Chrysin attenuates inflammation by regulating M1/M2 status via activating PPARγ

Biochemical Pharmacology

Volumn 89, Issue 4, 2014, Pages 503-514

  Feng, Xiujing ^a   Qin, Haohan ^a   Shi, Qian ^b   Zhang, Yang ^a   Zhou, Feifei ^a   Wu, Haochen ^a   Ding, Sen ^a   Niu, Zhiyuan ^a   Lu, Yan ^a   Shen, Pingping ^a  

^a NANJING UNIVERSITY   (China)

^b Mays Cancer Center at UT Health San Antonio   (United States)

Author keywords

Chrysin; Inflammation; M1 M2 status; PPAR

Indexed keywords

CHRYSIN; PEROXISOME PROLIFERATOR ACTIVATED RECEPTOR GAMMA;

ADIPOSE TISSUE; ANIMAL CELL; ANIMAL EXPERIMENT; ANIMAL MODEL; ANIMAL TISSUE; ANTIINFLAMMATORY ACTIVITY; ARTICLE; BODY WEIGHT; CELL CULTURE; CONTROLLED STUDY; FATTY LIVER; GENE EXPRESSION; GENE TARGETING; HUMAN; HUMAN CELL; IN VITRO STUDY; INFLAMMATION; INFLAMMATORY DISEASE; LIPID DIET; MALE; MOUSE; NONHUMAN; OBESITY; PATHOGENESIS; PERITONEUM MACROPHAGE; PHENOTYPE; PRIORITY JOURNAL; TRANSCRIPTION INITIATION;

CHRYSIN; INFLAMMATION; M1/M2 STATUS; PPARΓ;

ADIPOSE TISSUE; ANIMALS; ANTI-INFLAMMATORY AGENTS, NON-STEROIDAL; CELL DIVISION; CELL LINE, TRANSFORMED; CELL SURVIVAL; CELLS, CULTURED; DOSE-RESPONSE RELATIONSHIP, DRUG; FATTY LIVER; FLAVONOIDS; HUMANS; LIVER; MACROPHAGES, PERITONEAL; MALE; MICE; MICE, INBRED C57BL; MUSCLE, SKELETAL; MYOSITIS; OBESITY; PPAR GAMMA; RANDOM ALLOCATION; SPECIFIC PATHOGEN-FREE ORGANISMS; TRANSCRIPTION, GENETIC;

EID: 84901636216     PISSN: 00062952     EISSN: 18732968     Source Type: Journal    
DOI: 10.1016/j.bcp.2014.03.016     Document Type: Article

References (63)

1. R. Milanino, and V. Buchner Copper: role of the 'endogenous' and 'exogenous' metal on the development and control of inflammatory processes Rev Environ Health 21 3 2006 153 215 (Pubitemid 46030347)
2. C. Nathan, and A. Ding Nonresolving inflammation Cell 140 6 2010 871 882
3. N. Fujiwara, and K. Kobayashi Macrophages in inflammation Curr Drug Targets Inflamm Allergy 4 3 2005 281 286 (Pubitemid 40873112)
4. G. Chinetti-Gbaguidi, and B. Staels Macrophage polarization in metabolic disorders: functions and regulation Curr Opin Lipidol 22 5 2011 365 372
5. A. Mantovani, A. Sica, and M. Locati Macrophage polarization comes of age Immunity 23 4 2005 344 346 (Pubitemid 41443435)
6. A. Mantovani, A. Sica, S. Sozzani, P. Allavena, A. Vecchi, and M. Locati The chemokine system in diverse forms of macrophage activation and polarization Trends Immunol 25 12 2004 677 686 (Pubitemid 39457982)
7. J.I. Odegaard, R.R. Ricardo-Gonzalez, A. Red Eagle, D. Vats, C.R. Morel, and M.H. Goforth et al. Alternative M2 activation of Kupffer cells by PPARdelta ameliorates obesity-induced insulin resistance Cell Metab 7 6 2008 496 507 (Pubitemid 351729205)
8. J.I. Odegaard, R.R. Ricardo-Gonzalez, M.H. Goforth, C.R. Morel, V. Subramanian, and L. Mukundan et al. Macrophage-specific PPARgamma controls alternative activation and improves insulin resistance Nature 447 7148 2007 1116 1120 (Pubitemid 47014427)
9. S. Fujisaka, I. Usui, A. Bukhari, M. Ikutani, T. Oya, and Y. Kanatani et al. Regulatory mechanisms for adipose tissue M1 and M2 macrophages in diet-induced obese mice Diabetes 58 11 2009 2574 2582
10. C.N. Lumeng, J.L. Bodzin, and A.R. Saltiel Obesity induces a phenotypic switch in adipose tissue macrophage polarization J Clin Invest 117 1 2007 175 184 (Pubitemid 46048464)
11. F.O. Martinez, A. Sica, A. Mantovani, and M. Locati Macrophage activation and polarization Front Biosci 13 2008 453 461 (Pubitemid 351599757)
12. X.M. Yu, T. Phan, P.N. Patel, R. Jaskula-Sztul, and H. Chen Chrysin activates Notch1 signaling and suppresses tumor growth of anaplastic thyroid carcinoma in vitro and in vivo Cancer 119 4 2013 774 781
13. S. Sultana, K. Verma, and R. Khan Nephroprotective efficacy of chrysin against cisplatin-induced toxicity via attenuation of oxidative stress J Pharm Pharmacol 64 6 2012 872 881
14. D. Sirovina, N. Orsolic, M.Z. Koncic, G. Kovacevic, V. Benkovic, and G. Gregorovic Quercetin vs chrysin: effect on liver histopathology in diabetic mice Hum Exp Toxicol 32 10 2013 1058 1066
15. S. Hougee, A. Sanders, J. Faber, Y.M. Graus, W.B. van den Berg, and J. Garssen et al. Decreased pro-inflammatory cytokine production by LPS-stimulated PBMC upon in vitro incubation with the flavonoids apigenin, luteolin or chrysin, due to selective elimination of monocytes/macrophages Biochem Pharmacol 69 2 2005 241 248 (Pubitemid 41556570)
16. K.J. Woo, Y.J. Jeong, H. Inoue, J.W. Park, and T.K. Kwon Chrysin suppresses lipopolysaccharide-induced cyclooxygenase-2 expression through the inhibition of nuclear factor for IL-6 (NF-IL6) DNA-binding activity FEBS Lett 579 3 2005 705 711
17. Q. Du, X. Gu, J. Cai, M. Huang, and M. Su Chrysin attenuates allergic airway inflammation by modulating the transcription factors T-bet and GATA-3 in mice Mol Med Rep 6 1 2012 100 104
18. C.J. Liu, and J.Y. Lin Anti-inflammatory effects of phenolic extracts from strawberry and mulberry fruits on cytokine secretion profiles using mouse primary splenocytes and peritoneal macrophages Int Immunopharmacol 16 2 2013 165 170
19. Y. Bae, S. Lee, and S.H. Kim Chrysin suppresses mast cell-mediated allergic inflammation: involvement of calcium, caspase-1 and nuclear factor-kappaB Toxicol Appl Pharmacol 254 1 2011 56 64
20. J.T. Huang, J.S. Welch, M. Ricote, C.J. Binder, T.M. Willson, and C. Kelly et al. Interleukin-4-dependent production of PPAR-gamma ligands in macrophages by 12/15-lipoxygenase Nature 400 6742 1999 378 382 (Pubitemid 29344205)
21. D. Vats, L. Mukundan, J.I. Odegaard, L. Zhang, K.L. Smith, and C.R. Morel et al. Oxidative metabolism and PGC-1beta attenuate macrophage-mediated inflammation Cell Metab 4 1 2006 13 24 (Pubitemid 43942258)
22. M.A. Bouhlel, B. Derudas, E. Rigamonti, R. Dievart, J. Brozek, and S. Haulon et al. PPARgamma activation primes human monocytes into alternative M2 macrophages with anti-inflammatory properties Cell Metab 6 2 2007 137 143 (Pubitemid 47189091)
23. E. Rigamonti, G. Chinetti-Gbaguidi, and B. Staels Regulation of macrophage functions by PPAR-alpha, PPAR-gamma, and LXRs in mice and men Arterioscler Thromb Vasc Biol 28 6 2008 1050 1059
24. L.S. Doshi, M.K. Brahma, U.A. Bahirat, A.V. Dixit, and K.V. Nemmani Discovery and development of selective PPAR gamma modulators as safe and effective antidiabetic agents Expert Opin Invest Drugs 19 4 2010 489 512
25. E.K. Shin, H.S. Kwon, Y.H. Kim, H.K. Shin, and J.K. Kim Chrysin, a natural flavone, improves murine inflammatory bowel diseases Biochem Biophys Res Commun 381 4 2009 502 507
26. Y. Bae, S. Lee, and S.H. Kim Chrysin suppresses mast cell-mediated allergic inflammation: Involvement of calcium, caspase-1 and nuclear factor-kappa B Toxicol Appl Pharmacol 254 1 2011 56 64
27. L.Z. Liu, J. Fang, Q. Zhou, X. Hu, X. Shi, and B.H. Jiang Apigenin inhibits expression of vascular endothelial growth factor and angiogenesis in human lung cancer cells: implication of chemoprevention of lung cancer Mol Pharmacol 68 3 2005 635 643 (Pubitemid 41206017)
28. W. Dou, J. Zhang, E. Zhang, A. Sun, L. Ding, and G. Chou et al. Chrysin ameliorates chemically induced colitis in the mouse through modulation of a PXR/NF-kappaB signaling pathway J Pharmacol Exp Ther 345 3 2013 473 482
29. S.G. Sheth, F.D. Gordon, and S. Chopra Nonalcoholic steatohepatitis Ann Intern Med 126 2 1997 137 145 (Pubitemid 27058588)
30. I. Guevara, J. Iwanejko, A. Dembinska-Kiec, J. Pankiewicz, A. Wanat, and P. Anna et al. Determination of nitrite/nitrate in human biological material by the simple Griess reaction Clin Chim Acta 274 2 1998 177 188 (Pubitemid 28269300)
31. K.J. Livak, and T.D. Schmittgen Analysis of relative gene expression data using real-time quantitative PCR and the 2(-Delta Delta C(T)) method Methods 25 4 2001 402 408 (Pubitemid 34164012)
32. W. Yang, Y. Lu, Y. Xu, L. Xu, W. Zheng, and Y. Wu et al. Estrogen represses hepatocellular carcinoma (HCC) growth via inhibiting alternative activation of tumor-associated macrophages (TAMs) J Biol Chem 287 48 2012 40140 40149
33. B.A. Weeks, A.S. Keisler, Q.N. Myrvik, and J.E. Warinner Differential uptake of neutral red by macrophages from three species of estuarine fish Dev Comp Immunol 11 1 1987 117 124
34. X. Pang, Y. Wei, Y. Zhang, M. Zhang, Y. Lu, and P. Shen Peroxisome proliferator-activated receptor-gamma activation inhibits hepatocellular carcinoma cell invasion by upregulating plasminogen activator inhibitor-1 Cancer Sci 104 6 2013 672 680
35. X. Bao, J. Cui, Y. Wu, X. Han, C. Gao, and Z. Hua et al. The roles of endogenous reactive oxygen species and nitric oxide in triptolide-induced apoptotic cell death in macrophages J Mol Med (Berl) 85 1 2007 85 98 (Pubitemid 46020945)
36. M. Ricote, A.C. Li, T.M. Willson, C.J. Kelly, and C.K. Glass The peroxisome proliferator-activated receptor-gamma is a negative regulator of macrophage activation Nature 391 6662 1998 79 82 (Pubitemid 28079218)
37. B.B. Kahn, and J.S. Flier Obesity and insulin resistance J Clin Invest 106 4 2000 473 481 (Pubitemid 30666380)
38. J. Wilding Obesity and type 2 diabetes mellitus Diabet Med 17 5 2000 400 402 (Pubitemid 30353810)
39. M.A. Miller, and F.P. Cappuccio Inflammation, sleep, obesity and cardiovascular disease Curr Vasc Pharmacol 5 2 2007 93 102
40. S. Chitturi, S. Abeygunasekera, G.C. Farrell, J. Holmes-Walker, J.M. Hui, and C. Fung et al. NASH and insulin resistance: insulin hypersecretion and specific association with the insulin resistance syndrome Hepatology 35 2 2002 373 379 (Pubitemid 34106377)
41. E.E. Calle, and M.J. Thun Obesity and cancer Oncogene 23 38 2004 6365 6378 (Pubitemid 39265505)
42. E.J.B. Ramos, Y. Xu, I. Romanova, F. Middleton, C. Chen, and R. Quinn et al. Is obesity an inflammatory disease? Surgery 134 2 2003 329 335 (Pubitemid 37070357)
43. T. Goto, Y.I. Kim, N. Takahashi, and T. Kawada Natural compounds regulate energy metabolism by the modulating the activity of lipid-sensing nuclear receptors Mol Nutr Food Res 57 1 2013 20 33
44. T. Sohda, K. Meguro, and Y. Kawamatsu Studies on antidiabetic agents. IV. Synthesis and activity of the metabolites of 5-[4-(1-methylcyclohexylmethoxy) benzyl] -2,4-thiazolidinedione (ciglitazone) Chem Pharm Bull (Tokyo) 32 6 1984 2267 2278 (Pubitemid 14084196)
45. C.L. Tsou, W. Peters, Y. Si, S. Slaymaker, A.M. Aslanian, and S.P. Weisberg et al. Critical roles for CCR2 and MCP-3 in monocyte mobilization from bone marrow and recruitment to inflammatory sites J Clin Invest 117 4 2007 902 909 (Pubitemid 46556746)
46. S.P. Weisberg, D. Hunter, R. Huber, J. Lemieux, S. Slaymaker, and K. Vaddi et al. CCR2 modulates inflammatory and metabolic effects of high-fat feeding J Clin Invest 116 1 2006 115 124 (Pubitemid 43121796)
47. M.C. Arkan, A.L. Hevener, F.R. Greten, S. Maeda, Z.W. Li, and J.M. Long et al. IKK-beta links inflammation to obesity-induced insulin resistance Nat Med 11 2 2005 191 198 (Pubitemid 40321355)
48. H. Kanda, S. Tateya, Y. Tamori, K. Kotani, K. Hiasa, and R. Kitazawa et al. MCP-1 contributes to macrophage infiltration into adipose tissue, insulin resistance, and hepatic steatosis in obesity J Clin Invest 116 6 2006 1494 1505
49. S.P. Weisberg, D. McCann, M. Desai, M. Rosenbaum, R.L. Leibel, and A.W. Ferrante Jr. Obesity is associated with macrophage accumulation in adipose tissue J Clin Invest 112 12 2003 1796 1808 (Pubitemid 38063703)
50. J.M. Bruun, J.W. Helge, B. Richelsen, and B. Stallknecht Diet and exercise reduce low-grade inflammation and macrophage infiltration in adipose tissue but not in skeletal muscle in severely obese subjects Am J Physiol Endocrinol Metab 290 5 2006 E961 E967
51. S. Gordon, and P.R. Taylor Monocyte and macrophage heterogeneity Nat Rev Immunol 5 12 2005 953 964 (Pubitemid 41746764)
52. N. Kawanishi, H. Yano, Y. Yokogawa, and K. Suzuki Exercise training inhibits inflammation in adipose tissue via both suppression of macrophage infiltration and acceleration of phenotypic switching from M1 to M2 macrophages in high-fat-diet-induced obese mice Exerc Immunol Rev 16 2010 105 118
53. K.T. Uysal, S.M. Wiesbrock, M.W. Marino, and G.S. Hotamisligil Protection from obesity-induced insulin resistance in mice lacking TNF-alpha function Nature 389 6651 1997 610 614 (Pubitemid 27446179)
54. D. Patsouris, P.P. Li, D. Thapar, J. Chapman, J.M. Olefsky, and J.G. Neels Ablation of CD11c-positive cells normalizes insulin sensitivity in obese insulin resistant animals Cell Metab 8 4 2008 301 309
55. T. Lawrence, and G. Natoli Transcriptional regulation of macrophage polarization: enabling diversity with identity Nat Rev Immunol 11 11 2011 750 761
56. P. Mandal, B.T. Pratt, M. Barnes, M.R. McMullen, and L.E. Nagy Molecular mechanism for adiponectin-dependent M2 macrophage polarization: link between the metabolic and innate immune activity of full-length adiponectin J Biol Chem 286 15 2011 13460 13469
57. X. Yang, J. Gartner, L. Zhu, S. Wang, and R.C. Brunham IL-10 gene knockout mice show enhanced Th1-like protective immunity and absent granuloma formation following Chlamydia trachomatis lung infection J Immunol 162 2 1999 1010 1017 (Pubitemid 29035428)
58. A. Mantovani, S. Sozzani, M. Locati, P. Allavena, and A. Sica Macrophage polarization: tumor-associated macrophages as a paradigm for polarized M2 mononuclear phagocytes Trends Immunol 23 11 2002 549 555 (Pubitemid 35223554)
59. J.M. Lehmann, L.B. Moore, T.A. Smith-Oliver, W.O. Wilkison, T.M. Willson, and S.A. Kliewer An antidiabetic thiazolidinedione is a high affinity ligand for peroxisome proliferator-activated receptor gamma (PPAR gamma) J Biol Chem 270 22 1995 12953 12956
60. F. Picard, and J. Auwerx PPAR(gamma) and glucose homeostasis Annu Rev Nutr 22 2002 167 197
61. Y.C. Liang, S.H. Tsai, D.C. Tsai, S.Y. Lin-Shiau, and J.K. Lin Suppression of inducible cyclooxygenase and nitric oxide synthase through activation of peroxisome proliferator-activated receptor-gamma by flavonoids in mouse macrophages FEBS Lett 496 1 2001 12 18
62. L.M. Leesnitzer, D.J. Parks, R.K. Bledsoe, J.E. Cobb, J.L. Collins, and T.G. Consler et al. Functional consequences of cysteine modification in the ligand binding sites of peroxisome proliferator activated receptors by GW9662 Biochemistry 41 21 2002 6640 6650 (Pubitemid 34547354)
63. N.K. Salam, T.H. Huang, B.P. Kota, M.S. Kim, Y. Li, and D.E. Hibbs Novel PPAR-gamma agonists identified from a natural product library: a virtual screening, induced-fit docking and biological assay study Chem Biol Drug Des 71 1 2008 57 70