A novel synthetic derivative of melatonin, 5-hydroxy-2'-isobutyl-streptochlorin (HIS), inhibits inflammatory responses via regulation of TRIF-dependent signaling and inflammasome activation

Toxicology and Applied Pharmacology

Volumn 284, Issue 2, 2015, Pages 227-235

  Shim, Do Wan ^a   Shin, Hee Jae ^b   Han, Ji Won ^a   Ji, Young Eun ^a   Jang, Cheol Hun ^a   Koppula, Sushruta ^a   Kang, Tae Bong ^a   Lee, Kwang Ho ^a  

^a Konkuk University   (South Korea)

^b Korea Research Institute of Ships and Ocean Engineering   (South Korea)

Author keywords

ALI; Anti inflammation; Inflammasome; Melatonin; Sepsis; Streptochlorin

Indexed keywords

ANTIINFLAMMATORY AGENT; CYCLOOXYGENASE 2; INDOLE DERIVATIVE; INFLAMMASOME; INTERLEUKIN 1BETA; INTERLEUKIN 6; LIPOPOLYSACCHARIDE; MELATONIN; NITRIC OXIDE; OXAZOLE DERIVATIVE; REACTIVE OXYGEN METABOLITE; STREPTOCHLORIN; TICAM-1 PROTEIN, MOUSE; TUMOR NECROSIS FACTOR ALPHA; VESICULAR TRANSPORT ADAPTOR PROTEIN;

ACUTE LUNG INJURY; ANALOGS AND DERIVATIVES; ANIMAL; BAGG ALBINO MOUSE; C57BL MOUSE; CELL LINE; DISEASE MODEL; DRUG EFFECTS; FEMALE; INFLAMMATION; MACROPHAGE; METABOLISM; MITOCHONDRION; MOUSE; RANDOMIZATION; SHOCK, SEPTIC; SIGNAL TRANSDUCTION;

ACUTE LUNG INJURY; ADAPTOR PROTEINS, VESICULAR TRANSPORT; ANIMALS; ANTI-INFLAMMATORY AGENTS; CELL LINE; CYCLOOXYGENASE 2; DISEASE MODELS, ANIMAL; FEMALE; INDOLES; INFLAMMASOMES; INFLAMMATION; INTERLEUKIN-1BETA; INTERLEUKIN-6; LIPOPOLYSACCHARIDES; MACROPHAGES; MELATONIN; MICE; MICE, INBRED BALB C; MICE, INBRED C57BL; MITOCHONDRIA; NITRIC OXIDE; OXAZOLES; RANDOM ALLOCATION; REACTIVE OXYGEN SPECIES; SHOCK, SEPTIC; SIGNAL TRANSDUCTION; TUMOR NECROSIS FACTOR-ALPHA;

EID: 84932119293     PISSN: 0041008X     EISSN: 10960333     Source Type: Journal    
DOI: 10.1016/j.taap.2015.02.006     Document Type: Article

References (47)

1. Akira S., Takeda K. Toll-like receptor signalling. Nat. Rev. Immunol. 2004, 4:499-511.
2. Akira S., Uematsu S., Takeuchi O. Pathogen recognition and innate immunity. Cell 2006, 124:783-801.
3. Anisimov V.N., Zavarzina N.Y., Zabezhinski M.A., Popovich I.G., Zimina O.A., Shtylick A.V., Arutjunyan A.V., Oparina T.I., Prokopenko V.M., Mikhalski A.I. Melatonin increases both life span and tumor incidence in female CBA mice. J. Gerontol. A Biol. Sci. Med. Sci. 2001, 56:B311-B323.
4. Choi E., Jin J., Lee J., Choi J., Choi I.S., Kim S. Melatonin inhibits Prevotella intermedia lipopolysaccharide-induced production of nitric oxide and interleukin-6 in murine macrophages by suppressing NF-κB and STAT1 activity. J. Pineal Res. 2011, 50:197-206.
5. Covert M.W., Leung T.H., Gaston J.E., Baltimore D. Achieving stability of lipopolysaccharide-induced NF-κB activation. Science 2005, 309:1854-1857.
6. Cuzzocrea S., Reiter R.J. Pharmacological actions of melatonin in acute and chronic inflammation. Curr. Top. Med. Chem. 2002, 2:153-165.
7. Dinarello C.A. Biologic basis for interleukin-1 in disease. Blood 1996, 87:2095-2147.
8. Fitzgerald K.A., McWhirter S.M., Faia K.L., Rowe D.C., Latz E., Golenbock D.T., Coyle A.J., Liao S., Maniatis T. IKK& and TBK1 are essential components of the IRF3 signaling pathway. Nat. Immunol. 2003, 4:491-496.
9. Gasse P., Riteau N., Charron S., Girre S., Fick L., Pétrilli V., Tschopp J., Lagente V., Quesniaux V.F., Ryffel B. Uric acid is a danger signal activating NALP3 inflammasome in lung injury inflammation and fibrosis. Am. J. Respir. Crit. Care Med. 2009, 179:903-913.
10. Halle A., Hornung V., Petzold G.C., Stewart C.R., Monks B.G., Reinheckel T., Fitzgerald K.A., Latz E., Moore K.J., Golenbock D.T. The NALP3 inflammasome is involved in the innate immune response to amyloid-β. Nat. Immunol. 2008, 9:857-865.
11. Hawkins P., Stephens L. PI3K signalling in inflammation. Biochim. Biophys. Acta 2014, (Epub ahead of print).
12. Heid M.E., Keyel P.A., Kamga C., Shiva S., Watkins S.C., Salter R.D. Mitochondrial reactive oxygen species induces NLRP3-dependent lysosomal damage and inflammasome activation. J. Immunol. 2013, 191:5230-5238.
13. Jacobs A.T., Ignarro L.J. Lipopolysaccharide-induced expression of interferon-β mediates the timing of inducible nitric-oxide synthase induction in RAW 264.7 macrophages. J. Biol. Chem. 2001, 276:47950-47957.
14. Jones B.W., Means T.K., Heldwein K.A., Keen M.A., Hill P.J., Belisle J.T., Fenton M.J. Different toll-like receptor agonists induce distinct macrophage responses. J. Leukoc. Biol. 2001, 69:1036-1044.
15. Kagan J.C., Su T., Horng T., Chow A., Akira S., Medzhitov R. TRAM couples endocytosis of toll-like receptor 4 to the induction of interferon-β. Nat. Immunol. 2008, 9:361-368.
16. Kang S.J., Wang S., Hara H., Peterson E.P., Namura S., Amin-Hanjani S., Huang Z., Srinivasan A., Tomaselli K.J., Thornberry N.A., Moskowitz M.A., Yuan J. Dual role of caspase-11 in mediating activation of caspase-1 and caspase-3 under pathological conditions. J. Cell Biol. 2000, 149:613-622.
17. Kawai T., Akira S. Toll-like receptors and their crosstalk with other innate receptors in infection and immunity. Immunity 2011, 34:637-650.
18. Kimura H., Hokari R., Miura S., Shigematsu T., Hirokawa M., Akiba Y., Kurose I., Higuchi H., Fujimori H., Tsuzuki Y. Increased expression of an inducible isoform of nitric oxide synthase and the formation of peroxynitrite in colonic mucosa of patients with active ulcerative colitis. Gut 1998, 42:180-187.
19. Lamkanfi M. Emerging inflammasome effector mechanisms. Nat. Rev. Immunol. 2011, 11:213-220.
20. Lawrence T., Willoughby D.A., Gilroy D.W. Anti-inflammatory lipid mediators and insights into the resolution of inflammation. Nat. Rev. Immunol. 2002, 2:787-795.
21. Lee S., Shin H.J., Kim D., Shim D., Kim T., Ye S., Won H., Koppula S., Kang T., Lee K. Streptochlorin suppresses allergic dermatitis and mast cell activation via regulation of Lyn/Fyn and Syk signaling pathways in cellular and mouse models. PLoS One 2013, 8:e74194.
22. Levy D.E., Darnell J. Stats: transcriptional control and biological impact. Nat. Rev. Mol. Cell Biol. 2002, 3:651-662.
23. Mariathasan S., Weiss D.S., Newton K., McBride J., O'Rourke K., Roose-Girma M., Lee W.P., Weinrauch Y., Monack D.M., Dixit V.M. Cryopyrin activates the inflammasome in response to toxins and ATP. Nature 2006, 440:228-232.
24. Martinon F., Burns K., Tschopp J. The inflammasome: a molecular platform triggering activation of inflammatory caspases and processing of proIL-β. Mol. Cell 2002, 10:417-426.
25. Martinon F., Mayor A., Tschopp J. The inflammasomes: guardians of the body. Annu. Rev. Immunol. 2009, 27:229-265.
26. Meduri G.U., Kohler G., Headley S., Tolley E., Stentz F., Postlethwaite A. Inflammatory cytokines in the BAL of patients with ARDS persistent elevation over time predicts poor outcome. CHEST J. 1995, 108:1303-1314.
27. Miguel R.N., Wong J., Westoll J.F., Brooks H.J., O'Neill L.A., Gay N.J., Bryant C.E., Monie T.P. A dimer of the toll-like receptor 4 cytoplasmic domain provides a specific scaffold for the recruitment of signalling adaptor proteins. PLoS One 2007, 2:e788.
28. Moynagh P.N. TLR signalling and activation of IRFs: revisiting old friends from the NF-kB pathway. Trends Immunol. 2005, 26:469-476.
29. Netea M.G., Fantuzzi G., Kullberg B.J., Stuyt R.J., Pulido E.J., McIntyre R.C., Joosten L.A., Van der Meer J.W., Dinarello C.A. Neutralization of IL-18 reduces neutrophil tissue accumulation and protects mice against lethal Escherichia coli and Salmonella typhimurium endotoxemia. J. Immunol. 2000, 164:2644-2649.
30. Nishiya T., Kajita E., Miwa S., DeFranco A.L. TLR3 and TLR7 are targeted to the same intracellular compartments by distinct regulatory elements. J. Biol. Chem. 2005, 280:37107-37117.
31. Nosal'ova V., Zeman M., Černá S., Navarova J., Zakálová M. Protective effect of melatonin in acetic acid induced colitis in rats. J. Pineal Res. 2007, 42:364-370.
32. O'Neill L.A., Bowie A.G. The family of five: TIR-domain-containing adaptors in toll-like receptor signalling. Nat. Rev. Immunol. 2007, 7:353-364.
33. Rathinam V.A., Vanaja S.K., Fitzgerald K.A. Regulation of inflammasome signaling. Nat. Immunol. 2012, 13:333-342.
34. Rathinam V.A., Vanaja S.K., Waggoner L., Sokolovska A., Becker C., Stuart L.M., Leong J.M., Fitzgerald K.A. TRIF licenses caspase-11-dependent NLRP3 inflammasome activation by gram-negative bacteria. Cell 2012, 150:606-619.
35. Samavati L., Rastogi R., Du W., Hüttemann M., Fite A., Franchi L. STAT3 tyrosine phosphorylation is critical for interleukin-1 beta and interleukin-6 production in response to lipopolysaccharide and live bacteria. Mol. Immunol. 2009, 46:1867-1877.
36. Sarkar A., Hall M.W., Exline M., Hart J., Knatz N., Gatson N.T., Wewers M.D. Caspase-1 regulates Escherichia coli sepsis and splenic B cell apoptosis independently of interleukin-1β and interleukin-18. Am. J. Respir. Crit. Care Med. 2006, 174:1003-1010.
37. Schnyder-Candrian S., Quesniaux V.F., Di Padova F., Maillet I., Noulin N., Couillin I., Moser R., Erard F., Vargaftig B.B., Ryffel B. Dual effects of p38 MAPK on TNF-dependent bronchoconstriction and TNF-independent neutrophil recruitment in lipopolysaccharide-induced acute respiratory distress syndrome. J. Immunol. 2005, 175:262-269.
38. Schrader L.I., Kinzenbaw D.A., Johnson A.W., Faraci F.M., Didion S.P. IL-6 deficiency protects against angiotensin II-induced endothelial dysfunction and hypertrophy. Arterioscler. Thromb. Vasc. Biol. 2007, 27:2576-2581.
39. Shim D.W., Han J.W., Sun X., Jang C.H., Koppula S., Kim T.J., Kang T.B., Lee K.H. Lysimachia clethroides Duby extract attenuates inflammatory response in Raw 264.7 macrophages stimulated with lipopolysaccharide and in acute lung injury mouse model. J. Ethnopharmacol. 2013, 150:1007-1015.
40. Smith W.L., Marnett L.J., DeWitt D.L. Prostaglandin and thromboxane biosynthesis. Pharmacol. Ther. 1991, 49:153-179.
41. Terry P.D., Villinger F., Bubenik G.A., Sitaraman S.V. Melatonin and ulcerative colitis: evidence, biological mechanisms, and future research. Inflamm. Bowel Dis. 2009, 15:134-140.
42. Toshchakov V., Jones B.W., Perera P., Thomas K., Cody M.J., Zhang S., Williams B.R., Major J., Hamilton T.A., Fenton M.J. TLR4, but not TLR2, mediates IFN-β-induced STAT1α/β-dependent gene expression in macrophages. Nat. Immunol. 2002, 3:392-398.
43. van de Veerdonk F.L., Netea M.G., Dinarello C.A., Joosten L.A. Inflammasome activation and IL-1β and IL-18 processing during infection. Trends Immunol. 2011, 32:110-116.
44. Wesoly J., Szweykowska-Kulinska Z., Bluyssen H.A. STAT activation and differential complex formation dictate selectivity of interferon responses. Acta Biochim. Pol. Engl. Ed. 2007, 54:27.
45. Xia M., Liang Y., Wang H., Chen X., Huang Y., Zhang Z., Chen Y., Zhang C., Zhao M., Xu D. Melatonin modulates TLR4-mediated inflammatory genes through MyD88-and TRIF-dependent signaling pathways in lipopolysaccharide-stimulated RAW264. 7 cells. J. Pineal Res. 2012, 53:325-334.
46. Yamamoto M., Sato S., Hemmi H., Hoshino K., Kaisho T., Sanjo H., Takeuchi O., Sugiyama M., Okabe M., Takeda K. Role of adaptor TRIF in the MyD88-independent toll-like receptor signaling pathway. Science 2003, 301:640-643.
47. Zhou R., Yazdi A.S., Menu P., Tschopp J. A role for mitochondria in NLRP3 inflammasome activation. Nature 2011, 469:221-225.