Ginger extracts influence the expression of IL-27 and IL-33 in the central nervous system in experimental autoimmune encephalomyelitis and ameliorates the clinical symptoms of disease

Journal of Neuroimmunology

Volumn 276, Issue 1-2, 2014, Pages 80-88

  Jafarzadeh, A ^a,b,c   Mohammadi Kordkhayli, M ^b   Ahangar Parvin, R ^c   Azizi, V ^c   Khoramdel Azad, H ^c   Shamsizadeh, A ^c   Ayoobi, A ^c   Nemati, M ^b   Hassan, Z M ^d   Moazeni, S M ^d   Khaksari, M ^a,b  

^a KERMAN UNIVERSITY OF MEDICAL SCIENCES   (Iran)

^b KERMAN UNIVERSITY OF MEDICAL SCIENCES   (Iran)

^c RAFSANJAN UNIVERSITY OF MEDICAL SCIENCES   (Iran)

^d TARBIAT MODARES UNIVERSITY   (Iran)

Author keywords

Clinical symptoms; Experimental autoimmune encephalomyelitis; Ginger; IL 27; IL 33

Indexed keywords

GINGER EXTRACT; INTERLEUKIN 27; INTERLEUKIN 33; FREUND ADJUVANT; GAMMA INTERFERON; INTERLEUKIN 7; INTERLEUKIN DERIVATIVE; INTERLEUKIN-33, MOUSE; MYELIN OLIGODENDROCYTE GLYCOPROTEIN; MYELIN OLIGODENDROCYTE GLYCOPROTEIN (35-55); PEPTIDE FRAGMENT; PLANT EXTRACT;

ANIMAL EXPERIMENT; ANIMAL MODEL; ANIMAL TISSUE; ANTIINFLAMMATORY ACTIVITY; ARTICLE; CONTROLLED STUDY; CYTOKINE PRODUCTION; EXPERIMENTAL AUTOIMMUNE ENCEPHALOMYELITIS; FEMALE; FEVER; FLUSHING; MOUSE; MYALGIA; NONHUMAN; PATHOGENESIS; PROTEIN EXPRESSION; SPINAL CORD; ANIMAL; BLOOD; BODY WEIGHT; C57BL MOUSE; CENTRAL NERVOUS SYSTEM; CHEMICALLY INDUCED; CHEMISTRY; DISEASE MODEL; DOSE RESPONSE; DRUG EFFECTS; ENCEPHALOMYELITIS, AUTOIMMUNE, EXPERIMENTAL; GENETICS; GINGER; METABOLISM; NEUTROPHIL CHEMOTAXIS; PHYTOTHERAPY; TIME; TOXICITY;

ANIMALS; BODY WEIGHT; CENTRAL NERVOUS SYSTEM; CHEMOTAXIS, LEUKOCYTE; DISEASE MODELS, ANIMAL; DOSE-RESPONSE RELATIONSHIP, DRUG; ENCEPHALOMYELITIS, AUTOIMMUNE, EXPERIMENTAL; FEMALE; FREUND'S ADJUVANT; GINGER; INTERFERON-GAMMA; INTERLEUKIN-27; INTERLEUKIN-7; INTERLEUKINS; MICE; MICE, INBRED C57BL; MYELIN-OLIGODENDROCYTE GLYCOPROTEIN; PEPTIDE FRAGMENTS; PHYTOTHERAPY; PLANT EXTRACTS; TIME FACTORS;

EID: 84908553762     PISSN: 01655728     EISSN: 18728421     Source Type: Journal    
DOI: 10.1016/j.jneuroim.2014.08.614     Document Type: Article

References (77)

1. Ahui M.L.B., Champy P., Ramadan A., Pham Van L., Araujo L., Brou André K., Diem S., Damotte D., Kati-Coulibaly S., Offoumou M.A. Ginger prevents Th2-mediated immune responses in a mouse model of airway inflammation. Int. Immunopharmacol. 2008, 8:1626-1632.
2. Ajith T., Aswathy M., Hema U. Protective effect of Zingiber officinale roscoe against anticancer drug doxorubicin-induced acute nephrotoxicity. Food Chem. Toxicol. 2008, 46:3178-3181.
3. Aktan F., Henness S., Tran V.H., Duke C.C., Roufogalis B.D., Ammit A.J. Gingerol metabolite and a synthetic analogue Capsarol inhibit macrophage NF-kappaB-mediated iNOS gene expression and enzyme activity. Planta Med. 2006, 72:727-734.
4. Batten M., Li J., Yi S., Kljavin N.M., Danilenko D.M., Lucas S., Lee J., de Sauvage F.J., Ghilardi N. Interleukin 27 limits autoimmune encephalomyelitis by suppressing the development of interleukin 17-producing T cells. Nat. Immunol. 2006, 7:929-936.
5. Bettelli E., Sullivan B., Szabo S.J., Sobel R.A., Glimcher L.H., Kuchroo V.K. Loss of T-bet, but not STAT1, prevents the development of experimental autoimmune encephalomyelitis. J. Exp. Med. 2004, 200:79-87.
6. Bhat H., Sampath P., Pai R., Bollor R., Baliga M., Fayad R. Indian medicinal plants as immunomodulators: scientific validation of the ethnomedicinal beliefs. Bioactive Food as Dietary Interventions for Arthritis and Related Inflammatory Diseases: Bioactive Food in Chronic Disease States 2012, 215.
7. Bourgeois E., Van L.P., Samson M., Diem S., Barra A., Roga S., Gombert J.M., Schneider E., Dy M., Gourdy P. The pro-Th2 cytokine IL-33 directly interacts with invariant NKT and NK cells to induce IFN-γ production. Eur. J. Immunol. 2009, 39:1046-1055.
8. Buc M. Role of regulatory T cells in pathogenesis and biological therapy of multiple sclerosis. Mediators Inflamm. 2013, 2013:963748.
9. Choi Y.Y., Kim M.H., Hong J., Kim S.-H., Yang W.M. Dried ginger (Zingiber officinalis) inhibits inflammation in a lipopolysaccharide-induced mouse model. Evidence-Based Complementary and Alternative Medicine 2013.
10. Choi Y.Y., Kim M.H., Hong J., Kim S.H., Yang W.M. Dried ginger (Zingiber officinalis) inhibits inflammation in a lipopolysaccharide-induced mouse model. Evid. Based Complement. Alternat. Med. 2013, 2013:914563.
11. Christophi G.P., Gruber R.C., Panos M., Christophi R.L., Jubelt B., Massa P.T. Interleukin-33 upregulation in peripheral leukocytes and CNS of multiple sclerosis patients. Clin. Immunol. 2012, 142:308-319.
12. Constantinescu C.S., Farooqi N., O'Brien K., Gran B. Experimental autoimmune encephalomyelitis (EAE) as a model for multiple sclerosis (MS). Br. J. Pharmacol. 2011, 164:1079-1106.
13. Conti P., DiGioacchino M. MCP-1 and RANTES are mediators of acute and chronic inflammation. Allergy Asthma Proc. 2001, 22:133-137.
14. Domingues H.S., Mues M., Lassmann H., Wekerle H., Krishnamoorthy G. Functional and pathogenic differences of Th1 and Th17 cells in experimental autoimmune encephalomyelitis. PLoS One 2010, 5:e15531.
15. Drozdov V.N., Kim V.A., Tkachenko E.V., Varvanina G.G. Influence of a specific ginger combination on gastropathy conditions in patients with osteoarthritis of the knee or hip. J. Altern. Complement. Med. 2012, 18:583-588.
16. Dungan L.S., McGuinness N.C., Boon L., Lynch M.A., Mills K.H. Innate IFN-gamma promotes development of experimental autoimmune encephalomyelitis: a role for NK cells and M1 macrophages. Eur. J. Immunol. 2014, 2014:201444612.
17. El-Abhar H.S., Hammad L.N., Gawad H.S.A. Modulating effect of ginger extract on rats with ulcerative colitis. J. Ethnopharmacol. 2008, 118:367-372.
18. Fletcher J.M., Lalor S.J., Sweeney C.M., Tubridy N., Mills K.H. T cells in multiple sclerosis and experimental autoimmune encephalomyelitis. Clin. Exp. Immunol. 2010, 162:1-11.
19. Grzanna R., Phan P., Polotsky A., Lindmark L., Frondoza C.G. Ginger extract inhibits β-amyloid peptide-induced cytokine and chemokine expression in cultured THP-1 monocytes. J. Altern. Complement. Med. 2004, 10:1009-1013.
20. Ha S.K., Moon E., Ju M.S., Kim D.H., Ryu J.H., Oh M.S., Kim S.Y. 6-Shogaol, a ginger product, modulates neuroinflammation: a new approach to neuroprotection. Neuropharmacology 2012, 63:211-223.
21. Haniadka R., Saldanha E., Sunita V., Palatty P.L., Fayad R., Baliga M.S. A review of the gastroprotective effects of ginger (Zingiber officinale Roscoe). Food Funct. 2013, 4:845-855.
22. Hofstetter H.H., Ibrahim S.M., Koczan D., Kruse N., Weishaupt A., Toyka K.V., Gold R. Therapeutic efficacy of IL-17 neutralization in murine experimental autoimmune encephalomyelitis. Cell. Immunol. 2005, 237:123-130.
23. Hofstetter H., Gold R., Hartung H. Th17 cells in MS and experimental autoimmune encephalomyelitis. Int. MS J. 2009, 16:12-18.
24. Hudson C.A., Christophi G.P., Gruber R.C., Wilmore J.R., Lawrence D.A., Massa P.T. Induction of IL-33 expression and activity in central nervous system glia. J. Leukoc. Biol. 2008, 84:631-643.
25. Ivanov I.I., McKenzie B.S., Zhou L., Tadokoro C.E., Lepelley A., Lafaille J.J., Cua D.J., Littman D.R. The orphan nuclear receptor RORγt directs the differentiation program of proinflammatory IL-17+T helper cells. Cell 2006, 126:1121-1133.
26. Jadidi-Niaragh F., Mirshafiey A. Th17 cell, the new player of neuroinflammatory process in multiple sclerosis. Scand. J. Immunol. 2011, 74:1-13.
27. Jiang H.R., Milovanović M., Allan D., Niedbala W., Besnard A.G., Fukada S.Y., Alves-Filho J.C., Togbe D., Goodyear C.S., Linington C. IL-33 attenuates EAE by suppressing IL-17 and IFN-γ production and inducing alternatively activated macrophages. Eur. J. Immunol. 2012, 42:1804-1814.
28. Jovanova-Nesic K., Shoenfeld Y. Autoimmunity in the brain: the pathogenesis insight from cell biology. Ann. N. Y. Acad. Sci. 2007, 1107:142-154.
29. Jutel M., Akdis C.A. T-cell subset regulation in atopy. Curr. Allergy Asthma Rep. 2011, 11:139-145.
30. Kohm A.P., Carpentier P.A., Anger H.A., Miller S.D. Cutting edge: CD4+ CD25+ regulatory T cells suppress antigen-specific autoreactive immune responses and central nervous system inflammation during active experimental autoimmune encephalomyelitis. J. Immunol. 2002, 169:4712-4716.
31. Komai-Koma M., Xu D., Li Y., McKenzie A.N., McInnes I.B., Liew F.Y. IL-33 is a chemoattractant for human Th2 cells. Eur. J. Immunol. 2007, 37:2779-2786.
32. Komiyama Y., Nakae S., Matsuki T., Nambu A., Ishigame H., Kakuta S., Sudo K., Iwakura Y. IL-17 plays an important role in the development of experimental autoimmune encephalomyelitis. J. Immunol. 2006, 177:566-573.
33. Korn T., Reddy J., Gao W., Bettelli E., Awasthi A., Petersen T.R., Bäckström B.T., Sobel R.A., Wucherpfennig K.W., Strom T.B. Myelin-specific regulatory T cells accumulate in the CNS but fail to control autoimmune inflammation. Nat. Med. 2007, 13:423-431.
34. Kroenke M.A., Carlson T.J., Andjelkovic A.V., Segal B.M. IL-12- and IL-23-modulated T cells induce distinct types of EAE based on histology, CNS chemokine profile, and response to cytokine inhibition. J. Exp. Med. 2008, 205:1535-1541.
35. Kuo P.-L., Hsu Y.-L., Huang M.-S., Tsai M.-J., Ko Y.-C. Ginger suppresses phthalate ester-induced airway remodeling. J. Agric. Food Chem. 2011, 59:3429-3438.
36. Langrish C.L., Chen Y., Blumenschein W.M., Mattson J., Basham B., Sedgwick J.D., McClanahan T., Kastelein R.A., Cua D.J. IL-23 drives a pathogenic T cell population that induces autoimmune inflammation. J. Exp. Med. 2005, 201:233-240.
37. Lee H.Y., Park S.H., Lee M., Kim H.J., Ryu S.Y., Kim N.D., Hwang B.Y., Hong J.T., Han S.B., Kim Y. 1-Dehydro-[10]-gingerdione from ginger inhibits IKKβ activity for NF-κB activation and suppresses NF-κB-regulated expression of inflammatory genes. Br. J. Pharmacol. 2012, 167:128-140.
38. Lefrancais E., Cayrol C. Mechanisms of IL-33 processing and secretion: differences and similarities between IL-1 family members. Eur. Cytokine Netw. 2012, 23:120-127.
39. Levy A.S., Simon O.R. Six-shogaol inhibits production of tumour necrosis factor alpha, interleukin-1 beta and nitric oxide from lipopolysaccharide-stimulated RAW 264.7 macrophages. West Indian Med. J. 2009, 58:295-300.
40. Li M., Li Y., Liu X., Gao X., Wang Y. IL-33 blockade suppresses the development of experimental autoimmune encephalomyelitis in C57BL/6 mice. J. Neuroimmunol. 2012, 247:25-31.
41. Li X., Li T.T., Zhang X.H., Hou L.F., Yang X.Q., Zhu F.H., Tang W., Zuo J.P. Artemisinin analogue SM934 ameliorates murine experimental autoimmune encephalomyelitis through enhancing the expansion and functions of regulatory T cell. PLoS One 2013, 8:e74108.
42. Ling H., Yang H., Tan S.H., Chui W.K., Chew E.H. 6-Shogaol, an active constituent of ginger, inhibits breast cancer cell invasion by reducing matrix metalloproteinase-9 expression via blockade of nuclear factor-κB activation. Br. J. Pharmacol. 2010, 161:1763-1777.
43. Liu Y., Holdbrooks A.T., De Sarno P., Rowse A.L., Yanagisawa L.L., McFarland B.C., Harrington L.E., Raman C., Sabbaj S., Benveniste E.N., Qin H. Therapeutic efficacy of suppressing the Jak/STAT pathway in multiple models of experimental autoimmune encephalomyelitis. J. Immunol. 2014, 192:59-72.
44. Lloyd C.M. IL-33 family members and asthma-bridging innate and adaptive immune responses. Curr. Opin. Immunol. 2010, 22:800-806.
45. Lucas S., Ghilardi N., Li J., de Sauvage F.J. IL-27 regulates IL-12 responsiveness of naive CD4+ T cells through Stat1-dependent and -independent mechanisms. Proc. Natl. Acad. Sci. U. S. A. 2003, 100:15047-15052.
46. Milo R., Miller A. Revised diagnostic criteria of multiple sclerosis. Autoimmun. Rev. 2014, 9972:012.
47. Milovanovic M., Volarevic V., Ljujic B., Radosavljevic G., Jovanovic I., Arsenijevic N., Lukic M.L. Deletion of IL-33R (ST2) abrogates resistance to EAE in BALB/C mice by enhancing polarization of APC to inflammatory phenotype. PLoS One 2012, 7:e45225.
48. Milovanovic M., Volarevic V., Radosavljevic G., Jovanovic I., Pejnovic N., Arsenijevic N., Lukic M.L. IL-33/ST2 axis in inflammation and immunopathology. Immunol. Res. 2012, 52:89-99.
49. Mix E., Meyer-Rienecker H., Hartung H.P., Zettl U.K. Animal models of multiple sclerosis-potentials and limitations. Prog. Neurobiol. 2010, 92:386-404.
50. Nakae S., Morita H., Ohno T., Arae K., Matsumoto K., Saito H. Role of interleukin-33 in innate-type immune cells in allergy. Allergol. Int. 2013, 62:13-20.
51. Ni J., Shu Y.Y., Zhu Y.N., Fu Y.F., Tang W., Zhong X.G., Wang H., Yang Y.F., Ren J., Wang M.W., Zuo J.P. COX-2 inhibitors ameliorate experimental autoimmune encephalomyelitis through modulating IFN-gamma and IL-10 production by inhibiting T-bet expression. J. Neuroimmunol. 2007, 186:94-103.
52. Nunes T., Bernardazzi C., de Souza H.S. Interleukin-33 and inflammatory bowel diseases: lessons from human studies. Mediators Inflamm. 2014, 2014:423957.
53. Palmer G., Talabot-Ayer D., Lamacchia C., Toy D., Seemayer C.A., Viatte S., Finckh A., Smith D.E., Gabay C. Inhibition of interleukin-33 signaling attenuates the severity of experimental arthritis. Arthritis Rheum. 2009, 60:738-749.
54. Peterson R.A. Regulatory T-cells: diverse phenotypes integral to immune homeostasis and suppression. Toxicol. Pathol. 2012, 40:186-204.
55. Priya Rani M., Padmakumari K., Sankarikutty B., Lijo Cherian O., Nisha V., Raghu K. Inhibitory potential of ginger extracts against enzymes linked to type 2 diabetes, inflammation and induced oxidative stress. Int. J. Food Sci. Nutr. 2011, 62:106-110.
56. Rahnama P., Montazeri A., Huseini H.F., Kianbakht S., Naseri M. Effect of Zingiber officinale R. rhizomes (ginger) on pain relief in primary dysmenorrhea: a placebo randomized trial. BMC Complement. Altern. Med. 2012, 12:92.
57. Ramadan G., El-Menshawy O. Protective effects of ginger-turmeric rhizomes mixture on joint inflammation, atherogenesis, kidney dysfunction and other complications in a rat model of human rheumatoid arthritis. Int. J. Rheum. Dis. 2013, 16:219-229.
58. Rawji K.S., Yong V.W. The benefits and detriments of macrophages/microglia in models of multiple sclerosis. Clin. Dev. Immunol. 2013, 2013:948976.
59. Rostami A., Ciric B. Role of Th17 cells in the pathogenesis of CNS inflammatory demyelination. J. Neurol. Sci. 2013, 333:76-87.
60. Sattler S., Smits H.H., Xu D., Huang F.P. The evolutionary role of the IL-33/ST2 system in host immune defence. Arch. Immunol. Ther. Exp. (Warsz) 2013, 61:107-117.
61. Schmitz J., Owyang A., Oldham E., Song Y., Murphy E., McClanahan T.K., Zurawski G., Moshrefi M., Qin J., Li X. IL-33, an interleukin-1-like cytokine that signals via the IL-1 receptor-related protein ST2 and induces T helper type 2-associated cytokines. Immunity 2005, 23:479-490.
62. Stumhofer J.S., Hunter C.A. Advances in understanding the anti-inflammatory properties of IL-27. Immunol. Lett. 2008, 117:123-130.
63. Stumhofer J.S., Laurence A., Wilson E.H., Huang E., Tato C.M., Johnson L.M., Villarino A.V., Huang Q., Yoshimura A., Sehy D. Interleukin 27 negatively regulates the development of interleukin 17-producing T helper cells during chronic inflammation of the central nervous system. Nat. Immunol. 2006, 7:937-945.
64. Su Z., Lin J., Lu F., Zhang X., Zhang L., Gandhi N.B., de Paiva C.S., Pflugfelder S.C., Li D.Q. Potential autocrine regulation of interleukin-33/ST2 signaling of dendritic cells in allergic inflammation. Mucosal Immunol. 2013, 6:921-930.
65. Takeuchi C., Yamagata K., Takemiya T. Variation in experimental autoimmune encephalomyelitis scores in a mouse model of multiple sclerosis. World J. Neurol. 2013, 3:56-61.
66. Tang S., Huang H., Hu F., Zhou W., Guo J., Jiang H., Mu R., Li Z. Increased IL-33 in synovial fluid and paired serum is associated with disease activity and autoantibodies in rheumatoid arthritis. Clin. Dev. Immunol. 2013, 2013:985301.
67. Tripathi S., Maier K.G., Bruch D., Kittur D.S. Effect of 6-gingerol on pro-inflammatory cytokine production and costimulatory molecule expression in murine peritoneal macrophages. J. Surg. Res. 2007, 138:209-213.
68. Tripathi S., Bruch D., Kittur D.S. Ginger extract inhibits LPS induced macrophage activation and function. BMC Complement. Altern. Med. 2008, 8:1.
69. Tumani H., Kassubek J., Hijazi M., Lehmensiek V., Unrath A., Sussmuth S., Lauda F., Kapfer T., Fang L., Senel M., Brettschneider J. Patterns of TH1/TH2 cytokines predict clinical response in multiple sclerosis patients treated with glatiramer acetate. Eur. Neurol. 2011, 65:164-169.
70. Vahdat Shariatpanahi Z., Mokhtari M., Taleban F.A., Alavi F., Salehi Surmaghi M.H., Mehrabi Y., Shahbazi S. Effect of enteral feeding with ginger extract in acute respiratory distress syndrome. J. Crit. Care 2013, 28:217.e211-217.e216.
71. Villalvilla A., da Silva J.A., Largo R., Gualillo O., Vieira P.C., Herrero-Beaumont G., Gomez R. 6-Shogaol inhibits chondrocytes' innate immune responses and cathepsin-K activity. Mol. Nutr. Food Res. 2014, 58:256-266.
72. Wang Z., Hong J., Sun W., Xu G., Li N., Chen X., Liu A., Xu L., Sun B., Zhang J.Z. Role of IFN-γ in induction of Foxp3 and conversion of CD4+ CD25-T cells to CD4+ Tregs. J. Clin. Investig. 2006, 116:2434-2441.
73. Wang Z., Hasegawa J., Wang X., Matsuda A., Tokuda T., Miura N., Watanabe T. Protective effects of ginger against aspirin-induced gastric ulcers in rats. Yonago Acta Med. 2011, 54:11.
74. Wang S., Ding L., Liu S.S., Wang C., Leng R.X., Chen G.M., Fan Y.G., Pan H.F., Ye D.Q. IL-33: a potential therapeutic target in autoimmune diseases. J. Investig. Med. 2012, 60:1151-1156.
75. Xiao B.G., Ma C.G., Xu L.Y., Link H., Lu C.Z. IL-12/IFN-gamma/NO axis plays critical role in development of Th1-mediated experimental autoimmune encephalomyelitis. Mol. Immunol. 2008, 45:1191-1196.
76. Yang X.O., Pappu B.P., Nurieva R., Akimzhanov A., Kang H.S., Chung Y., Ma L., Shah B., Panopoulos A.D., Schluns K.S. T helper 17 lineage differentiation is programmed by orphan nuclear receptors RORα and RORγ. Immunity 2008, 28:29-39.
77. Zhu C., Cao Y., Zhang R., Song Y., Liu W., Pan F., Li Y., Zhu Y., Liu F., Wu J. Stimulatory effect of LPS and feedback effect of PGE2 on IL-27 production. Scand. J. Immunol. 2010, 72:469-475.