Endogenous hydrogen sulfide regulates inflammatory response by activating the ERK pathway in polymicrobial sepsis

Journal of Immunology

Volumn 181, Issue 6, 2008, Pages 4320-4331

  Zhang, Huili ^a,c   Moochhala, Shabbir M ^b   Bhatia, Madhav ^a  

^a NATIONAL UNIVERSITY OF SINGAPORE   (Singapore)

^b DSO NATIONAL LABORATORIES   (Singapore)

^c SHANGHAI JIAO TONG UNIVERSITY SCHOOL OF MEDICINE   (China)

Author keywords

[No Author keywords available]

Indexed keywords

2 (2 AMINO 3 METHOXYPHENYL)CHROMONE; CHEMOKINE; CYTOKINE; HYDROGEN SULFIDE; I KAPPA B ALPHA; IMMUNOGLOBULIN ENHANCER BINDING PROTEIN; MITOGEN ACTIVATED PROTEIN KINASE; MITOGEN ACTIVATED PROTEIN KINASE 1; MITOGEN ACTIVATED PROTEIN KINASE 3; PROPARGYLGLYCINE; SODIUM CHLORIDE; SODIUM DITHIONITE; AUTACOID;

ANIMAL EXPERIMENT; ANIMAL MODEL; ARTICLE; CECUM; CONTROLLED STUDY; CYTOKINE PRODUCTION; ENZYME INHIBITION; IMMUNITY; INFLAMMATION; LIGATION; LIVER; LUNG; MALE; MICROORGANISM; MOUSE; NONHUMAN; PRIORITY JOURNAL; PROTEIN DEGRADATION; PROTEIN PHOSPHORYLATION; PUNCTURE; SEPSIS; SIGNAL TRANSDUCTION; SYNTHESIS; ANIMAL; BACTEREMIA; BLOOD; ENZYME ACTIVATION; ENZYMOLOGY; IMMUNOLOGY; METABOLISM; PATHOLOGY; PERITONITIS; PHYSIOLOGY; UPREGULATION;

ANIMALS; BACTEREMIA; CECUM; ENZYME ACTIVATION; HYDROGEN SULFIDE; INFLAMMATION MEDIATORS; LIGATION; MALE; MICE; MITOGEN-ACTIVATED PROTEIN KINASE 1; MITOGEN-ACTIVATED PROTEIN KINASE 3; NF-KAPPA B; PERITONITIS; PUNCTURES; SEPSIS; SIGNAL TRANSDUCTION; UP-REGULATION;

EID: 56149107741     PISSN: 00221767     EISSN: 15506606     Source Type: Journal    
DOI: 10.4049/jimmunol.181.6.4320     Document Type: Article

References (44)

1. 2S be the third endogenous gaseous transmitter? FASEB J. 16: 1792-1798.
2. Moore, P. K., M. Bhatia, and S. M. Moochhala. 2003. Hydrogen sulfide: from the smell of the past to the mediator of the future? Trends Pharmacol. Sci. 24: 609-611.
3. 2S): the third gas of interest for pharmacologists. Pharmacol. Rep. 59: 4-24.
4. Martin, G. S., D. M. Mannino, S. Eaton, and M. Moss. 2003. The epidemiology of sepsis in the United States from 1979 through 2000. N. Engl. J. Med. 348: 1546-1554. (Pubitemid 36437931)
5. Angus, D. C., W. T. Linde-Zwirble, J. Lidicker, G. Clermont, J. Carcillo, and M. R. Pinsky. 2001. Epidemiology of severe sepsis in the United States: analysis of incidence, outcome, and associated costs of care. Crit. Care Med. 29: 1303-1310.
6. Zhang, H., L. Zhi, P. K. Moore, and M. Bhatia. 2006. Role of hydrogen sulfide in cecal ligation and puncture-induced sepsis in the mouse. Am. J. Physiol. 290: L1193-L1201.
7. Zhang, H., L. Zhi, S. M. Moochhala, P. K. Moore, and M. Bhatia. 2007. Hydrogen sulfide acts as an inflammatory mediator in cecal ligation and puncture induced sepsis in mice by up-regulating the production of cytokines and chemokines via NF-κB. Am. J. Physiol. 292: L960-L971.
8. Li, L., M. Bhatia, Y. Z. Zhu, Y. C. Zhu, R. D. Ramnath, Z. J. Wang, F. B. Anuar, M. Whiteman, M. Salto-Tellez, and P. K. Moore. 2005. Hydrogen sulfide is a novel mediator of lipopolysaccharide-induced inflammation in the mouse. FASEB J. 19: 1196-1198. (Pubitemid 40946463)
9. Collin, M., F. B. Anuar, O. Murch, M. Bhatia, P. K. Moore, and C. Thiemermann. 2005. Inhibition of endogenous hydrogen sulfide formation reduces the organ injury caused by endotoxemia. Br. J. Pharmacol. 146: 498-505. (Pubitemid 41487065)
10. Bhatia, M., J. Sidhapuriwala, S. M. Moochhala, and P. K. Moore. 2005. Hydrogen sulphide is a mediator of carrageenan-induced hindpaw oedema in the rat. Br. J. Pharmacol. 145: 141-144. (Pubitemid 40756518)
11. Bhatia, M., F. L. Wong, D. Fu, H. Y. Law, S. M. Moochhala, and P. K. Moore. 2005. Role of hydrogen sulfide in acute pancreatitis and associated lung injury. FASEB J. 19: 623-625. (Pubitemid 40471265)
12. Kyriakis, J. M., and J. Avruch. 2001. Mammalian mitogen-activated protein kinase signal transduction pathways activated by stress and inflammation. Physiol. Rev. 81: 808-860.
13. Brown, M. A., and W. K. Jones. 2004. NF-κB action in sepsis: the innate immune system and the heart. Front. Biosci. 9: 1201-1217. (Pubitemid 39060836)
14. Jiang, B., S. Xu, X. Hou, D. R. Pimentel, P. Brecher, and R. A. Cohen. 2004. Temporal control of NF-κB activation by ERK differentially regulates interleukin-1β-induced gene expression. J. Biol. Chem. 279: 1323-1329. (Pubitemid 38082657)
15. Choi, M. S., S. H. Lee, H. S. Cho, Y. Kim, Y. P. Yun, H. Y. Jung, J. K. Jung, B. C. Lee, H. B. Pyo, and J. T. Hong. 2007. Inhibitory effect of obovatol on nitric oxide production and activation of NF-κB/MAP kinases in lipopolysaccharide-treated RAW 264.7 cells. Eur. J. Pharmacol. 556: 181-189. (Pubitemid 46098933)
16. Dumitru, C. D., J. D. Ceci, C. Tsatsanis, D. Kontoyiannis, K. Stamatakis, J. H. Lin, C. Patriotis, N. A. Jenkins, N. G. Copeland, G. Kollias, and P. N. Tsichlis. 2000. TNF-α induction by LPS is regulated posttranscriptionally via a Tpl2/ERK-dependent pathway. Cell 103: 1071-1083.
17. Riedemann, N. C., R. F Guo, and P. A. Ward. 2003. The enigma of sepsis. J. Clin. Invest. 112: 460-467.
18. Baker, C. C., I. H. Chaudry, H. O. Gaines, and A. E. Baue. 1983. Evaluation of factors affecting mortality rate after sepsis in a murine cecal ligation and puncture model. Surgery 94: 331-335.
19. Minutoli, L., P. Antonuccio, C. Romeo, P. A. Nicotina, A. Bitto, S. Arena, F. Polito, D. Altavilla, N. Turiaco, A. Cutrupi, et al. 2005. Evidence for a role of mitogen-activated protein kinase 3/mitogen-activated protein kinase in the development of testicular ischemia-reperfusion injury. Biol. Reprod. 73: 730-736. (Pubitemid 41356132)
20. Tamaoki, J., E. Tagaya, K. Kawatani, J. Nakata, Y. Endo, and A. Nagai. 2004. Airway mucosal thickening and bronchial hyperresponsiveness induced by inhaled β2-agonist in mice. Chest 126: 205-212. (Pubitemid 38943139)
21. Siegel, L. M. 1965. A direct microdetermination for sulfide. Anal. Biochem. 11: 126-132.
22. Chunyu, Z., D. Junbao, B. Dingfang, Y. Hui, T. Xiuying, and T. Chaoshu. 2003. The regulatory effect of hydrogen sulfide on hypoxic pulmonary hypertension in rats. Biochem. Biophys. Res. Commun. 302: 810-816. (Pubitemid 36294046)
23. ATP channel opener. EMBO J. 20: 6008-6016.
24. Labarca, C., and K. Paigen. 1980. A simple, rapid, and sensitive DNA assay procedure. Anal. Biochem. 102: 344-352. (Pubitemid 10115803)
25. Ishii, I., N. Akahoshi, X. N. Yu, Y. Kobayashi, K. Namekata, G. Komak, and H. Kimura. 2004. Murine cystathionine γ-lyase: complete cNDA and genomic sequences, promoter activity, tissue distribution and developmental expression. Biochem. J. 381: 113-123. (Pubitemid 38932217)
26. Liu, S. F., and A. B. Malik. 2006. NF-κB activation as a pathological mechanism of septic shock and inflammation. Am. J. Physiol. 290: L622-L645.
27. Zhang, H., A. Hegde, S. W. Ng, S. Adhikari, S. M. Moochhala, and M. Bhatia. 2007. Hydrogen sulfide up-regulates substance P in polymicrobial sepsis-associated lung injury. J. Immunol. 179: 4153-4160.
28. Penner, C. G., G. Gang, C. Wray, J. E. Fischer, and P. O. Hasselgren. 2001. The transcription factors NF-κB and AP-1 are differentially regulated in skeletal muscle during sepsis. Biochem. Biophys. Res. Commun. 281: 1331-1336.
29. Chang, C. K., M. V. Albarillo, and W. Schumer. 2001. Therapeutic effect of dimethyl sulfoxide on ICAM-1 gene expression and activation of NF-κB and AP-1 in septic rats. J. Surg. Res. 95: 181-187.
30. Arnalich, F., E. Garcia-Palomero, J. Lopez, M. Jimenez, R. Madero, J. Renart, J. J. Vazquez, and C. Montiel. 2000. Predictive value of nuclear factor κB activity and plasma cytokine levels in patients with sepsis. Infect. Immun. 68: 1942-1945. (Pubitemid 30164821)
31. Zhang, F. X., C. J. Kirschning, R. Mancinelli, X. P. Xu, Y. Jin, E. Faure, A. Mantovani, M. Rothe, M. Muzio, and M. Arditi. 1999. Bacterial lipopolysaccharide activates nuclear factor-κB through interleukin-1 signaling mediators in cultured human dermal endothelial cells and mononuclear phagocytes. J. Biol. Chem. 274: 7611-7614. (Pubitemid 129518142)
32. Cario, E., I. M. Rosenberg, S. L. Brandwein, P. L. Beck, H. C. Reinecker, and D. K. Podolsky. 2000. Lipopolysaccharide activates distinct signaling pathways in intestinal epithelial cell lines expressing Toll-like receptors. J. Immunol. 164: 966-972. (Pubitemid 30043724)
33. Yang, G., X. Sun, and R. Wang. 2004. Hydrogen sulfide-induced apoptosis of human aorta smooth muscle cells via the activation of mitogen-activated protein kinases and caspase-3. FASEB J. 18: 1782-1784. (Pubitemid 39561683)
34. Yang, G., K. Cao, L. Wu, and R. Wang. 2004. Cystathionine γ-lyase overexpression inhibits cell proliferation via a H2S-dependent modulation of ERK1/2 phosphorylation and p21Cip/WAK-1. J. Biol. Chem. 279: 49199-49205. (Pubitemid 39625803)
35. Yang, G., L. Wu, and R. Wang. 2006. Pro-apoptotic effect of endogenous H2S on human aorta smooth muscle cells. FASEB J. 20: 553-555. (Pubitemid 46671247)
36. Deplancke, B., and H. R. Gaskins. 2003. Hydrogen sulfide induces serum independent cell cycle entry in nontransformed rat intestinal epithelial cells. FASEB J. 17: 1310-1312.
37. Jeong, S. O., H. O. Pae, G. S. Oh, G. S. Jeong, B. S. Lee, S. Lee, D. Y. Kim, H. Y. Rhew, K. M. Lee, and H. T. Chung. 2006. Hydrogen sulfide potentiates interleukin-1β-induced nitric oxide production via enhancement of extracellular signal-regulated kinase activation in rat vascular smooth muscle cells. Biochem. Biophys. Res. Commun. 345: 938-944.
38. Zhi, L., A. D. Ang, H. Zhang, P. K. Moore, and M. Bhatia. 2007. Hydrogen sulfide induces the synthesis of proinflammatory cytokines in human monocyte cell line U937 via the ERK-NF-κB pathway. J. Leukocyte Biol. 81: 1322-1332. (Pubitemid 46702052)
39. Oh, G. S., H. O. Pae, B. S. Lee, B. N. Kim, J. M. Kim, H. R. Kim, S. B. Jeon, W. K. Jeon, H. J. Chae, and H. T. Chung. 2006. Hydrogen sulfide inhibits nitric oxide production and nuclear factor-κB via heme oxygenase-1 expression in RAW264.7 macrophages stimulated with lipopolysaccharide. Free Radical Biol. Med. 41: 106-119.
40. Rinaldi, L., G. Gobbi, M. Pambianco, C. Micheloni, P. Mirandola, and M. Vitale. 2006. Hydrogen sulfide prevents apoptosis of human PMN via inhibition of p38 and caspase 3. Lab. Invest. 86: 391-397.
41. Lee, S. W., Y. S. Hu, L. F. Hu, Q. Lu, G. S. Dawe, P. K. Moore, P. T. Wong, and J. S. Bian. 2006. Hydrogen sulphide regulates calcium homeostasis in microglial cells. Glia 54: 116-124.
42. Ghosh, S., and M. Karin. 2002. Missing pieces in the NF-κB puzzle. Cell 109: S81-S96.
43. 2+ accelerates nuclear translocation of nuclear factor κB in osteoclasts. J. Biol. Chem. 278: 8286-8293.
44. Anuar, F., M. Whiteman, J. L. Siau, S. E. Kwong, M. Bhatia, and P. K. Moore. 2006. Nitric oxide-releasing flurbiprofen reduces formation of proinflammatory hydrogen sulfide in lipopolysaccharide-treated rat. Br. J. Pharmacol. 147: 966-974.