Naringenin inhibits dendritic cell maturation and has therapeutic effects in a murine model of collagen-induced arthritis

Journal of Nutritional Biochemistry

Volumn 26, Issue 12, 2015, Pages 1467-1478

  Li, Yi Rong ^a   Chen, Der Yuan ^a,b   Chu, Ching Liang ^c   Li, Shiming ^d,e   Chen, Yu Kuo ^f   Wu, Chao Ling ^g   Lin, Chi Chen ^a,b  

^a NATIONAL CHUNG HSING UNIVERSITY   (Taiwan)

^b TAICHUNG VETERANS GENERAL HOSPITAL   (Taiwan)

^c NATIONAL TAIWAN UNIVERSITY   (Taiwan)

^d RUTGERS UNIVERSITY   (United States)

^e HUANGGANG NORMAL UNIVERSITY   (China)

^f NATIONAL PINGTUNG UNIVERSITY OF SCIENCE AND TECHNOLOGY   (Taiwan)

^g NATIONAL CHENG KUNG UNIVERSITY   (Taiwan)

Author keywords

Collagen induced arthritis; Dendritic cells; Flavonoid; Maturation; Naringenin

Indexed keywords

CHEMOKINE; COLLAGEN TYPE 2; CYTOKINE; IMMUNOGLOBULIN ENHANCER BINDING PROTEIN; IMMUNOGLOBULIN G; LIPOPOLYSACCHARIDE; MITOGEN ACTIVATED PROTEIN KINASE; NARINGENIN; COLLAGEN; FLAVANONE DERIVATIVE; LIGAND;

ADULT; ANIMAL EXPERIMENT; ANIMAL MODEL; ANIMAL TISSUE; ARTHRITIS; ARTICLE; CELL CONTACT; CELL MATURATION; CONTROLLED STUDY; CYTOKINE PRODUCTION; DENDRITIC CELL; DISEASE SEVERITY; DOSE RESPONSE; DRUG EFFECT; DRUG MECHANISM; IMMUNOSTIMULATION; LYMPHOCYTE PROLIFERATION; MALE; MOUSE; NONHUMAN; PROTEIN EXPRESSION; SIGNAL TRANSDUCTION; SPLEEN; STENT; T LYMPHOCYTE; T LYMPHOCYTE ACTIVATION; TH1 CELL; TH17 CELL; ANIMAL; BLOOD; C57BL MOUSE; CD4+ T LYMPHOCYTE; CELL PROLIFERATION; CELL SURVIVAL; CHEMISTRY; CYTOLOGY; DISEASE MODEL; EXPERIMENTAL ARTHRITIS; INFLAMMATION; METABOLISM; ORAL DRUG ADMINISTRATION; RHEUMATOID ARTHRITIS; TRANSGENIC MOUSE;

ADMINISTRATION, ORAL; ANIMALS; ARTHRITIS, EXPERIMENTAL; ARTHRITIS, RHEUMATOID; CD4-POSITIVE T-LYMPHOCYTES; CELL PROLIFERATION; CELL SURVIVAL; COLLAGEN; DENDRITIC CELLS; DISEASE MODELS, ANIMAL; DOSE-RESPONSE RELATIONSHIP, DRUG; FLAVANONES; IMMUNOGLOBULIN G; INFLAMMATION; LIGANDS; LIPOPOLYSACCHARIDES; MALE; MICE; MICE, INBRED C57BL; MICE, TRANSGENIC; NF-KAPPA B; SIGNAL TRANSDUCTION; SPLEEN; TH1 CELLS; TH17 CELLS;

EID: 84983179854     PISSN: 09552863     EISSN: 18734847     Source Type: Journal    
DOI: 10.1016/j.jnutbio.2015.07.016     Document Type: Article

References (64)

1. Guerder S., Joncker N., Mahiddine K., Serre L. Dendritic cells in tolerance and autoimmune diabetes. Curr Opin Immunol 2013, 25:670-675.
2. Chung C.Y., Ysebaert D., Berneman Z.N., Cools N. Dendritic cells: cellular mediators for immunological tolerance. Clin Dev Immunol 2013, 2013:972865.
3. Dudek A.M., Martin S., Garg A.D., Agostinis P. Immature, semi-mature, and fully mature dendritic cells: toward a DC-cancer cells interface that augments anticancer immunity. Front Immunol 2013, 4:438.
4. Gallo P.M., Gallucci S. The dendritic cell response to classic, emerging, and homeostatic danger signals. Implications for autoimmunity. Front Immunol 2013, 4:138.
5. Kourilovitch M., Galarza-Maldonado C., Ortiz-Prado E. Diagnosis and classification of rheumatoid arthritis. J Autoimmun 2014, 48-49:26-30.
6. Rodríguez-Fernández J.L. Antigen presentation by dendritic cells in rheumatoid arthritis. Curr Top Med Chem 2013, 13:712-719.
7. Sarkar S., Fox D.A. Dendritic cells in rheumatoid arthritis. Front Biosci 2005, 10:656-665.
8. Wang Z.Y., Morinobu A., Kawano S., Saegusa J., Wang B., Kumagai S. Gold sodium thiomalate suppresses the differentiation and function of human dendritic cells from peripheral blood monocytes. Clin Exp Rheumatol 2002, 20:683-688.
9. Zeyda M., Kirsch B.M., Geyeregger R., Stuhlmeier K.M., Zlabinger G.J., Hörl W.H., et al. Inhibition of human dendritic cell maturation and function by the novel immunosuppressant FK778. Transplantation 2005, 80:1105-1111.
10. Kirsch B.M., Zeyda M., Stuhlmeier K., Grisar J., Smolen J.S., Watschinger B., et al. The active metabolite of leflunomide, A77 1726, interferes with dendritic cell function. Arthritis Res Ther 2005, 7:R694-R703.
11. Wang S., Moustaid-Moussa N., Chen L., Mo H., Shastri A., Su R., et al. Novel insights of dietary polyphenols and obesity. J Nutr Biochem 2014, 25:1-18.
12. Babu P.V., Liu D., Gilbert E.R. Recent advances in understanding the anti-diabetic actions of dietary flavonoids. J Nutr Biochem 2013, 24:1777-1789.
13. Rodriguez-Mateos A., Vauzour D., Krueger C.G., Shanmuganayagam D., Reed J., Calani L., et al. Bioavailability, bioactivity and impact on health of dietary flavonoids and related compounds: an update. Arch Toxicol 2014, 88:1803-1853.
14. Mota K.S., Dias G.E., Pinto M.E., Luiz-Ferreira A., Souza-Brito A.R., Hiruma-Lima C.A., et al. Flavonoids with gastroprotective activity. Molecules 2009, 14:979-1012.
15. Agrawal A.D. Pharmacological activities of flavonoids: a review. Int J Pharm Sci Nanotechnol 2011, 4:1394-1398.
16. Patil C.S., Singh V.P., Satyanarayan P.S., Jain N.K., Singh A., Kulkarni S.K. Protective effect of flavonoids against aging- and lipopolysaccharide-induced cognitive impairment in mice. Pharmacology 2003, 69:59-67.
17. Del Cornò M., Scazzocchio B., Masella R., Gessani S. Regulation of dendritic cell function by dietary polyphenols. Crit Rev Food Sci Nutr 2014, in press.
18. Mir I.A., Tiku A.B. Chemopreventive and therapeutic potential of "naringenin," a flavanone present in citrus fruits. Nutr Cancer 2015, 67:27-42.
19. Patel K., Singh G.K., Patel D.K. A review on pharmacological and analytical aspects of naringenin. Chin J Integr Med 2014, in press.
20. Lv Y., Zhang B., Xing G., Wang F., Hu Z. Protective effect of naringenin against acetaminophen-induced acute liver injury in metallothionein (MT)-null mice. Food Funct 2013, 4:297-302.
21. - mice. J Lipid Res 2013, 54:711-724.
22. Annadurai T., Muralidharan A.R., Joseph T., Hsu M.J., Thomas P.A., Geraldine P. Antihyperglycemic and antioxidant effects of a flavanone, naringenin, in streptozotocin-nicotinamide-induced experimental diabetic rats. J Physiol Biochem 2012, 68:307-318.
23. Du G., Jin L., Han X., Song Z., Zhang H., Liang W. Naringenin: a potential immunomodulator for inhibiting lung fibrosis and metastasis. Cancer Res 2009, 69:3205-3212.
24. Moon P.D., Choi I.H., Kim H.M. Naringenin suppresses the production of thymic stromal lymphopoietin through the blockade of RIP2 and caspase-1 signal cascade in mast cells. Eur J Pharmacol 2011, 671:128-132.
25. Bodet C., La V.D., Epifano F., Grenier D. Naringenin has anti-inflammatory properties in macrophage and ex vivo human whole-blood models. J Periodontal Res 2008, 43:400-407.
26. Fang F., Tang Y., Gao Z., Xu Q. A novel regulatory mechanism of naringenin through inhibition of T lymphocyte function in contact hypersensitivity suppression. Biochem Biophys Res Commun 2010, 397:163-169.
27. Li S., Lin Y.C., Ho C.T., Lin P.Y., Suzawa M., Wang H.C., et al. Formulated extract from multiple citrus peels impairs dendritic cell functions and attenuates allergic contact hypersensitivity. Int Immunopharmacol 2014, 20:12-23.
28. Brand D.D., Latham K.A., Rosloniec E.F. Collagen-induced arthritis. Nat Protoc 2007, 2:1269-1275.
29. Yoo S.A., Park B.H., Park G.S., Koh H.S., Lee M.S., Ryu S.H., et al. Calcineurin is expressed and plays a critical role in inflammatory arthritis. J Immunol 2006, 177:2681-2690.
30. Iwasaki A., Medzhitov R. Toll-like receptor control of the adaptive immune responses. Nat Immunol 2004, 5:987-995.
31. Courtenay J.S., Dallman M.J., Dayan A.D., Martin A., Mosedale B. Immunization against heterologous type II collagen induces arthritis in mice. Nature 1980, 283:666.
32. Azizi G., Jadidi-Niaragh F., Mirshafiey A. Th17 Cells in Immunopathogenesis and treatment of rheumatoid arthritis. Int J Rheum Dis 2013, 16:243-253.
33. Huang R.Y., Yu Y.L., Cheng W.C., OuYang C.N., Fu E., Chu C.L. Immunosuppressive effect of quercetin on dendritic cell activation and function. J Immunol 2010, 15(184):6815-6821.
34. Yoon M.S., Lee J.S., Choi B.M., Jeong Y.I., Lee C.M., Park J.H., et al. Apigenin inhibits immunostimulatory function of dendritic cells: implication of immunotherapeutic adjuvant. Mol Pharmacol 2006, 70:1033-1044.
35. Kim G.Y., Kim K.H., Lee S.H., Yoon M.S., Lee H.J., Moon D.O., et al. Curcumin inhibits immunostimulatory function of dendritic cells: MAPKs and translocation of NF-κB as potential targets. J Immunol 2005, 174:8116-8124.
36. Dou W., Zhang J., Sun A., Zhang E., Ding L., Mukherjee S., et al. Protective effect of naringenin against experimental colitis via suppression of Toll-like receptor 4/NF-κB signalling. Br J Nutr 2013, 110:599-608.
37. Vafeiadou K., Vauzour D., Lee H.Y., Rodriguez-Mateos A., Williams R.J., Spencer J.P. The citrus flavanone naringenin inhibits inflammatory signalling in glial cells and protects against neuroinflammatory injury. Arch Biochem Biophys 2009, 484:100-109.
38. Park H.Y., Kim G.Y., Choi Y.H. Naringenin attenuates the release of pro-inflammatory mediators from lipopolysaccharide-stimulated BV2 microglia by inactivating nuclear factor-κB and inhibiting mitogen-activated protein kinases. Int J Mol Med 2012, 30:204-210.
39. Lin W.C., Lin J.Y. Five bitter compounds display different anti-inflammatory effects through modulating cytokine secretion using mouse primary slenocytes in vitro. J Agric Food Chem 2011, 59:184-192.
40. Parola C., Salogni L., Vaira X., Scutera S., Somma P., Salvi V., et al. Selective activation of human dendritic cells by OM-85 through a NF-kB and MAPK dependent pathway. PLoS One 2013, 8:e82867.
41. Nakahara T., Moroi Y., Uchi H., Furue M. Differential role of MAPK signaling in human dendritic cell maturation and Th1/Th2 engagement. J Dermatol Sci 2006, 42:1-11.
42. Kim G.Y., Kim K.H., Lee S.H., Yoon M.S., Lee H.J., Moon D.O., et al. Curcumin inhibits immunostimulatory function of dendritic cells: MAPKs and translocation of NF-kappa B as potential targets. J Immunol 2005, 174:8116-8124.
43. Ott P.A., Bhardwaj N. Impact of MAPK pathway activation in BRAF(V600) melanoma on T Cell and dendritic cell function. Front Immunol 2013, 4:346.
44. Xu C., Chen J., Zhang J., Hu X., Zhou X., Lu Z., et al. Naringenin inhibits angiotensin II-induced vascular smooth muscle cells proliferation and migration and decreases neointimal hyperplasia in balloon injured rat carotid arteries through suppressing oxidative stress. Biol Pharm Bull 2013, 36:1549-1555.
45. Amakura Y., Tsutsumi T., Sasaki K., Nakamura M., Yoshida T., Maitani T. Influence of food polyphenols on aryl hydrocarbon receptor-signaling pathway estimated by in vitro bioassay. Phytochemistry 2008, 69:3117-3130.
46. Esser C., Rannug A., Stockinger B. The aryl hydrocarbon receptor in immunity. Trends Immunol 2009, 30:447-454.
47. Hao N., Whitelaw M.L. The emerging roles of AhR in physiology and immunity. Biochem Pharmacol 2013, 86:561-570.
48. Wang H.K., Yeh C.H., Iwamoto T., Satsu H., Shimizu M., Totsuka M. Dietary flavonoid naringenin induces regulatory T cells via an aryl hydrocarbon receptor mediated pathway. J Agric Food Chem 2012, 60:2171-2178.
49. Kim T.H., Kim G.D., Ahn H.J., Cho J.J., Park Y.S., Park C.S. The inhibitory effect of naringenin on atopic dermatitis induced by DNFB in NC/Nga mice. Life Sci 2013, 93:516-524.
50. Cooles F.A., Isaacs J.D., Anderson A.E. Treg cells in rheumatoid arthritis: an update. Curr Rheumatol Rep 2013, 15:352.
51. Shi Y., Tan Y., Mao S., Gu W. Naringenin inhibits allergen-induced airway remodeling in a murine model of asthma. Mol Med Rep 2014, 9:1204-1208.
52. Seyedrezazadeh E., Kolahian S., Shahbazfar A.A., Ansarin K., Pour Moghaddam M., Sakhinia M., et al. Effects of the flavanone combination hesperetin-naringenin, and orange and grapefruit juices, on airway inflammation and remodeling in a murine asthma model. Phytother Res 2015, in press.
53. Cooles F.A., Isaacs J.D., Anderson A.E. Treg cells in rheumatoid arthritis: an update. Curr Rheumatol Rep 2013, 15:352.
54. Chao C.L., Weng C.S., Chang N.C., Lin J.S., Kao S.T., Ho F.M. Naringenin more effectively inhibits inducible nitric oxide synthase and cyclooxygenase-2 expression in macrophages than in microglia. Nutr Res 2010, 30:858-864.
55. Lyu S.Y., Park W.B. Production of cytokine and NO by RAW 264.7 macrophages and PBMC in vitro incubation with flavonoids. Arch Pharm Res 2005, 28:573-581.
56. La V.D., Tanabe S., Grenier D. Naringenin inhibits human osteoclastogenesis and osteoclastic bone resorption. J Periodontal Res 2009, 44:193-198.
57. Park M., Kim K., Lee Y.M., Rhyu M.R., Kim H.Y. Naringenin stimulates cholecystokinin secretion in STC-1 cells. Nutr Res Pract 2014, 8:146-150.
58. Cavia-Saiz M., Busto M.D., Pilar-Izquierdo M.C., Ortega N., Perez-Mateos M., Muñiz P. Antioxidant properties, radical scavenging activity and biomolecule protection capacity of flavonoid naringenin and its glycoside naringin: a comparative study. J Sci Food Agric 2010, 90:1238-1244.
59. Zhu L., Wang J., Wei T., Gao J., He H., Chang X., et al. Effects of Naringenin on Inflammation in Complete Freund's Adjuvant-Induced Arthritis by Regulating Bax/Bcl-2 Balance. Inflammation 2015, 38:245-251.
60. Kawaguchi K., Maruyama H., Hasunuma R., Kumazawa Y. Suppression of inflammatory responses after onset of collagen-induced arthritis in mice by oral administration of the citrus flavanone naringin. Immunopharmacol Immunotoxicol 2011, 33:723-729.
61. Ahmad S.F., Zoheir K.M., Abdel-Hamied H.E., Ashour A.E., Bakheet S.A., Attia S.M., et al. Amelioration of autoimmune arthritis by naringin through modulation of T regulatory cells and Th1/Th2 cytokines. Cell Immunol 2014, 287:112-120.
62. Kanaze F.I., Bounartzi M.I., Georgarakis M., Niopas I. Pharmacokinetics of the citrus flavanone aglycones hesperetin and naringenin after single oral administration in human subjects. Eur J Clin Nutr 2007, 61:472-477.
63. Erlund I., Meririnne E., Alfthan G., Aro A. Plasma kinetics and urinary excretion of the flavanones naringenin and hesperetin in humans after ingestion of orange juice and grapefruit juice. J Nutr 2001, 131:235-241.
64. Breinholt V.M., Svendsen G.W., Dragsted L.O., Hossaini A. The citrus-derived flavonoid naringenin exerts uterotrophic effects in female mice at human relevant doses. Basic Clin Pharmacol Toxicol 2004, 94:30-36.