Protective effects of low-concentration hydrogen sulfide on rheumatoid joint disease

doi:10.3969/j.issn.2095-4344.2014.11.004

Abstract

Abstract:

BACKGROUND: Rheumatoid arthritis is a common chronic systemic autoimmune disease which is characterized by synovial lesions and bone erosion. The clinical treatment is still a difficulty.

OBJECTIVE: To explore the effect of exogenous hydrogen sulfide on the articular lesions in rheumatoid arthritis rats.

METHODS: Sprague-Dawley rats were divided into four groups: control group, model group, high concentrations of hydrogen sulfide intervention group, low concentrations of hydrogen sulfide intervention group. At 2 and 4 weeks after intervention, the arthritis index, levels of serum inflammatory cytokines (tumor necrotic factor-α and interleukin-1β), pathological change of synovial tissue, average absorbance of knee joint specimens using collagen-II immunohistochemical staining were measured.

RESULTS AND CONCLUSION: The arthritis index, levels of serum inflammatory cytokines and inflammatory infiltration of synovial staining in the model group and two intervention groups were higher than that in control group, the high concentrations of hydrogen sulfide intervention group was significantly higher than the model

group (P < 0.05) while the low concentrations of hydrogen sulfide intervention group was lower than the model group (P < 0.05). The average absorbance of knee cartilage specimens using collagen-II immunohistochemical staining was lower in the model group and two hydrogen sulfide intervention groups compared with the control group, the high concentrations of hydrogen sulfide intervention group was significantly lower than the model group (P < 0.05) while low concentrations of hydrogen sulfide intervention group was higher than the model group (P < 0.05). Hydrogen sulfide has a regulatory effect on rheumatoid arthritis, high concentrations of hydrogen sulfide aggravate arthritis and cartilage degradation, low concentrations of hydrogen sulfide reduce arthritis and protect cartilage.

中国组织工程研究杂志出版内容重点：组织构建；骨细胞；软骨细胞；细胞培养；成纤维细胞；血管内皮细胞；骨质疏松；组织工程

全文链接：

Key words: arthritis, rheumatoid, hydrogen sulfide, tumor necrosis factor-alpha, interleukin-1 beta, collagen type II, synovial membrane, cartilage

CLC Number:

R318

Zhou Zhi, Liu Kai-xiang, Xie Yue, Wang Li-ming. Protective effects of low-concentration hydrogen sulfide on rheumatoid joint disease[J]. Chinese Journal of Tissue Engineering Research, 2014, 18(11): 1659-1664.

Figures/Tables 2

References

[1] 陆再英,钟南山.内科学[M].7版.北京:人民卫生出版社,2008:848.

[2] 杜军保,金红芳,唐朝枢.昔日的废气,今天的气体明星——硫化氢从基础研究走向临床实践[J].中华医学杂志,2011,91(43): 3028-3029.

[3] Sowmya S, Swathi Y, Yeo AL,et al. Hydrogen sulfide: regulatory role on blood pressure in hyperhomocysteinemia.Vascul Pharmacol. 2010;53(3-4):138-143.

[4] Tamizhselvi R, Moore PK, Bhatia M.Inhibition of hydrogen sulfide synthesis attenuates chemokine production and protects mice against acute pancreatitis and associated lung injury.Pancreas. 2008;36(4):e24-31.

[5] Simões SI, Delgado TC, Lopes RM,et al.Developments in the rat adjuvant arthritis model and its use in therapeutic evaluation of novel non-invasive treatment by SOD in Transfersomes.J Control Release. 2005;103(2):419-434.

[6] 顾强荣,王黎明,徐燕,等.胶体磷酸铬32P关节腔内注射改善佐剂型关节炎大鼠的相关指标[J].中国组织工程研究与临床康复, 2007,11(9):1654-1658.

[7] Abd El-Rahman RS, Suddek GM, Gameil NM,et al.Protective potential of MMR vaccine against complete Freund's adjuvant-induced inflammation in rats.Inflammopharmacology. 2011;19(6):343-348.

[8] 宋珊珊,张玲玲,魏伟.实验性关节炎动物模型建立及病理机制研究进展[J].中国药理学通报,2011,27(12):1648-1652.

[9] Bevaart L, Vervoordeldonk MJ, Tak PP.Evaluation of therapeutic targets in animal models of arthritis: how does it relate to rheumatoid arthritis?Arthritis Rheum. 2010;62(8): 2192-2205.

[10] Esser RE, Hildebrand AR, Angelo RA,et al.Measurement of radiographic changes in adjuvant-induced arthritis in rats by quantitative image analysis.Arthritis Rheum.1995;38(1): 129-138.

[11] Philippe L, Gegout-Pottie P, Guingamp C,et al. Relations between functional, inflammatory, and degenerative parameters during adjuvant arthritis in rats.Am J Physiol. 1997;273(4 Pt 2):R1550-1556.

[12] 杨军平,邱丽瑛,肖亮,等.自拟通痹汤对Ⅱ型胶原性关节炎关节软骨的作用[J].中国组织工程研究,2012,16(42):7843-7848.

[13] 刘曦,邵福灵,刘爱京.沙利度胺与胶原诱导型关节炎大鼠炎症因子的表达[J].中国组织工程研究与临床康复,2010,14(20): 3666-3668.

[14] 陈疆,熊新贵,梁清华,等.类风湿性关节炎患者关节滑膜组织蛋白质组学[J].中国组织工程研究,2012,16(28):5206-5211.

[15] Ma Y, Pope RM.The role of macrophages in rheumatoid arthritis.Curr Pharm Des. 2005;11(5):569-580.

[16] Mishra R, Singh A, Chandra V,et al.A comparative analysis of serological parameters and oxidative stress in osteoarthritis and rheumatoid arthritis.Rheumatol Int. 2012;32(8):2377- 2382.

[17] Warenycia MW, Goodwin LR, Benishin CG,et al.Acute hydrogen sulfide poisoning. Demonstration of selective uptake of sulfide by the brainstem by measurement of brain sulfide levels.Biochem Pharmacol. 1989;38(6):973-981.

[18] Martelli A, Testai L, Breschi MC,et al.Hydrogen sulphide: novel opportunity for drug discovery.Med Res Rev. 2010. [Epub ahead of print]

[19] Li L, Bhatia M, Zhu YZ,et al.Hydrogen sulfide is a novel mediator of lipopolysaccharide-induced inflammation in the mouse.FASEB J. 2005;19(9):1196-1198.

[20] Rinaldi L, Gobbi G, Pambianco M,et al.Hydrogen sulfide prevents apoptosis of human PMN via inhibition of p38 and caspase 3.Lab Invest. 2006;86(4):391-397.

[21] Bhatia M, Sidhapuriwala J, Moochhala SM,et al.Hydrogen sulphide is a mediator of carrageenan-induced hindpaw oedema in the rat.Br J Pharmacol. 2005;145(2): 141-144.

[22] Alvira CM, Abate A, Yang G,et al.Nuclear factor-kappaB activation in neonatal mouse lung protects against lipopolysaccharide-induced inflammation.Am J Respir Crit Care Med. 2007;175(8):805-815.

[23] Cheng DS, Han W, Chen SM,et al.Airway epithelium controls lung inflammation and injury through the NF-kappa B pathway.J Immunol. 2007;178(10):6504-6513.

[24] Tamizhselvi R, Koh YH, Sun J,et al.Hydrogen sulfide induces ICAM-1 expression and neutrophil adhesion to caerulein-treated pancreatic acinar cells through NF-kappaB and Src-family kinases pathway.Exp Cell Res. 2010;316(9): 1625-1636.

[25] Sivarajah A, Collino M, Yasin M,et al.Anti-apoptotic and anti-inflammatory effects of hydrogen sulfide in a rat model of regional myocardial I/R.Shock. 2009;31(3):267-274.

[26] Hirata I, Naito Y, Takagi T, et al. Endogenous hydrogen sulfide is an anti-inflammatory molecule in dextran sodium sulfate-induced colitis in mice.Dig Dis Sci. 2011;56(5): 1379-1386.

[27] Tamizhselvi R, Sun J, Koh YH,et al.Effect of hydrogen sulfide on the phosphatidylinositol 3-kinase-protein kinase B pathway and on caerulein-induced cytokine production in isolated mouse pancreatic acinar cells.J Pharmacol Exp Ther. 2009; 329(3):1166-1177.

[28] Whiteman M, Haigh R, Tarr JM,et al.Detection of hydrogen sulfide in plasma and knee-joint synovial fluid from rheumatoid arthritis patients: relation to clinical and laboratory measures of inflammation.Ann N Y Acad Sci. 2010;1203: 146-150.

[29] Chen WP, Tang JL, Bao JP,et al.Effects of diallyl sulphide in chondrocyte and cartilage in experimental osteoarthritis in rabbit.Phytother Res. 2011;25(3):351-356.

[30] Kloesch B, Liszt M, Krehan D,et al.High concentrations of hydrogen sulphide elevate the expression of a series of pro-inflammatory genes in fibroblast-like synoviocytes derived from rheumatoid and osteoarthritis patients.Immunol Lett. 2012;141(2):197-203.

[31] Kloesch B, Liszt M, Steiner G,et al.Inhibitors of p38 and ERK1/2 MAPkinase and hydrogen sulphide block constitutive and IL-1β-induced IL-6 and IL-8 expression in the human chondrocyte cell line C-28/I2.Rheumatol Int. 2012;32(3): 729-736.

[32] Williams FM, Skinner J, Spector TD,et al.Dietary garlic and hip osteoarthritis: evidence of a protective effect and putative mechanism of action.BMC Musculoskelet Disord. 2010;11: 280.

[33] Lee HS, Lee CH, Tsai HC,et al.Inhibition of cyclooxygenase 2 expression by diallyl sulfide on joint inflammation induced by urate crystal and IL-1beta.Osteoarthritis Cartilage. 2009; 17(1):91-99.

[34] Ekundi-Valentim E, Santos KT, Camargo EA, et al.Differing effects of exogenous and endogenous hydrogen sulphide in carrageenan-induced knee joint synovitis in the rat.Br J Pharmacol. 2010;159(7):1463-1474.

[35] Szekanecz Z, Koch AE.Angiogenesis and its targeting in rheumatoid arthritis.Vascul Pharmacol. 2009;51(1):1-7.

[36] Komorowski J, Jerczyńska H, Siejka A, et al.Effect of thalidomide affecting VEGF secretion, cell migration, adhesion and capillary tube formation of human endothelial EA.hy 926 cells.Life Sci. 2006;78(22):2558-2563.

[37] Lainer DT, Brahn E.New antiangiogenic strategies for the treatment of proliferative synovitis.Expert Opin Investig Drugs. 2005;14(1):1-17.

[38] Esposito E, Cuzzocrea S.TNF-alpha as a therapeutic target in inflammatory diseases, ischemia-reperfusion injury and trauma.Curr Med Chem. 2009;16(24):3152-3167.

[39] Tweedie D, Sambamurti K, Greig NH.TNF-alpha inhibition as a treatment strategy for neurodegenerative disorders: new drug candidates and targets.Curr Alzheimer Res. 2007;4(4): 378-385.

[40] Deng A, Harvey V, Sina B,et al.Interstitial granulomatous dermatitis associated with the use of tumor necrosis factor alpha inhibitors.Arch Dermatol. 2006;142(2):198-202.

[41] Greig NH, Giordano T, Zhu X,et al.Thalidomide-based TNF-alpha inhibitors for neurodegenerative diseases.Acta Neurobiol Exp (Wars). 2004;64(1):1-9.

[42] Davis JC Jr.Understanding the role of tumor necrosis factor inhibition in ankylosing spondylitis.Semin Arthritis Rheum. 2005;34(4):668-677.

[43] Kapoor M, Martel-Pelletier J, Lajeunesse D,et al.Role of proinflammatory cytokines in the pathophysiology of osteoarthritis.Nat Rev Rheumatol. 2011;7(1):33-42.

[44] Egeblad M, Werb Z.New functions for the matrix metalloproteinases in cancer progression.Nat Rev Cancer. 2002;2(3):161-174.

[45] Hunziker EB.Articular cartilage repair: basic science and clinical progress. A review of the current status and prospects.Osteoarthritis Cartilage. 2002;10(6):432-463.

[46] Ishiguro N.Cartilage degradation in rheumatoid arthritis.Clin Calcium. 2009;19(3):347-354.

[47] Skoumal M, Haberhauer G, Kolarz G,et al.Serum cathepsin K levels of patients with longstanding rheumatoid arthritis: correlation with radiological destruction.Arthritis Res Ther. 2005;7(1):R65-70.

[48] Leong DJ, Gu XI, Li Y,et al.Matrix metalloproteinase-3 in articular cartilage is upregulated by joint immobilization and suppressed by passive joint motion.Matrix Biol. 2010;29(5): 420-426.

[49] Cho TJ, Lehmann W, Edgar C,et al.Tumor necrosis factor alpha activation of the apoptotic cascade in murine articular chondrocytes is associated with the induction of metalloproteinases and specific pro-resorptive factors.Arthritis Rheum. 2003;48(10):2845-2854.

[50] Glasson SS, Askew R, Sheppard B,et al.Characterization of and osteoarthritis susceptibility in ADAMTS-4-knockout mice.Arthritis Rheum. 2004;50(8):2547-2558.

[51] Lohmander LS, Brandt KD, Mazzuca SA,et al.Use of the plasma stromelysin (matrix metalloproteinase 3) concentration to predict joint space narrowing in knee osteoarthritis.Arthritis Rheum. 2005;52(10):3160-3167.