α-Lipoic acid prevents against cisplatin cytotoxicity via activation of the NRF2/HO-1 antioxidant pathway
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Joohyung Lee aff001; So-Young Jung aff001; Keum-Jin Yang aff001; Yoonho Kim aff001; Dohee Lee aff001; Min Hyeong Lee aff001; Dong-Kee Kim aff001
Působiště autorů:
Department of Otolaryngology, Daejeon St. Mary’s Hospital, College of Medicine, The Catholic University of Korea, Daejeon, Republic of Korea
aff001
Vyšlo v časopise:
PLoS ONE 14(12)
Kategorie:
Research Article
prolekare.web.journal.doi_sk:
https://doi.org/10.1371/journal.pone.0226769
Souhrn
The production of reactive oxygen species (ROS) by cisplatin is one of the major mechanisms of cisplatin-induced cytotoxicity. We examined the preventive effect of α-lipoic acid (LA) on cisplatin-induced toxicity via its antioxidant effects on in vitro and ex vivo culture systems. To elucidate the mechanism of the antioxidant activity of LA, NRF2 was inhibited using NRF2 siRNA, and the change in antioxidant activity of LA was characterized. MTT assays showed that LA was safe at concentrations up to 0.5 mM in HEI-OC1 cells and had a protective effect against cisplatin-induced cytotoxicity. Intracellular ROS production in HEI-OC1 cells was rapidly increased by cisplatin for up to 48 h. However, treatment with LA significantly reduced the production of ROS and increased the expression of the antioxidant proteins HO-1 and SOD1. Ex vivo, the organs of Corti of the group pretreated with LA exhibited better preservation than the group that received cisplatin alone. We also confirmed the nuclear translocation of NRF2 after LA administration, and that NRF2 inhibition decreased the antioxidant activity of LA. Together, these results indicate that the antioxidant activity of LA was through the activation of the NRF2/HO-1 antioxidant pathway.
Klíčová slova:
Small interfering RNAs – Cytokines – Deafness – Antioxidants – Cytotoxicity – Reactive oxygen species – Cochlea – Organ of Corti
Zdroje
1. Karasawa T, Steyger PS. An integrated view of cisplatin-induced nephrotoxicity and ototoxicity. Toxicology letters. 2015;237(3):219–27. doi: 10.1016/j.toxlet.2015.06.012 26101797
2. Brock PR, Knight KR, Freyer DR, Campbell KC, Steyger PS, Blakley BW, et al. Platinum-induced ototoxicity in children: a consensus review on mechanisms, predisposition, and protection, including a new International Society of Pediatric Oncology Boston ototoxicity scale. Journal of clinical oncology: official journal of the American Society of Clinical Oncology. 2012;30(19):2408–17.
3. Knight KR, Kraemer DF, Winter C, Neuwelt EA. Early changes in auditory function as a result of platinum chemotherapy: use of extended high-frequency audiometry and evoked distortion product otoacoustic emissions. Journal of clinical oncology: official journal of the American Society of Clinical Oncology. 2007;25(10):1190–5.
4. Brinkman TM, Bass JK, Li Z, Ness KK, Gajjar A, Pappo AS, et al. Treatment-induced hearing loss and adult social outcomes in survivors of childhood CNS and non-CNS solid tumors: Results from the St. Jude Lifetime Cohort Study. Cancer. 2015;121(22):4053–61. doi: 10.1002/cncr.29604 26287566
5. Strauss M, Towfighi J, Lord S, Lipton A, Harvey HA, Brown B. Cis-platinum ototoxicity: clinical experience and temporal bone histopathology. The Laryngoscope. 1983;93(12):1554–9. doi: 10.1288/00005537-198312000-00007 6685804
6. Rybak LP, Whitworth CA, Mukherjea D, Ramkumar V. Mechanisms of cisplatin-induced ototoxicity and prevention. Hearing research. 2007;226(1–2):157–67. doi: 10.1016/j.heares.2006.09.015 17113254
7. Kopke RD, Liu W, Gabaizadeh R, Jacono A, Feghali J, Spray D, et al. Use of organotypic cultures of Corti's organ to study the protective effects of antioxidant molecules on cisplatin-induced damage of auditory hair cells. The American journal of otology. 1997;18(5):559–71. 9303151
8. Banfi B, Malgrange B, Knisz J, Steger K, Dubois-Dauphin M, Krause KH. NOX3, a superoxide-generating NADPH oxidase of the inner ear. The Journal of biological chemistry. 2004;279(44):46065–72. doi: 10.1074/jbc.M403046200 15326186
9. Mukherjea D, Jajoo S, Sheehan K, Kaur T, Sheth S, Bunch J, et al. NOX3 NADPH oxidase couples transient receptor potential vanilloid 1 to signal transducer and activator of transcription 1-mediated inflammation and hearing loss. Antioxidants & redox signaling. 2011;14(6):999–1010.
10. Smyth JF, Bowman A, Perren T, Wilkinson P, Prescott RJ, Quinn KJ, et al. Glutathione reduces the toxicity and improves quality of life of women diagnosed with ovarian cancer treated with cisplatin: results of a double-blind, randomised trial. Annals of oncology: official journal of the European Society for Medical Oncology. 1997;8(6):569–73.
11. Cascinu S, Cordella L, Del Ferro E, Fronzoni M, Catalano G. Neuroprotective effect of reduced glutathione on cisplatin-based chemotherapy in advanced gastric cancer: a randomized double-blind placebo-controlled trial. Journal of clinical oncology: official journal of the American Society of Clinical Oncology. 1995;13(1):26–32.
12. Kottschade LA, Sloan JA, Mazurczak MA, Johnson DB, Murphy BP, Rowland KM, et al. The use of vitamin E for the prevention of chemotherapy-induced peripheral neuropathy: results of a randomized phase III clinical trial. Supportive care in cancer: official journal of the Multinational Association of Supportive Care in Cancer. 2011;19(11):1769–77.
13. Pace A, Giannarelli D, Galie E, Savarese A, Carpano S, Della Giulia M, et al. Vitamin E neuroprotection for cisplatin neuropathy: a randomized, placebo-controlled trial. Neurology. 2010;74(9):762–6. doi: 10.1212/WNL.0b013e3181d5279e 20194916
14. Sarafraz Z, Ahmadi A, Daneshi A. Transtympanic Injections of N-acetylcysteine and Dexamethasone for Prevention of Cisplatin-Induced Ototoxicity: Double Blind Randomized Clinical Trial. Int Tinnitus J. 2018;22(1):40–5. doi: 10.5935/0946-5448.20180007 29993216
15. Hinduja S, Kraus KS, Manohar S, Salvi RJ. D-methionine protects against cisplatin-induced neurotoxicity in the hippocampus of the adult rat. Neurotoxicity research. 2015;27(3):199–204. doi: 10.1007/s12640-014-9503-y 25488710
16. Brock PR, Maibach R, Childs M, Rajput K, Roebuck D, Sullivan MJ, et al. Sodium Thiosulfate for Protection from Cisplatin-Induced Hearing Loss. The New England journal of medicine. 2018;378(25):2376–85. doi: 10.1056/NEJMoa1801109 29924955
17. Kim J, Cho HJ, Sagong B, Kim SJ, Lee JT, So HS, et al. Alpha-lipoic acid protects against cisplatin-induced ototoxicity via the regulation of MAPKs and proinflammatory cytokines. Biochemical and biophysical research communications. 2014;449(2):183–9. doi: 10.1016/j.bbrc.2014.04.118 24796665
18. Kim KH, Lee B, Kim YR, Kim MA, Ryu N, Jung DJ, et al. Evaluating protective and therapeutic effects of alpha-lipoic acid on cisplatin-induced ototoxicity. Cell death & disease. 2018;9(8):827.
19. Koo DY, Lee SH, Lee S, Chang J, Jung HH, Im GJ. Comparison of the effects of lipoic acid and glutathione against cisplatin-induced ototoxicity in auditory cells. International journal of pediatric otorhinolaryngology. 2016;91:30–6. doi: 10.1016/j.ijporl.2016.10.008 27863638
20. Rochette L, Ghibu S, Richard C, Zeller M, Cottin Y, Vergely C. Direct and indirect antioxidant properties of alpha-lipoic acid and therapeutic potential. Molecular nutrition & food research. 2013;57(1):114–25.
21. Packer L, Witt EH, Tritschler HJ. alpha-Lipoic acid as a biological antioxidant. Free radical biology & medicine. 1995;19(2):227–50.
22. Lv C, Maharjan S, Wang Q, Sun Y, Han X, Wang S, et al. alpha-Lipoic Acid Promotes Neurological Recovery After Ischemic Stroke by Activating the Nrf2/HO-1 Pathway to Attenuate Oxidative Damage. Cellular physiology and biochemistry: international journal of experimental cellular physiology, biochemistry, and pharmacology. 2017;43(3):1273–87.
23. Xia D, Zhai X, Wang H, Chen Z, Fu C, Zhu M. Alpha lipoic acid inhibits oxidative stress-induced apoptosis by modulating of Nrf2 signalling pathway after traumatic brain injury. J Cell Mol Med. 2019;23(6):4088–96. doi: 10.1111/jcmm.14296 30989783
24. Kalinec GM, Webster P, Lim DJ, Kalinec F. A cochlear cell line as an in vitro system for drug ototoxicity screening. Audiology & neuro-otology. 2003;8(4):177–89.
25. Itoh K, Wakabayashi N, Katoh Y, Ishii T, Igarashi K, Engel JD, et al. Keap1 represses nuclear activation of antioxidant responsive elements by Nrf2 through binding to the amino-terminal Neh2 domain. Genes Dev. 1999;13(1):76–86. doi: 10.1101/gad.13.1.76 9887101
26. Ozkul Y, Songu M, Basoglu MS, Ozturkcan S, Katilmis H. Evaluation of the protective effect of alpha-lipoic acid on cisplatin ototoxicity using distortion-product otoacoustic emission measurements: an experimental animal study. The Journal of craniofacial surgery. 2014;25(4):1515–8. doi: 10.1097/SCS.0000000000000881 24905944
27. Morse D, Choi AM. Heme oxygenase-1: from bench to bedside. American journal of respiratory and critical care medicine. 2005;172(6):660–70. doi: 10.1164/rccm.200404-465SO 15901614
28. Ruiz S, Pergola PE, Zager RA, Vaziri ND. Targeting the transcription factor Nrf2 to ameliorate oxidative stress and inflammation in chronic kidney disease. Kidney international. 2013;83(6):1029–41. doi: 10.1038/ki.2012.439 23325084
29. Sea K, Sohn SH, Durazo A, Sheng Y, Shaw BF, Cao X, et al. Insights into the role of the unusual disulfide bond in copper-zinc superoxide dismutase. The Journal of biological chemistry. 2015;290(4):2405–18. doi: 10.1074/jbc.M114.588798 25433341
30. Petronilho F, Florentino D, Danielski LG, Vieira LC, Martins MM, Vieira A, et al. Alpha-Lipoic Acid Attenuates Oxidative Damage in Organs After Sepsis. Inflammation. 2016;39(1):357–65. doi: 10.1007/s10753-015-0256-4 26431839
31. Pinar N, Cakirca G, Ozgur T, Kaplan M. The protective effects of alpha lipoic acid on methotrexate induced testis injury in rats. Biomedicine & pharmacotherapy = Biomedecine & pharmacotherapie. 2018;97:1486–92.
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