vitro. Int. Arch. Allergy Immunol. 137(Suppl. 1): 35-44.
27. Murphy, S. R., E. S. Schelegle, P. C. Edwards, L. A. Miller, D. M. Hyde, and L. S. Van Winkle. 2012. Postnatal exposure history and airways: oxidant stress responses in airway explants. Am. J. Respir. Cell Mol. Biol. 47: 815-823.
28. Liu, Y., J. Zhang, B. Yi, M. Chen, J. Qi, Y. Yin, X. Lu, J. F. Jasmin, and J. Sun. 2014. Nur77 suppresses pulmonary artery smooth muscle cell proliferation through inhibition of the STAT3/Pim-1/NFAT pathway. Am. J. Respir. Cell Mol. Biol. 50: 379-388.
29. Daan de Boer, J., J. J. Roelofs, A. F. de Vos, R. de Beer, M. Schouten, T. J. Hommes, A. J. Hoogendijk, O. J. de Boer, I. Stroo, J. S. van der Zee, et al. 2013. Lipopolysaccharide inhibits Th2 lung inflammation induced by house dust mite allergens in mice. Am. J. Respir. Cell Mol. Biol. 48: 382-389.
30. van Rijt, L. S., H. Kuipers, N. Vos, D. Hijdra, H. C. Hoogsteden, and B. N. Lambrecht. 2004. A rapid flow cytometric method for determining the cellular composition of bronchoalveolar lavage fluid cells in mouse models of asthma. J. Immunol. Methods 288: 111-121.
31. Kurakula, K., E. van der Wal, D. Geerts, C. M. van Tiel, and C. J. de Vries. 2011. FHL2 protein is a novel co-repressor of nuclear receptor Nur77. J. Biol. Chem. 286: 44336-44343.
32. Kurakula, K., M. Vos, I. Otermin Rubio, G. Marinković, R. Buettner, L. C. Heukamp, J. Stap, V. de Waard, C. M. van Tiel, and C. J. de Vries. 2014. The LIM-only protein FHL2 reduces vascular lesion formation involving inhibition of proliferation and migration of smooth muscle cells. PLoS One 9: e94931.
33. Plaisance, S., W. Vanden Berghe, E. Boone, W. Fiers, and G. Haegeman. 1997. Recombination signal sequence binding protein Jkappa is constitutively bound to the NF-kB site of the interleukin-6 promoter and acts as a negative regulatory factor. Mol. Cell. Biol. 17: 3733-3743.
34. Himes, B. E., X. Jiang, R. Hu, A. C. Wu, J. A. Lasky-Su, B. J. Klanderman, J. Ziniti, J. Senter-Sylvia, J. J. Lima, C. G. Irvin, et al. 2012. Genome-wide association analysis in asthma subjects identifies SPATS2L as a novel bronchodilator response gene. PLoS Genet. 8: e1002824.
35. Himes, B. E., W. Qiu, B. Klanderman, J. Ziniti, J. Senter-Sylvia, S. J. Szefler, R. F. Lemanske, Jr., R. S. Zeiger, R. C. Strunk, F. D. Martinez, et al. 2013. ITGB5 and AGFG1 variants are associated with severity of airway responsiveness. BMC Med. Genet. 14: 86.
36. Wang, T., Q. Jiang, C. Chan, K. S. Gorski, E. McCadden, D. Kardian, D. Pardoll, and K. A. Whartenby. 2009. Inhibition of activation-induced death of dendritic cells and enhancement of vaccine efficacy via blockade of MINOR. Blood 113: 2906-2913.
37. Shin, H. J., B. H. Lee, M. G. Yeo, S. H. Oh, J. D. Park, K. K. Park, J. H. Chung, C. K. Moon, and M. O. Lee. 2004. Induction of orphan nuclear receptor Nur77 gene expression and its role in cadmium-induced apoptosis in lung. Carcinogenesis 25: 1467-1475.
38. Van Hove, C. L., T. Maes, D. D. Cataldo, M. M. Guéders, E. Palmans, G. F. Joos, and K. G. Tournoy. 2009. Comparison of acute inflammatory and chronic structural asthma-like responses between C57BL/6 and BALB/c mice. Int. Arch. Allergy Immunol. 149: 195-207.
39. Gueders, M. M., G. Paulissen, C. Crahay, F. Quesada-Calvo, J. Hacha, C. Van Hove, K. Tournoy, R. Louis, J. M. Foidart, A. Noël, and D. D. Cataldo. 2009. Mouse models of asthma: a comparison between C57BL/6 and BALB/c strains regarding bronchial responsiveness, inflammation, and cytokine production. Inflamm. Res. 58: 845-854.
40. Wansa, K. D., J. M. Harris, G. Yan, P. Ordentlich, and G. E. Muscat. 2003. The AF-1 domain of the orphan nuclear receptor NOR-1 mediates trans-activation, coactivator recruitment, and activation by the purine anti-metabolite 6-mercaptopurine. J. Biol. Chem. 278: 24776-24790.
41. Zhan, Y., X. Du, H. Chen, J. Liu, B. Zhao, D. Huang, G. Li, Q. Xu, M. Zhang, B. C. Weimer, et al. 2008. Cytosporone B is an agonist for nuclear orphan receptor Nur77. Nat. Chem. Biol. 4: 548-556.