Dietary blue pigments derived from genipin, attenuate inflammation by inhibiting LPS-induced iNOS and COX-2 expression via the NF-κB inactivation

PLoS ONE

Volumn 7, Issue 3, 2012, Pages

  Wang, Qiang Song ^a   Xiang, Yaozu ^b   Cui, Yuan Lu ^a   Lin, Ke Ming ^a   Zhang, Xin Fang ^a  

^a TIANJIN UNIVERSITY OF TRADITIONAL CHINESE MEDICINE   (China)

^b IMPERIAL COLLEGE LONDON   (United Kingdom)

Author keywords

[No Author keywords available]

Indexed keywords

ANTIINFLAMMATORY AGENT; BLUE PIGMENT DERIVED FROM GENIPIN; CYCLOOXYGENASE 2; GRANULOCYTE COLONY STIMULATING FACTOR; I KAPPA B ALPHA; I KAPPA B KINASE ALPHA; I KAPPA B KINASE BETA; IMMUNOGLOBULIN ENHANCER BINDING PROTEIN; INDUCIBLE NITRIC OXIDE SYNTHASE; INTERCELLULAR ADHESION MOLECULE 1; INTERLEUKIN 1 RECEPTOR BLOCKING AGENT; INTERLEUKIN 1ALPHA; INTERLEUKIN 6; LIPOPOLYSACCHARIDE; MACROPHAGE INFLAMMATORY PROTEIN 1BETA; MESSENGER RNA; NITRIC OXIDE; NUCLEAR FACTOR KAPPA B KINASE P50; PIGMENT; PROSTAGLANDIN E2; RANTES; TRANSCRIPTION FACTOR RELA; TUMOR NECROSIS FACTOR ALPHA; UNCLASSIFIED DRUG; CYTOKINE; GENIPIN; IRIDOID; NITRITE;

ANIMAL CELL; ANIMAL EXPERIMENT; ANIMAL MODEL; ANTIINFLAMMATORY ACTIVITY; ARTICLE; CELL SECRETION; CELL STIMULATION; CONCENTRATION RESPONSE; CONTROLLED STUDY; CYTOKINE PRODUCTION; DOSE RESPONSE; DOWN REGULATION; DRUG DOSE COMPARISON; DRUG STRUCTURE; ENZYME INHIBITION; ENZYME LINKED IMMUNOSORBENT ASSAY; GENE EXPRESSION; IN VITRO STUDY; IN VIVO STUDY; MACROPHAGE; MALE; MOUSE; NONHUMAN; PAW EDEMA; PROSTAGLANDIN SYNTHESIS; PROTEIN BLOOD LEVEL; PROTEIN DEGRADATION; PROTEIN DNA BINDING; PROTEIN EXPRESSION; PROTEIN PHOSPHORYLATION; REAL TIME POLYMERASE CHAIN REACTION; REVERSE TRANSCRIPTION POLYMERASE CHAIN REACTION; ANIMAL; CELL LINE; CHEMICAL MODEL; CHEMISTRY; CYTOLOGY; GENE EXPRESSION REGULATION; INFLAMMATION; INSTITUTE FOR CANCER RESEARCH MOUSE; METABOLISM; PIGMENTATION;

GARDENIA; MUS;

ANIMALS; CELL LINE; CYCLOOXYGENASE 2; CYTOKINES; DINOPROSTONE; GENE EXPRESSION REGULATION, ENZYMOLOGIC; INFLAMMATION; IRIDOIDS; LIPOPOLYSACCHARIDES; MACROPHAGES; MALE; MICE; MICE, INBRED ICR; MODELS, CHEMICAL; NF-KAPPA B; NITRIC OXIDE SYNTHASE TYPE II; NITRITES; PIGMENTATION;

EID: 84859118071     PISSN: None     EISSN: 19326203     Source Type: Journal    
DOI: 10.1371/journal.pone.0034122     Document Type: Article

References (61)

1. Fujikama S, Fukui Y, Koga K, Kumada J, (1987) Brilliant skyblue pigment formation from Gardenia fruits. Journal of Fermentation Technology 65: 419-424.
2. Park JE, Lee JY, Kim HG, Hahn TR, Paik YS, (2002) Isolation and characterization of water-soluble intermediates of blue pigments transformed from geniposide of Gardenia jasminoides. J Agric Food Chem 50: 6511-6514.
3. Paik Y, Lee C, Cho M, Hahn T, (2001) Physical stability of the blue pigments formed from geniposide of gardenia fruits: effects of pH, temperature, and light. J Agric Food Chem 49: 430-432.
4. Baggiolini M, (1998) Chemokines and leukocyte traffic. Nature 392: 565-568.
5. Palmer RM, Ashton DS, Moncada S, (1988) Vascular endothelial cells synthesize nitric oxide from L-arginine. Nature 333: 664-666.
6. Lowenstein CJ, Hill SL, Lafond-Walker A, Wu J, Allen G, et al. (1996) Nitric oxide inhibits viral replication in murine myocarditis. J Clin Invest 97: 1837-1843.
7. Hibbs JB Jr, Taintor RR, Vavrin Z, (1987) Macrophage cytotoxicity: role for L-arginine deiminase and imino nitrogen oxidation to nitrite. Science 235: 473-476.
8. Grahames CB, Michel AD, Chessell IP, Humphrey PP, (1999) Pharmacological characterization of ATP- and LPS-induced IL-1beta release in human monocytes. Br J Pharmacol 127: 1915-1921.
9. Mehta VB, Hart J, Wewers MD, (2001) ATP-stimulated release of interleukin (IL)-1beta and IL-18 requires priming by lipopolysaccharide and is independent of caspase-1 cleavage. J Biol Chem 276: 3820-3826.
10. Van Snick J, (1990) Interleukin-6: an overview. Annu Rev Immunol 8: 253-278.
11. Marletta MA, (1993) Nitric oxide synthase structure and mechanism. J Biol Chem 268: 12231-12234.
12. Kleinert H, Pautz A, Linker K, Schwarz PM, (2004) Regulation of the expression of inducible nitric oxide synthase. Eur J Pharmacol 500: 255-266.
13. Harris SG, Padilla J, Koumas L, Ray D, Phipps RP, (2002) Prostaglandins as modulators of immunity. Trends Immunol 23: 144-150.
14. Lawrence T, Gilroy DW, Colville-Nash PR, Willoughby DA, (2001) Possible new role for NF-kappaB in the resolution of inflammation. Nat Med 7: 1291-1297.
15. Baldwin AS Jr, (1996) The NF-kappa B and I kappa B proteins: new discoveries and insights. Annu Rev Immunol 14: 649-683.
16. Baeuerle PA, Baltimore D, (1996) NF-kappa B: ten years after. Cell 87: 13-20.
17. Surh YJ, Chun KS, Cha HH, Han SS, Keum YS, et al. (2001) Molecular mechanisms underlying chemopreventive activities of anti-inflammatory phytochemicals: down-regulation of COX-2 and iNOS through suppression of NF-kappa B activation. Mutat Res 480-481: 243-268.
18. Lappas M, Permezel M, Georgiou HM, Rice GE, (2002) Nuclear factor kappa B regulation of proinflammatory cytokines in human gestational tissues in vitro. Biol Reprod 67: 668-673.
19. Makarov SS, (2000) NF-kappaB as a therapeutic target in chronic inflammation: recent advances. Mol Med Today 6: 441-448.
20. Renard P, Raes M, (1999) The proinflammatory transcription factor NFkappaB: a potential target for novel therapeutical strategies. Cell Biol Toxicol 15: 341-344.
21. Cho JY, Kim PS, Park J, Yoo ES, Baik KU, et al. (2000) Inhibitor of tumor necrosis factor-alpha production in lipopolysaccharide-stimulated RAW264.7 cells from Amorpha fruticosa. J Ethnopharmacol 70: 127-133.
22. Hinz B, Brune K, Pahl A, (2000) Nitric oxide inhibits inducible nitric oxide synthase mRNA expression in RAW 264.7 macrophages. Biochem Biophys Res Commun 271: 353-357.
23. Hinz B, Brune K, Pahl A, (2000) Prostaglandin E(2) upregulates cyclooxygenase-2 expression in lipopolysaccharide-stimulated RAW 264.7 macrophages. Biochem Biophys Res Commun 272: 744-748.
24. Seo WG, Pae HO, Oh GS, Kim NY, Kwon TO, et al. (2001) The aqueous extract of Rhodiola sachalinensis root enhances the expression of inducible nitric oxide synthase gene in RAW264.7 macrophages. J Ethnopharmacol 76: 119-123.
25. Suh N, Honda T, Finlay HJ, Barchowsky A, Williams C, et al. (1998) Novel triterpenoids suppress inducible nitric oxide synthase (iNOS) and inducible cyclooxygenase (COX-2) in mouse macrophages. Cancer Res 58: 717-723.
26. Fujikama S, Fukui Y, Koga K, (1987) Structure of genipocyanin G1, a spontaneous reaction product between genipin and glycine. Tetrahedron Letters 28: 4699-4700.
27. Versteeg HH, Nijhuis E, van den Brink GR, Evertzen M, Pynaert GN, et al. (2000) A new phosphospecific cell-based ELISA for p42/p44 mitogen-activated protein kinase (MAPK), p38 MAPK, protein kinase B and cAMP-response-element-binding protein. Biochem J 350 Pt 3: 717-722.
28. Wang QS, Cui YL, Wang YF, Chi W, (2011) Effects of compounds from Bi-Qi Capsule on the expression of inflammatory mediators in lipopolysaccharide-stimulated RAW 264.7 macrophages. J Ethnopharmacol 136: 480-487.
29. Raspotnig G, Fauler G, Jantscher A, Windischhofer W, Schachl K, et al. (1999) Colorimetric determination of cell numbers by Janus green staining. Anal Biochem 275: 74-83.
30. Kang HG, Jenabi JM, Zhang J, Keshelava N, Shimada H, et al. (2007) E-cadherin cell-cell adhesion in ewing tumor cells mediates suppression of anoikis through activation of the ErbB4 tyrosine kinase. Cancer Res 67: 3094-3105.
31. Marcondes AM, Mhyre AJ, Stirewalt DL, Kim SH, Dinarello CA, et al. (2008) Dysregulation of IL-32 in myelodysplastic syndrome and chronic myelomonocytic leukemia modulates apoptosis and impairs NK function. Proc Natl Acad Sci U S A 105: 2865-2870.
32. Feron M, Guevel L, Rouger K, Dubreil L, Arnaud MC, et al. (2009) PTEN contributes to profound PI3K/Akt signaling pathway deregulation in dystrophin-deficient dog muscle. Am J Pathol 174: 1459-1470.
33. Livak KJ, Schmittgen TD, (2001) Analysis of relative gene expression data using real-time quantitative PCR and the 2(-Delta Delta C(T)) Method. Methods 25: 402-408.
34. De Gois S, Schafer MK, Defamie N, Chen C, Ricci A, et al. (2005) Homeostatic scaling of vesicular glutamate and GABA transporter expression in rat neocortical circuits. J Neurosci 25: 7121-7133.
35. Shin EM, Zhou HY, Guo LY, Kim JA, Lee SH, et al. (2008) Anti-inflammatory effects of glycyrol isolated from Glycyrrhiza uralensis in LPS-stimulated RAW264.7 macrophages. Int Immunopharmacol 8: 1524-1532.
36. Fukuzawa M, Satoh J, Sagara M, Muto G, Muto Y, et al. (1997) Angiotensin converting enzyme inhibitors suppress production of tumor necrosis factor-alpha in vitro and in vivo. Immunopharmacology 36: 49-55.
37. Tanaka M, Yamazaki M, Chiba K, (2009) Neuroprotective action of genipin on tunicamycin induced cytotoxicity in neuro2a cells. Biol Pharm Bull 32: 1220-1223.
38. Koo HJ, Song YS, Kim HJ, Lee YH, Hong SM, et al. (2004) Antiinflammatory effects of genipin, an active principle of gardenia. Eur J Pharmacol 495: 201-208.
39. Takeuchi S, Goto T, Mikami K, Miura K, Ohshima S, et al. (2005) Genipin prevents fulminant hepatic failure resulting in reduction of lethality through the suppression of TNF-alpha production. Hepatol Res 33: 298-305.
40. Chang WH, Chang Y, Lai PH, Sung HW, (2003) A genipin-crosslinked gelatin membrane as wound-dressing material: in vitro and in vivo studies. J Biomater Sci Polym Ed 14: 481-495.
41. Sung HW, Huang DM, Chang WH, Huang LL, Tsai CC, et al. (1999) Gelatin-derived bioadhesives for closing skin wounds: an in vivo study. J Biomater Sci Polym Ed 10: 751-771.
42. Liu BS, Yao CH, Chen YS, Hsu SH, (2003) In vitro evaluation of degradation and cytotoxicity of a novel composite as a bone substitute. J Biomed Mater Res A 67: 1163-1169.
43. Tsai CC, Chang Y, Sung HW, Hsu JC, Chen CN, (2001) Effects of heparin immobilization on the surface characteristics of a biological tissue fixed with a naturally occurring crosslinking agent (genipin): an in vitro study. Biomaterials 22: 523-533.
44. Levinton-Shamuilov G, Cohen Y, Azoury M, Chaikovsky A, Almog J, (2005) Genipin, a novel fingerprint reagent with colorimetric and fluorogenic activity, part II: optimization, scope and limitations. J Forensic Sci 50: 1367-1371.
45. Zhang CH, (2006) Food Colorants Data Book Beijing China Measurement Press.
46. Rafi MM, Shafaie Y, (2007) Dietary lutein modulates inducible nitric oxide synthase (iNOS) gene and protein expression in mouse macrophage cells (RAW 264.7). Mol Nutr Food Res 51: 333-340.
47. Korhonen R, Lahti A, Kankaanranta H, Moilanen E, (2005) Nitric oxide production and signaling in inflammation. Curr Drug Targets Inflamm Allergy 4: 471-479.
48. Vane JR, (1971) Inhibition of prostaglandin synthesis as a mechanism of action for aspirin-like drugs. Nat New Biol 231: 232-235.
49. Masferrer JL, Zweifel BS, Manning PT, Hauser SD, Leahy KM, et al. (1994) Selective inhibition of inducible cyclooxygenase 2 in vivo is antiinflammatory and nonulcerogenic. Proc Natl Acad Sci U S A 91: 3228-3232.
50. Seibert K, Zhang Y, Leahy K, Hauser S, Masferrer J, et al. (1994) Pharmacological and biochemical demonstration of the role of cyclooxygenase 2 in inflammation and pain. Proc Natl Acad Sci U S A 91: 12013-12017.
51. Moncada S, Palmer RM, Higgs EA, (1991) Nitric oxide: physiology, pathophysiology, and pharmacology. Pharmacol Rev 43: 109-142.
52. Locksley RM, Killeen N, Lenardo MJ, (2001) The TNF and TNF receptor superfamilies: integrating mammalian biology. Cell 104: 487-501.
53. Burger D, Dayer JM, Palmer G, Gabay C, (2006) Is IL-1 a good therapeutic target in the treatment of arthritis? Best Pract Res Clin Rheumatol 20: 879-896.
54. Rose-John S, Waetzig GH, Scheller J, Grotzinger J, Seegert D, (2007) The IL-6/sIL-6R complex as a novel target for therapeutic approaches. Expert Opin Ther Targets 11: 613-624.
55. Baeuerle PA, Henkel T, (1994) Function and activation of NF-kappa B in the immune system. Annu Rev Immunol 12: 141-179.
56. Brown K, Park S, Kanno T, Franzoso G, Siebenlist U, (1993) Mutual regulation of the transcriptional activator NF-kappa B and its inhibitor, I kappa B-alpha. Proc Natl Acad Sci U S A 90: 2532-2536.
57. Rodriguez MS, Thompson J, Hay RT, Dargemont C, (1999) Nuclear retention of IkappaBalpha protects it from signal-induced degradation and inhibits nuclear factor kappaB transcriptional activation. J Biol Chem 274: 9108-9115.
58. May MJ, Ghosh S, (1999) IkappaB kinases: kinsmen with different crafts. Science 284: 271-273.
59. Jeon YJ, Han SH, Lee YW, Lee M, Yang KH, et al. (2000) Dexamethasone inhibits IL-1 beta gene expression in LPS-stimulated RAW 264.7 cells by blocking NF-kappa B/Rel and AP-1 activation. Immunopharmacology 48: 173-183.
60. Avni D, Ernst O, Philosoph A, Zor T, (2010) Role of CREB in modulation of TNFalpha and IL-10 expression in LPS-stimulated RAW264.7 macrophages. Mol Immunol 47: 1396-1403.
61. Godambe SA, Chaplin DD, Takova T, Bellone CJ, (1994) Upstream NFIL-6-like site located within a DNase I hypersensitivity region mediates LPS-induced transcription of the murine interleukin-1 beta gene. J Immunol 153: 143-152.