Modulation of palmitic acid-induced cell death by ergothioneine: Evidence of an anti-inflammatory action

BioFactors

Volumn 33, Issue 4, 2008, Pages 237-247

  Laurenza, Incoronata ^b   Colognato, Renato ^a   Migliore, Lucia ^a   Del Prato, Stefano ^b   Benzi, Luca ^b  

^a UNIVERSITY OF PISA   (Italy)

^b CISANELLO HOSPITAL   (Italy)

Author keywords

[No Author keywords available]

Indexed keywords

FATTY ACID; INTERLEUKIN 6; MITOGEN ACTIVATED PROTEIN KINASE; PALMITIC ACID; STRESS ACTIVATED PROTEIN KINASE; THIONEINE;

ANIMAL CELL; ANTIINFLAMMATORY ACTIVITY; ARTICLE; CELL DEATH; CELL VIABILITY; CONTROLLED STUDY; ENZYME ACTIVITY; IN VITRO STUDY; INCUBATION TIME; MOUSE; NONHUMAN; PRIORITY JOURNAL; PROTEIN EXPRESSION; TIME; WESTERN BLOTTING; ANIMAL; CELL CULTURE; DRUG ANTAGONISM; DRUG EFFECT; GENETICS; MYOBLAST; SIGNAL TRANSDUCTION;

ANIMALS; CELL DEATH; CELLS, CULTURED; ERGOTHIONEINE; INTERLEUKIN-6; MAP KINASE SIGNALING SYSTEM; MICE; MYOBLASTS; PALMITIC ACID;

EID: 67649769428     PISSN: 09516433     EISSN: None     Source Type: Journal    
DOI: 10.1002/biof.5520330401     Document Type: Article

References (66)

1. D. Akanmu, R. Cecchini, O.I. Aruoma and B. Halliwell, The antioxidant action of ergothioneine. Arch Biochem Biophys 288 (1991), 10-16.
2. O.I. Aruoma, M. Whiteman, T.G. England and B. Halliwell, Antioxidant action of ergothioneine: assessment of its ability to scavenge peroxynitrite, Biochem Biophys Res Commun 231 (1997), 389-391.
3. O.P. Bachmann, D.B. Dahl, K. Brechtel, J. Machann, M. Haap, T. Maier, M. Loviscach, M. Stumvoll, C.D. Claussen, F. Schick, H.U. Haring and S. Jacob, Effects of intravenous and dietary lipid challenge on intramyocellular lipid content and the relation with insulin sensitivity in humans. Diabetes 50 (2001), 2579-2584. (Pubitemid 33642777)
4. J.P. Bastard, C. Jardel, E. Bruckert, P. Blondy, J. Capeau, M. Laville, H. Vidal and B. Hainque, Elevated levels of interleukin 6 are reduced in serum and subcutaneous adipose tissue of obese women after weight loss, J Clin Endocrinol Metab 85 (2000), 3338-3342.
5. J.P. Bastard, M. Maachi, J.T. Van Nhieu, C. Jardel, E. Bruckert, A. Grimaldi, J.J. Robert, J. Capeau and B. Hainque, Adipose tissue IL-6 content correlates with resistance to insulin activation of glucose uptake both in vivo and in vitro, J Clin Endocrinol Metab 87 (2002), 2084-2089.
6. B. Caballero, Vitamin E improves the action of insulin, Nutr Rev 51 (1993), 339-340.
7. H. Chen, R.J. Karne, G. Hall, V. Campia, J.A. Panza, R.O. Cannon 3rd, Y. Wang, A. Katz, M. Levine and M.J. Quon, High-dose oral vitamin C partially replenishes vitamin C levels in patients with Type 2 diabetes and low vitamin C levels but does not improve endothelial dysfunction or insulin resistance, Am J Physiol Heart Circ Physiol 290 (2006), H137-H145.
8. J.A. Chavez, W.L. Holland, J.a Bär, K. Sandhoff and S.A. Summers, Acid Ceramidase Overexpression Prevents the Inhibitory Effects of Saturated Fatty Acids on Insulin Signaling, J Biol Chem 280 (2005), 20148-20153.
9. R. Colognato, I. Laurenza, I. Fontana, F. Coppede', G. Siciliano, S. Coecke, O.I. Aruoma, L. Benzi and L. Migliore. Modulation of hydrogen peroxide-induced DNA damage, MAPKs activation and cell death in PC12 by ergothioneine, Clin Nutr 25 (2006), 135-145.
10. R.A. DeFronzo and E. Ferrannini, Insulin resistance. A multifaceted syndrome responsible for NIDDM, obesity, hypertension, dyslipidemia, and atherosclerotic cardiovascular disease, Diabetes Care 14 (1991), 173-194.
11. M. Deiana, A. Rosa, V. Casu, R. Piga and M.A. Dessi, Ergothioneine modulates oxidative damage in the kidney and liver of rats in vivo: Studies upon the profile of polyunsaturated fatty acids, Clin Nutr 23 (2004), 183-193.
12. W. Droge and R. Breitkreutz, N-acetyl-cysteine in the therapy of HIV-positive patients, Curr Opin Clin Nutr Metab Care 2 (1999), 493-498.
13. J. Ey, E. Schoemig and D. Taubert, Dietary Sources and Antioxidant Effects of Ergothioneine, J Agric Food Chem 55 (2007), 6466-6474.
14. J.L. Evans and I.D. Goldfine, a-Lipoic acid: a multi-functional antioxidant that improves insulin sensitivity in patients with type 2 diabetes, Diabetes Technol Therap 2 (2000), 401-413.
15. J.L. Evans, C.J. Heymann, I.D. Goldfine and L.A. Gavin, Pharmacokinetics, tolerability, and fructosamine-lowering effect of a novel, controlled release formulation of a-lipoic acid, Endocr Pract 8 (2002), 29-35.
16. M.A. Febbraio and B.K. Pedersen, Muscle-derived interleukin-6: mechanisms for activation and possible biological roles, FASEB J 16 (2002), 1335-1347.
17. L.D. Ferreira, L.K. Pulawa, D.R. Jensen and R.H. Eckel, Overexpressing human lipoprotein lipase in mouse skeletal muscle is associated with insulin resistance, Diabetes 50 (2001), 1064-1068.
18. N.D. Fisher and N.K. Hollenberg, Flavanols for cardiovascular health: the science behind the sweetness, J Hypertens 23 (2005), 1453-1459. (Pubitemid 41104812)
19. N.D. Fisher, M. Hughes, M. Gerhard-Herman and N.K. Hollenberg, Flavanol-rich cocoa induces nitric-oxide-dependent vasodilation in healthy humans, J Hypertens 21 (2003), 2281-2286.
20. C.G. Fraga, Cocoa, diabetes, and hypertension: should we eat more chocolate? Am J Clin Nutr 81 (2005), 541-542.
21. A.M. Fulghesu, M. Ciampelli, G. Muzj, C. Belosi, L. Selvaggi, G.F. Ayala and A. Lanzone, N-acetyl-cysteine treatment improves insulin sensitivity in women with polycystic ovary syndrome, Fertil Steril 77 (2002), 1128-1135. (Pubitemid 34626318)
22. C. Gauthier-Rouviere, M. Vandromme, D. Tuil, N. Lautredou, M. Morris, M. Soulez, A. Kahn, A. Fernandez and N. Lamb, Expression and activity of serum response factor is required for expression of the muscle-determining factor MyoD in both dividing and differentiating mouse C2C12 myoblasts, Mol Biol Cell 7 (1996), 719-729.
23. R.F. Grimble, Inflammatory status and insulin resistance, Curr Opin Clin Nutr Metab Care 5 (2002), 551-559.
24. D. Grundemann, S. Harlfinger, S. Golz, A. Geerts, A. Lazar, R. Berkels, N. Jung, A. Rubbert and E. Schomig, Discovery of the ergothioneine transporter, Proc Natl Acad Sci USA 102 (2005), 5256-5261.
25. F. Guerrero-Romero and M. Rodriguez-Moran, Complementary therapies for diabetes: the case for chromium, magnesium, and antioxidants, Arch Med Res 36 (2005), 250-257.
26. S.M. Hirabara, L.R. Silveira, L.C. Alberici, V.G. Leandro, R.H. Lambertucci, G.C. Polimeno, M.F. Cury Boaventura, J. Procopio, A.E. Vercesi and R. Curi, Acute effect of fatty acids on metabolism and mitochondrial coupling in skeletal muscle, Biochimica et Biophysica Acta 1757 (2006), 57-66. (Pubitemid 43113322)
27. N. Hirai, H. Kawano, O. Hirashima, T. Motoyama, Y. Moriyama, T. Sakamoto, K. Kugiyama, H. Ogawa, K. Nakao and H. Yasue, Insulin resistance and endothelial dysfunction in smokers: effects of vitamin C, Am J Physiol 279 (2000), H1172-H1178.
28. O. Hirashima, H. Kawano, T. Motoyama, N. Hirai, M. Ohgushi, K. Kugiyama, H. Ogawa and H. Yasue, Improvement of endothelial function and insulin sensitivity with vitamin C in patients with coronary spastic angina: possible role of reactive oxygen species, J Am Coll Cardiol 35 (2000), 1860-1866.
29. H.C. Hung, K.J. Joshipura, R. Jiang, F.B. Hu, D. Hunter, S.A. Smith- Warner, G.A. Colditz, B. Rosner, D. Spiegelman and W.C.Willett, Fruit and vegetable intake and risk of major chronic disease, J Natl Cancer Inst 96 (2004), 1577-1584.
30. S.I. Itani, N.B. Ruderman, F. Schmieder and G. Boden, Lipid-induced insulin resistance in human muscle is associated with changes in diacylglycerol, protein kinase C, and IkappaB-alpha, Diabetes 51 (2002), 2005-2011.
31. C. Jacob, A scent of therapy: pharmacological implications of natural products containing redox-active sulfur atoms, Nat Prod Rep. 23 (2006), 851-863.
32. P.J. Klover and R.A. Mooney, Hepatocytes: critical for glucose homeostasis, Int J Biochem Cell Biol 36 (2004), 753-758.
33. J.K. Kim, J.J. Fillmore, Y. Chen, C.Yu, I.K. Moore, M. Pypaert, E.P. Lutz, Y. Kako,W.Velez-Carrasco, I.J. Goldberg, J.L. Breslow and G.I. Shulman, Tissue-specific overexpression of lipoprotein lipase causes tissue-specific insulin resistance, Proc Natl Acad Sci USA 98 (2001), 7522-7527. (Pubitemid 32567981)
34. C. Lagathu, J.P. Bastard, M. Auclair, M. Maachi, J. Capeau and M. Caron, Chronic interleukin-6 (IL-6) treatment increased IL-6 secretion and induced insulin resistance in adipocyte: prevention by rosiglitazone, Biochem Biophys Res Commun 311 (2003), 372-379.
35. K. Lakhani, G.M. Prelevic, A.M. Seifalian, W.U. Atiomo and P. Hardiman, Polycystic ovary syndrome, diabetes and cardiovascular disease: risks and risk factors, J Obstet Gynaecol 24 (2004), 613-621. (Pubitemid 39655416)
36. C.J. Lyon, R.E. Law and W.A. Hsueh, Adiposity, inflammation, and atherogenesis, Endocrinology 144 (2003), 2195-2200
37. T. Maeda, M. Hirayama, D.Kobayashi, K. Miyazawa and I. Tamai, Mechanism of the regulation of organic cation/carnitine transporter 1 (SLC22A4) by rheumatoid arthritis-associated transcriptional factor RUNX1 and inflammatory cytokines, Drug Metab Dispos 35 (2007), 394-401.
38. L.T. May, G. Torcia, F. Cozzolino, A. Ray, S.B. Tatter, U. Santhanam, P.B. Sehgal and D. Stern, Interleukin-6 gene expression in human endothelial cells: RNA start sites, multiple IL-6 proteins and inhibition of proliferation, Biochem Biophys Res Commun 159 (1989), 991-998.
39. D.B. Melville, S. Eich and M.L. Ludwig, The biosynthesis of ergothioneine, J Biol Chem 224 (1957), 871-877.
40. H. Mitsuyama and J. May, Uptake and antioxidant effects of ergothioneine in human erythrocytes, Clin Sci 97 (1999), 407-411. (Pubitemid 29473740)
41. J.A. Moncaster, T.D. Walsh, S.M. Gentleman, L.S. Jen and O.I. Aruoma, Ergothioneine treatment protects neurons against Nmethyl- D-aspartate excitotoxicity in an in vivo rat retinal model, Neurosci Lett 328 (2002), 55-59.
42. E. Montell, M. Turini, M. Marotta, M. Roberts, V. Noe, C.J. Ciudad, K. Mace and A.M. Gomez-Foix, Am J Physiol Endocrinol Metab 280 (2001), E229-E237.
43. R.A. Mooney, J. Senn, S. Cameron, N. Inamdar, L.M. Boivin, Y. Shang and R.W. Furlanetto, Suppressors of cytokine signaling-1 and -6 associate with and inhibit the insulin receptor. A potential mechanism for cytokine-mediated insulin resistance, J Biol Chem. 276 (2001), 25889-25893. (Pubitemid 37412793)
44. S. Neschen, I. Moore, W. Regittnig, C.L. Yu, Y. Wang, M. Pypaert, K.F. Petersen and G.I. Shulman. n-3 Fatty acids preserve insulin sensitivity in vivo in a peroxisome proliferator-activated receptor-alpha-dependent manner, Am J Physiol Endocrinol Metab 282 (2002), E395-E401.
45. G. Paolisso, A. D'Amore, D. Galzerano, V. Balbi, D. Gingliano and M. Varricchio, Daily vitamin E supplements improve metabolic control but not insulin secretion in elderly type II diabetic patients, Diabetes Care 16 (1993), 1433-1437.
46. G. Paolisso, A. D'Amore, D. Giugliano, A. Ceriello, M. Varricchio and F. D'Onofrio, Pharmacological doses of vitamin E improve insulin action in healthy subjects and non-insulin-dependent diabetic patients, Am J Clin Nutr 57 (1993), 650-656. (Pubitemid 23132798)
47. G. Paolisso, G. Di Maro, D. Galzerano, F. Cacciapuoti, G. Varricchio and M. Varricchio, Pharmacological doses of vitamin E and insulin action in elderly subjects, Am J Clin Nutr 59 (1994), 1291-1296.
48. V.D. Peltekova, R.F. Wintle, L.A. Rubin, C.I. Amos, Q. Huang, X. Gu, B. Newman, M. Van Oene, D. Cescon, G. Greenberg, A.M. Griffiths, P.H. St George-Hyslop and K.A. Siminovitch, Functional variants of OCTN cation transporter genes are associated with Crohn disease, Nat Genet 36 (2004), 471-475.
49. G. Perseghin, K. Petersen and G.I. Shulman, Cellular mechanism of insulin resistance: potential links with inflammation, Int J Obes Relat Metab Disord (Suppl 3) (2003), S6-S11.
50. A.D. Pradhan, J.E. Manson, N. Rifai, J.E. Buring and P.M. Ridker, C-reactive protein, interleukin 6, and risk of developing type 2 diabetes mellitus, JAMA 286 (2001), 327-334. (Pubitemid 32656163)
51. I. Rahman, P.S. Gilmour, L.A. Jimenez, S.K. Biswas, F. Antonicelli and O.I. Aruoma, Ergothioneine inhibits oxidative stress- and TNF-α-induced NF-κB activation and interleukin-8 release in alveolar epithelial cells, Biochem Biophys Res Commun 302 (2003), 860-864.
52. D. Rein, S. Lotito, R.R. Holt, C.L. Keen, H.H. Schmitz and C.G. Fraga, Epicatechin in human plasma: in vivo determination and effect of chocolate consumption on plasma oxidation status, J Nutr 130 (2000), 2109S-2114S.
53. J. Rieusset, K. Bouzakri, E. Chevillotte, N. Ricard, D. Jacquet, J.P. Bastard, M. Laville and H. Vidal, Suppressor of cytokine signaling 3 expression and insulin resistance in skeletal muscle of obese and type 2 diabetic patients, Diabetes 53 (2004), 2232-2241.
54. V. Rotter, I. Nagaev and U. Smith, Interleukin-6 (IL-6) induces insulin resistance in 3T3-L1 adipocytes and is, like IL-8 and tumor necrosis factor-alpha, overexpressed in human fat cells from insulin-resistant subjects, J Biol Chem 278 (2003), 45777-45784.
55. J.J. Senn, Toll-like Receptor-2 Is Essential for the Development of Palmitate-induced Insulin Resistance in Myotubes, J Biol Chem 281 (2006), 26865-26875.
56. R. Sinha, S. Dufour, K.F. Petersen, V. LeBon, S. Enoksson, Y.Z. Ma, M. Savoye, D.L. Rothman, G.I. Shulman and S. Caprio, Assessment of skeletal muscle triglyceride content by (1)H nuclear magnetic resonance spectroscopy in lean and obese adolescents: relationships to insulin sensitivity, total body fat, and central adiposity, Diabetes 51 (2002), 1022-1027.
57. M.R. Shalaby, A. Waage and T. Espevik, Cytokine regulation of interleukin 6 production by human endothelial cells, Cell Immunol 121 (1989), 372-382. (Pubitemid 19179597)
58. P. Storz, H. Doppler, A. Wernig, K. Pfizenmaier and G. Muller, Cross-talk mechanisms in the development of insulin resistance of skeletal muscle cells palmitate rather than tumour necrosis factor inhibits insulin-dependent protein kinase B (PKB)/Akt stimulation and glucose uptake, Eur J Biochem 266 (1999), 17-25.
59. D. Taubert, G. Grimberg, N. Jung, A. Rubbert and E. Schomig, Functional role of the 503F variant of the organic cation transporter OCTN1 in Crohn's disease, Gut 54 (2005), 1505-1506.
60. H.J. Teede, C. Meyer and R.J. Norman, Insulin-sensitisers in the treatment of polycystic ovary syndrome, Expert Opin Pharmacother 6 (2005), 2419-2427. (Pubitemid 41701044)
61. A.L. Thompson, M.Y. Lim-Fraser, E.W. Kraegen and G.J. Cooney, Effects of individual fatty acids on glucose uptake and glycogen synthesis in soleus muscle in vitro, Am J Physiol Endocrinol Metab 279 (2000), E577-E584.
62. S. Tokuhiro, R. Yamada, X. Chang, A. Suzuki, Y. Kochi, T. Sawada, M. Suzuki, M. Nagasaki, M. Ohtsuki, M. Ono et al., SLC22A4 and RUNX1: identification of RA susceptible genes, J Mol Med 82 (2004), 558-564.
63. H.P. Torok, J. Glas, L. Tonenchi, P. Lohse, B. Muller-Myhsok, O. Limbersky, C. Neugebauer, F. Schnitzler, J. Seiderer, C. Tillack, S. Brand, G. Bruennler, P. Jagiello, J.T. Epplen, T. Griga, W. Klein, U. Schiemann, M. Folwaczny, T. Ochsenkuehn and C. Folwaczny, Polymorphisms in the DLG5 and OCTN cation transporter genes in Crohn's disease, Gut 54 (2005), 1421-1427. (Pubitemid 41375199)
64. M. Yilmaz, N. Bukan, G. Ayvaz, A. Karakoc, F. Toruner, N. Cakir and M. Arslan, The effects of rosiglitazone and metformin on oxidative stress and homocysteine levels in lean patients with polycystic ovary syndrome, Hum Reprod 20 (2005), 3333-3340. (Pubitemid 41742509)
65. J.S. Yudkin, M. Kumari, S.E. Humphries and V. Mohamed-Ali, Inflammation, obesity, stress and coronary heart disease: is interleukin-6 the link? Atherosclerosis 148 (2000), 209-214. (Pubitemid 30064452)
66. D. Ziegler, H. Nowak, P. Kempler, P. Vargha and P.A. Low, Treatment of symptomatic diabetic polyneuropathy with the antioxidant alpha-lipoic acid: a meta-analysis, Diabet Med 21 (2004), 114-121. (Pubitemid 38221809)