Impact of divergent effects of astaxanthin on insulin signaling in L6 cells

Endocrinology

Volumn 154, Issue 8, 2013, Pages 2600-2612

  Ishiki, Manabu ^a   Nishida, Yasuhiro ^b   Ishibashi, Hiroshi ^b   Wada, Tsutomu ^a   Fujisaka, Shiho ^a   Takikawa, Akiko ^a   Urakaze, Masaharu ^c   Sasaoka, Toshiyasu ^a   Usui, Isao ^a   Tobe, Kazuyuki ^a  

^a UNIVERSITY OF TOYAMA   (Japan)

^b AstaReal Co Ltd   (Japan)

^c Department of Surgery   (Japan)

Author keywords

[No Author keywords available]

Indexed keywords

ALPHA TOCOPHEROL; ASTAXANTHIN; DEOXYGLUCOSE; DICHLOROFLUORESCEIN; GLUCOSE TRANSPORTER 4; INSULIN RECEPTOR SUBSTRATE; INSULIN RECEPTOR SUBSTRATE 1; MITOGEN ACTIVATED PROTEIN KINASE; PALMITIC ACID; PROTEIN KINASE B; REACTIVE OXYGEN METABOLITE; STRESS ACTIVATED PROTEIN KINASE; THIOCTIC ACID; TUMOR NECROSIS FACTOR ALPHA; TYROSINE;

ARTICLE; BINDING AFFINITY; CELL PROTECTION; CONTROLLED STUDY; GLUCOSE TRANSPORT; IN VITRO STUDY; INSULIN BINDING; INSULIN RESISTANCE; NONHUMAN; OXIDATIVE STRESS; PRIORITY JOURNAL; PROTEIN PHOSPHORYLATION; RAT; SIGNAL TRANSDUCTION; WESTERN BLOTTING;

ALPHA-TOCOPHEROL; ANIMALS; ANTIOXIDANTS; BLOTTING, WESTERN; CELL LINE; DEOXYGLUCOSE; GLUCOSE TRANSPORTER TYPE 4; HYPOGLYCEMIC AGENTS; INSULIN; INSULIN RECEPTOR SUBSTRATE PROTEINS; INSULIN RESISTANCE; JNK MITOGEN-ACTIVATED PROTEIN KINASES; MYOBLASTS; PHOSPHORYLATION; PROTEIN TRANSPORT; PROTO-ONCOGENE PROTEINS C-AKT; RATS; REACTIVE OXYGEN SPECIES; SIGNAL TRANSDUCTION; THIOCTIC ACID; TUMOR NECROSIS FACTOR-ALPHA; XANTHOPHYLLS;

EID: 84880689746     PISSN: 00137227     EISSN: 19457170     Source Type: Journal    
DOI: 10.1210/en.2012-2198     Document Type: Article

References (66)

1. Friedman JM. Obesity in the new millennium. Nature. 2000;404: 632-634.
2. Gems D, Partridge L. Stress-response hormesis and aging: "that which does not kill us makes us stronger." Cell Metab. 2008;7:200-203.
3. Barbieri E, Sestili P. Reactive oxygen species in skeletal muscle signaling. J Signal Transduct. 2012;2012:982794.
4. Han D, Ybanez MD, Ahmadi S, Yeh K, Kaplowitz N. Redox regulation of tumor necrosis factor signaling. Antioxid Redox Signal. 2009;11:2245-2263.
5. Fernandez-Sanchez A, Madrigal-Santillan E, Bautista M, et al. Inflammation, oxidative stress, and obesity. Int J Mol Sci. 2011;12: 3117-3132.
6. Rains JL, Jain SK. Oxidative stress, insulin signaling, and diabetes. Free Radic Biol Med. 2011;50:567-575.
7. Rehman A, Nourooz-Zadeh J, Moller W, Tritschler H, Pereira P, Halliwell B. Increased oxidative damage to allDNAbases in patients with type II diabetes mellitus. FEBS Lett. 1999;448:120-122.
8. Houstis N, Rosen ED, Lander ES. Reactive oxygen species have a causal role in multiple forms of insulin resistance. Nature. 2006; 440:944-948.
9. Maxwell SR, Thomason H, Sandler D, et al. Poor glycaemic control is associated with reduced serum free radical scavenging (antioxidant) activity in non-insulin-dependent diabetes mellitus. Ann Clin Biochem. 1997;34(Pt 6):638-644.
10. Opara EC, Abdel-Rahman E, Soliman S, et al. Depletion of total antioxidant capacity in type 2 diabetes. Metabolism. 1999;48: 1414-1417.
11. Evans JL, Maddux BA, Goldfine ID. The molecular basis for oxidative stress-induced insulin resistance. Antioxid Redox Signal. 2005;7:1040-1052.
12. Deiuliis JA, Kampfrath T, Ying Z, Maiseyeu A, Rajagopalan S. Lipoic acid attenuates innate immune infiltration and activation in the visceral adipose tissue of obese insulin resistant mice. Lipids. 2011;46:1021-1032.
13. Shibata A, Kiba Y, Akati N, Fukuzawa K, Terada H. Molecular characteristics of astaxanthin and ?-carotene in the phospholipid monolayer and their distributions in the phospholipid bilayer.Chem Phys Lipids. 2001;113:11-22.
14. Spiller GA, Dewell A. Safety of an astaxanthin-rich Haematococcus pluvialis algal extract: A randomized clinical trial. JMedFood. 2003; 6:51-56.
15. McNulty HP, Byun J, Lockwood SF, Jacob RF, Mason RP. Differential effects of carotenoids on lipid peroxidation due to membrane interactions: X-ray diffraction analysis. Biochim Biophys Acta. 2007;1768:167-174.
16. Nakagawa K, Miyazawa T, Carpentero Burdeos G, et al. Antioxidant effect of astaxanthin on phospholipid peroxidation in human erythrocytes. Br J Nutr. 2011;105:1563-1571.
17. Subczynski WK, Wisniewska A, Widomska J. Location of macular xanthophylls in the most vulnerable regions of photoreceptor outersegment membranes. Arch Biochem Biophys. 2010;504:61-66.
18. Gao X, Lowry PR, Zhou X, et al. PI3K/Akt signaling requires spatial compartmentalization in plasma membrane microdomains. Proc Natl Acad Sci USA. 2011;108:14509-14514.
19. Naito Y, Uchiyama K, Hasegawa G, et al. Prevention of diabetic nephropathy by treatment with astaxanthin in diabetic db/db mice. Biofactors. 2004;20:49-59.
20. Hussein G, Nakagawa T, Goto H, Shimada Y, Matsumoto K, Sankawa U, Watanabe H. Astaxanthin ameliorates features of metabolic syndrome in SHR/NDmcr-cp. Life Sci. 2007;80:522-529.
21. Aoi W, Naito Y, Takanami Y, et al. Astaxanthin improves muscle lipid metabolism in exercise via inhibitory effect of oxidative CPT I modification. Biochem Biophys Res Commun. 2008;366:892-897.
22. Winnick JJ, Sherman WM, Habash DL, et al. Short-term aerobic exercise training in obese humans with type 2 diabetes mellitus improves whole-body insulin sensitivity through gains in peripheral, not hepatic, insulin sensitivity. J Clin Endocrinol Metab. 2008;93: 771-778.
23. Wang Q, Khayat Z, Kishi K, Ebina Y, Klip A. GLUT4 translocation by insulin in intact muscle cells: Detection by a fast and quantitative assay. FEBS Lett. 1998;427:193-197.
24. Hoehn KL, Hohnen-Behrens C, Cederberg A, et al. IRS1-independent defects define major nodes of insulin resistance. Cell Metab. 2008;7:421-433.
25. Ishiki M, Randhawa VK, Poon V, Jebailey L, Klip A. Insulin regulates the membrane arrival, fusion, and C-terminal unmasking of glucose transporter-4 via distinct phosphoinositides. J Biol Chem. 2005;280:28792-28802.
26. Niu W, Huang C, Nawaz Z, et al. Maturation of the regulation of GLUT4 activity by p38 MAPK during L6 cell myogenesis. J Biol Chem. 2003;278:17953-17962.
27. Manabe E, Handa O, Naito Y, et al. Astaxanthin protects mesangial cells from hyperglycemia-induced oxidative signaling. J Cell Biochem. 2008;103:1925-1937.
28. Berdichevsky A, Guarente L, Bose A. Acute oxidative stress can reverse insulin resistance by inactivation of cytoplasmic JNK. J Biol Chem. 2010;285:21581-21589.
29. Gual P, Le Marchand-Brustel Y, Tanti JF. Positive and negative regulation of insulin signaling through IRS-1 phosphorylation. Biochimie. 2005;87:99-109.
30. Tuncman G, Hirosumi J, Solinas G, Chang L, KarinM,Hotamisligil GS. Functional in vivo interactions between JNK1 and JNK2 isoforms in obesity and insulin resistance. Proc Natl Acad Sci USA. 2006;103:10741-10746.
31. Nakamura S, Takamura T, Matsuzawa-Nagata N, et al. Palmitate induces insulin resistance in H4IIEC3 hepatocytes through reactive oxygen species produced by mitochondria. J Biol Chem. 2009;284: 14809-14818.
32. Kozlovsky N, Rudich A, Potashnik R, Bashan N. Reactive oxygen species activate glucose transport in L6 myotubes. Free Radic Biol Med. 1997;23:859-869.
33. Estrada DE, Ewart HS, Tsakiridis T, et al. Stimulation of glucose uptake by the natural coenzyme ?-lipoic acid/thioctic acid: Participation of elements of the insulin signaling pathway. Diabetes. 1996; 45:1798-1804.
34. Yasunari K, Kohno M, Kano H, Yokokawa K, Minami M, Yoshikawa J. Antioxidants improve impaired insulin-mediated glucose uptake and prevent migration and proliferation of cultured rabbit coronary smooth muscle cells induced by high glucose. Circulation. 1999;99:1370-1378.
35. Bhuvaneswari S, Anuradha CV. Astaxanthin prevents loss of insulin signaling and improves glucose metabolism in liver of insulin resistant mice. Can J Physiol Pharmacol. 2012;90:1544-1552.
36. Furukawa S, Fujita T, Shimabukuro M, et al. Increased oxidative stress in obesity and its impact on metabolic syndrome. J Clin Invest. 2004;114:1752-1761.
37. Fan W, Morinaga H, Kim JJ, et al. FoxO1 regulates Tlr4 inflam matory pathway signalling in macrophages. EMBO J. 2010;29: 4223-4236.
38. Saberi M, Woods NB, de Luca C, et al. Hematopoietic cell-specific deletion of toll-like receptor 4 ameliorates hepatic and adipose tissue insulin resistance in high-fat-fed mice. Cell Metab. 2009;10:419-429.
39. Wei Y, Chen K, Whaley-Connell AT, Stump CS, Ibdah JA, Sowers JR. Skeletal muscle insulin resistance: Role of inflammatory cytokines and reactive oxygen species. Am J Physiol Regul Integr Comp Physiol. 2008;294:R673-R680.
40. Hotamisligil GS, Arner P, Caro JF, Atkinson RL, Spiegelman BM. Increased adipose tissue expression of tumor necrosis factor-β in human obesity and insulin resistance. J Clin Invest. 1995;95:2409-2415.
41. Uysal KT, Wiesbrock SM, Marino MW, Hotamisligil GS. Protection from obesity-induced insulin resistance in mice lacking TNF-α function. Nature. 1997;389:610-614.
42. Shen HM, Pervaiz S. TNF receptor superfamily-induced cell death: Redox-dependent execution. FASEB J. 2006;20:1589-1598.
43. Kamata H, Honda S, Maeda S, Chang L, Hirata H, Karin M. Reactive oxygen species promote TNF-α-induced death and sustained JNK activation by inhibiting MAP kinase phosphatases. Cell. 2005; 120:649-661.
44. Lambertucci RH, Hirabara SM, Silveira Ldos R, Levada-Pires AC, Curi R, Pithon-Curi TC. Palmitate increases superoxide production through mitochondrial electron transport chain and NADPH oxidase activity in skeletal muscle cells. J Cell Physiol. 2008;216:796-804.
45. Holland WL, Bikman BT, Wang LP, et al. Lipid-induced insulin resistance mediated by the proinflammatory receptorTLR4requires saturated fatty acid-induced ceramide biosynthesis in mice. J Clin Invest. 2011;121:1858-1870.
46. Chavez JA, Summers SA. A ceramide-centric view of insulin resistance. Cell Metab. 2012;15:585-594.
47. Yuzefovych L, Wilson G, Rachek L. Different effects of oleate vs. palmitate on mitochondrial function, apoptosis, and insulin signaling in L6 skeletal muscle cells: Role of oxidative stress. Am J Physiol Endocrinol Metab. 2010;299:E1096-E1105.
48. Wen H, Gris D, Lei Y, et al Fatty acid-induced NLRP3-ASC inflammasome activation interferes with insulin signaling. Nat Immunol. 2011;12:408-415.
49. Lee SJ, Bai SK, Lee KS, et al. Astaxanthin inhibits nitric oxide production and inflammatory gene expression by suppressing IkB kinase-dependent NF-kB activation. Mol Cells. 2003;16:97-105.
50. Badal S, Brown PD, Ragoobirsingh D. Nitric oxide agents impair insulin-mediated signal transduction in rat skeletal muscle. BMC Biochem. 2006;7:17.
51. Shaul PW, Smart EJ, Robinson LJ, et al. Acylation targets emdothelial nitric-oxide synthase to plasmalemmal caveolae. J Biol Chem. 1996;271:6518-6522.
52. Possel H, Noack H, Augustin W, Keilhoff G, Wolf G. 2,7- Dihydrodichlorofluorescein diacetate as a fluorescent marker for peroxynitrite formation. FEBS Lett. 1997;416:175-178.
53. Tarpey MM, Wink DA, Grisham MB. Methods for detection of reactive metabolites of oxygen and nitrogen: In vitro and in vivo considerations. Am J Physiol Regul Integr Comp Physiol. 2004; 286:R431-R444.
54. Brand MD, Esteves TC. Physiological functions of the mitochondrial uncoupling proteins UCP2 and UCP3. Cell Metab. 2005;2: 85-93.
55. Aguirre V, Werner ED, Giraud J, Lee YH, Shoelson SE, White MF. Phosphorylation of Ser307 in insulin receptor substrate-1 blocks interactions with the insulin receptor and inhibits insulin action. J Biol Chem. 2002;277:1531-1537.
56. Cabrera-Poch N, Sanchez-Ruiloba L, Rodriguez-Martinez M, Iglesias T. Lipid raft disruption triggers protein kinase C and Src-dependent protein kinaseDactivation and Kidins220 phosphorylation in neuronal cells. J Biol Chem. 2004;279:28592-28602.
57. DiNitto JP, Lambright DG. Membrane and juxtamembrane targeting by PH and PTB domains. Biochim Biophys Acta. 2006;1761: 850-867.
58. Jensen M, Hansen B, De Meyts P, Schaffer L, Urso B. Activation of the insulin receptor by insulin and a synthetic peptide leads to divergent metabolic and mitogenic signaling and responses. J Biol Chem. 2007;282:35179-35186.
59. Ugi S, Imamura T, Maegawa H, et al. Protein phosphatase 2A negatively regulates insulin's metabolic signaling pathway by inhibiting Akt (protein kinase B) activity in 3T3-L1 adipocytes. Mol Cell Biol. 2004;24:8778-8789.
60. Kraut-Cohen J, Muller WJ, Elson A. Protein-tyrosine phosphatase epsilon regulates Shc signaling in a kinase-specific manner: Increasing coherence in tyrosine phosphatase signaling. J Biol Chem. 2008; 283:4612-4621.
61. Ishida Y, Ohara T, Okuno Y, et al. α-Lipoic acid and insulin autoimmune syndrome. Diabetes Care. 2007;30:2240-2241.
62. Rudich A, Tirosh A, Potashnik R, Khamaisi M, Bashan N. Lipoic acid protects against oxidative stress induced impairment in insulin stimulation of protein kinase B and glucose transport in 3T3-L1 adipocytes. Diabetologia. 1999;42:949-957.
63. Cho KJ, Moini H, Shon HK, Chung AS, Packer L. α-Lipoic acid decreases thiol reactivity of the insulin receptor and protein tyrosine phosphatase 1B in 3T3-L1 adipocytes. Biochem Pharmacol. 2003; 66:849-858.
64. Yao Y, Li R, Ma Y, et al. α-Lipoic acid increases tolerance of cardiomyoblasts to glucose/glucose oxidase-induced injury via ROSdependent ERK1/2 activation. Biochim Biophys Acta. 2012;1823: 920-929.
65. Moini H, Packer L, Saris NE. Antioxidant and prooxidant activities of ?-lipoic acid and dihydrolipoic acid. Toxicol Appl Pharmacol. 2002;182:84-90.
66. Ristow M, Zarse K, Oberbach A, et al. Antioxidants prevent healthpromoting effects of physical exercise in humans. Proc Natl Acad Sci USA. 2009;106:8665-8670.