Ginsenoside Rh1 potentiates dexamethasone’s anti-inflammatory effects for chronic inflammatory disease by reversing dexamethasone-induced resistance

Arthritis Research & Therapy - Tập 16 - Trang 1-11 - 2014
Jun Li1, Juan Du1, Dong Liu1, Binbin Cheng1, Fanfu Fang1, Li Weng1, Chen Wang1, Changquan Ling1
1Department of Traditional Chinese Medicine, Changhai Hospital, Second Military Medical University, Shanghai, P.R. China

Tóm tắt

Acquired resistance to glucocorticoids constitutes a major clinical challenge, often overlooked in the search for compounds to improve the effect of classic steroids. We sought to unravel how a plant-original compound, ginsenoside Rh1, potentiates dexmethasone (DEX)’s potential anti-inflammation properties. Ginsenoside Rh1 combined with DEX was applied in a short-term and long-term treatment protocol for inflammation. Its potential mechanism on anti-inflammation was explored. In addition, the effect of Rh1 on the side-effect induced by DEX was studied. Furthermore, the in vivo anti-inflammatory effects of Rh1 combined with DEX were evaluated in a collagen-induced arthritis (CIA) mice model. Ginsenoside Rh1 potentiates DEX’s anti-inflammatory effects even after prolonged DEX treatment. Rh1 could improve the glucocorticoid receptor (GR)’s transrepression on nuclear factor kappa B (NF-κB) and transactivation on dual specificity protein phosphatase 1 (DUSP1), which is responsible for DEX’s anti-inflammatory effects. Parallel Western blot assay and radioligand binding analysis revealed that Rh1 could increase the expression and binding of GR. This is in sharp contrast to DEX alone, showing a direct link among prolonged treatment, decreasing GR and the abolishment of anti-inflammation. Interestingly, Rh1 does not enhance the transactivation of glucocorticoid-responsive elements (GRE) driven genes - gluconeogenic enzyme glucose-6-phosphatase (G6P) and phosphoenolpyruvate carboxykinasee phosphatase (PEPCK) in primary mouse hepatocytes, a mechanism partly held accountable for the metabolic side-effects. Similar results were found in CIA mice. Rh1 could potentiate DEX’s anti-inflammatory effects and does not cause a hyperglycemic side effect. Ginsenoside Rh1 combined with DEX may be a promising candidate treatment option for chronic inflammatory diseases in need of long-term immunosuppression therapies.

Tài liệu tham khảo

Sliwinska-Stanczyk P, Pazdur J, Ziolkowska M, Jaworski J, Kaminska-Tchorzewska E, Lacki JK: The effect of methylprednisolone on proliferation of PBMCs obtained from steroid-sensitive and steroid-resistant rheumatoid arthritis patients. Scand J Rheumatol. 2007, 36: 167-171. Kirwan JR: Glucocorticoid resistance in patients with rheumatoid arthritis. Scand J Rheumatol. 2007, 36: 165-166. Schaaf MJ, Cidlowski JA: Molecular mechanisms of glucocorticoid action and resistance. J Steroid Biochem Mol Biol. 2002, 83: 37-48. Buttgereit F, Saag KG, Cutolo M, da Silva JA, Bijlsma JW: The molecular basis for the effectiveness, toxicity, and resistance to glucocorticoids: focus on the treatment of rheumatoid arthritis. Scand J Rheumatol. 2005, 34: 14-21. Ramamoorthy S, Cidlowski JA: Exploring the molecular mechanisms of glucocorticoid receptor action from sensitivity to resistance. Endocr Dev. 2013, 24: 41-56. Barnes PJ: Anti-inflammatory actions of glucocorticoids: molecular mechanisms. Clin Sci (Lond). 1998, 94: 557-572. Vayssiere BM, Dupont S, Choquart A, Petit F, Garcia T, Marchandeau C, Gronemeyer H, Resche-Rigon M: Synthetic glucocorticoids that dissociate transactivation and AP-1 transrepression exhibit antiinflammatory activity in vivo. Mol Endocrinol. 1997, 11: 1245-1255. Schacke H, Rehwinkel H, Asadullah K: Dissociated glucocorticoid receptor ligands: compounds with an improved therapeutic index. Curr Opin Investig Drugs. 2005, 6: 503-507. Gossye V, Elewaut D, Van Beneden K, Dewint P, Haegeman G, De Bosscher K: A plant-derived glucocorticoid receptor modulator attenuates inflammation without provoking ligand-induced resistance. Ann Rheum Dis. 2010, 69: 291-296. Elenkov IJ, Chrousos GP: Stress hormones, proinflammatory and antiinflammatory cytokines, and autoimmunity. Ann N Y Acad Sci. 2002, 966: 290-303. Vollmer TR, Stockhausen A, Zhang JZ: Anti-inflammatory effects of mapracorat, a novel selective glucocorticoid receptor agonist, is partially mediated by MAP kinase phosphatase-1 (MKP-1). J Biol Chem. 2012, 287: 35212-35221. Perretti M, D’Acquisto F: Annexin A1 and glucocorticoids as effectors of the resolution of inflammation. Nat Rev Immunol. 2009, 9: 62-70. Coghlan MJ, Jacobson PB, Lane B, Nakane M, Lin CW, Elmore SW, Kym PR, Luly JR, Carter GW, Turner R, Tyree CM, Hu J, Elgort M, Rosen J, Miner JN: A novel antiinflammatory maintains glucocorticoid efficacy with reduced side effects. Mol Endocrinol. 2003, 17: 860-869. De Bosscher K, Vanden Berghe W, Beck IM, Van Molle W, Hennuyer N, Hapgood J, Libert C, Staels B, Louw A, Haegeman G: A fully dissociated compound of plant origin for inflammatory gene repression. Proc Natl Acad Sci U S A. 2005, 102: 15827-15832. Schacke H, Schottelius A, Docke WD, Strehlke P, Jaroch S, Schmees N, Rehwinkel H, Hennekes H, Asadullah K: Dissociation of transactivation from transrepression by a selective glucocorticoid receptor agonist leads to separation of therapeutic effects from side effects. Proc Natl Acad Sci U S A. 2004, 101: 227-232. Ling C, Li M, Tan J: [Experimental study on protective effect of Chinese herbal medicine on glucocorticoid receptor]. Zhongguo Zhong xi yi jie he za zhi. 1999, 19: 302-303. Li M, Ling CQ, Huang XQ, Shen ZL: [Effects of ginsenosides extracted from ginseng stem and leaves on glucocorticoid receptor in different viscera in heat-damaged rats]. Zhong Xi Yi Jie He Xue Bao. 2006, 4: 156-159. Binbin C, Yinglu F, Juan D, Changquan L: Upregulation effect of ginsenosides on glucocorticoid receptor in rat liver. Horm Metab Res. 2009, 41: 531-536. Wang Y, Singh R, Xiang Y, Greenbaum LE, Czaja MJ: Nuclear factor kappaB up-regulation of CCAAT/enhancer-binding protein beta mediates hepatocyte resistance to tumor necrosis factor alpha toxicity. Hepatology. 2010, 52: 2118-2126. Du J, Cheng B, Zhu X, Ling C: Ginsenoside Rg1, a novel glucocorticoid receptor agonist of plant origin, maintains glucocorticoid efficacy with reduced side effects. J Immunol. 2011, 187: 942-950. Ding DF, Li XF, Xu H, Wang Z, Liang QQ, Li CG, Wang YJ: Mechanism of resveratrol on the promotion of induced pluripotent stem cells. J Integr Med. 2013, 11: 389-396. Miner JN, Ardecky B, Benbatoul K, Griffiths K, Larson CJ, Mais DE, Marschke K, Rosen J, Vajda E, Zhi L, Negro-Vilar A: Antiinflammatory glucocorticoid receptor ligand with reduced side effects exhibits an altered protein-protein interaction profile. Proc Natl Acad Sci U S A. 2007, 104: 19244-19249. Anthony DD, Haqqi TM: Collagen-induced arthritis in mice: an animal model to study the pathogenesis of rheumatoid arthritis. Clin Exp Rheumatol. 1999, 17: 240-244. Barnes PJ, Adcock IM: Glucocorticoid resistance in inflammatory diseases. Lancet. 2009, 373: 1905-1917. Schacke H, Berger M, Rehwinkel H, Asadullah K: Selective glucocorticoid receptor agonists (SEGRAs): novel ligands with an improved therapeutic index. Mol Cell Endocrinol. 2007, 275: 109-117. Clark AR: Anti-inflammatory functions of glucocorticoid-induced genes. Mol Cell Endocrinol. 2007, 275: 79-97. Szatmary Z, Garabedian MJ, Vilcek J: Inhibition of glucocorticoid receptor-mediated transcriptional activation by p38 mitogen-activated protein (MAP) kinase. J Biol Chem. 2004, 279: 43708-43715.