Effects of hydrogen-rich saline on early acute kidney injury in severely burned rats by suppressing oxidative stress induced apoptosis and inflammation

Journal of Translational Medicine

Volumn 13, Issue 1, 2015, Pages

  Guo, Song Xue ^a   Fang, Quan ^a   You, Chuan Gang ^a   Jin, Yun Yun ^a   Wang, Xin Gang ^a   Hu, Xin Lei ^a   Han, Chun Mao ^a  

^a ZHEJIANG UNIVERSITY   (China)

Author keywords

Acute kidney injury; Apoptosis; Burn insults; Hydrogen; Inflammation; Reactive oxygen species

Indexed keywords

AUTACOID; CASPASE 3; CATALASE; CREATININE; GLUTATHIONE PEROXIDASE; HYDROGEN RICH SODIUM CHLORIDE; IMMUNOGLOBULIN ENHANCER BINDING PROTEIN; INTERCELLULAR ADHESION MOLECULE 1; INTERLEUKIN 10; INTERLEUKIN 1BETA; INTERLEUKIN 6; MALONALDEHYDE; MITOGEN ACTIVATED PROTEIN KINASE; MITOGEN ACTIVATED PROTEIN KINASE P38; MYELOPEROXIDASE; NEUTROPHIL GELATINASE ASSOCIATED LIPOCALIN; PROTEIN KINASE B; SODIUM CHLORIDE; STRESS ACTIVATED PROTEIN KINASE; SUPEROXIDE DISMUTASE; TUMOR NECROSIS FACTOR ALPHA; UNCLASSIFIED DRUG; ACUTE PHASE PROTEIN; HYDROGEN; LIPOCALIN; NEUTROPHIL GELATINASE-ASSOCIATED LIPOCALIN PROTEIN, RAT; ONCOPROTEIN; PEROXIDASE;

ACUTE KIDNEY FAILURE; ANIMAL CELL; ANIMAL EXPERIMENT; ANIMAL MODEL; ANIMAL TISSUE; ANTIINFLAMMATORY ACTIVITY; ANTIOXIDANT ACTIVITY; APOPTOSIS; ARTICLE; BLOOD ANALYSIS; BURN; CONTROLLED STUDY; CREATININE BLOOD LEVEL; DISEASE SEVERITY; ENZYME ACTIVITY; ENZYME INHIBITION; ENZYME LINKED IMMUNOSORBENT ASSAY; ENZYME PHOSPHORYLATION; ENZYME REGULATION; HISTOPATHOLOGY; IMMUNOFLUORESCENCE; INFLAMMATION; KIDNEY FUNCTION; KIDNEY PARENCHYMA; KIDNEY TUBULE CELL; MALE; NONHUMAN; OXIDATION REDUCTION POTENTIAL; OXIDATIVE STRESS; PROTEIN EXPRESSION; QUANTITATIVE ANALYSIS; RAT; REAL TIME POLYMERASE CHAIN REACTION; SIGNAL TRANSDUCTION; WESTERN BLOTTING; ACUTE KIDNEY INJURY; ANIMAL; BIOLOGICAL MODEL; BLOOD; BURNS; COMPLICATION; DRUG EFFECTS; IMMUNOHISTOCHEMISTRY; KIDNEY TUBULE; METABOLISM; PATHOLOGY; SPRAGUE DAWLEY RAT;

ACUTE KIDNEY INJURY; ACUTE-PHASE PROTEINS; ANIMALS; APOPTOSIS; BLOTTING, WESTERN; BURNS; CREATININE; HYDROGEN; IMMUNOHISTOCHEMISTRY; INFLAMMATION; INFLAMMATION MEDIATORS; KIDNEY TUBULES; LIPOCALINS; MALE; MODELS, BIOLOGICAL; OXIDATIVE STRESS; PEROXIDASE; PROTO-ONCOGENE PROTEINS; RATS, SPRAGUE-DAWLEY; REAL-TIME POLYMERASE CHAIN REACTION; SIGNAL TRANSDUCTION; SODIUM CHLORIDE;

EID: 85019200817     PISSN: None     EISSN: 14795876     Source Type: Journal    
DOI: 10.1186/s12967-015-0548-3     Document Type: Article

References (89)

1. Palmieri T, Lavrentieva A, Greenhalgh DG (2010) Acute kidney injury in critically ill burn patients. Risk factors, progression and impact on mortality. Burns 36:205-211
2. Steinvall I, Bak Z, Sjoberg F (2008) Acute kidney injury is common, parallels organ dysfunction or failure, and carries appreciable mortality in patients with major burns: a prospective exploratory cohort study. Crit Care 12:R124
3. Mustonen KM, Vuola J (2008) Acute renal failure in intensive care burn patients (ARF in burn patients). J Burn Care Res 29:227-237
4. Sun IF, Lee SS, Lin SD, Lai CS (2007) Continuous arteriovenous hemodialysis and continuous venovenous hemofiltration in burn patients with acute renal failure. Kaohsiung J Med Sci 23:344-351
5. Yavuz S, Anarat A, Acarturk S, Dalay AC, Kesiktas E, Yavuz M et al (2014) Neutrophil gelatinase associated lipocalin as an indicator of acute kidney injury and inflammation in burned children. Burns 40:648-654
6. Sahu BD, Rentam KK, Putcha UK, Kuncha M, Vegi GM, Sistla R (2011) Carnosic acid attenuates renal injury in an experimental model of rat cisplatin-induced nephrotoxicity. Food Chem Toxicol 49:3090-3097
7. Wagener FA, Dekker D, Berden JH, Scharstuhl A, van der Vlag J (2009) The role of reactive oxygen species in apoptosis of the diabetic kidney. Apoptosis 14:1451-1458
8. Li H, Huang K, Liu X, Liu J, Lu X, Tao K et al (2014) Lithium chloride suppresses colorectal cancer cell survival and proliferation through ROS/GSK-3 beta/NF-kappa B signaling pathway. Oxid Med Cell Longev 2014:241864
9. Zhao L, Wang YB, Qin SR, Ma XM, Sun XJ, Wang ML et al (2013) Protective effect of hydrogen-rich saline on ischemia/reperfusion injury in rat skin flap. J Zhejiang Univ Sci B 14:382-391
10. Feliers D, Kasinath BS (2011) Erk in kidney diseases. J Signal Transduct 2011:768512
11. Kunduzova OR, Bianchi P, Pizzinat N, Escourrou G, Seguelas MH, Parini A et al (2002) Regulation of JNK/ERK activation, cell apoptosis, and tissue regeneration by monoamine oxidases after renal ischemia-reperfusion. FASEB J 16:1129-1131
12. Schroeter H, Boyd C, Spencer JP, Williams RJ, Cadenas E, Rice-Evans C (2002) MAPK signaling in neurodegeneration: influences of flavonoids and of nitric oxide. Neurobiol Aging 23:861-880
13. Ohsawa I, Ishikawa M, Takahashi K, Watanabe M, Nishimaki K, Yamagata K et al (2007) Hydrogen acts as a therapeutic antioxidant by selectively reducing cytotoxic oxygen radicals. Nat Med 13:688-694
14. Kurioka T, Matsunobu T, Satoh Y, Niwa K, Shiotani A (2014) Inhaled hydrogen gas therapy for prevention of noise-induced hearing loss through reducing reactive oxygen species. Neurosci Res 89:69-74
15. Hayashida K, Sano M, Ohsawa I, Shinmura K, Tamaki K, Kimura K et al (2008) Inhalation of hydrogen gas reduces infarct size in the rat model of myocardial ischemia-reperfusion injury. Biochem Biophys Res Commun 373:30-35
16. Zhuang Z, Zhou ML, You WC, Zhu L, Ma CY, Sun XJ et al (2012) Hydrogen-rich saline alleviates early brain injury via reducing oxidative stress and brain edema following experimental subarachnoid hemorrhage in rabbits. BMC Neurosci 13:47
17. Buchholz BM, Kaczorowski DJ, Sugimoto R, Yang R, Wang Y, Billiar TR et al (2008) Hydrogen inhalation ameliorates oxidative stress in transplantation induced intestinal graft injury. Am J Transpl 8:2015-2024
18. Kajiya M, Sato K, Silva MJ, Ouhara K, Do PM, Shanmugam KT et al (2009) Hydrogen from intestinal bacteria is protective for concanavalin A-induced hepatitis. Biochem Biophys Res Commun 386:316-321
19. Kajiya M, Silva MJ, Sato K, Ouhara K, Kawai T (2009) Hydrogen mediates suppression of colon inflammation induced by dextran sodium sulfate. Biochem Biophys Res Commun 386:11-15
20. Xie K, Yu Y, Huang Y, Zheng L, Li J, Chen H et al (2012) Molecular hydrogen ameliorates lipopolysaccharide-induced acute lung injury in mice through reducing inflammation and apoptosis. Shock 37:548-555
21. Cardinal JS, Zhan J, Wang Y, Sugimoto R, Tsung A, McCurry KR et al (2010) Oral hydrogen water prevents chronic allograft nephropathy in rats. Kidney Int 77:101-109
22. Fukuda KI, Asoh S, Ishikawa M, Yamamoto Y, Ohsawa I, Ohta S (2007) Inhalation of hydrogen gas suppresses hepatic injury caused by ischemia/reperfusion through reducing oxidative stress. Biochem Biophys Res Commun 361:670-674
23. Hong Y, Guo S, Chen S, Sun C, Zhang J, Sun X (2012) Beneficial effect of hydrogen-rich saline on cerebral vasospasm after experimental subarachnoid hemorrhage in rats. J Neurosci Res 90:1670-1680
24. Guo SX, Jin YY, Fang Q, You CG, Wang XG, Hu XL et al (2015) Beneficial effects of hydrogen-rich saline on early burn-wound progression in rats. PLoS One 10:e0124897
25. Wang X, Yu P, YongYang, Liu X, Jiang J, Liu D et al (2015) Hydrogen-rich saline resuscitation alleviates inflammation induced by severe burn with delayed resuscitation. Burns 41:379-385
26. Gao C, Huan J, Li W, Tang J (2009) Protective effects of ulinastatin on pancreatic and renal damage in rats following early scald injury. Burns 35:547-552
27. Abali AE, Cabioglu T, Ozdemir H, Haberal M (2015) Interactive effects of acupuncture on pain and distress in major burns: an experiment with rats. Burns 41:833-842
28. Xie K, Yu Y, Chen H, Han H, Sun X, Wang G (2013) Therapeutic effects of hydrogen-rich saline on peritonitis-induced septic shock in rats. Br J Anaesth 110:148-149
29. Guo C, Liang F, Shah Masood W, Yan X (2014) Hydrogen sulfide protected gastric epithelial cell from ischemia/reperfusion injury by Keap1 s-sulfhydration, MAPK dependent anti-apoptosis and NF-kappaB dependent anti-inflammation pathway. Eur J Pharmacol 725:70-78
30. Feng Y, Liu Y, Wang L, Cai X, Wang D, Wu K et al (2013) Sustained oxidative stress causes late acute renal failure via duplex regulation on p38 MAPK and Akt phosphorylation in severely burned rats. PLoS One 8:e54593
31. Homma K, Yoshida T, Yamashita M, Hayashida K, Hayashi M, Hori S (2015) Inhalation of hydrogen gas is beneficial for preventing contrast-induced acute kidney injury in rats. Nephron Exp Nephrol 128:116-122. doi: 10.1159/000369068
32. Merter AA, Mayir B, Erdogan O, Colak T (2015) Protective effects of amifostine on ischemia-reperfusion injury of rat kidneys. Indian J Pharmacol 47:185-189
33. Yan R, Li Y, Zhang L, Xia N, Liu Q, Sun H et al (2015) Augmenter of liver regeneration attenuates inflammation of renal ischemia/reperfusion injury through the NF-kappa B pathway in rats. Int Urol Nephrol 47:861-868
34. Hong DY, Lee JH, Park SO, Baek KJ, Lee KR (2013) Plasma neutrophil gelatinase-associated lipocalin as early biomarker for acute kidney injury in burn patients. J Burn Care Res 34:e326-e332
35. Si YN, Bao HG, Xu L, Wang XL, Shen Y, Wang JS et al (2014) Dexmedetomidine protects against ischemia/reperfusion injury in rat kidney. Eur Rev Med Pharmacol Sci 18:1843-1851
36. Tasanarong A, Kongkham S, Itharat A (2014) Antioxidant effect of Phyllanthus emblica extract prevents contrast-induced acute kidney injury. BMC Complement Altern Med 14:138
37. Chung KK, Stewart IJ, Gisler C, Simmons JW, Aden JK, Tilley MA et al (2012) The acute kidney injury network (AKIN) criteria applied in burns. J Burn Care Res 33:483-490
38. Arora S, Kaur T, Kaur A, Singh AP (2014) Glycine aggravates ischemia reperfusion-induced acute kidney injury through N-methyl-d-aspartate receptor activation in rats. Mol Cell Biochem 393:123-131
39. Billings FT, Yu C, Byrne JG, Petracek MR, Pretorius M (2014) Heme oxygenase-1 and acute kidney injury following cardiac surgery. Cardiorenal Med 4:12-21
40. Fang Y, Fu XJ, Gu C, Xu P, Wang Y, Yu WR et al (2011) Hydrogen-rich saline protects against acute lung injury induced by extensive burn in rat model. J Burn Care Res 32:e82-e91
41. Palipoch S (2013) A review of oxidative stress in acute kidney injury: protective role of medicinal plants-derived antioxidants. Afr J Tradit Complement Altern Med 10:88-93
42. Parihar A, Parihar MS, Milner S, Bhat S (2008) Oxidative stress and anti-oxidative mobilization in burn injury. Burns 34:6-17
43. Elks CM, Reed SD, Mariappan N, Shukitt-Hale B, Joseph JA, Ingram DK et al (2011) A blueberry-enriched diet attenuates nephropathy in a rat model of hypertension via reduction in oxidative stress. PLoS One 6:e24028
44. Shah S (2001) Role of iron in progressive renal disease. Am J Kidney Dis 37:S30-S33
45. Nishihashi T, Trandafir CC, Wang A, Ji X, Shimizu Y, Kurahashi K (2006) Hypersensitivity to hydroxyl radicals in rat basilar artery after subarachnoid hemorrhage. J Pharmacol Sci 100:234-236
46. Dagher PC, Mai EM, Hato T, Lee SY, Anderson MD, Karozos SC et al (2012) The p53 inhibitor pifithrin-alpha can stimulate fibrosis in a rat model of ischemic acute kidney injury. Am J Physiol Ren Physiol 302:F284-F291
47. Mariano F, Cantaluppi V, Stella M, Romanazzi GM, Assenzio B, Cairo M et al (2008) Circulating plasma factors induce tubular and glomerular alterations in septic burns patients. Crit Care 12:R42
48. Rana A, Sathyanarayana P, Lieberthal W (2001) Role of apoptosis of renal tubular cells in acute renal failure: therapeutic implications. Apoptosis 6:83-102
49. Yuan L, Wu MJ, Sun HY, Xiong J, Zhang Y, Liu CY et al (2011) VEGF-modified human embryonic mesenchymal stem cell implantation enhances protection against cisplatin-induced acute kidney injury. Am J Physiol Ren Physiol 300:F207-F218
50. Linkermann A, Chen G, Dong G, Kunzendorf U, Krautwald S, Dong Z (2014) Regulated cell death in AKI. J Am Soc Nephrol 25:2689-2701
51. Colpaert K, Hoste EA (2008) Acute kidney injury in burns: a story of volume and inflammation. Crit Care 12:192
52. Kinsey GR, Sharma R, Okusa MD (2013) Regulatory T cells in AKI. J Am Soc Nephrol 24:1720-1726
53. Proskuryakov SY, Konoplyannikov AG, Gabai VL (2003) Necrosis: a specific form of programmed cell death? Exp Cell Res 283:1-16
54. Ipaktchi K, Mattar A, Niederbichler AD, Hoesel LM, Vollmannshauser S, Hemmila MR et al (2006) Attenuating burn wound inflammatory signaling reduces systemic inflammation and acute lung injury. J Immunol 177:8065-8071
55. Hoesel LM, Mattar AF, Arbabi S, Niederbichler AD, Ipaktchi K, Su GL et al (2009) Local wound p38 MAPK inhibition attenuates burn-induced cardiac dysfunction. Surgery 146:775-785
56. Korkmaz A, Kolankaya D (2010) Protective effect of rutin on the ischemia/reperfusion induced damage in rat kidney. J Surg Res 164:309-315
57. Dalboni MA, Quinto BM, Grabulosa CC, Narciso R, Monte JC, Durao M Jr et al (2013) Tumour necrosis factor-alpha plus interleukin-10 low producer phenotype predicts acute kidney injury and death in intensive care unit patients. Clin Exp Immunol 173:242-249
58. Chen HG, Xie KL, Han HZ, Wang WN, Liu DQ, Wang GL et al (2013) Heme oxygenase-1 mediates the anti-inflammatory effect of molecular hydrogen in LPS-stimulated RAW 264.7 macrophages. Int J Surg 11:1060-1066
59. Fujii Y, Shirai M, Inamori S, Shimouchi A, Sonobe T, Tsuchimochi H et al (2013) Insufflation of hydrogen gas restrains the inflammatory response of cardiopulmonary bypass in a rat model. Artif Organs 37:136-141
60. Chen XL, Sun L, Guo F, Wang F, Liu S, Liang X et al (2012) High-mobility group box-1 induces proinflammatory cytokines production of Kupffer cells through TLRs-dependent signaling pathway after burn injury. PLoS One 7:e50668
61. Liu CM, Ma JQ, Sun YZ (2012) Puerarin protects rat kidney from lead-induced apoptosis by modulating the PI3K/Akt/eNOS pathway. Toxicol Appl Pharmacol 258:330-342
62. Chen XL, Xia ZF, Yu YX, Wei D, Wang CR, Ben DF (2005) p38 mitogen-activated protein kinase inhibition attenuates burn-induced liver injury in rats. Burns 31:320-330
63. Ipaktchi K, Mattar A, Niederbichler AD, Hoesel LM, Hemmila MR, Su GL et al (2006) Topical p38MAPK inhibition reduces dermal inflammation and epithelial apoptosis in burn wounds. Shock 26:201-209
64. Kita T, Ogawa M, Sato H, Kasai K, Tanaka T, Tanaka N (2008) Role of p38 mitogen-activated protein kinase pathway on heart failure in the infant rat after burn injury. Int J Exp Pathol 89:55-63
65. Cao W, Xie YH, Li XQ, Zhang XK, Chen YT, Kang R et al (2011) Burn-induced apoptosis of cardiomyocytes is survivin dependent and regulated by PI3 K/Akt, p38 MAPK and ERK pathways. Basic Res Cardiol 106:1207-1220
66. Lv GF, Dong ML, Hu DH, Zhang WF, Wang YC, Tang CW (2011) Insulin-mediated inhibition of p38 mitogen-activated protein kinase protects cardiomyocytes in severe burns. J Burn Care Res 32:591-599
67. Kita T, Yamaguchi H, Sato H, Kasai K, Tanaka T, Tanaka N (2004) Role of p38 mitogen-activated protein kinase pathway on renal failure in the infant rat after burn injury. Shock 21:535-542
68. Cassidy H, Radford R, Slyne J, O'Connell S, Slattery C, Ryan MP et al (2012) The role of MAPK in drug-induced kidney injury. J Signal Transduct 2012:463617
69. Malik S, Suchal K, Gamad N, Dinda AK, Arya DS, Bhatia J (2015) Telmisartan ameliorates cisplatin-induced nephrotoxicity by inhibiting MAPK mediated inflammation and apoptosis. Eur J Pharmacol 748:54-60
70. Tournier C, Hess P, Yang DD, Xu J, Turner TK, Nimnual A et al (2000) Requirement of JNK for stress-induced activation of the cytochrome c-mediated death pathway. Science 288:870-874
71. Marshall AH, Brooks NC, Hiyama Y, Qa'aty N, Al-Mousawi A, Finnerty CC et al (2013) Hepatic apoptosis postburn is mediated by c-Jun N-terminal kinase 2. Shock 39:183-188
72. Syrkina OL, Quinn DA, Jung W, Ouyang B, Hales CA (2007) Inhibition of JNK activation prolongs survival after smoke inhalation from fires. Am J Physiol Lung Cell Mol Physiol 292:L984-L991
73. Kyriakis JM, Banerjee P, Nikolakaki E, Dai T, Rubie EA, Ahmad MF et al (1994) The stress-activated protein kinase subfamily of c-Jun kinases. Nature 369:156-160
74. Seo JH, Lim JW, Kim H (2013) Differential role of ERK and p38 on NF-kappa B activation in Helicobacter pylori-infected gastric epithelial cells. J Cancer Prev 18:346-350
75. Torres M, Forman HJ (2003) Redox signaling and the MAP kinase pathways. BioFactors 17:287-296
76. Itoh T, Fujita Y, Ito M, Masuda A, Ohno K, Ichihara M et al (2009) Molecular hydrogen suppresses FcepsilonRI-mediated signal transduction and prevents degranulation of mast cells. Biochem Biophys Res Commun 389:651-656
77. Qiu X, Li H, Tang H, Jin Y, Li W, YuSun et al (2011) Hydrogen inhalation ameliorates lipopolysaccharide-induced acute lung injury in mice. Int Immunopharmacol 11:2130-2137
78. 2*(-) promote oridonin-induced phagocytosis of apoptotic cells by human histocytic lymphoma U937 cells. Int Immunopharmacol 15:414-423
79. Xu XF, Zhang J (2013) Saturated hydrogen saline attenuates endotoxin-induced acute liver dysfunction in rats. Physiol Res 62:395-403
80. Sobue S, Yamai K, Ito M, Ohno K, Ito M, Iwamoto T et al (2015) Simultaneous oral and inhalational intake of molecular hydrogen additively suppresses signaling pathways in rodents. Mol Cell Biochem 403:231-241
81. Li ZY, Yang Y, Ming M, Liu B (2011) Mitochondrial ROS generation for regulation of autophagic pathways in cancer. Biochem Biophys Res Commun 414:5-8
82. Kono H, Nakagawa K, Morita S, Shinoda K, Mizuno R, Kikuchi E et al (2013) Effect of a novel nuclear factor-kappaB activation inhibitor on renal ischemia-reperfusion injury. Transplantation 96:863-870
83. Lee JH, Jo YH, Kim K, Lee JH, Rim KP, Kwon WY et al (2013) Effect of N-acetylcysteine (NAC) on acute lung injury and acute kidney injury in hemorrhagic shock. Resuscitation 84:121-127
84. Nozaki Y, Kinoshita K, Yano T, Asato K, Shiga T, Hino S et al (2012) Signaling through the interleukin-18 receptor alpha attenuates inflammation in cisplatin-induced acute kidney injury. Kidney Int 82:892-902
85. Rodrigues CE, Sanches TR, Volpini RA, Shimizu MH, Kuriki PS, Camara NO et al (2012) Effects of continuous erythropoietin receptor activator in sepsis-induced acute kidney injury and multi-organ dysfunction. PLoS One 7:e29893
86. Sleeman P, Patel NN, Lin H, Walkden GJ, Ray P, Welsh GI et al (2013) High fat feeding promotes obesity and renal inflammation and protects against post cardiopulmonary bypass acute kidney injury in swine. Crit Care 17:R262
87. Zhang D, Li Y, Liu Y, Xiang X, Dong Z (2013) Paclitaxel ameliorates lipopolysaccharide-induced kidney injury by binding myeloid differentiation protein-2 to block Toll-like receptor 4-mediated nuclear factor-kappaB activation and cytokine production. J Pharmacol Exp Ther 345:69-75
88. Zhao H, Watts HR, Chong M, Huang H, Tralau-Stewart C, Maxwell PH et al (2013) Xenon treatment protects against cold ischemia associated delayed graft function and prolongs graft survival in rats. Am J Transpl 13:2006-2018
89. 2 inhibits TNF-alpha-induced lectin-like oxidized LDL receptor-1 expression by inhibiting nuclear factor kappaB activation in endothelial cells. Biotechnol Lett 33:1715-1722