Mirtazapine protects against cisplatin-induced oxidative stress and DNA damage in the rat brain

Psychiatry and Clinical Neurosciences

Volumn 67, Issue 1, 2013, Pages 50-58

  Gulec, Mustafa ^a   Oral, Elif ^a   Dursun, Onur B ^a   Yucel, Atakan ^a   Hacimuftuoglu, Ahmet ^a   Akcay, Fatih ^a   Suleyman, Halis ^a  

^a ATATURK UNIVERSITY   (Turkey)

Author keywords

cisplatin; mirtazapine; neurotoxicity; oxidative stress; protective

Indexed keywords

8 HYDROXYGUANINE; CISPLATIN; GLUTATHIONE; MALONALDEHYDE; MIRTAZAPINE; MYELOPEROXIDASE; NITRIC OXIDE;

ANIMAL MODEL; ANIMAL TISSUE; ANTIOXIDANT ACTIVITY; ARTICLE; BRAIN TISSUE; CANCER CHEMOTHERAPY; CHEMOPROPHYLAXIS; CONTROLLED STUDY; DNA DAMAGE; DOSE RESPONSE; MALE; NEUROPROTECTION; NEUROTOXICITY; NONHUMAN; OUTCOME ASSESSMENT; OXIDATIVE STRESS; RAT;

ANIMALS; ANTINEOPLASTIC AGENTS; ANTIOXIDANTS; BRAIN; CISPLATIN; DNA DAMAGE; GLUTATHIONE; GUANINE; MALE; MALONDIALDEHYDE; MIANSERIN; NITRIC OXIDE; OXIDATIVE STRESS; PEROXIDASE; RATS; RATS, WISTAR; SUPEROXIDE DISMUTASE;

EID: 84872703014     PISSN: 13231316     EISSN: 14401819     Source Type: Journal    
DOI: 10.1111/j.1440-1819.2012.02395.x     Document Type: Article

References (86)

1. Cerri S, Piccolini VM, Santin G, et al. The developmental neurotoxicity study of platinum compounds. Effects of cisplatin versus a novel Pt(II) complex on rat cerebellum. Neurotoxicol. Teratol. 2011; 33: 273-281.
2. McWhinney SR, Goldberg RM, McLeod HL,. Platinum neurotoxicity pharmacogenetics. Mol. Cancer Ther. 2009; 8: 10-16.
3. Joseph D, Dubashi B, Karthikeyan B, Jain A,. Arterial occlusion precipitated by cisplatin based chemotherapy. Curr. Oncol. 2010; 17: 71-72.
4. Lee KW, Jeong JY, Lim BJ, et al. Sildenafil attenuates renal injury in an experimental model of rat cisplatin-induced nephrotoxicity. Toxicology 2009; 257: 137-143.
5. Amptoulach S, Tsavaris N,. Neurotoxicity caused by the treatment with platinum analogues. Chemother. Res. Pract. 2011; 2011: 1-5.
6. Nowis D, Legat M, Bil J, et al. Erythropoietin reduces cisplatin-induced neurotoxicity without impairment of cytotoxic effects against tumor cells. Int. J. Oncol. 2007; 31: 1547-1552.
7. Podratz JL, Staff NP, Froemel D, et al. Drosophila melanogaster: A new model to study cisplatin-induced neurotoxicity. Neurobiol. Dis. 2011; 43: 330-337.
8. Carozzi VA, Chiorazzi A, Canta A, et al. Glutamate carboxypeptidase inhibition reduces the severity of chemotherapy-induced peripheral neurotoxicity in rat. Neurotox. Res. 2010; 17: 380-391.
9. Liu JJ, Jamieson SM, Subramaniam J, et al. Neuronal expression of copper transporter 1 in rat dorsal root ganglia: Association with platinum neurotoxicity. Cancer Chemother. Pharmacol. 2009; 64: 847-856.
10. Bernocchi G, Bottone MG, Piccolini VM, et al. Developing central nervous system and vulnerability to platinum compounds. Chemother. Res. Pract. 2011; 2011: 1-14.
11. Vilmar A, Santoni-Rugiu E, Sørensen JB,. ERCC1, toxicity and quality of life in advanced NSCLC patients randomized in a large multicentre phase III trial. Eur. J. Cancer 2010; 46: 1554-1562.
12. James SE, Dunham M, Carrion-Jones M, Murashov A, Lu Q,. Rho kinase inhibitor Y-27632 facilitates recovery from experimental peripheral neuropathy induced by anti-cancer drug cisplatin. Neurotoxicology 2010; 31: 188-194.
13. Carozzi V, Chiorazzi A, Canta A, et al. Effect of the chronic combined administration of cisplatin and paclitaxel in a rat model of peripheral neurotoxicity. Eur. J. Cancer 2009; 45: 656-665.
14. Hino K, Nishikawa M, Sato E, Inoue M,. L-carnitine inhibits hypoglycemia-induced brain damage in the rat. Brain Res. 2005; 1053: 77-87.
15. Altun ZS, Gunes D, Aktas S, Erbayraktar Z, Olgun N,. Protective effects of acetyl-L-carnitine on cisplatin cytotoxicity and oxidative stress in neuroblastoma. Neurochem. Res. 2010; 35: 437-443.
16. Gunes D, Kirkim G, Kolatan E, et al. Evaluation of the effect of acetyl L-carnitine on experimental cisplatin ototoxicity and neurotoxicity. Chemotherapy 2011; 57: 186-194.
17. Maggioni D, Nicolini G, Chiorazzi A, Meregalli C, Cavaletti G, Tredici G,. Different effects of erythropoietin in cisplatin- and docetaxel-induced neurotoxicity: An in vitro study. J. Neurosci. Res. 2010; 88: 3171-3179.
18. Tuncer S, Dalkilic N, Akif Dunbar M, Keles B,. Comparative effects of alpha lipoic acid and melatonin on cisplatin-induced neurotoxicity. Int. J. Neurosci. 2010; 120: 655-663.
19. Gulec M, Selvi Y, Boysan M, Aydin A, Besiroglu L, Agargun MY,. Ongoing or re-emerging subjective insomnia symptoms after full/partial remission or recovery of major depressive disorder mainly with the selective serotonin reuptake inhibitors and risk of relapse or recurrence: A 52-week follow-up study. J. Affect. Disord. 2011; 134: 257-265.
20. Bilici M, Ozturk C, Dursun H, et al. Protective effect of mirtazapine on indomethacin-induced ulcer in rats and its relationship with oxidant and antioxidant parameters. Dig. Dis. Sci. 2009; 54: 1868-1875.
21. Sener MT, Sener E, Tok A, et al. Biochemical and histologic study of lethal cisplatin nephrotoxicity prevention by mirtazapine. Pharmacol. Rep. 2012; 64: 594-602.
22. Gaona-Gaona L, Molina-Jijon E, Tapia E, et al. Protective effect of sulforaphane pretreatment against cisplatin-induced liver and mitochondrial oxidant damage in rats. Toxicology 2011; 286: 20-27.
23. Ajith TA, Nivitha V, Usha S,. Zingiber officinale Roscoe alone and in combination with alpha-tocopherol protect the kidney against cisplatin-induced acute renal failure. Food Chem. Toxicol. 2007; 45: 921-927.
24. Sedlak J, Lindsay RH,. Estimation of total, protein-bound, and nonprotein sulfhydryl groups in tissue with Ellman's reagent. Anal. Biochem. 1968; 25: 192-205.
25. Bories PN, Bories C,. Nitrate determination in biological fluids by an enzymatic one-step assay with nitrate reductase. Clin. Chem. 1995; 41: 904-907.
26. Moshage H, Kok B, Huizenga JR, Jansen PL,. Nitrite and nitrate determinations in plasma: A critical evaluation. Clin. Chem. 1995; 41: 892-896.
27. Polat B, Suleyman H, Alp HH,. Adaptation of rat gastric tissue against indomethacin toxicity. Chem. Biol. Interact. 2010; 186: 82-89.
28. Ohkawa H, Ohishi N, Yagi K,. Assay for lipid peroxides in animal tissues by thiobarbituric acid reaction. Anal. Biochem. 1979; 95: 351-358.
29. Bradley PP, Priebat DA, Christensen RD, Rothstein G,. Measurement of cutaneous inflammation: Estimation of neutrophil content with an enzyme marker. J. Invest. Dermatol. 1982; 78: 206-209.
30. Shigenaga MK, Aboujaoude EN, Chen Q, Ames BN,. Assays of oxidative DNA damage biomarkers 8-oxo-2'-deoxyguanosine and 8-oxoguanine in nuclear DNA and biological fluids by high-performance liquid chromatography with electrochemical detection. Methods Enzymol. 1994; 234: 16-33.
31. Kaur H, Halliwell B,. Measurement of oxidized and methylated DNA bases by HPLC with electrochemical detection. Biochem. J. 1996; 318 (Pt 1): 21-23.
32. Floyd RA, Watson JJ, Wong PK, Altmiller DH, Rickard RC,. Hydroxyl free radical adduct of deoxyguanosine: Sensitive detection and mechanisms of formation. Free Radic. Res. Commun. 1986; 1: 163-172.
33. Asami S, Hirano T, Yamaguchi R, Tomioka Y, Itoh H, Kasai H,. Increase of a type of oxidative DNA damage, 8-hydroxyguanine, and its repair activity in human leukocytes by cigarette smoking. Cancer Res. 1996; 56: 2546-2549.
34. Cavaliere R, Schiff D,. Neurologic toxicities of cancer therapies. Curr. Neurol. Neurosci. Rep. 2006; 6: 218-226.
35. Al Moundhri MS, Al-Salam S, Al Mahrouqee A, Beegam S, Ali BH,. The effect of curcumin on oxaliplatin and cisplatin neurotoxicity in rats: Some behavioral, biochemical, and histopathological studies. J. Med. Toxicol. 2012. doi: 10.1007/s13181-012-0239-x.
36. Arrieta Ó, Hernández-Pedro N, Fernández- González-Aragõn MC, et al. Retinoic acid reduces chemotherapy-induced neuropathy in an animal model and patients with lung cancer. Neurology 2011; 77: 987-995.
37. Canta A, Chiorazzi A, Carozzi V, et al. In vivo comparative study of the cytotoxicity of a liposomal formulation of cisplatin (lipoplatin™). Cancer Chemother. Pharmacol. 2011; 68: 1001-1008.
38. Carozzi VA, Canta A, Oggioni N, et al. Neurophysiological and neuropathological characterization of new murine models of chemotherapy-induced chronic peripheral neuropathies. Exp. Neurol. 2010; 226: 301-309.
39. Scuteri A, Galimberti A, Maggioni D, et al. Role of MAPKs in platinum-induced neuronal apoptosis. Neurotoxicology 2009; 30: 312-319.
40. Kim HJ, Lee JH, Kim SJ, et al. Roles of NADPH oxidases in cisplatin-induced reactive oxygen species generation and ototoxicity. J. Neurosci. 2010; 30: 3933-3946.
41. Maher P,. The effects of stress and aging on glutathione metabolism. Ageing Res. Rev. 2005; 4: 288-314.
42. Martins NM, Santos NA, Curti C, Bianchi ML, Santos AC,. Cisplatin induces mitochondrial oxidative stress with resultant energetic metabolism impairment, membrane rigidification and apoptosis in rat liver. J. Appl. Toxicol. 2008; 28: 337-344.
43. Rjiba-Touati K, Ayed-Boussema I, Belarbia A, Achour A, Bacha H,. Recombinant human erythropoietin prevents cisplatin-induced genotoxicity in rat liver and heart tissues via an antioxidant process. Drug Chem. Toxicol. 2012; 35: 134-140.
44. Sohn SI, Rim HK, Kim YH, et al. The ameliorative effect of 23-hydroxytormentic acid isolated from Rubus coreanus on cisplatin-induced nephrotoxicity in rats. Biol. Pharm. Bull. 2011; 34: 1508-1513.
45. Ilbey YO, Ozbek E, Cekmen M, Simsek A, Otunctemur A, Somay A,. Protective effect of curcumin in cisplatin-induced oxidative injury in rat testis: Mitogen-activated protein kinase and nuclear factor-kappa B signaling pathways. Hum. Reprod. 2009; 24: 1717-1725.
46. Chirino YI, Pedraza-Chaverri J,. Role of oxidative and nitrosative stress in cisplatin-induced nephrotoxicity. Exp. Toxicol. Pathol. 2009; 61: 223-242.
47. Azambuja AA, Lunardelli A, Nunes FB, et al. Effect of fructose-1,6-bisphosphate on the nephrotoxicity induced by cisplatin in rats. Inflammation 2011; 34: 67-71.
48. Mansour HH, Hafez HF, Fahmy NM,. Silymarin modulates cisplatin-induced oxidative stress and hepatotoxicity in rats. J. Biochem. Mol. Biol. 2006; 39: 656-661.
49. Pisu MB, Guioli S, Conforti E, Bernocchi G,. Signal molecules and receptors in the differential development of cerebellum lobules. Acute effects of cisplatin on nitric oxide and glutamate systems in Purkinje cell population. Brain Res. Dev. Brain Res. 2003; 145: 229-240.
50. Jarve RK, Aggarwal SK,. Cisplatin-induced inhibition of the calcium-calmodulin complex, neuronal nitric oxide synthase activation and their role in stomach distention. Cancer Chemother. Pharmacol. 1997; 39: 341-348.
51. Kim CS, Choi JS, Park JW, et al. Altered regulation of nitric oxide and natriuretic peptide system in cisplatin-induced nephropathy. Regul. Pept. 2012; 174: 65-70.
52. Saleh S, El-Demerdash E,. Protective effects of L-arginine against cisplatin-induced renal oxidative stress and toxicity: role of nitric oxide. Basic Clin. Pharmacol. Toxicol. 2005; 97: 91-97.
53. Pourahmad J, Hosseini MJ, Eskandari MR, Shekarabi SM, Daraei B,. Mitochondrial/lysosomal toxic cross-talk plays a key role in cisplatin nephrotoxicity. Xenobiotica 2010; 40: 763-771.
54. Mihara Y, Egashira N, Sada H, et al. Involvement of spinal NR2B-containing NMDA receptors in oxaliplatin-induced mechanical allodynia in rats. Mol. Pain 2011; 7: 8.
55. Pan H, Mukhopadhyay P, Rajesh M, et al. Cannabidiol attenuates cisplatin-induced nephrotoxicity by decreasing oxidative/nitrosative stress, inflammation, and cell death. J. Pharmacol. Exp. Ther. 2009; 328: 708-714.
56. Ilbey YO, Ozbek E, Simsek A, Otunctemur A, Cekmen M, Somay A,. Potential chemoprotective effect of melatonin in cyclophosphamide- and cisplatin-induced testicular damage in rats. Fertil. Steril. 2009; 92: 1124-1132.
57. El-Awady el SE, Moustafa YM, Abo-Elmatty DM, Radwan A,. Cisplatin-induced cardiotoxicity: mechanisms and cardioprotective strategies. Eur. J. Pharmacol. 2011; 650: 335-341.
58. Karadeniz A, Simsek N, Karakus E, et al. Royal jelly modulates oxidative stress and apoptosis in liver and kidneys of rats treated with cisplatin. Oxid. Med. Cell. Longev. 2011; 2011: 1-10.
59. Sahu BD, Rentam KK, Putcha UK, Kuncha M, Vegi GM, Sistla R,. Carnosic acid attenuates renal injury in an experimental model of rat cisplatin-induced nephrotoxicity. Food Chem. Toxicol. 2011; 49: 3090-3097.
60. Song TY, Chen CL, Liao JW, Ou HC, Tsai MS,. Ergothioneine protects against neuronal injury induced by cisplatin both in vitro and in vivo. Food Chem. Toxicol. 2010; 48: 3492-3499.
61. Muthuraman A, Singla SK, Peters A,. Exploring the potential of flunarizine for cisplatin-induced painful uremic neuropathy in rats. Int. Neurourol. J. 2011; 15: 127-134.
62. Ozkol H, Musa D, Tuluce Y, Koyuncu I,. Ameliorative influence of Urtica dioica L against cisplatin-induced toxicity in mice bearing Ehrlich ascites carcinoma. Drug Chem. Toxicol. 2012; 35: 251-257.
63. Sanchez-Gonzalez PD, Lopez-Hernandez FJ, Perez-Barriocanal F, Morales AI, Lopez-Novoa JM,. Quercetin reduces cisplatin nephrotoxicity in rats without compromising its anti-tumour activity. Nephrol. Dial. Transplant. 2011; 26: 3484-3495.
64. Iseri S, Ercan F, Gedik N, Yuksel M, Alican I,. Simvastatin attenuates cisplatin-induced kidney and liver damage in rats. Toxicology 2007; 230: 256-264.
65. Kizek R, Adam V, Hrabeta J, et al. Anthracyclines and ellipticines as DNA-damaging anticancer drugs: Recent advances. Pharmacol. Ther. 2012; 133: 26-39.
66. Hirano T, Kawai K, Ootsuyama Y, Orimo H, Kasai H,. Detection of a mouse OGG1 fragment during caspase-dependent apoptosis: Oxidative DNA damage and apoptosis. Cancer Sci. 2004; 95: 634-638.
67. Kostova I,. Platinum complexes as anticancer agents. Recent Pat. Anticancer Drug Discov. 2006; 1: 1-22.
68. Fischer SJ, Benson LM, Fauq A, Naylor S, Windebank AJ,. Cisplatin and dimethyl sulfoxide react to form an adducted compound with reduced cytotoxicity and neurotoxicity. Neurotoxicology 2008; 29: 444-452.
69. Bulat N, Widmann C,. Caspase substrates and neurodegenerative diseases. Brain Res. Bull. 2009; 80: 251-267.
70. Ludwig T, Oberleithner H,. Platinum complex toxicity in cultured renal epithelia. Cell. Physiol. Biochem. 2004; 14: 431-440.
71. Siddik ZH,. Cisplatin: Mode of cytotoxic action and molecular basis of resistance. Oncogene 2003; 22: 7265-7279.
72. Wu YJ, Muldoon LL, Neuwelt EA,. The chemoprotective agent N-acetylcysteine blocks cisplatin-induced apoptosis through caspase signaling pathway. J. Pharmacol. Exp. Ther. 2005; 312: 424-431.
73. Schuler M, Bossy-Wetzel E, Goldstein JC, Fitzgerald P, Green DR,. p53 induces apoptosis by caspase activation through mitochondrial cytochrome c release. J. Biol. Chem. 2000; 275: 7337-7342.
74. Zhan Y, van de Water B, Wang YP, Stevens JL,. The roles of caspase-3 and bcl-2 in chemically-induced apoptosis but not necrosis of renal epithelial cells. Oncogene 1999; 18: 6505-6512.
75. Dickey DT, Wu YJ, Muldoon LL, Neuwelt EA,. Protection against cisplatin-induced toxicities by N-acetylcysteine and sodium thiosulfate as assessed at the molecular, cellular, and in vivo levels. J. Pharmacol. Exp. Ther. 2005; 314: 1052-1058.
76. Dietrich J, Han R, Yang Y, Mayer-Proschel M, Noble M,. CNS progenitor cells and oligodendrocytes are targets of chemotherapeutic agents in vitro and in vivo. J. Biol. 2006; 5: 22.
77. Sioka C, Kyritsis AP,. Central and peripheral nervous system toxicity of common chemotherapeutic agents. Cancer Chemother. Pharmacol. 2009; 63: 761-767.
78. Church MW, Blakley BW, Burgio DL, Gupta AK,. WR-2721 (Amifostine) ameliorates cisplatin-induced hearing loss but causes neurotoxicity in hamsters: Dose-dependent effects. J. Assoc. Res. Otolaryngol. 2004; 5: 227-237.
79. Ago Y, Nakamura S, Baba A, Matsuda T,. Neuropsychotoxicity of abused drugs: Effects of serotonin receptor ligands on methamphetamine- and cocaine-induced behavioral sensitization in mice. J. Pharmacol. Sci. 2008; 106: 15-21.
80. Maurya AN, Deshpande SB,. Involvement of 5-hydroxytryptaminergic transmission for the Mesobuthus tamulus venom-induced depression of spinal reflexes in neonatal rat in vitro. Neurosci. Lett. 2010; 482: 35-39.
81. Yamamura S, Abe M, Nakagawa M, Ochi S, Ueno S, Okada M,. Different actions for acute and chronic administration of mirtazapine on serotonergic transmission associated with raphe nuclei and their innervation cortical regions. Neuropharmacology 2011; 60: 550-560.
82. Tok A, Sener E, Albayrak A, et al. Effect of mirtazapine on oxidative stress created in rat kidneys by ischemia-reperfusion. Ren. Fail. 2012; 34: 103-110.
83. Cankurtaran ES, Ozalp E, Soygur H, Akbiyik DI, Turhan L, Alkis N,. Mirtazapine improves sleep and lowers anxiety and depression in cancer patients: Superiority over imipramine. Support. Care Cancer 2008; 16: 1291-1298.
84. Ersoy MA, Noyan AM, Elbi H,. An open-label long-term naturalistic study of mirtazapine treatment for depression in cancer patients. Clin. Drug Investig. 2008; 28: 113-120.
85. Kim SW, Shin IS, Kim JM, et al. Effectiveness of mirtazapine for nausea and insomnia in cancer patients with depression. Psychiatry Clin. Neurosci. 2008; 62: 75-83.
86. Riechelmann RP, Burman D, Tannock IF, Rodin G, Zimmermann C,. Phase II trial of mirtazapine for cancer-related cachexia and anorexia. Am. J. Hosp. Palliat. Care 2010; 27: 106-110.