Astaxanthin attenuates early acute kidney injury following severe burns in rats by ameliorating oxidative stress and mitochondrial-related apoptosis

Marine Drugs

Volumn 13, Issue 4, 2015, Pages 2105-2123

  Guo, Song Xue ^a   Zhou, Han Lei ^a   Huang, Chun Lan ^a   You, Chuan Gang ^a   Fang, Quan ^a   Wu, Pan ^a   Wang, Xin Gang ^a   Han, Chun Mao ^a  

^a ZHEJIANG UNIVERSITY SCHOOL OF MEDICINE   (China)

Author keywords

Acute kidney injury; Apoptosis; Astaxanthin; Burn; Mitochondria; Oxidative stress

Indexed keywords

2 MORPHOLINO 8 PHENYLCHROMONE; ASTAXANTHIN; CASPASE 3; CASPASE 9; CREATININE; CYTOCHROME C; NEUTROPHIL GELATINASE ASSOCIATED LIPOCALIN; PROTEIN BAD; PROTEIN KINASE B; ACUTE PHASE PROTEIN; ANTIOXIDANT; APOPTOSIS REGULATORY PROTEIN; BIOLOGICAL MARKER; ENZYME INHIBITOR; LIPOCALIN; NEUTROPHIL GELATINASE-ASSOCIATED LIPOCALIN PROTEIN, RAT; ONCOPROTEIN; PHOSPHATIDYLINOSITOL 3 KINASE; XANTHOPHYLL;

ACUTE KIDNEY FAILURE; ANIMAL EXPERIMENT; ANIMAL MODEL; ANIMAL TISSUE; APOPTOSIS; ARTICLE; BURN; CONTROLLED STUDY; CREATININE BLOOD LEVEL; DISEASE SEVERITY; DOWN REGULATION; DRUG MECHANISM; KIDNEY TUBULE DAMAGE; MITOCHONDRION; NONHUMAN; OXIDATIVE STRESS; PROTEIN EXPRESSION; PROTEIN LOCALIZATION; PROTEIN PHOSPHORYLATION; RAT; RENAL PROTECTION; UPREGULATION; ACUTE KIDNEY INJURY; ANIMAL; ANTAGONISTS AND INHIBITORS; BLOOD; BURNS; DOSE RESPONSE; DRUG EFFECTS; GENETICS; INTRAVENOUS DRUG ADMINISTRATION; KIDNEY; MALE; METABOLISM; PATHOLOGY; PATHOPHYSIOLOGY; PHOSPHORYLATION; PROTEIN PROCESSING; RANDOMIZATION; SIGNAL TRANSDUCTION; SPRAGUE DAWLEY RAT;

RATTUS;

ACUTE KIDNEY INJURY; ACUTE-PHASE PROTEINS; ANIMALS; ANTIOXIDANTS; APOPTOSIS; APOPTOSIS REGULATORY PROTEINS; BIOMARKERS; BURNS; CREATININE; DOSE-RESPONSE RELATIONSHIP, DRUG; ENZYME INHIBITORS; INJECTIONS, INTRAVENOUS; KIDNEY; LIPOCALINS; MALE; OXIDATIVE STRESS; PHOSPHATIDYLINOSITOL 3-KINASE; PHOSPHORYLATION; PROTEIN PROCESSING, POST-TRANSLATIONAL; PROTO-ONCOGENE PROTEINS; RANDOM ALLOCATION; RATS, SPRAGUE-DAWLEY; SIGNAL TRANSDUCTION; XANTHOPHYLLS;

EID: 84928484943     PISSN: None     EISSN: 16603397     Source Type: Journal    
DOI: 10.3390/md13042105     Document Type: Article

References (63)

1. Mosier, M.J.; Pham, T.N.; Klein, M.B.; Gibran, N.S.; Arnoldo, B.D.; Gamelli, R.L.; Tompkins, R.G.; Herndon, D.N. Early acute kidney injury predicts progressive renal dysfunction and higher mortality in severely burned adults. J. Burn Care Res. 2010, 31, 83-92.
2. Palmieri, T.; Lavrentieva, A.; Greenhalgh, D.G. Acute kidney injury in critically ill burn patients. Risk factors, progression and impact on mortality. Burns 2010, 36, 205-211.
3. Steinvall, I.; Bak, Z.; Sjoberg, F. 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 2008, 12, R124.
4. Leblanc, M.; Thibeault, Y.; Querin, S. Continuous haemofiltration and haemodiafiltration for acute renal failure in severely burned patients. Burns 1997, 23, 160-165.
5. Coca, S.G.; Bauling, P.; Schifftner, T.; Howard, C.S.; Teitelbaum, I.; Parikh, C.R. Contribution of acute kidney injury toward morbidity and mortality in burns: A contemporary analysis. Am. J. Kidney Dis. 2007, 49, 517-523.
6. Colpaert, K.; Hoste, E.A. Acute kidney injury in burns: A story of volume and inflammation. Crit. Care 2008, 12, 192.
7. Mustonen, K.M.; Vuola, J. Acute renal failure in intensive care burn patients (arf in burn patients). J. Burn Care Res. 2008, 29, 227-237.
8. Yavuz, S.; Anarat, A.; Acarturk, S.; Dalay, A.C.; Kesiktas, E.; Yavuz, M.; Acarturk, T.O. Neutrophil gelatinase associated lipocalin as an indicator of acute kidney injury and inflammation in burned children. Burns 2014, 40, 648-654.
9. Hoetzenecker, W.; Echtenacher, B.; Guenova, E.; Hoetzenecker, K.; Woelbing, F.; Bruck, J.; Teske, A.; Valtcheva, N.; Fuchs, K.; Kneilling, M.; et al. Ros-induced atf3 causes susceptibility to secondary infections during sepsis-associated immunosuppression. Nat. Med. 2012, 18, 128-134.
10. Parihar, A.; Parihar, M.S.; Milner, S.; Bhat, S. Oxidative stress and anti-oxidative mobilization in burn injury. Burns 2008, 34, 6-17.
11. Sedeek, M.; Callera, G.; Montezano, A.; Gutsol, A.; Heitz, F.; Szyndralewiez, C.; Page, P.; Kennedy, C.R.; Burns, K.D.; Touyz, R.M.; et al. Critical role of nox4-based nadph oxidase in glucose-induced oxidative stress in the kidney: Implications in type 2 diabetic nephropathy. Am. J. Physiol. Ren. Physiol. 2010, 299, F1348-F1358.
12. Zhang, X.S.; Zhang, X.; Zhou, M.L.; Zhou, X.M.; Li, N.; Li, W.; Cong, Z.X.; Sun, Q.; Zhuang, Z.; Wang, C.X.; et al. Amelioration of oxidative stress and protection against early brain injury by astaxanthin after experimental subarachnoid hemorrhage. J. Neurosurg. 2014, 121, 42-54.
13. Horton, J.W. Free radicals and lipid peroxidation mediated injury in burn trauma: The role of antioxidant therapy. Toxicology 2003, 189, 75-88.
14. Gravante, G.; Delogu, D.; Sconocchia, G. "Systemic apoptotic response" after thermal burns. Apoptosis 2007, 12, 259-270.
15. Quoilin, C.; Mouithys-Mickalad, A.; Lecart, S.; Fontaine-Aupart, M.P.; Hoebeke, M. Evidence of oxidative stress and mitochondrial respiratory chain dysfunction in an in vitro model of sepsis-induced kidney injury. Biochim. Biophys. Acta 2014, 1837, 1790-1800.
16. Sahu, B.D.; Rentam, K.K.; Putcha, U.K.; Kuncha, M.; Vegi, G.M.; Sistla, R. Carnosic acid attenuates renal injury in an experimental model of rat cisplatin-induced nephrotoxicity. Food Chem. Toxicol. 2011, 49, 3090-3097.
17. Wagener, F.A.; Dekker, D.; Berden, J.H.; Scharstuhl, A.; van der Vlag, J. The role of reactive oxygen species in apoptosis of the diabetic kidney. Apoptosis 2009, 14, 1451-1458.
18. Feng, Y.; Liu, Y.; Wang, L.; Cai, X.; Wang, D.; Wu, K.; Chen, H.; Li, J.; Lei, W. Sustained oxidative stress causes late acute renal failure via duplex regulation on p38 mapk and akt phosphorylation in severely burned rats. PLoS ONE 2013, 8, e54593.
19. Jiang, L.; Luo, M.; Liu, D.; Chen, B.; Zhang, W.; Mai, L.; Zeng, J.; Huang, N.; Huang, Y.; Mo, X.; et al. Bad overexpression inhibits cell growth and induces apoptosis via mitochondrial-dependent pathway in non-small cell lung cancer. Cancer Cell Int. 2013, 13, 53.
20. Datta, S.R.; Dudek, H.; Tao, X.; Masters, S.; Fu, H.; Gotoh, Y.; Greenberg, M.E. Akt phosphorylation of bad couples survival signals to the cell-intrinsic death machinery. Cell 1997, 91, 231-241.
21. Stoyanoff, T.R.; Todaro, J.S.; Aguirre, M.V.; Zimmermann, M.C.; Brandan, N.C. Amelioration of lipopolysaccharide-induced acute kidney injury by erythropoietin: Involvement of mitochondria-regulated apoptosis. Toxicology 2014, 318, 13-21.
22. Li, Y.; Zeng, M.; Chen, W.; Liu, C.; Wang, F.; Han, X.; Zuo, Z.; Peng, S. Dexmedetomidine reduces isoflurane-induced neuroapoptosis partly by preserving pi3k/akt pathway in the hippocampus of neonatal rats. PLoS ONE 2014, 9, e93639.
23. Zhang, X.S.; Zhang, X.; Wu, Q.; Li, W.; Zhang, Q.R.; Wang, C.X.; Zhou, X.M.; Li, H.; Shi, J.X.; Zhou, M.L. Astaxanthin alleviates early brain injury following subarachnoid hemorrhage in rats: Possible involvement of akt/bad signaling. Mar. Drugs 2014, 12, 4291-4310.
24. Noshita, N.; Lewen, A.; Sugawara, T.; Chan, P.H. Evidence of phosphorylation of akt and neuronal survival after transient focal cerebral ischemia in mice. J. Cereb. Blood Flow Metab. 2001, 21, 1442-1450.
25. Choi, H.D.; Kang, H.E.; Yang, S.H.; Lee, M.G.; Shin, W.G. Pharmacokinetics and first-pass metabolism of astaxanthin in rats. Br. J. Nutr. 2011, 105, 220-227.
26. Shen, H.; Kuo, C.C.; Chou, J.; Delvolve, A.; Jackson, S.N.; Post, J.; Woods, A.S.; Hoffer, B.J.; Wang, Y.; Harvey, B.K. Astaxanthin reduces ischemic brain injury in adult rats. FASEB J. 2009, 23, 1958-1968.
27. Naguib, Y.M. Antioxidant activities of astaxanthin and related carotenoids. J. Agric. Food Chem. 2000, 48, 1150-1154.
28. Lee, D.H.; Lee, Y.J.; Kwon, K.H. Neuroprotective effects of astaxanthin in oxygen-glucose deprivation in sh-sy5y cells and global cerebral ischemia in rat. J. Clin. Biochem. Nutr. 2010, 47, 121-129.
29. Kim, Y.J.; Kim, Y.A.; Yokozawa, T. Protection against oxidative stress, inflammation, and apoptosis of high-glucose-exposed proximal tubular epithelial cells by astaxanthin. J. Agric. Food Chem. 2009, 57, 8793-8797.
30. Sila, A.; Ghlissi, Z.; Kamoun, Z.; Makni, M.; Nasri, M.; Bougatef, A.; Sahnoun, Z. Astaxanthin from shrimp by-products ameliorates nephropathy in diabetic rats. Eur. J. Nutr. 2015, 54, 301-307.
31. Qiu, X.; Fu, K.; Zhao, X.; Zhang, Y.; Yuan, Y.; Zhang, S.; Gu, X.; Guo, H. Protective effects of astaxanthin against ischemia/reperfusion induced renal injury in mice. J. Transl. Med. 2015, 13, 28.
32. Gal, A.F.; Andrei, S.; Cernea, C.; Taulescu, M.; Catoi, C. Effects of astaxanthin supplementation on chemically induced tumorigenesis in wistar rats. Acta Vet. Scand. 2012, 54, 50.
33. Lauver, D.A.; Lockwood, S.F.; Lucchesi, B.R. Disodium disuccinate astaxanthin (cardax) attenuates complement activation and reduces myocardial injury following ischemia/reperfusion. J. Pharmacol. Exp. Ther. 2005, 314, 686-692.
34. Nagendraprabhu, P.; Sudhandiran, G. Astaxanthin inhibits tumor invasion by decreasing extracellular matrix production and induces apoptosis in experimental rat colon carcinogenesis by modulating the expressions of erk-2, nfkb and cox-2. Investig. New Drugs 2011, 29, 207-224.
35. Arunkumar, E.; Bhuvaneswari, S.; Anuradha, C.V. An intervention study in obese mice with astaxanthin, a marine carotenoid - Effects on insulin signaling and pro-inflammatory cytokines. Food Funct. 2012, 3, 120-126.
36. Fassett, R.G.; Coombes, J.S. Astaxanthin, oxidative stress, inflammation and cardiovascular disease. Future Cardiol. 2009, 5, 333-342.
37. Sener, G.; Sehirli, A.O.; Gedik, N.; Dulger, G.A. Rosiglitazone, a ppar-gamma ligand, protects against burn-induced oxidative injury of remote organs. Burns 2007, 33, 587-593.
38. Li, P.K.; Burdmann, E.A.; Mehta, R.L. Acute kidney injury: Acute kidney injury-Global health alert. Nat. Rev. Nephrol. 2013, 9, 133-135.
39. Guerin, M.; Huntley, M.E.; Olaizola, M. Haematococcus astaxanthin: Applications for human health and nutrition. Trends Biotechnol. 2003, 21, 210-216.
40. Yuan, J.P.; Peng, J.; Yin, K.; Wang, J.H. Potential health-promoting effects of astaxanthin: A high-value carotenoid mostly from microalgae. Mol. Nutr. Food Res. 2011, 55, 150-165.
41. Hong, D.Y.; Lee, J.H.; Park, S.O.; Baek, K.J.; Lee, K.R. Plasma neutrophil gelatinase-associated lipocalin as early biomarker for acute kidney injury in burn patients. J. Burn Care Res. 2013, 34, e326-e332.
42. Si, Y.N.; Bao, H.G.; Xu, L.; Wang, X.L.; Shen, Y.; Wang, J.S.; Yang, X.B. Dexmedetomidine protects against ischemia/reperfusion injury in rat kidney. Eur. Rev. Med. Pharmacol. Sci. 2014, 18, 1843-1851.
43. Tasanarong, A.; Kongkham, S.; Itharat, A. Antioxidant effect of phyllanthus emblica extract prevents contrast-induced acute kidney injury. BMC Complement. Altern. Med. 2014, 14, 138.
44. Arora, S.; Kaur, T.; Kaur, A.; Singh, A.P. Glycine aggravates ischemia reperfusion-induced acute kidney injury through n-methyl-d-aspartate receptor activation in rats. Mol. Cell. Biochem. 2014, 393, 123-131.
45. Billings, F.T.; Yu, C.; Byrne, J.G.; Petracek, M.R.; Pretorius, M. Heme oxygenase-1 and acute kidney injury following cardiac surgery. Cardiorenal Med. 2014, 4, 12-21.
46. Fang, Y.; Fu, X.J.; Gu, C.; Xu, P.; Wang, Y.; Yu, W.R.; Sun, Q.; Sun, X.J.; Yao, M. Hydrogen-rich saline protects against acute lung injury induced by extensive burn in rat model. J. Burn Care Res. 2011, 32, e82-e91.
47. Palipoch, S. A review of oxidative stress in acute kidney injury: Protective role of medicinal plants-derived antioxidants. Afr. J. Tradit. Complement. Altern. Med. 2013, 10, 88-93.
48. Elks, C.M.; Reed, S.D.; Mariappan, N.; Shukitt-Hale, B.; Joseph, J.A.; Ingram, D.K.; Francis, J. A blueberry-enriched diet attenuates nephropathy in a rat model of hypertension via reduction in oxidative stress. PLoS ONE 2011, 6, e24028.
49. Shah, S. Role of iron in progressive renal disease. Am. J. Kidney Dis. 2001, 37, S30-S33.
50. Rael, L.T.; Bar-Or, R.; Mains, C.W.; Slone, D.S.; Levy, A.S.; Bar-Or, D. Plasma oxidation-reduction potential and protein oxidation in traumatic brain injury. J. Neurotrauma 2009, 26, 1203-1211.
51. Rael, L.T.; Bar-Or, R.; Ambruso, D.R.; Mains, C.W.; Slone, D.S.; Craun, M.L.; Bar-Or, D. The effect of storage on the accumulation of oxidative biomarkers in donated packed red blood cells. J. Trauma 2009, 66, 76-81.
52. Hong, Y.; Guo, S.; Chen, S.; Sun, C.; Zhang, J.; Sun, X. Beneficial effect of hydrogen-rich saline on cerebral vasospasm after experimental subarachnoid hemorrhage in rats. J. Neurosci. Res. 2012, 90, 1670-1680.
53. Dagher, P.C.; Mai, E.M.; Hato, T.; Lee, S.Y.; Anderson, M.D.; Karozos, S.C.; Mang, H.E.; Knipe, N.L.; Plotkin, Z.; Sutton, T.A. The p53 inhibitor pifithrin-alpha can stimulate fibrosis in a rat model of ischemic acute kidney injury. Am. J. Physiol. -Ren. 2012, 302, F284-F291.
54. Mariano, F.; Cantaluppi, V.; Stella, M.; Romanazzi, G.M.; Assenzio, B.; Cairo, M.; Biancone, L.; Triolo, G.; Ranieri, V.M.; Camussi, G. Circulating plasma factors induce tubular and glomerular alterations in septic burns patients. Crit. Care 2008, 12, R42.
55. Rana, A.; Sathyanarayana, P.; Lieberthal, W. Role of apoptosis of renal tubular cells in acute renal failure: Therapeutic implications. Apoptosis 2001, 6, 83-102.
56. Yuan, L.; Wu, M.J.; Sun, H.Y.; Xiong, J.; Zhang, Y.; Liu, C.Y.; Fu, L.L.; Liu, D.M.; Liu, H.Q.; Mei, C.L. Vegf-modified human embryonic mesenchymal stem cell implantation enhances protection against cisplatin-induced acute kidney injury. Am. J. Physiol. Ren. Physiol. 2011, 300, F207-F218.
57. Liu, C.M.; Ma, J.Q.; Sun, Y.Z. Puerarin protects rat kidney from lead-induced apoptosis by modulating the pi3k/akt/enos pathway. Toxicol. Appl. Pharmacol. 2012, 258, 330-342.
58. Chalah, A.; Khosravi-Far, R. The mitochondrial death pathway. Adv. Exp. Med. Biol. 2008, 615, 25-45.
59. Rong, Y.; Distelhorst, C.W. Bcl-2 protein family members: Versatile regulators of calcium signaling in cell survival and apoptosis. Ann. Rev. Physiol. 2008, 70, 73-91.
60. Small, D.M.; Gobe, G.C. Cytochrome c: Potential as a noninvasive biomarker of drug-induced acute kidney injury. Expert Opin. Drug Metab. Toxicol. 2012, 8, 655-664.
61. Gao, C.; Huan, J.; Li, W.; Tang, J. Protective effects of ulinastatin on pancreatic and renal damage in rats following early scald injury. Burns 2009, 35, 547-552.
62. Abali, A.E.; Cabioglu, T.; Ozdemir, H.; Haberal, M. Interactive effects of acupuncture on pain and distress in major burns: An experiment with rats. Burns 2014, in press.
63. Yuan, X.; Jing, S.; Wu, L.; Chen, L.; Fang, J. Pharmacological postconditioning with tanshinone iia attenuates myocardial ischemia-reperfusion injury in rats by activating the phosphatidylinositol 3-kinase pathway. Exp. Ther. Med. 2014, 8, 973-977.