Ergothioneine protects against neuronal injury induced by cisplatin both in vitro and in vivo

Food and Chemical Toxicology

Volumn 48, Issue 12, 2010, Pages 3492-3499

  Song, Tuzz Ying ^a   Chen, Chien Lin ^b   Liao, Jiunn Wang ^c   Ou, Hsiu Chung ^d   Tsai, Ming Shiun ^b  

^a CHUNG CHOU INSTITUTE OF TECHNOLOGY   (Taiwan)

^b DA YEH UNIVERSITY   (Taiwan)

^c NATIONAL CHUNG HSING UNIVERSITY   (Taiwan)

^d CHINA MEDICAL UNIVERSITY   (Taiwan)

Author keywords

Acetylcholinesterase activity; Avoidance tests; Cisplatin; Ergothioneine; Neuron cells; Oxidative stress

Indexed keywords

ACETYLCHOLINESTERASE; BRAIN ENZYME; CISPLATIN; GLUTATHIONE; GLUTATHIONE DISULFIDE; THIONEINE;

AMNESIA; ANIMAL CELL; ANIMAL EXPERIMENT; ANIMAL MODEL; ANIMAL TISSUE; ARTICLE; AVOIDANCE BEHAVIOR; BRAIN CELL; BRAIN METABOLISM; BRAIN TISSUE; CELL PROLIFERATION; CONTROLLED STUDY; DENDRITE; DRUG CYTOTOXICITY; DRUG EFFECT; DRUG EFFICACY; DRUG MECHANISM; ENZYME ACTIVITY; IN VITRO STUDY; IN VIVO STUDY; INCUBATION TIME; LEARNING DISORDER; LIPID PEROXIDATION; NERVE CELL GROWTH; NERVE CELL INHIBITION; NERVE CELL LESION; NEUROPROTECTION; NEUROTOXICITY; NONHUMAN; OXIDATIVE STRESS; PHEOCHROMOCYTOMA CELL; RAT; TREATMENT DURATION; WEIGHT REDUCTION;

ACETYLCHOLINESTERASE; ANIMALS; ANTINEOPLASTIC AGENTS; ANTIOXIDANTS; AVOIDANCE LEARNING; BODY WEIGHT; BRAIN CHEMISTRY; CELL SURVIVAL; CELLS, CULTURED; CEREBRAL CORTEX; CISPLATIN; ERGOTHIONEINE; GLUTATHIONE; LIPID PEROXIDATION; MICE; MICE, INBRED CBA; NEURONS; NEUROPROTECTIVE AGENTS; PC12 CELLS; RATS; RATS, SPRAGUE-DAWLEY; THIOBARBITURIC ACID REACTIVE SUBSTANCES;

MUS; RATTUS;

EID: 78049433030     PISSN: 02786915     EISSN: None     Source Type: Journal    
DOI: 10.1016/j.fct.2010.09.030     Document Type: Article

References (58)

1. Alvarez A., Alarcón R., Opazo C., Campos E.O., Mun oz F.J., Caldéron F.H., Dajas F., Gentry M.K., Doctor B.P., De Mello F.G., Inestrosa N.C. Stable complexes involving acetylcholinesterase and amyloid-β peptide change the biochemical properties of the enzyme and increase the neurotoxicity of Alzheimer's fibrils. J. Neurosci. 1998, 18:3213-3223.
2. Anniko M., Sobin A. Cisplatin: evaluation of its ototoxic potential. Am. J. Otolaryngol. 1986, 7:276-293.
3. Aruoma O.I., Spencer J.P., Mahmood N. Protection against oxidative damage and cell death by the natural antioxidant ergothioneine. Food Chem. Toxicol. 1999, 37:1043-1053.
4. Aruoma O.I., Whiteman M., England T.G., Halliwell B. Antioxidant action of ergothioneine: assessment of its ability to scavenge peroxynitrite. Biochem. Biophys. Res. Commun. 1997, 231:389-391.
5. Atack J.R., Perry E.K., Bonham J.R., Perry R.H., Tomlinson B.E., Blessed G., Fairbairn A. Molecular forms of acetylcholinesterase in senile dementia of Alzheimer's type: selective loss of the intermediate (10S) form. Neurosci. Lett. 1983, 40:199-204.
6. Basinger M.A., Jones M.M., Holscher M.A. l-Methionine antagonism of cis-platinum nephrotoxicity. Toxicol. Appl. Pharmacol. 1990, 103:1-15.
7. Bohm S., Oriana S., Spatti G., Re Di F., Breasciani G., Pirovano C., Grosso I., Martini C., Caraceni A., Pilotti S., Zunino F. Dose intensification of platinum compounds with glutathione protection as induction chemotherapy for advanced ovarian carcinoma. Oncology 1999, 57:115-120.
8. Buege A.J., Aust S.D. Microsomal lipid peroxidation. Methods Enzymol. 1978, 52:302-310.
9. Deiana M., Rosa A., Casu V., Piga R., Assunta Dessì M., Aruoma O.I. l-ergothioneine modulates oxidative damage in the kidney and liver of rats in vivo: studies upon the profile of polyunsaturated fatty acids. Clin. Nutr. 2004, 23:183-193.
10. Dietrich J., Han R., Yang Y., Mayer-Pröschel M., Noble M. CNS progenitor cells and oligodendrocytes are targets of chemotherapeutic agents in vitro and in vivo. J. Biol. 2006, 5:22.
11. Dubost N.J., Beelman R., Peterson D., Royse D. Identification and quantification of ergothioneine in cultivated mushrooms using liquid chromatography-mass spectroscopy. Int. J. Med. Mushrooms 2007, 8:215-222.
12. Ellman G.L., Courtney K.D., Andres V.J., Featherstone R.M. A new and rapid colorimetric determination of acetylcholinesterase activity. Biochem. Pharmacol. 1961, 7:88-95.
13. Epand R.M., Epand R.F. Study of the ergothioneine concentration in the blood of individuals with diabetes mellitus. J. Clin. Chem. Biochem. 1988, 26:623-626.
14. Epand R.M. The role of dietary ergothioneine in the development of diabetes mellitus. Med. Hypoth. 1982, 9:207-213.
15. Esposito M., Vannozzi M.O., Viale M., Fulco R.A., Collecchi P., Merlo F., De Cian F., Zicca A., Cadoni A., Poirier M.C. Para-aminobenzoic acid suppression of cis-diamminedichloroplatinum(II) nephrotoxicity. Carcinogenesis 1993, 12:2595-2599.
16. Fraser R. Blood ergothioneine levels in diabetes mellitus. J. Lab. Clin. Med. 1950, 35:960.
17. Gabaizadeh R., Staecker H., Liu W., Van De Water T.R. BDNF protection of auditory neurons from cisplatin involves changes in intracellular levels of both reactive oxygen species and glutathione. Mol. Brain Res. 1997, 50:71-78.
18. Gerritsen van der Hoop R., Hamers F.P., Neijt J.P., Veldman H., Gispen W.H., Jennekens F.G. Protection against cisplatin induced neurotoxicity by ORG 2766: histological and electrophysiological evidence. J. Neurol. Sci. 1994, 126:109-115.
19. Gründemann D., Stephanie H., Golz S., Geerts A., Lazar A., Berkels R., Jung N., Rubbert A., Schömig E. Discovery of the ergothioneine transporter. PNAS 2005, 102:5256-5261.
20. Guijarro M.V., Indart A., Aruoma O.I., Viana M., Bonet B. Effects of ergothioneine on diabetic embryopathy in pregnant rats. Food Chem Toxicol. 2002, 40:1751-1755.
21. Hagrman D., Goodisman J., Dabrowiak J.C., Souid A.K. Kinetic study on the reaction of cisplatin with metallothionein. Drug Metab. Dispos. 2003, 31:916-923.
22. Hara M., Yoshida M., Nishijima H., Yokosuka M., Iigo M., Ohtani-Kaneko R., Shimada A., Hasegawa T., Akama Y., Hirata K. Melatonin, a pineal secretory product with antioxidant properties, protects against cisplatin-induced nephrotoxicity in rats. J. Pineal. Res. 2001, 30:129-138.
23. Hol E.M., Mandys V., Sodaar P., Gispen W.H., Bär P.R. Protection by an ACTH4-9 analogue against the toxic effects of cisplatin and taxol on sensory neurons and glial cells in vitro. J. Neurosci. Res. 1994, 39:178-185.
24. Huang H.M., Ou H.C., Hsieh S.J. Antioxidants prevent amyloid peptide-induced apoptosis and alteration of calcium homeostasis in cultured cortical neurons. Life Sci. 2000, 66:1879-1892.
25. Inestrosa N.C., Alvarez A., Pérez C.A., Moreno R.D., Vicente M., Linker C., Casanueva O.I., Soto C., Garrido J. Acetylcholinesterase accelerates assembly of amyloid β-peptides into Alzheimer's fibrils: possible role of the peripheral site of the enzyme. Neuron 1996, 16:881-891.
26. Jang J.H., Aruoma O.I., Jen L.S., Chung H.Y., Surh Y.J. Ergothioneine rescues PC12 cells from β-amyloid-induced apoptotic death. Free Rad. Biol. Med. 2004, 36:288-299.
27. Jhoo J.H., Kim H.C., Nabeshima T., Yamada K., Shin E.J., Jhoo W.K., Kim W., Kang K.S., Jo S.A., Woo J.I. β-Amyloid (1-42)-induced learning and memory deficits in mice. Involvement of oxidative burdens in the hippocampus and cerebral cortex. Behav. Brain Res. 2004, 155:185-196.
28. Kaizer R.R., Corrêa M.C., Spanevello R.M., Morsch V.M., Mazzanti C.M., Gonçalves J.F., Schetinger M.R. Acetylcholinesterase activation and enhanced lipid peroxidation after long-term exposure to low levels of aluminum on different mouse brain regions. J. Inorg. Biochem. 2005, 99:1865-1870.
29. Kaya H., Oral B., Ozguner F., Tahan V., Babar Y., Delibas N. The effect of melatonin application on lipid peroxidation during cyclophosphamide therapy in female rats. Zentralbl. Gynakol. 1999, 121:499-502.
30. Krall W.J., Sramek J.J., Cutler N.R. Cholinesterase inhibitors: a therapeutic strategy for Alzheimer disease. Ann. Pharmacother. 1999, 33:441-450.
31. Liu J.F., Lo A., Yang F.L., Wang T.Y., Cheng C.M., Shaw N.S., Kao M.D., Chuang C.Y., Huang C.J. Analysis of vitamin E, selenium, and other nutrients in planed balanced diets in Taiwan. Nutr. Sci. J. 2002, 27:221-231.
32. Melville D.B., Horner W.H., Otken C.C., Ludwig M.L. Studies of the origin of ergothioneine in animals. J. Biol. Chem. 1955, 213:61-68.
33. Melville D.B. l-Ergothioneine. Vitam. Horm. 1958, 17:155-204.
34. Mendonça L.M., Dos Santos G.C., Antonucci G.A., Dos Santos A.C., Bianchi Mde L., Antunes L.M. Evaluation of the cytotoxicity and genotoxicity of curcumin in PC12 cells. Mutat. Res. 2009, 675:29-34.
35. Moncaster J.A., Walsh D.T., Gentleman S.M., Jen L.S., Aruoma O.I. Ergothioneine treatment protects neurons against N-methyl-d-aspartate excitotoxicity in an in vivo rat retinal model. Neurosci. Lett. 2002, 328:55-59.
36. Montilla P., Vardgas J.F., Tunez I.F., Munez de Agueda M.C., Valdelvira M.E., Cabrera E.S. Oxidative stress in diabetic rats induced by streptozotocin: monoxide, NO stimulates insulin secretion by inducing calcium release from protective effects of melatonin. J. Pineal. Res. 1998, 25:94-100.
37. Morán M.A., Mufson E.J., Gómez-Ramos P. Colocalization of cholinesterases with β amyloid protein in aged and Alzheimer's brains. Acta Neuropathol. 1993, 85:362-369.
38. Okatani Y., Wakatsuki A., Morioka N., Watanabe K. Melatonin inhibits the vasorelaxant action of peroxynitrite in human umbilical artery. J. Pineal. Res. 1999, 27:111-115.
39. Pardridge W. Glucose transport and phosphorylation: which is rate limiting for brain glucose utilization?. Ann. Neurol. 1994, 35:511-512.
40. Pedersen A.D., Rossen P., Mehlsen M.Y., Pedersen C.G., Zachariae R., von der Maase H. Cisplatin-based therapy: a neurological and neuropsychological review. Psycho oncol. 2000, 9:29-39.
41. Ravi R., Somani S.M., Rybak L.P. Mechanisms of cisplatin ototoxicity: antioxidant system. Pharmacol. Toxicol. 1995, 76:386-394.
42. Recchia F., Lalli A., Lombardo M., De Filippis S., Saggio G., Fabbri F., Rosselli M., Capomolla E., Rea S. Ifosfamide, cisplatin, and 13-cis retinoic acid for patients with advanced or recurrent squamous cell carcinoma of the head and neck: a phase I-II study. Cancer 2001, 92:814-821.
43. Rybak L., Ravi R., Somani S.M. Mechanism of protection by diethyldithiocarbamate against cisplatin ototoxicity: antioxidant system. Fund. Appl. Toxicol. 1995, 26:293-300.
44. Sadowitz P.D., Hubbard B.A., Dabrowiak J.C., Goodisman J., Tacka K.A., Aktas M.K., Cunningham M.J., Dubowy R.L., Souid A.K. Kinetics of cisplatin binding to cellular DNA and modulations by thiol-blocking agents and thiol drugs. Drug Metab. Dispos. 2002, 30:183-190.
45. Schofield J.D., Chen X. Analysis of free reduced and free oxidized glutathione in wheat flour. J. Creal. Sci. 1995, 21:127-136.
46. Screnci D., McKeage M.J. Platinum neurotoxicity: clinical profiles, experimental models and neuroprotective approaches. J. Inorg. Biochem. 1999, 77:105-110.
47. Sener G., Satiroglu H., Kabasakal L., Arbak S., Oner S., Ercan F., Keyer-Uysa M. The protective effect of melatonin on cisplatin nephrotoxicity. Fundam. Clin. Pharmacol. 2000, 14:553-560.
48. Shires T.K., Brummel M.C., Pulido J.S., Stegink L.D. Ergothioneine distribution in bovine and porcine ocular tissues. Comp. Biochem. Physiol. C Pharmacol. Toxicol. Endocrinol. 1997, 117:117-120.
49. Somani S.M., Ravi R., Rybak L.P. Diethyldithiocarbamate protection against cisplatin nephrotoxicity: antioxidant system. Drug Chem. Toxicol. 1995, 18:151-170.
50. Sweeney C. History of testicular cancer chemotherapy: maximizing efficacy, minimizing toxicity. Semin. Urol. Oncol. 2001, 19:170-179.
51. Ta L.E., Espeset L., Podratz J., Windebank A.J. Neurotoxicity of oxaliplatin and cisplatin for dorsal root ganglion neurons correlates with platinum-DNA binding. Neuro. Toxicol. 2006, 27:992-1002.
52. Tan D.X., Chen D., Poeggeler B., Manchester L.C., Reiter R.J. Melatonin: a potent endogenous hydroxyl radical scavenger. Endocr. J. 1993, 1:57-60.
53. Tesoriere L., D'Arpa D., Conti S., Giaccone V., Pintaudi A.M., Livrea M.A. Melatonin protects human red blood cells from oxidative hemolysis: new insights into the radical-scavenging activity. J. Pineal. Res. 1999, 27:95-105.
54. Thigpen T., Vance R., Puneky L., Khansurt T. Chemotherapy in advanced ovarian carcinoma: current standards of care based on randomised trials. Gynecol. Oncol. 1994, 55:S97-S107.
55. Touster O.J. The l-ergothioneine content of human erythrocytes, the effect of age, race, malignancy and pregnancy. J. Biol. Chem. 1951, 188:371.
56. Tredici G., Cavaletti G., Petruccioli M.G., Fabbrica D., Tedeschi M., Venturino P. Low-dose glutathione administration in the prevention of cisplatin-induced peripheral neuropathy in rats. Neurotoxicology 1994, 15:701-704.
57. Ulrich J., Meier-Ruge W., Probst A., Meier E., Ipsen S. Senile plaques: staining for acetylcholinesterase and A4 protein: a comparative study in the hippocampus and entorhinal cortex. Acta Neuropathol. 1990, 80:624-628.
58. Van Basten J.P., Schrafford-Koops H., Sleijfer D.T., Pras E., van Driel M.F., Hoekstra H.J. Current concept about testicular cancer. Eur. J. Surg. Oncol. 1997, 23:354-360.