Uptake and protective effects of ergothioneine in human endothelial cells

Journal of Pharmacology and Experimental Therapeutics

Volumn 350, Issue 3, 2014, Pages 691-700

  Li, Rachel W S ^a   Yang, C ^b   Sit, Albert S M ^a   Kwan, Y W ^c   Lee, Simon M Y ^d   Hoi, Maggie P M ^d   Chan, S W ^e   Hausman, Marvin ^f   Vanhoutte, Paul M ^a   Leung, George P H ^a  

^a UNIVERSITY OF HONG KONG   (Hong Kong)

^b YUNNAN MINZU UNIVERSITY   (China)

^c CHINESE UNIVERSITY OF HONG KONG   (Hong Kong)

^d University of Macau   (Macao)

^e HONG KONG POLYTECHNIC UNIVERSITY   (Hong Kong)

^f Entia Biosciences Inc   (United States)

Author keywords

[No Author keywords available]

Indexed keywords

ACETYLCHOLINE; ANTIOXIDANT; CATALASE; DICHLORODIHYDROFLUORESCEIN; GLUCOSE; GLUTATHIONE REDUCTASE; LUCIGENIN; ORGANIC CATION TRANSPORTER 1; PYROGALLOL; REACTIVE OXYGEN METABOLITE; REDUCED NICOTINAMIDE ADENINE DINUCLEOTIDE PHOSPHATE OXIDASE 1; SMALL INTERFERING RNA; SUPEROXIDE DISMUTASE; THIONEINE; XANTHINE; XANTHINE OXIDASE;

ADULT; ANIMAL TISSUE; APOPTOSIS; ARTICLE; BASILAR ARTERY; CAPILLARY ENDOTHELIAL CELL; CELL PROTECTION; CELL VIABILITY; CONTROLLED STUDY; DRUG EFFECT; HUMAN; HUMAN CELL; MALE; MOUSE; MTT ASSAY; NONHUMAN; OXIDATIVE STRESS; PRIORITY JOURNAL; PROTEIN EXPRESSION; REVERSE TRANSCRIPTION POLYMERASE CHAIN REACTION; RNA ISOLATION; STREPTOZOTOCIN-INDUCED DIABETES MELLITUS; WESTERN BLOTTING; ANIMAL; CELL CULTURE; CELL SURVIVAL; DRUG ANTAGONISM; ENDOTHELIUM CELL; METABOLISM; PHYSIOLOGY; RAT; SPRAGUE DAWLEY RAT;

ANIMALS; ANTIOXIDANTS; CELL SURVIVAL; CELLS, CULTURED; CYTOPROTECTION; ENDOTHELIAL CELLS; ERGOTHIONEINE; HUMANS; MALE; OXIDATIVE STRESS; RATS; RATS, SPRAGUE-DAWLEY; REACTIVE OXYGEN SPECIES;

EID: 84907424488     PISSN: 00223565     EISSN: 15210103     Source Type: Journal    
DOI: 10.1124/jpet.114.214049     Document Type: Article

References (60)

1. Abrahamsson T, Brandt U, Marklund SL, and Sjöqvist PO (1992) Vascular bound recombinant extracellular superoxide dismutase type C protects against the detrimental effects of superoxide radicals on endothelium-dependent arterial relaxation. Circ Res 70:264-271.
2. Akanmu D, Cecchini R, Aruoma OI, and Halliwell B (1991) The antioxidant action of ergothioneine. Arch Biochem Biophys 288:10-16.
3. Aruoma OI, Spencer JP, and Mahmood N (1999) Protection against oxidative damage and cell death by the natural antioxidant ergothioneine. Food Chem Toxicol 37:1043-1053.
4. Aruoma OI, Whiteman M, England TG, and Halliwell B (1997) Antioxidant action of ergothioneine: assessment of its ability to scavenge peroxynitrite. Biochem Biophys Res Commun 231:389-391.
5. Asmus KD, Bensasson RV, Bernier JL, Houssin R, and Land EJ (1996) One-electron oxidation of ergothioneine and analogues investigated by pulse radiolysis: redox reaction involving ergothioneine and vitamin C. Biochem J 315:625-629.
6. Bedirli A, Sakrak O, Muhtaroglu S, Soyuer I, Guler I, Riza Erdogan A, and Sozuer EM (2004) Ergothioneine pretreatment protects the liver from ischemia-reperfusion injury caused by increasing hepatic heat shock protein 70. J Surg Res 122:96-102.
7. Bohlen HG and Lash JM (1993) Topical hyperglycemia rapidly suppresses EDRF-mediated vasodilation of normal rat arterioles. Am J Physiol 265:H219-H225.
8. Cargnoni A, Bernocchi P, Ceconi C, Curello S, and Ferrari R (1995) In vitro administration of ergothioneine failed to protect isolated ischaemic and reperfused rabbit heart. Biochim Biophys Acta 1270:173-178.
9. Colognato R, Laurenza I, Fontana I, Coppedé F, Siciliano G, Coecke S, Aruoma OI, Benzi L, and Migliore L (2006) Modulation of hydrogen peroxide-induced DNA damage, MAPKs activation and cell death in PC12 by ergothioneine. Clin Nutr 25:135-145.
10. Deiana M, Rosa A, Casu V, Piga R, Assunta Dessì M, and Aruoma OI (2004) L-ergothioneine modulates oxidative damage in the kidney and liver of rats in vivo: studies upon the profile of polyunsaturated fatty acids. Clin Nutr 23:183-193.
11. Epand RM, Epand RF, and Wong SC (1988) Study of the ergothioneine concentration in the blood of individuals with diabetes mellitus. J Clin Chem Clin Biochem 26:623-626.
12. Ey J, Schömig E, and Taubert D (2007) Dietary sources and antioxidant effects of ergothioneine. J Agric Food Chem 55:6466-6474.
13. Félétou M and Vanhoutte PM (2006) Endothelial dysfunction: a multifaceted disorder (The Wiggers Award Lecture). Am J Physiol Heart Circ Physiol 291:H985-H1002.
14. Furchgott RF and Zawadzki JV (1980) The obligatory role of endothelial cells in the relaxation of arterial smooth muscle by acetylcholine. Nature 288:373-376.
15. Gazis A, White DJ, Page SR, and Cockcroft JR (1999) Effect of oral vitamin E (alpha-tocopherol) supplementation on vascular endothelial function in Type 2 diabetes mellitus. Diabet Med 16:304-311.
16. Grigat S, Harlfinger S, Pal S, Striebinger R, Golz S, Geerts A, Lazar A, Schömig E, and Gründemann D (2007) Probing the substrate specificity of the ergothioneine transporter with methimazole, hercynine, and organic cations. Biochem Pharmacol 74:309-316.
17. Gründemann D, Harlfinger S, Golz S, Geerts A, Lazar A, Berkels R, Jung N, Rubbert A, and Schömig E (2005) Discovery of the ergothioneine transporter. Proc Natl Acad Sci USA 102:5256-5261.
18. Gryglewski RJ, Palmer RM, and Moncada S (1986) Superoxide anion is involved in the breakdown of endothelium-derived vascular relaxing factor. Nature 320:454-456.
19. Guo X, Liu WL, Chen LW, and Guo ZG (2000) High glucose impairs endothelium-dependent relaxation in rabbit aorta. Acta Pharmacol Sin 21:169-173.
20. Guzik TJ, Mussa S, Gastaldi D, Sadowski J, Ratnatunga C, Pillai R, and Channon KM (2002) Mechanisms of increased vascular superoxide production in human diabetes mellitus: role of NAD(P)H oxidase and endothelial nitric oxide synthase. Circulation 105:1656-1662.
21. Halliwell B (2009) The wanderings of a free radical. Free Radic Biol Med 46:531-542.
22. Hartman PE (1990) Ergothioneine as antioxidant. Methods Enzymol 186:310-318.
23. Hartman PE, Dixon WJ, Dahl TA, and Daub ME (1988) Multiple modes of photodynamic action by cercosporin. Photochem Photobiol 47:699-703.
24. Ishihara Y, Sekine M, Hatano A, and Shimamoto N (2008) Sustained contraction and endothelial dysfunction induced by reactive oxygen species in porcine coronary artery. Biol Pharm Bull 31:1667-1672.
25. Jang JH, Aruoma OI, Jen LS, Chung HY, and Surh YJ (2004) Ergothioneine rescues PC12 cells from beta-amyloid-induced apoptotic death. Free Radic Biol Med 36:288-299.
26. Kamata K, Makino A, Kanie N, Oda S, Matsumoto T, Kobayashi T, Kikuchi T, Nishimura M, and Honda T (2006) Effects of anthocyanidin derivative (HK-008) on relaxation in rat perfused mesenterial bed. J Smooth Muscle Res 42:75-88.
27. Kaneko I, Takeuchi Y, Yamaoka Y, Tanaka Y, Fukuda T, Fukumori Y, Mayumi T, and Hama T (1980) Quantitative determination of ergothioneine in plasma and tissues by TLC-densitometry. Chem Pharm Bull (Tokyo) 28:3093-3097.
28. Kawano H, Otani M, Takeyama K, Kawai Y, Mayumi T, and Hama T (1982) Studies on ergothioneine. VI. Distribution and fluctuations of ergothioneine in rats. Chem Pharm Bull (Tokyo) 30:1760-1765.
29. Keegan A, Walbank H, Cotter MA, and Cameron NE (1995) Chronic vitamin E treatment prevents defective endothelium-dependent relaxation in diabetic rat aorta. Diabetologia 38:1475-1478.
30. Koepsell H, Lips K, and Volk C (2007) Polyspecific organic cation transporters: structure, function, physiological roles, and biopharmaceutical implications. Pharm Res 24:1227-1251.
31. Leo CH, Hart JL, and Woodman OL (2011) Impairment of both nitric oxide-mediated and EDHF-type relaxation in small mesenteric arteries from rats with streptozotocin-induced diabetes. Br J Pharmacol 162:365-377.
32. Liao WC, Wu WH, Tsai PC, Wang HF, Liu YH, and Chan CF (2012) Kinetics of ergothioneine inhibition of mushroom tyrosinase. Appl Biochem Biotechnol 166:259-267.
33. Markova NG, Karaman-Jurukovska N, Dong KK, Damaghi N, Smiles KA, and Yarosh DB (2009) Skin cells and tissue are capable of using L-ergothioneine as an integral component of their antioxidant defense system. Free Radic Biol Med 46:1168-1176.
34. Mayumi T, Kawano H, Sakamoto Y, Suehisa E, Kawai Y, and Hama T (1978) Studies on ergothioneine. V. Determination by high performance liquid chromatography and application to metabolic research. Chem Pharm Bull (Tokyo) 26:3772-3778.
35. Moncaster JA, Walsh DT, Gentleman SM, Jen LS, and Aruoma OI (2002) Ergothioneine treatment protects neurons against N-methyl-D-aspartate excitotoxicity in an in vivo rat retinal model. Neurosci Lett 328:55-59.
36. Moreno-Manzano V, Ishikawa Y, Lucio-Cazana J, and Kitamura M (2000) Selective involvement of superoxide anion, but not downstream compounds hydrogen peroxide and peroxynitrite, in tumor necrosis factor-alpha-induced apoptosis of rat mesangial cells. J Biol Chem 275:12684-12691.
37. Motohashi N and Mori I (1986) Thiol-induced hydroxyl radical formation and scavenger effect of thiocarbamides on hydroxyl radicals. J Inorg Biochem 26:205-212.
38. Myhre O, Andersen JM, Aarnes H, and Fonnum F (2003) Evaluation of the probes 2′,7′-dichlorofluorescin diacetate, luminol, and lucigenin as indicators of reactive species formation. Biochem Pharmacol 65:1575-1582.
39. Nakamura T, Yoshida K, Yabuuchi H, Maeda T, and Tamai I (2008) Functional characterization of ergothioneine transport by rat organic cation/carnitine transporter Octn1 (slc22a4). Biol Pharm Bull 31:1580-1584.
40. Obayashi K, Kurihara K, Okano Y, Masaki H, and Yarosh DB (2005) L-Ergothioneine scavenges superoxide and singlet oxygen and suppresses TNF-α and MMP-1 expression in UV-irradiated human dermal fibroblasts. J Cosmet Sci 56:17-27.
41. Paul BD and Snyder SH (2010) The unusual amino acid L-ergothioneine is a physiologic cytoprotectant. Cell Death Differ 17:1134-1140.
42. Pellegrini MP, Newby DE, Johnston NR, Maxwell S, and Webb DJ (2004) Vitamin C has no effect on endothelium-dependent vasomotion and acute endogenous fibrinolysis in healthy smokers. J Cardiovasc Pharmacol 44:117-124.
43. Pieper GM, Meier DA, and Hager SR (1995) Endothelial dysfunction in a model of hyperglycemia and hyperinsulinemia. Am J Physiol 269:H845-H850.
44. Pieper GM, Moore-Hilton G, and Roza AM (1996) Evaluation of the mechanism of endothelial dysfunction in the genetically-diabetic BB rat. Life Sci 58:PL147-PL152.
45. Pieper GM, Langenstroer P, and Siebeneich W (1997) Diabetic-induced endothelial dysfunction in rat aorta: role of hydroxyl radicals. Cardiovasc Res 34:145-156.
46. Pieper GM and Siebeneich W (1998) Oral administration of the antioxidant, N-acetylcysteine, abrogates diabetes-induced endothelial dysfunction. J Cardiovasc Pharmacol 32:101-105.
47. Radi R, Rubbo H, Thomson L, and Prodanov E (1990) Luminol chemiluminescence using xanthine and hypoxanthine as xanthine oxidase substrates. Free Radic Biol Med 8:121-126.
48. Rahman I, Gilmour PS, Jimenez LA, Biswas SK, Antonicelli F, and Aruoma OI (2003) Ergothioneine inhibits oxidative stress- and TNF-alpha-induced NF-kappa B activation and interleukin-8 release in alveolar epithelial cells. Biochem Biophys Res Commun 302:860-864.
49. Rougee M, Bensasson RV, Land EJ, and Pariente R (1988) Deactivation of singlet molecular oxygen by thiols and related compounds, possible protectors against skin photosensitivity. Photochem Photobiol 47:485-489.
50. Rubanyi GM and Vanhoutte PM (1986) Superoxide anions and hyperoxia inactivate endothelium-derived relaxing factor. Am J Physiol 250:H822-H827.
51. Saeki K, Hayakawa S, Isemura M, and Miyase T (2000) Importance of a pyrogallol-type structure in catechin compounds for apoptosis-inducing activity. Phytochemistry 53:391-394.
52. Sakrak O, Kerem M, Bedirli A, Pasaoglu H, Akyurek N, Ofluoglu E, and Gültekin FA (2008) Ergothioneine modulates proinflammatory cytokines and heat shock protein 70 in mesenteric ischemia and reperfusion injury. J Surg Res 144:36-42.
53. Sawada M, Nakashima S, Kiyono T, Nakagawa M, Yamada J, Yamakawa H, Banno Y, Shinoda J, Nishimura Y, and Nozawa Y, et al. (2001) p53 regulates ceramide formation by neutral sphingomyelinase through reactive oxygen species in human glioma cells. Oncogene 20:1368-1378.
54. Shi Y, Ku DD, Man RY, and Vanhoutte PM (2006) Augmented endothelium-derived hyperpolarizing factor-mediated relaxations attenuate endothelial dysfunction in femoral and mesenteric, but not in carotid arteries from type I diabetic rats. J Pharmacol Exp Ther 318:276-281.
55. Song TY, Chen CL, Liao JW, Ou HC, and Tsai MS (2010) Ergothioneine protects against neuronal injury induced by cisplatin both in vitro and in vivo. Food Chem Toxicol 48:3492-3499.
56. Sotgia S, Pisanu E, Pintus G, Erre GL, Pinna GA, Deiana L, Carru C, and Zinellu A (2013) Plasma L-ergothioneine measurement by high-performance liquid chromatography and capillary electrophoresis after a pre-column derivatization with 5-iodoacetamidofluorescein (5-IAF) and fluorescence detection. PLoS ONE 8:e70374.
57. Tamai I, Yabuuchi H, Nezu J, Sai Y, Oku A, Shimane M, and Tsuji A (1997) Cloning and characterization of a novel human pH-dependent organic cation transporter, OCTN1. FEBS Lett 419:107-111.
58. Tarpey MM and Fridovich I (2001) Methods of detection of vascular reactive species: nitric oxide, superoxide, hydrogen peroxide, and peroxynitrite. Circ Res 89:224-236.
59. Tesfamariam B and Cohen RA (1992) Role of superoxide anion and endothelium in vasoconstrictor action of prostaglandin endoperoxide. Am J Physiol 262:H1915-H1919.
60. Ting HH, Timimi FK, Boles KS, Creager SJ, Ganz P, and Creager MA (1996) Vitamin C improves endothelium-dependent vasodilation in patients with non-insulin-dependent diabetes mellitus. J Clin Invest 97:22-28.