Protective effects of hydrogen sulfide inhalation on oxidative stress in rats with cotton smoke inhalation‑induced lung injury

Han,Zhi‑Hai; Jiang,Yi; Duan,Yun‑You; Wang,Xiao‑Yang; Huang,Yan; Fang,Ting‑Zheng

doi:10.3892/etm.2015.2482

Protective effects of hydrogen sulfide inhalation on oxidative stress in rats with cotton smoke inhalation‑induced lung injury

Authors:
- Zhi‑Hai Han
- Yi Jiang
- Yun‑You Duan
- Xiao‑Yang Wang
- Yan Huang
- Ting‑Zheng Fang
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Affiliations: Pulmonary and Critical Care Medicine of PLA Navy General Hospital, Beijing 100048, P.R. China, Political Department Clinic of Shenyang Military Area Command, Shenyang, Liaoning 110032, P.R. China
Published online on: May 8, 2015 https://doi.org/10.3892/etm.2015.2482
Pages: 164-168

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Abstract

The aim of the present study was to investigate the mechanism by which hydrogen sulfide (H2S) inhalation protects against oxidative stress in rats with cotton smoke inhalation‑induced lung injury. A total of 24 male Sprague‑Dawley rats were separated randomly into four groups, which included the control, H2S, smoke and smoke + H2S groups. A rat model of cotton smoke inhalation‑induced lung injury was established following inhalation of 30% oxygen for 6 h. In addition, H2S (80 ppm) was inhaled by the rats in the H2S and smoke + H2S groups for 6 h following smoke or sham‑smoke inhalation. Enzyme‑linked immunosorbent assays were performed to measure various indices in the rat lung homogenate, while the levels of nuclear factor (NF)‑κBp65 in the lung tissue of the rats were determined and semiquantitatively analyzed using immunohistochemistry. In addition, quantitative fluorescence polymerase chain reaction was employed to detect the mRNA expression of inducible nitric oxide synthase (iNOS) in the rat lung tissue. The concentrations of malondialdehyde (MDA), nitric oxide (NO), inducible iNOS and NF‑κBp65, as well as the sum‑integrated optical density of NF‑κBp65 and the relative mRNA expression of iNOS, in the rat lung tissue from the smoke + H2S group were significantly lower when compared with the smoke group. The concentrations of MDA, NO, iNOS and NF‑κBp65 in the H2S group were comparable to that of the control group. Therefore, inhalation of 80 ppm H2S may reduce iNOS mRNA transcription and the production of iNOS and NO in rats by inhibiting NF‑κBp65 activation, subsequently decreasing oxidative stress and cotton smoke inhalation‑induced lung injury.

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1	Ballard-Croft C, Sumpter LR, Broaddus R, Alexander J, Wang D and Zwischenberger JB: Ovine smoke/burn ARDS model: a new ventilator-controlled smoke delivery system. J Surg Res. 164:e155–e162. 2010. View Article : Google Scholar : PubMed/NCBI
2	Esechie A, Kiss L, Olah G, Horváth EM, Hawkins H, Szabo C and Traber DL: Protective effect of hydrogen sulfide in a murine model of acute lung injury induced by combined burn and smoke inhalation. Clin Sci (Lond). 115:91–97. 2008. View Article : Google Scholar : PubMed/NCBI
3	Papapetropoulos A, Pyriochou A, Altaany Z, et al: Hydrogen sulfide is an endogenous stimulator of angiogenesis. Proc Natl Acad Sci USA. 106:21972–21977. 2009. View Article : Google Scholar : PubMed/NCBI
4	Szabó C and Papapetropoulos A: Hydrogen sulphide and angiogenesis: mechanisms and applications. Br J Pharmacol. 164:853–865. 2011. View Article : Google Scholar : PubMed/NCBI
5	Yang G, Wu L, Jiang B, et al: H₂S as a physiologic vasorelaxant: hypertension in mice with deletion of cystathionine gamma-lyase. Science. 322:587–590. 2008. View Article : Google Scholar : PubMed/NCBI
6	Muzaffar S, Jeremy JY, Sparatore A, Del Soldato P, Angelini GD and Shukla N: H₂S-donating sildenafil (ACS6) inhibits superoxide formation and gp91phox expression in arterial endothelial cells: role of protein kinases A and G. Br J Pharmacol. 155:984–994. 2008. View Article : Google Scholar : PubMed/NCBI
7	Li PC, Chen WC, Chang LC and Lin SC: Substance P acts via the neurokinin receptor 1 to elicit bronchoconstriction, oxidative stress, and upregulated ICAM-1 expression after oil smoke exposure. Am J Physiol Lung Cell Mol Physiol. 294:L912–L920. 2008. View Article : Google Scholar : PubMed/NCBI
8	Zhu XY, Gu H and Ni X: Hydrogen sulfide in the endocrine and reproductive systems. Expert Rev Clin Pharmacol. 4:75–82. 2011. View Article : Google Scholar : PubMed/NCBI
9	Tokuda K, Kida K, Marutani E, et al: Inhaled hydrogen sulfide prevents endotoxin-induced systemic inflammation and improves survival by altering sulfide metabolism in mice. Antioxid Redox Signal. 17:11–21. 2012. View Article : Google Scholar : PubMed/NCBI
10	Faller S, Zimmermann KK, Strosing KM, et al: Inhaled hydrogen sulfide protects against lipopolysaccharide-induced acute lung injury in mice. Med Gas Res. 2:262012. View Article : Google Scholar : PubMed/NCBI
11	Faller S, Ryter SW, Choi AM, Loop T, Schmidt R and Hoetzel A: Inhaled hydrogen sulfide protects against ventilator-induced lung injury. Anesthesiology. 113:104–115. 2010. View Article : Google Scholar : PubMed/NCBI
12	Zhang Y, Han Z, Duan Y, et al: The influence of inhalation H2S lung in rats. Jie Fang Jun Yi Xue Yuan Xue Bao. 35:1241–1244. 2014.
13	McPherson C: Regulation of animal care and research? NIH's opinion. J Animal Sci. 51:492–496. 1980.
14	National Research Council (US) Committee for the Update of the Guide for the Care and Use of Laboratory Animals, . Guide for the Care and Use of Laboratory Animals. 8th. National Academies Press (US); Washington (DC): 2011
15	Lee HM, Greeley GH, Herndon DN, Sinha M, Luxon BA and Englander EW: A rat model of smoke inhalation injury: influence of combustion smoke on gene expression in the brain. Toxicol Appl Pharmacol. 208:255–265. 2005. View Article : Google Scholar : PubMed/NCBI
16	Huang PS, Tang GJ, Chen CH and Kou YR: Whole-body moderate hypothermia confers protection from wood smoke-induced acute lung injury in rats: the therapeutic window. Crit Care Med. 34:1160–1167. 2006. View Article : Google Scholar : PubMed/NCBI
17	Zou YY, Lu J, Poon DJ, Kaur C, Cao Q, Teo AL and Ling EA: Combustion smoke exposure induces up-regulated expression of vascular endothelial growth factor, aquaporin 4, nitric oxide synthases and vascular permeability in the retina of adult rats. Neuroscience. 160:698–709. 2009. View Article : Google Scholar : PubMed/NCBI
18	Rehberg S, Maybauer MO, Enkhbaatar P, Maybauer DM, Yamamoto Y and Traber DL: Pathophysiology, management and treatment of smoke inhalation injury. Expert Rev Respir Med. 3:283–297. 2009. View Article : Google Scholar : PubMed/NCBI
19	Enkhbaatar P and Traber DL: Pathophysiology of acute lung injury in combined burn and smoke inhalation injury. Clin Sci (Lond). 107:137–143. 2004. View Article : Google Scholar : PubMed/NCBI
20	Cox RA, Jacob S, Oliveras G, et al: Pulmonary expression of nitric oxide synthase isoforms in sheep with smoke inhalation and burn injury. Exp Lung Res. 35:104–118. 2009. View Article : Google Scholar : PubMed/NCBI
21	Westphal M, Enkhbaatar P, Schmalstieg FC, et al: Neuronal nitric oxide synthase inhibition attenuates cardiopulmonary dysfunctions after combined burn and smoke inhalation injury in sheep. Crit Care Med. 36:1196–1204. 2008. View Article : Google Scholar : PubMed/NCBI
22	Rehberg S, Maybauer MO, Maybauer DM, Traber LD, Enkhbaatar P and Traber DL: The role of nitric oxide and reactive nitrogen species in experimental ARDS. Front Biosci (Schol Ed). 2:18–29. 2010. View Article : Google Scholar : PubMed/NCBI
23	Westphal M, Rehberg S, Maybauer MO, et al: Cardiopulmonary effects of low-dose arginine vasopressin in ovine acute lung injury. Crit Care Med. 39:357–363. 2011. View Article : Google Scholar : PubMed/NCBI
24	Calvert JW: The summer of hydrogen sulfide: highlights from two international conferences. Med Gas Res. 3:52013. View Article : Google Scholar : PubMed/NCBI
25	Gadalla MM and Snyder SH: Hydrogen sulfide as a gasotransmitter. J Neurochem. 113:14–26. 2010. View Article : Google Scholar : PubMed/NCBI
26	Liu WL, Liu ZW, Li TS, Wang C and Zhao B: Hydrogen sulfide donor regulates alveolar epithelial cell apoptosis in rats with acute lung injury. Chin Med J (Engl). 126:494–499. 2013.PubMed/NCBI
27	Oh GS, Pae HO, Lee BS, et al: Hydrogen sulfide inhibits nitric oxide production and nuclear factor-kappaB via heme oxygenase-1 expression in RAW264.7 macrophages stimulated with lipopolysaccharide. Free Radic Biol Med. 41:106–119. 2006. View Article : Google Scholar : PubMed/NCBI
28	Wagner F, Asfar P, Calzia E, Radermacher P and Szabó C: Bench-to-bedside review: Hydrogen sulfide - the third gaseous transmitter: applications for critical care. Crit Care. 13:2132009. View Article : Google Scholar : PubMed/NCBI
29	Jeong SO, Pae HO, Oh GS, et al: Hydrogen sulfide potentiates interleukin-1beta-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. 2006. View Article : Google Scholar : PubMed/NCBI
30	Zhi L, Ang AD, Zhang H, Moore PK and Bhatia M: Hydrogen sulfide induces the synthesis of proinflammatory cytokines in human monocyte cell line U937 via the ERK-NF-kappaB pathway. J Leukoc Biol. 81:1322–1332. 2007. View Article : Google Scholar : PubMed/NCBI
31	Hu LF, Wong PT, Moore PK and Bian JS: Hydrogen sulfide attenuates lipopolysaccharide-induced inflammation by inhibition of p38 mitogen-activated protein kinase in microglia. J Neurochem. 100:1121–1128. 2007. View Article : Google Scholar : PubMed/NCBI
32	Janssen-Heininger YM, Poynter ME and Baeuerle PA: Recent advances towards understanding redox mechanisms in the activation of nuclear factor kappaB. Free Radic Biol Med. 28:1317–1327. 2000. View Article : Google Scholar : PubMed/NCBI
33	LaLonde C, Nayak U, Hennigan J and Demling R: Plasma catalase and glutathione levels are decreased in response to inhalation injury. J Burn Care Rehabil. 18:515–519. 1997. View Article : Google Scholar : PubMed/NCBI
34	Paul BD and Snyder SH: H₂S signalling through protein sulfhydration and beyond. Nat Rev Mol Cell Biol. 13:499–507. 2012. View Article : Google Scholar : PubMed/NCBI
35	Whiteman M, Armstrong JS, Chu SH, et al: The novel neuromodulator hydrogen sulfide: an endogenous peroxynitrite scavenger? J Neurochem. 90:765–768. 2004. View Article : Google Scholar : PubMed/NCBI
36	Whiteman M, Cheung NS, Zhu YZ, et al: Hydrogen sulphide: a novel inhibitor of hypochlorous acid-mediated oxidative damage in the brain? Biochem Biophys Res Commun. 326:794–798. 2005. View Article : Google Scholar : PubMed/NCBI
37	Arai M, Yoshioka S, Nishimura R and Okuda K: FAS/FASL-mediated cell death in the bovine endometrium. Anim Reprod Sci. 151:97–104. 2014. View Article : Google Scholar : PubMed/NCBI