Astaxanthin protects mesangial cells from hyperglycemia-induced oxidative signaling

Journal of Cellular Biochemistry

Volumn 103, Issue 6, 2008, Pages 1925-1937

  Manabe, Emiko ^a   Handa, Osamu ^a   Naito, Yuji ^a   Mizushima, Katsura ^a   Akagiri, Satomi ^a   Adachi, Satoko ^a   Takagi, Tomohisa ^a   Kokura, Satoshi ^a   Maoka, Takashi ^b   Yoshikawa, Toshikazu ^a  

^a KYOTO PREFECTURAL UNIVERSITY OF MEDICINE   (Japan)

^b RESEARCH INSTITUTE FOR PRODUCTION DEVELOPMENT   (Japan)

Author keywords

Diabetic nephropathy; Hyperglycemia; Lipid peroxidation; Mesangial cell; Mitochondria; Nuclear transcription factors

Indexed keywords

ASTAXANTHIN; CYTOKINE;

ARTICLE; CYTOKINE PRODUCTION; DIABETIC NEPHROPATHY; HUMAN; HUMAN CELL; HUMAN CELL CULTURE; HYPERGLYCEMIA; IN VITRO STUDY; KIDNEY CELL CULTURE; MESANGIUM CELL; MITOCHONDRIAL MEMBRANE; OXIDATIVE STRESS; PATHOGENESIS; PRIORITY JOURNAL; PROTEIN EXPRESSION; THERAPY EFFECT; TRANSCRIPTION INITIATION; TREATMENT OUTCOME; TREATMENT RESPONSE;

CELL LINE; CHEMOKINE CCL2; DIABETIC NEUROPATHIES; HUMANS; HYPERGLYCEMIA; MESANGIAL CELLS; MITOCHONDRIA; MITOGEN-ACTIVATED PROTEIN KINASES; NF-KAPPA B; OXIDATION-REDUCTION; REACTIVE OXYGEN SPECIES; SIGNAL TRANSDUCTION; TRANSCRIPTION FACTOR AP-1; TRANSFORMING GROWTH FACTOR BETA1; XANTHOPHYLLS;

MUS;

EID: 41849088479     PISSN: 07302312     EISSN: 10974644     Source Type: Journal    
DOI: 10.1002/jcb.21583     Document Type: Article

References (49)

1. Baynes JW, Thorpe SR. 1999. Role of oxidative stress in diabetic complications: A new perspective on an old paradigm. Diabetes 48:1-9.
2. Bennedsen M, Wang X, Willen R, Wadstrom T, Andersen LP. 1999. Treatment of H. pylori infected mice with antioxidant astaxanthin reduces gastric inflammation, bacterial load and modulates cytokine release by splenocytes. Immunol Lett 70:185-189.
3. Cantrell A, McGarvey DJ, Truscott TG, Rancan F, Bohm F. 2003. Singlet oxygen quenching by dietary carotenoids in a model membrane environment. Arch Biochem Biophys 412:47-54.
4. Catherwood MA, Powell LA, Anderson P, McMaster D, Sharpe PC, Trimble ER. 2002. Glucose-induced oxidative stress in mesangial cells. Kidney Int 61:599-608.
5. Cepinskas G, Savickiene J, Ionescu CV, Kvietys PR. 2003. PMN transendothelial migration decreases nuclear NFkappaB in IL-1beta-activated endothelial cells: Role of PECAM-1. J Cell Biol 161:641-651.
6. Chew BP, Park JS, Wong MW, Wong TS. 1999. A comparison of the anticancer activities of dietary beta-carotene, canthaxanthin and astaxanthin in mice in vivo. Anticancer Res 19:1849-1853.
7. Choksi KB, Boylston WH, Rabek JP, Widger WR, Papaconstantinou J. 2004. Oxidatively damaged proteins of heart mitochondrial electron transport complexes. Biochim Biophys Acta 1688:95-101.
8. Coral-Hinostroza GN, Ytrestoyl T, Ruyter B, Bjerkeng B. 2004. Plasma appearance of unesterified astaxanthin geometrical E/Z and optical R/S isomers in men given single doses of a mixture of optical 3 and 3′R/S isomers of astaxanthin fatty acyl diesters. Comp Biochem Physiol C Toxicol Pharmacol 139:99-110.
9. Coughlan MT, Cooper ME, Forbes JM. 2007. Renal microvascular injury in diabetes: RAGE and redox signaling. Antioxid Redox Signal 9:331-342.
10. Diaz-Cazorla M, Perez-Sala D, Lamas S. 1999. Dual effect of nitric oxide donors on cyclooxygenase-2 expression in human mesangial cells. J Am Soc Nephrol 10:943-952.
11. Fukami K, Ueda S, Yamagishi S, Kato S, Inagaki Y, Takeuchi M, Motomiya Y, Bucala R, Iida S, Tamaki K, Imaizumi T, Cooper ME, Okuda S. 2004. AGEs activate mesangial TGF-beta-Smad signaling via an angiotensin II type I receptor interaction. Kidney Int 66:2137-2147.
12. Fukuzawa K, Inokami Y, Tokumura A, Terao J, Suzuki A. 1998. Rate constants for quenching singlet oxygen and activities for inhibiting lipid peroxidation of carotenoids and alpha-tocopherol in liposomes. Lipids 33:751-756.
13. Guijarro C, Egido J. 2001. Transcription factor-kappa B (NF-kappa B) and renal disease. Kidney Int 59:415-424.
14. Ha H, Lee HB. 2001. Oxidative stress in diabetic nephropathy: Basic and clinical information. Curr Diab Rep 1:282-287.
15. Ha H, Yu MR, Choi YJ, Kitamura M, Lee HB. 2002. Role of high glucose-induced nuclear factor-kappaB activation in monocyte chemoattractant protein-1 expression by mesangial cells. J Am Soc Nephrol 13:894-902.
16. Handa O, Naito Y, Takagi T, Shimozawa M, Kokura S, Yoshida N, Matsui H, Cepinskas G, Kvietys PR, Yoshikawa T. 2004. Tumor necrosis factor-alpha-induced cytokine-induced neutrophil chemoattractant-1 (CINC-1) production by rat gastric epithelial cells: Role of reactive oxygen species and nuclear factor-kappaB. J Pharmacol Exp Ther 309:670-676.
17. Handa O, Kokura S, Adachi S, Takagi T, Naito Y, Tanigawa T, Yoshida N, Yoshikawa T. 2006a. Methylparaben potentiates UV-induced damage of skin keratinocytes. Toxicology 227:62-72.
18. Handa O, Yoshida N, Fujita N, Tanaka Y, Ueda M, Takagi T, Kokura S, Naito Y, Okanoue T, Yoshikawa T. 2006b. Molecular mechanisms involved in anti-inflammatory effects of proton pump inhibitors. Inflamm Res 55:476-480.
19. Hinokio Y, Suzuki S, Hirai M, Chiba M, Hirai A, Toyota T. 1999. Oxidative DNA damage in diabetes mellitus: Its association with diabetic complications. Diabetologia 42:995-998.
20. Inoguchi T, Li P, Umeda F, Yu HY, Kakimoto M, Imamura M, Aoki T, Etoh T, Hashimoto T, Naruse M, Sano H, Utsumi H, Nawata H. 2000. High glucose level and free fatty acid stimulate reactive oxygen species production through protein kinase C-dependent activation of NAD(P)H oxidase in cultured vascular cells. Diabetes 49:1939-1945.
21. Jyonouchi H, Zhang L, Gross M, Tomita Y. 1994. Immunomodulating actions of carotenoids: Enhancement of in vivo and in vitro antibody production to T-dependent antigens. Nutr Cancer 21:47-58.
22. Jyonouchi H, Sun S, Tomita Y, Gross MD. 1995. Astaxanthin, a carotenoid without vitamin A activity, augments antibody responses in cultures including T-helper cell clones and suboptimal doses of antigen. J Nutr 125:2483-2492.
23. Kaneto H, Katakami N, Kawamori D, Miyatsuka T, Sakamoto K, Matsuoka TA, Matsuhisa M, Yamasaki Y. 2007. Involvement of oxidative stress in the pathogenesis of diabetes. Antioxid Redox Signal 9:355-366.
24. Kang BP, Frencher S, Reddy V, Kessler A, Malhotra A, Meggs LG. 2003. High glucose promotes mesangial cell apoptosis by oxidant-dependent mechanism. Am J Physiol Renal Physiol 284:F455-F466.
25. Kiritoshi S, Nishikawa T, Sonoda K, Kukidome D, Senokuchi T, Matsuo T, Matsumura T, Tokunaga H, Brownlee M, Araki E. 2003. Reactive oxygen species from mitochondria induce cyclooxygenase-2 gene expression in human mesangial cells: potential role in diabetic nephropathy. Diabetes 52:2570-2577.
26. Kobayashi M. 2000. In vivo antioxidant role of astaxanthin under oxidative stress in the green alga Haematococcus pluvialis. Appl Microbiol Biotechnol 54:550-555.
27. Kurihara H, Koda H, Asami S, Kiso Y, Tanaka T. 2002. Contribution of the antioxidative property of astaxanthin to its protective effect on the promotion of cancer metastasis in mice treated with restraint stress. Life Sci 70:2509-2520.
28. Lee HB, Yu MR, Yang Y, Jiang Z, Ha H. 2003. Reactive oxygen species-regulated signaling pathways in diabetic nephropathy. J Am Soc Nephrol 14:S241-S245.
29. Leonarduzzi G, Scavazza A, Biasi F, Chiarpotto E, Camandola S, Vogel S, Dargel R, Poli G. 1997. The lipid peroxidation end product 4-hydroxy-2,3-nonenal upregulates transforming growth factor beta1 expression in the macrophage lineage: a link between oxidative injury and fibrosclerosis. Faseb J 11:851-857.
30. Lok CE, Oliver MJ, Rothwell DM, Hux JE. 2004. The growing volume of diabetes-related dialysis: A population based study. Nephrol Dial Transplant 19:3098-3103.
31. Mezzano S, Aros C, Droguett A, Burgos ME, Ardiles L, Flores C, Schneider H, Ruiz-Ortega M, Egido J. 2004. NF-kappaB activation and overexpression of regulated genes in human diabetic nephropathy. Nephrol Dial Transplant 19:2505-2512.
32. Mishra R, Emancipator SN, Kern T, Simonson MS. 2005. High glucose evokes an intrinsic proapoptotic signaling pathway in mesangial cells. Kidney Int 67:82-93.
33. Naguib YM. 2000. Antioxidant activities of astaxanthin and related carotenoids. J Agric Food Chem 48:1150-1154.
34. Naito Y, Uchiyama K, Aoi W, Hasegawa G, Nakamura N, Yoshida N, Maoka T, Takahashi J, Yoshikawa T. 2004. Prevention of diabetic nephropathy by treatment with astaxanthin in diabetic db/db mice. Biofactors 20:49-59.
35. Naito Y, Uchiyama K, Mizushima K, Kuroda M, Akagiri S, Takagi T, Handa O, Kokura S, Yoshida N, Ichikawa H, Takahashi J, Yoshikawa T. 2006. Microarray profiling of gene expression patterns in glomerular cells of astaxanthin-treated diabetic mice: A nutrigenomic approach. Int J Mol Med 18:685-695.
36. Naito Y, Takagi T, Yoshikawa T. 2007. Neutrophil-dependent oxidative stress in ulcerative colitis. J Clin Biochem Nutr 41:18-26.
37. Nakai S, Wada A, Kitaoka T, Shinzato T, Nagura Y, Kikuchi K, Masakane I, Shinoda T, Yamazaki C, Sakai R, Marubayashi S, Morita O, Iseki K, Usami T, Kimata N, Suzuki K, Tabei K, Fushimi K, Miwa N, Yauchi M, Wakai K, Akiba T. 2006. An overview of regular dialysis treatment in Japan (as of 31 December 2004). Ther Apher Dial 10:476-497.
38. Nishikawa T, Edelstein D, Du XL, Yamagishi S, Matsumura T, Kaneda Y, Yorek MA, Beebe D, Oates PJ, Hammes HP, Giardino I, Brownlee M. 2000. Normalizing mitochondrial superoxide production blocks three pathways of hyperglycaemic damage. Nature 404:787-790.
39. Nishikawa T, Kukidome D, Sonoda K, Fujisawa K, Matsuhisa T, Motoshima H, Matsumura T, Araki E. 2007. Impact of mitochondrial ROS production on diabetic vascular complications. Diabetes Res Clin Pract 77:S41-S45.
40. Nitti M, Domenicotti C, d'Abramo C, Assereto S, Cottalasso D, Melloni E, Poli G, Biasi F, Marinari UM, Pronzato MA. 2002. Activation of PKC-beta isoforms mediates HNE-induced MCP-1 release by macrophages. Biochem Biophys Res Commun 294:547-552.
41. Ohgami K, Shiratori K, Kotake S, Nishida T, Mizuki N, Yazawa K, Ohno S. 2003. Effects of astaxanthin on lipopolysaccharide-induced inflammation in vitro and in vivo. Invest Ophthalmol Vis Sci 44:2694-2701.
42. Suzuki S, Hinokio Y, Komatu K, Ohtomo M, Onoda M, Hirai S, Hirai M, Hirai A, Chiba M, Kasuga S, Akai H, Toyota T. 1999. Oxidative damage to mitochondrial DNA and its relationship to diabetic complications. Diabetes Res Clin Pract 45:161-168.
43. Takahashi K, Watanabe M, Takimoto T, Akiba Y. 2004. Uptake and distribution of astaxanthin in several tissues and plasma lipoproteins in male broiler chickens fed a yeast (Phaffia rhodozyma) with a high concentration of astaxanthin. Br Poult Sci 45:133-138.
44. Tuttle KR, Johnson EC, Cooney SK, Anderberg RJ, Johnson EK, Clifton GD, Meek RL. 2005. Amino acids injure mesangial cells by advanced glycation end products, oxidative stress, and protein kinase C. Kidney Int 67:953-968.
45. Uchida K. 2005. Protein-bound 4-hydroxy-2-nonenal as a marker of oxidative stress. J Clin Biochem Nutr 36: pp 1-10.
46. Uchida K, Kumagai T. 2003. 4-hydroxy-2-nonenal as a COX-2 inducer. Mol Aspects Med 24:213-218.
47. Uchiyama K, Naito Y, Hasegawa G, Nakamura N, Takahashi J, Yoshikawa T. 2002. Astaxanthin protects beta-cells against glucose toxicity in diabetic db/db mice. Redox Rep 7:290-293.
48. Wild S, Roglic G, Green A, Sicree R, King H. 2004. Global prevalence of diabetes: Estimates for the year 2000 and projections for 2030. Diabetes Care 27:1047-1053.
49. Ziyadeh FN. 1993. The extracellular matrix in diabetic nephropathy. Am J Kidney Dis 22:736-744.