Grape seed proanthocyanidin extract-mediated regulation of STAT3 proteins contributes to Treg differentiation and attenuates inflammation in a murine model of obesity-associated arthritis

PLoS ONE

Volumn 8, Issue 11, 2013, Pages

  Jhun, Joo Yeon ^a   Moon, Su Jin ^a   Yoon, Bo Young ^b   Byun, Jae Kyung ^a   Kim, Eun Kyung ^a   Yang, Eun Ji ^a   Ju, Ji Hyeon ^a   Hong, Yeon Sik ^a   Min, Jun Ki ^a   Park, Sung Hwan ^a   Kim, Ho Youn ^a   Cho, Mi La ^a  

^a The Catholic University of Korea   (South Korea)

^b Inje University   (South Korea)

Author keywords

[No Author keywords available]

Indexed keywords

3 NITROTYROSINE; CYTOKINE; FLAVONOID; GRAPE SEED PROANTHOCYANIDIN EXTRACT; LIPID; STAT3 PROTEIN; STAT5 PROTEIN; UNCLASSIFIED DRUG;

ANIMAL CELL; ANIMAL EXPERIMENT; ANIMAL MODEL; ANIMAL TISSUE; ANTIINFLAMMATORY ACTIVITY; ARTICLE; CONTROLLED STUDY; DISEASE SEVERITY; IN VIVO STUDY; LIPID BLOOD LEVEL; LIPID DIET; LIPID STORAGE; LYMPHOCYTE DIFFERENTIATION; MOUSE; NONHUMAN; OBESITY; PROTEIN EXPRESSION; REGULATORY T LYMPHOCYTE; RHEUMATOID ARTHRITIS; SYNOVIUM; TH17 CELL; WEIGHT GAIN;

ADMINISTRATION, ORAL; ANIMALS; ARTHRITIS; ARTHRITIS, EXPERIMENTAL; CELL DIFFERENTIATION; CYTOKINES; DIET, HIGH-FAT; DISEASE MODELS, ANIMAL; GENE EXPRESSION; GRAPE SEED EXTRACT; HUMANS; INFLAMMATION; INFLAMMATION MEDIATORS; MICE, INBRED C57BL; MICROSCOPY, CONFOCAL; OBESITY; PROANTHOCYANIDINS; REVERSE TRANSCRIPTASE POLYMERASE CHAIN REACTION; STAT3 TRANSCRIPTION FACTOR; T-LYMPHOCYTES, REGULATORY; TH17 CELLS;

EID: 84892419264     PISSN: None     EISSN: 19326203     Source Type: Journal    
DOI: 10.1371/journal.pone.0078843     Document Type: Article

References (37)

1. Rasmussen SE, Frederiksen H, Struntze Krogholm K, Poulsen L (2005) Dietary proanthocyanidins: occurrence, dietary intake, bioavailability, and protection against cardiovascular disease. Mol Nutr Food Res 49: 159-174.
2. Bagchi D, Bagchi M, Stohs SJ, Das DK, Ray SD, et al. (2000) Free radicals and grape seed proanthocyanidin extract: importance in human health and disease prevention. Toxicology 148: 187-197.
3. Blade C, Arola L, Salvado MJ (2010) Hypolipidemic effects of proanthocyanidins and their underlying biochemical and molecular mechanisms. Mol Nutr Food Res 54: 37-59.
4. Terra X, Montagut G, Bustos M, Llopiz N, Ardevol A, et al. (2009) Grape-seed procyanidins prevent low-grade inflammation by modulating cytokine expression in rats fed a high-fat diet. J Nutr Biochem 20: 210-218.
5. Pajuelo D, Quesada H, Diaz S, Fernandez-Iglesias A, Arola-Arnal A, et al. (2012) Chronic dietary supplementation of proanthocyanidins corrects the mitochondrial dysfunction of brown adipose tissue caused by diet-induced obesity in Wistar rats. Br J Nutr 107: 170-178.
6. Thiruchenduran M, Vijayan NA, Sawaminathan JK, Devaraj SN (2011) Protective effect of grape seed proanthocyanidins against cholesterol cholic acid diet-induced hypercholesterolemia in rats. Cardiovasc Pathol 20: 361-368.
7. Li WG, Zhang XY, Wu YJ, Tian X (2001) Anti-inflammatory effect and mechanism of proanthocyanidins from grape seeds. Acta Pharmacol Sin 22: 1117-1120.
8. Tilg H, Moschen AR (2006) Adipocytokines: mediators linking adipose tissue, inflammation and immunity. Nat Rev Immunol 6: 772-783.
9. La Cava A, Matarese G (2004) The weight of leptin in immunity. Nat Rev Immunol 4: 371-379.
10. Weisberg SP, McCann D, Desai M, Rosenbaum M, Leibel RL, et al. (2003) Obesity is associated with macrophage accumulation in adipose tissue. J Clin Invest 112: 1796-1808.
11. Fantuzzi G (2005) Adipose tissue, adipokines, and inflammation. J Allergy Clin Immunol 115: 911-919; quiz 920.
12. Gainsford T, Willson TA, Metcalf D, Handman E, McFarlane C, et al. (1996) Leptin can induce proliferation, differentiation, and functional activation of hemopoietic cells. Proc Natl Acad Sci U S A 93: 14564-14568.
13. Matarese G, Moschos S, Mantzoros CS (2005) Leptin in immunology. J Immunol 174: 3137-3142.
14. Lord GM, Matarese G, Howard JK, Baker RJ, Bloom SR, et al. (1998) Leptin modulates the T-cell immune response and reverses starvation-induced immunosuppression. Nature 394: 897-901.
15. Feuerer M, Herrero L, Cipolletta D, Naaz A, Wong J, et al. (2009) Lean, but not obese, fat is enriched for a unique population of regulatory T cells that affect metabolic parameters. Nat Med 15: 930-939.
16. Winer S, Paltser G, Chan Y, Tsui H, Engleman E, et al. (2009) Obesity predisposes to Th17 bias. Eur J Immunol 39: 2629-2635.
17. Woo YJ, Joo YB, Jung YO, Ju JH, Cho ML, et al. (2011) Grape seed proanthocyanidin extract ameliorates monosodium iodoacetate-induced osteoarthritis. Exp Mol Med 43: 561-570.
18. Cho ML, Heo YJ, Park MK, Oh HJ, Park JS, et al. (2009) Grape seed proanthocyanidin extract (GSPE) attenuates collagen-induced arthritis. Immunol Lett 124: 102-110.
19. Jhun JY, Yoon BY, Park MK, Oh HJ, Byun JK, et al. (2012) Obesity aggravates the joint inflammation in a collagen-induced arthritis model through deviation to Th17 differentiation. Exp Mol Med 44: 424-431.
20. Inglis JJ, Simelyte E, McCann FE, Criado G, Williams RO (2008) Protocol for the induction of arthritis in C57BL/6 mice. Nat Protoc 3: 612-618.
21. Camps M, Ruckle T, Ji H, Ardissone V, Rintelen F, et al. (2005) Blockade of PI3Kgamma suppresses joint inflammation and damage in mouse models of rheumatoid arthritis. Nat Med 11: 936-943.
22. Rosloniec EF, Cremer M, Kang A, Myers LK (2001) Collagen-induced arthritis. Curr Protoc Immunol Chapter 15: Unit 15 15.
23. Durant L, Watford WT, Ramos HL, Laurence A, Vahedi G, et al. (2010) Diverse targets of the transcription factor STAT3 contribute to T cell pathogenicity and homeostasis. Immunity 32: 605-615.
24. Antov A, Yang L, Vig M, Baltimore D, Van Parijs L (2003) Essential role for STAT5 signaling in CD25+CD4+ regulatory T cell homeostasis and the maintenance of self-tolerance. J Immunol 171: 3435-3441.
25. Sakaguchi S, Sakaguchi N, Asano M, Itoh M, Toda M (1995) Immunologic self-tolerance maintained by activated T cells expressing IL-2 receptor alpha-chains (CD25). Breakdown of a single mechanism of self-tolerance causes various autoimmune diseases. J Immunol 155: 1151-1164.
26. Shevach EM, McHugh RS, Thornton AM, Piccirillo C, Natarajan K, et al. (2001) Control of autoimmunity by regulatory T cells. Adv Exp Med Biol 490: 21-32.
27. Lazarevic V, Chen X, Shim JH, Hwang ES, Jang E, et al. (2011) T-bet represses T(H)17 differentiation by preventing Runx1-mediated activation of the gene encoding RORgammat. Nat Immunol 12: 96-104.
28. Murray PJ (2007) The JAK-STAT signaling pathway: input and output integration. J Immunol 178: 2623-2629.
29. van Marken Lichtenbelt WD, Vanhommerig JW, Smulders NM, Drossaerts JM, Kemerink GJ, et al. (2009) Cold-activated brown adipose tissue in healthy men. N Engl J Med 360: 1500-1508.
30. Maddur MS, Miossec P, Kaveri SV, Bayry J (2012) Th17 cells: biology, pathogenesis of autoimmune and inflammatory diseases, and therapeutic strategies. Am J Pathol 181: 8-18.
31. Chaudhry A, Rudra D, Treuting P, Samstein RM, Liang Y, et al. (2009) CD4+ regulatory T cells control TH17 responses in a Stat3-dependent manner. Science 326: 986-991.
32. Wang D, Zhou Y, Lei W, Zhang K, Shi J, et al. (2010) Signal transducer and activator of transcription 3 (STAT3) regulates adipocyte differentiation via peroxisome-proliferator-activated receptor gamma (PPARgamma). Biol Cell 102: 1-12.
33. Bates SH, Stearns WH, Dundon TA, Schubert M, Tso AW, et al. (2003) STAT3 signalling is required for leptin regulation of energy balance but not reproduction. Nature 421: 856-859.
34. Sos BC, Harris C, Nordstrom SM, Tran JL, Balazs M, et al. (2011) Abrogation of growth hormone secretion rescues fatty liver in mice with hepatocyte-specific deletion of JAK2. J Clin Invest 121: 1412-1423.
35. Cui Y, Hosui A, Sun R, Shen K, Gavrilova O, et al. (2007) Loss of signal transducer and activator of transcription 5 leads to hepatosteatosis and impaired liver regeneration. Hepatology 46: 504-513.
36. Barclay JL, Nelson CN, Ishikawa M, Murray LA, Kerr LM, et al. (2011) GH-dependent STAT5 signaling plays an important role in hepatic lipid metabolism. Endocrinology 152: 181-192.
37. Park MK, Park JS, Cho ML, Oh HJ, Heo YJ, et al. (2011) Grape seed proanthocyanidin extract (GSPE) differentially regulates Foxp3(+) regulatory and IL-17(+) pathogenic T cell in autoimmune arthritis. Immunol Lett 135: 50-58.