Heme oxygenase-1 mediates the anti-inflammatory effect of molecular hydrogen in LPS-stimulated RAW 264.7 macrophages

International Journal of Surgery

Volumn 11, Issue 10, 2013, Pages 1060-1066

  Chen, Hong Guang ^a   Xie, Ke Liang ^a   Han, Huan Zhi ^a   Wang, Wei Na ^a   Liu, Da Quan ^b   Wang, Guo Lin ^a   Yu, Yong Hao ^a  

^a TIANJIN MEDICAL UNIVERSITY   (China)

^b Institute of Acute Abdomen   (China)

Author keywords

Heme oxygenase 1; Inflammatory cytokines; Macrophage; Molecular hydrogen

Indexed keywords

HEME OXYGENASE 1; HIGH MOBILITY GROUP B1 PROTEIN; HYDROGEN; INTERLEUKIN 10; INTERLEUKIN 1BETA; LACTATE DEHYDROGENASE; LIPOPOLYSACCHARIDE; PROTOPORPHYRIN ZINC; TUMOR NECROSIS FACTOR ALPHA;

ANIMAL CELL; ANIMAL CELL CULTURE; ANTIINFLAMMATORY ACTIVITY; ARTICLE; CELL DAMAGE; CELL VIABILITY; CYTOKINE RELEASE; CYTOTOXICITY; MACROPHAGE; NONHUMAN; PRIORITY JOURNAL; PROTEIN EXPRESSION;

3-(4,5)-DIMETHYLTHIAHIAZO (-Z-Y1)-3,5-DI-PHENYTETRAZOLIUMROMIDE; CARBON MONOXIDE; CO; DMEM; DULBECCO'S MODIFIED EAGLE MEDIUM; ECL; EDTA; EGTA; ELISA; ENHANCED CHEMILUMINESCENCE; ENZYME-LINKED IMMUNOSORBENT ASSAY; ETHYLENE GLYCOL TETRAACETIC ACID; ETHYLENEDIAMINETETRAACETIC ACID; FBS; FETAL BOVINE SERUM; H(2); HEME OXYGENASE-1; HIGH MOBILITY GROUP BOX-1; HMGB1; HO-1; I/R; IL-10; IL-1Β; IL-6; INFLAMMATORY CYTOKINES; INTERLEUKIN-1 BETA; INTERLEUKIN-10; INTERLEUKIN-6; ISCHEMIA-REPERFUSION; LACTATE DEHYDROGENASE; LDH; LIPOPOLYSACCHARIDE; LPS; MACROPHAGE; MACROPHAGE INFLAMMATORY PROTEIN; MCP; MIP; MOLECULAR HYDROGEN; MONOCYTE CHEMOATTRACTANT PROTEIN; MTT; NADPH; NICOTINAMIDE ADENINE DINUCLEOTIDE PHOSPHATE; NRF2; NUCLEAR FACTOR ERYTHROID 2-RELATED FACTOR 2; P/S; PENICILLIN/STREPTOMYCIN SOLUTIONS; PHENYLMETHANESULFONYL FLUORIDE; PMSF; POLYVINYLIDENE FLUORIDE; PVDF; RADIOIMMUNOPRECIPITATION ASSAY; RIPA; TBST; TNF-Α; TRIS-BUFFERED SALINE WITH TWEEN; TUMOR NECROSIS FACTOR-ALPHA; ZINC PROTOPORPHYRIN; ZNPP;

ANIMALS; ANTI-INFLAMMATORY AGENTS; CELL LINE, TRANSFORMED; CELL SURVIVAL; CYTOKINES; GENE EXPRESSION; HEME OXYGENASE-1; HYDROGEN; LIPOPOLYSACCHARIDES; MACROPHAGES; MICE;

EID: 84889094297     PISSN: 17439191     EISSN: 17439159     Source Type: Journal    
DOI: 10.1016/j.ijsu.2013.10.007     Document Type: Article

References (37)

1. Liu J., Liu Y., Zhang H., Chen G., Wang K., Xiao X. Klf4 promotes the expression, translocation, and release of HMGB1in Raw264.7 macrophages in response to LPS. Shock 2008, 30:260-266.
2. Riedemann N.C., Guo R.F., Ard P.A. Novel strategies for the treatment of sepsis. Nat Med 2003, 9:517-524.
3. Arumugam T.V., Okun E., Tang S.C., Thundyil J., Taylor S.M., Woodruff T.M. Toll-like receptors in ischemia-reperfusion injury. Shock 2009, 32:4-16.
4. Mantovani A., Allavena P., Sica A., Balkwill F. Cancer-related inflammation. Nature 2008, 454:436-444.
5. Glass C.K., Saijo K., Winner B., Marchetto M.C., Gage F.H. Mechanisms underlying inflammation in neurodegeneration. Cell 2010, 140:918-934.
6. Ohsawa I., Ishikawa M., Takahashi K., et al. Hydrogen acts as a therapeutic antioxidant by selectively reducing cytotoxic oxygen radicals. Nat Med 2007, 13:688-694.
7. Xie K., Yu Y., Huang Y., et al. Molecular hydrogen ameliorates lipopolysaccharide-induced acute lung injury in mice through reducing inflammation and apoptosis. Shock 2012, 37:548-555.
8. Xie K., Yu Y., Pei Y., et al. Protective effects of hydrogen gas on murine polymicrobial sepsis via reducing oxidative stress and HMGB 1 release. Shock 2010, 34:90-97.
9. Xie K., Yu Y., Zhang Z., et al. Hydrogen gas improves survival rate and organ damage in zymosan-induced generalized inflammation model. Shock 2010, 34:495-501.
10. Qu J., Li X., Wang J., Mi W., Xie K., Qiu J. Inhalation of hydrogen gas attenuates cisplatin-induced ototoxicity via reducing oxidative stress. Int J Pediatr Otorhinolaryngol 2012, 76:111-115.
11. Tomohiro I., Nanako H., Riyako T., et al. Molecular hydrogen inhibits lipopolysaccharide/interferon γ-induced nitric oxide production through modulation of signal transduction in macrophages. Biochem Biophys Res Commun 2011, 441:143-149.
12. Fukuda K., Asoh S., Ishikawa M., Yamamoto Y., Ohsawa I., Ohta S. Inhalation of hydrogen gas suppresses hepatic injury caused by ischemia/reperfusion through reducing oxidative stress. Biochem Biophys Res Commun 2007, 361:670-674.
13. Buchholz B.M., Kaczorowski D.J., Sugimoto R., et al. Hydrogen inhalation ameliorates oxidative stress in transplantation induced intestinal graft injury. Am J Transplant 2008, 8:2015-2024.
14. Ohsawa I., Nishimaki K., Yamagata K., Ishikawa M., Ohta S. Consumption of hydrogen water prevents atherosclerosis in apolipoprotein E knockout mice. Biochem Biophys Res Commun 2008, 377:1195-1198.
15. Fu Y., Ito M., Fujita Y., et al. Molecular hydrogen is protective against 6-hydroxydopamine-induced nigrostriatal degeneration in a rat model of Parkinson's disease. Neurosci Lett 2009, 453:81-85.
16. Cai J., Kang Z., Liu K., et al. Neuroprotective effects of hydrogen saline in neonatal hypoxia-ischemia rat model. Brain Res 2009, 1256:129-137.
17. Xu Z., Zhou J., Cai J., Zhu Z., Sun X., Jiang C. Anti-inflammation effects of hydrogen saline in LPS activated macrophages and carrageenan induced paw oedema. JInflamm 2012, 9:2-8.
18. Stefan W.R., Augustine M.K. Heme oxygenase-1: redox regulation of a stress protein in lung and cell culture models. Antioxid Redox Signal 2005, 7:80-91.
19. Li Q., Zhu Y., Jiang H., Jiang H., Xu H., Sun Y. Heme oxygenase-1 mediates the anti-inflammatory effect of isoflurane preconditioning in LPS-stimulated macrophages. Acta Pharmacol Sin 2009, 30:228-234.
20. Dijkstra G., Blokzijl H., Bok L., et al. Opposite effect of oxidative stress on inducible nitric oxide synthase and heme oxygenase-1 expression in intestinal inflammation: anti-inflammatory effect of carbon monoxide. JPathol 2004, 204:296-303.
21. Chung S.W., Liu X., Macias A.A., Baron R.M., Perrella M.A. Heme oxygenase-1-derived carbon monoxide enhances the host defense response to microbial sepsis in mice. JClin Invest 2008, 118:239-247.
22. Huang C.S., Kawamura T., Toyoda Y., Nakao A. Recent advances in hydrogen research as a therapeutic medical gas. Free Radic Res 2010, 44:971-982.
23. Ha Y.M., Ham S.A., Kim Y.M., et al. β1-Adrenergic receptor-mediated HO-1 induction, via PI3K and p38 MAPK, by isoproterenol in RAW 264.7 cells leads to inhibition of HMGB1 release in LPS-activated RAW 264.7 cells and increases in survival rate of CLP-induced septic mice. Biochem Pharmacol 2011, 82:769-777.
24. Fang F., Liu G.T. Protective effects of compound FLZ, a novel synthetic analogue of squamosamide, on β-amyloid-induced rat brain mitochondrial dysfunction invitro. Acta Pharmacol Sin 2009, 30:522-529.
25. Peleg A.Y., Hooper D.C. Hospital-acquired infections due to gram-negative bacteria. NEngl J Med 2010, 362:1804-1813.
26. Dinarello C.A. Proinflammatory and anti-inflammatory cytokines as mediators in the pathogenesis of septic shock. Chest 1997, 112:321S-329S.
27. Cohen J. The immunopathogenesis of sepsis. Nature 2002, 420(6917):885-891.
28. Wang H., Bloom O., Zhang M., et al. HMGB-1 as a late mediator of endotoxin lethality in mice. Science 1999, 285:248-251.
29. Yang H., Ochani M., Li J., et al. Reversing established sepsis with antagonists of endogenous high-mobility group box1. Proc Natl Acad Sci U S A 2004, 101:296-301.
30. Wang J.X., Hou L.F., Yang Y., Tang W., Li Y., Zuo J.P. SM905, an artemisinin derivative, inhibited NO and pro-inflammatory cytokine production by suppressing MAPK and NF-κB pathways in RAW 264.7 macrophages. Acta Pharmacol Sin 2009, 30:1428-1435.
31. Andersson U., Tracey K.J. HMGB1 is a therapeutic target for sterile inflammation and infection. Annu Rev Immunol 2011, 29:139-162.
32. Qu J., Gan Y.N., Xie K.L., et al. Inhalation of hydrogen gas attenuates ouabain-induced auditory neuropathy. Acta Pharmacol Sin 2012, 1:1-7.
33. Tsoyi K., Lee T.Y., Lee Y.S., et al. Heme-oxygenase-1 induction and carbon monoxide-releasing molecule inhibit lipopolysaccharide (LPS)-induced high mobility group box 1 release invitro and improve survival of mice in LPS- and cecal ligation and puncture-induced sepsis model invivo. Mol Pharmacol 2009, 76:173-182.
34. Takamiya R., Hung C.C., Hall S.R., et al. High mobility group box 1 contributes to lethality of endotoxemia in heme oxygenase-1-deficient mice. Am J Respir Cell Mol Biol 2009, 41:129-135.
35. Fujii H., Takahashi T., Nakahira K., et al. Protective role of heme oxygenase-1 in the intestinal tissue injury in an experimental model of sepsis. Crit Care Med 2003 Mar, 31(3):893-902.
36. Stefan S., Karin E., Lie H., Shinkatsu M., Sanetaka S., Sandra C. Molecular hydrogen reduces LPS-induced neuroinflammation and promotes recovery from sickness behaviour in mice. PLoS One 2012, 7:e42078.
37. Kensler T.W., Wakabayashi N., Biswal S. Cell survival responses to environmental stresses via the keap1-nrf2-are pathway. Annu Rev Pharmacol Toxicol 2007, 47:89-116.