N-acetylcysteine versus progesterone on the cisplatin-induced peripheral neurotoxicity

• Autorzy: Zaki S.M. , Mohamed E.A. , Motawie A.G. , Abdel Fattah S.
• Języki publikacji: EN

Abstrakty

EN

Background: Cisplatin-induced peripheral nerve neurotoxicity (CIPN) is the main obstacle in cisplatin treatment. The aim of this study was to compare the modulatory effects of N-acetylcysteine (NAC) and progesterone on CIPN, because there are scarce literature data on the protective effect of the progesterone on the CIPN. Materials and methods: Twenty-four rats were divided into four groups: control, cisplatin-treated, concomitant cisplatin-treated and NAC-treated, and concomitant cisplatin-treated and progesterone-treated. Electron microscopic, immunohistochemical, real time polymerase chain reaction and histomorphometric analysis; oxidative/antioxidative markers (MDA/GSH and SOD), neurotoxic/ neuroprotective markers (iNOS/nNOS), inflammatory mediators (TNF-α and NF-κB) and BAX were done. Results: The myelin sheath in the cisplatin-treated group elucidated infolding. The myelin was disfigured, degenerated, and extensively split with areas of focal loss. The axoplasm was atrophic. Ballooning and vacuolations of the mitochondria with alterations of Remak bundles structures were observed. Fewer of these changes were noted in the NAC and progesterone-treated groups. Decrease of the antioxidant SOD and GSH (81% and 64%) and increase of the oxidant MDA (9 folds), increment of the neurotoxic iNOS (1.9 folds) and decrement of the neuroprotective nNOS (64%) and elevation of the inflammatory mediators’ TNF-a and NF-kB (8.3 and 11 folds) in the cisplatin-treated group. Increase of the antioxidant SOD (1.3 and 2.5 folds) and GSH (120% and 79%) and decrease of the oxidant MDA (69% and 88%), decrement of the neurotoxic iNOS (56% and 68%) and increment of the neuroprotective nNOS (1.6 and one folds) and elevation of the inflammatory mediators’ TNF-a and NF-κB were observed in the NAC and progesterone-treated groups, respectively. Conclusions: The toxic effect of CIPN might be attributed to either oxidative or severe inflammatory stress. Progesterone is efficient in ameliorating these effects; however, NAC is better. (Folia Morphol 2018; 77, 2: 234–245)

• Wydawca: -
• Czasopismo: Folia Morphologica
• Rocznik: 2018
• Tom: 77
• Numer: 2
• Opis fizyczny: p.234–245,fig.,ref.

Twórcy

autor

Zaki S.M.

• Department of Anatomy and Embryology, Faculty of Medicine, Cairo University, Cairo, Egypt

autor

Mohamed E.A.

• Department of Anatomy and Embryology, Faculty of Medicine, Cairo University, Cairo, Egypt

autor

Motawie A.G.

• Department of Anatomy and Embryology, Faculty of Medicine, Cairo University, Cairo, Egypt

autor

Abdel Fattah S.

• Department of Anatomy and Embryology, Faculty of Medicine, Cairo University, Cairo, Egypt

Bibliografia

• 1. Abdel-Wahab WM, Moussa FI, Saad NA. Synergistic protective effect of -acetylcysteine and taurine against cisplatin-induced nephrotoxicity in rats. Drug Des Devel Ther. 2017; 11: 901–908, doi: 10.2147/DDDT.S131316, indexed in Pubmed: 28356716.
• 2. Akman T, Akman L, Erbas O, et al. The preventive effect of oxytocin to Cisplatin-induced neurotoxicity: an experimental rat model. Biomed Res Int. 2015; 2015: 167235, doi: 10.1155/2015/167235, indexed in Pubmed: 25688351.
• 3. Andrabi SS, Parvez S, Tabassum H. Progesterone induces neuroprotection following reperfusion-promoted mitochondrial dysfunction after focal cerebral ischemia in rats. Dis Model Mech. 2017; 10(6): 787–796, doi: 10.1242/dmm.025692, indexed in Pubmed: 28363987.
• 4. Argyriou AA, Bruna J, Marmiroli P, et al. Chemotherapyinduced peripheral neurotoxicity (CIPN): an update. Crit Rev Oncol Hematol. 2012; 82(1): 51–77, doi: 10.1016/j.critrevonc.2011.04.012, indexed in Pubmed: 21908200.
• 5. Balayssac D, Ferrier J, Descoeur J, et al. Chemotherapyinduced peripheral neuropathies: from clinical relevance to preclinical evidence. Expert Opin Drug Saf. 2011; 10(3): 407–417, doi: 10.1517/14740338.2011.543417, indexed in Pubmed: 21210753.
• 6. Birben E, Sahiner UM, Sackesen C, et al. Oxidative stress and antioxidant defense. World Allergy Organ J. 2012; 5(1): 9–19, doi: 10.1097/WOX.0b013e3182439613, indexed in Pubmed: 23268465.
• 7. Bobylev I, Joshi AR, Barham M, et al. Depletion of Mitofusin-2 Causes Mitochondrial Damage in Cisplatin-Induced Neuropathy. Mol Neurobiol. 2018; 55(2): 1227–1235, doi: 10.1007/s12035-016-0364-7, indexed in Pubmed: 28110471.
• 8. Boje KMK. Nitric oxide neurotoxicity in neurodegenerative diseases. Front Biosci. 2004; 9: 763–776, indexed in Pubmed: 14766406.
• 9. Carozzi VA, Marmiroli P, Cavaletti G. The role of oxidative stress and anti-oxidant treatment in platinum-induced peripheral neurotoxicity. Curr Cancer Drug Targets. 2010; 10(7): 670–682, indexed in Pubmed: 20578989.
• 10. Choi YM, Kim HK, Shim W, et al. Mechanism of cisplatininduced cytotoxicity is correlated to impaired metabolism due to mitochondrial ROS generation. PLoS One. 2015; 10(8): e0135083, doi: 10.1371/journal.pone.0135083, indexed in Pubmed: 26247588.
• 11. Dableh LJ, Henry JL. Progesterone prevents development of neuropathic pain in a rat model: Timing and duration of treatment are critical. J Pain Res. 2011; 4: 91–101, doi: 10.2147/JPR.S17009, indexed in Pubmed: 21559355.
• 12. Dawson VL, Dawson TM. Deadly conversations: nuclearmitochondrial cross-talk. J Bioenerg Biomembr. 2004; 36(4): 287–294, doi: 10.1023/B:JOBB.0000041755.22613.8d, indexed in Pubmed: 15377859.
• 13. de Pinto MC, Tommasi F, De Gara L. Changes in the antioxidant systems as part of the signaling pathway responsible for the programmed cell death activated by nitric oxide and reactive oxygen species in tobacco Bright-Yellow 2 cells. Plant Physiol. 2002; 130(2): 698–708, doi: 10.1104/pp.005629, indexed in Pubmed: 12376637.
• 14. Dickey DT, Muldoon LL, Doolittle ND, et al. Effect of N-acetylcysteine route of administration on chemoprotection against cisplatin-induced toxicity in rat models. Cancer Chemother Pharmacol. 2008; 62(2): 235–241, doi: 10.1007/s00280-007-0597-2, indexed in Pubmed: 17909806.
• 15. Drew PD, Chavis JA. Female sex steroids: effects upon microglial cell activation. J Neuroimmunol. 2000; 111(1-2): 77–85, indexed in Pubmed: 11063824.
• 16. Englander EW. DNA damage response in peripheral nervous system: coping with cancer therapy-induced DNA lesions. DNA Repair (Amst). 2013; 12(8): 685–690, doi: 10.1016/j.dnarep.2013.04.020, indexed in Pubmed: 23684797.
• 17. Fang C, Bourdette D, Banker G. Oxidative stress inhibits axonal transport: implications for neurodegenerative diseases. Mol Neurodegener. 2012; 7: 29, doi: 10.1186/1750-1326-7-29, indexed in Pubmed: 22709375.
• 18. Farshid AA, Tamaddonfard E, Najafi S. Effects of histidine and n-acetylcysteine on experimental lesions induced by doxorubicin in sciatic nerve of rats. Drug Chem Toxicol. 2015; 38(4): 436–441, doi: 10.3109/01480545.2014.981753, indexed in Pubmed: 25427688.
• 19. Galluzzi L, Vitale I, Michels J, et al. Systems biology of cisplatin resistance: past, present and future. Cell Death Dis. 2014; 5: e1257, doi: 10.1038/cddis.2013.428, indexed in Pubmed: 24874729.
• 20. George A, Buehl A, Sommer C. Wallerian degeneration after crush injury of rat sciatic nerve increases endo- and epineurial tumor necrosis factor-alpha protein. Neurosci Lett. 2004; 372(3): 215–219, doi: 10.1016/j.neulet.2004.09.075, indexed in Pubmed: 15542243.
• 21. Giordano S, Darley-Usmar V, Zhang J. Autophagy as an essential cellular antioxidant pathway in neurodegenerative disease. Redox Biol. 2014; 2: 82–90, doi: 10.1016/j.redox.2013.12.013, indexed in Pubmed: 24494187.
• 22. Gonzalez Deniselle MC, López-Costa JJ, Saavedra JP, et al. Progesterone neuroprotection in the Wobbler mouse, a genetic model of spinal cord motor neuron disease. Neurobiol Dis. 2002; 11(3): 457–468, indexed in Pubmed: 12586554.
• 23. Hart AM, Terenghi G, Wiberg M, et al. Sensory neuroprotection, mitochondrial preservation, and therapeutic potential of N-acetyl-cysteine after nerve injury. Neuroscience. 2004; 125(1): 91–101, doi: 10.1016/j.neuroscience.2003.12.040, indexed in Pubmed: 15051148.
• 24. Husain MA, Ishqi HM, Sarwar T, et al. Identification and expression analysis of alternatively spliced new transcript isoform of Bax gene in mouse. Gene. 2017; 621: 21–31, doi: 10.1016/j.gene.2017.04.020, indexed in Pubmed: 28412457.
• 25. Jain KK. Drug-induced neurological disorders. 3rd rev. and expanded ed. Cambridge, MA: Hogrefe Pub.; 2012. X, 452.
• 26. Kerksick C, Willoughby D. The antioxidant role of glutathione and N-acetyl-cysteine supplements and exerciseinduced oxidative stress. J Int Soc Sports Nutr. 2005; 2: 38–44, doi: 10.1186/1550-2783-2-2-38, indexed in Pubmed: 18500954.
• 27. Keswani SC, Bosch-Marcé M, Reed N, et al. Nitric oxide prevents axonal degeneration by inducing HIF-1-dependent expression of erythropoietin. Proc Natl Acad Sci USA. 2011; 108(12): 4986–4990, doi: 10.1073/pnas.1019591108, indexed in Pubmed: 21383158.
• 28. Khan M, Sekhon B, Jatana M, et al. Administration of N-acetylcysteine after focal cerebral ischemia protects brain and reduces inflammation in a rat model of experimental stroke. J Neurosci Res. 2004; 76(4): 519–527, doi: 10.1002/jnr.20087, indexed in Pubmed: 15114624.
• 29. Kim HJ, So HS, Lee JH, et al. Role of proinflammatory cytokines in cisplatin-induced vestibular hair cell damage. Head Neck. 2008; 30(11): 1445–1456, doi: 10.1002/hed.20892, indexed in Pubmed: 18642321.
• 30. Kim SJ, Lim JY, Lee JNo, et al. Activation of b-catenin by inhibitors of glycogen synthase kinase-3 ameliorates cisplatin-induced cytotoxicity and pro-inflammatory cytokine expression in HEI-OC1 cells. Toxicology. 2014; 320: 74–82, doi: 10.1016/j.tox.2014.01.013, indexed in Pubmed: 24560772.
• 31. Kobayashi M, To H, Yuzawa M, et al. Effects of dosing time and schedule on cisplatin-induced nephrotoxicity in rats. J Pharm Pharmacol. 2000; 52(10): 1233–1237, indexed in Pubmed: 11092567.
• 32. Lanté F, Meunier J, Guiramand J, et al. Late N-acetylcysteine treatment prevents the deficits induced in the offspring of dams exposed to an immune stress during gestation. Hippocampus. 2008; 18(6): 602–609, doi: 10.1002/hipo.20421, indexed in Pubmed: 18306297.
• 33. Lappas M, Permezel M, Rice GE. N-Acetyl-cysteine inhibits phospholipid metabolism, proinflammatory cytokine release, protease activity, and nuclear factor-kappaB deoxyribonucleic acid-binding activity in human fetal membranes in vitro. J Clin Endocrinol Metab. 2003; 88(4): 1723–1729, doi: 10.1210/jc.2002-021677, indexed in Pubmed: 12679464.
• 34. Lin H, Heo BHa, Yoon MHa. A New Rat Model of Cisplatininduced Neuropathic Pain. Korean J Pain. 2015; 28(4): 236–243, doi: 10.3344/kjp.2015.28.4.236, indexed in Pubmed: 26495078.
• 35. Low PA, Nickander KK, Tritschler HJ. The roles of oxidative stress and antioxidant treatment in experimental diabetic neuropathy. Diabetes. 1997; 46(Supplement_2): S38–S42, doi: 10.2337/diab.46.2.s38.
• 36. Melli G, Taiana M, Camozzi F, et al. Alpha-lipoic acid prevents mitochondrial damage and neurotoxicity in experimental chemotherapy neuropathy. Exp Neurol. 2008; 214(2): 276–284, doi: 10.1016/j.expneurol.2008.08.013, indexed in Pubmed: 18809400.
• 37. Meyer A, Laverny G, Allenbach Y, et al. IFN-beta-induced reactive oxygen species and mitochondrial damage contribute to muscle impairment and inflammation maintenance in dermatomyositis. Acta Neuropathol. 2017; 134(4): 655–666, doi: 10.1007/s00401-017-1731-9, indexed in Pubmed: 28623559.
• 38. Moorthy K, Sharma D, Basir SF, et al. Administration of estradiol and progesterone modulate the activities of antioxidant enzyme and aminotransferases in naturally menopausal rats. Exp Gerontol. 2005; 40(4): 295–302, doi: 10.1016/j.exger.2005.01.004, indexed in Pubmed: 15820610.
• 39. Owen JB, Butterfield DA. Measurement of oxidized/reduced glutathione ratio. Methods Mol Biol. 2010; 648: 269–277, doi: 10.1007/978-1-60761-756-3_18, indexed in Pubmed: 20700719.
• 40. Park HJ, Stokes JA, Pirie E, et al. Persistent hyperalgesia in the cisplatin-treated mouse as defined by threshold measures, the conditioned place preference paradigm, and changes in dorsal root ganglia activated transcription factor 3: the effects of gabapentin, ketorolac, and etanercept. Anesth Analg. 2013; 116(1): 224–231, doi: 10.1213/ANE.0b013e31826e1007, indexed in Pubmed: 23223118.
• 41. Park HJ. Chemotherapy induced peripheral neuropathic pain. Korean J Anesthesiol. 2014; 67(1): 4–7, doi: 10.4097/kjae.2014.67.1.4, indexed in Pubmed: 25097731.
• 42. Phensy A, Driskill C, Lindquist K, et al. Antioxidant treatment in male mice prevents mitochondrial and synaptic changes in an NMDA receptor dysfunction model of schizophrenia. eNeuro. 2017; 4(4), doi: 10.1523/ENEURO.0081-17.2017, indexed in Pubmed: 28819639.
• 43. Reid AJ, Shawcross SG, Hamilton AE, et al. N-acetylcysteine alters apoptotic gene expression in axotomised primary sensory afferent subpopulations. Neurosci Res. 2009; 65(2): 148–155, doi: 10.1016/j.neures.2009.06.008, indexed in Pubmed: 19559059.
• 44. Roof RL, Duvdevani R, Braswell L, et al. Progesterone facilitates cognitive recovery and reduces secondary neuronal loss caused by cortical contusion injury in male rats. Exp Neurol. 1994; 129(1): 64–69, doi: 10.1006/exnr.1994.1147, indexed in Pubmed: 7925843.
• 45. Roof RL, Duvdevani R, Heyburn JW, et al. Progesterone rapidly decreases brain edema: treatment delayed up to 24 hours is still effective. Exp Neurol. 1996; 138(2): 246–251, doi: 10.1006/exnr.1996.0063, indexed in Pubmed: 8620923.
• 46. Rybak LP, Kelly T. Ototoxicity: bioprotective mechanisms. Curr Opin Otolaryngol Head Neck Surg. 2003; 11(5): 328–333, indexed in Pubmed: 14502062.
• 47. Sahu BD, Kuncha M, Putcha UK, et al. Effect of metformin against cisplatin induced acute renal injury in rats: a biochemical and histoarchitectural evaluation. Exp Toxicol Pathol. 2013; 65(6): 933–940, doi: 10.1016/j.etp.2013.01.007, indexed in Pubmed: 23395153.
• 48. Sandireddy R, Yerra VG, Areti A, et al. Neuroinflammation and oxidative stress in diabetic neuropathy: futuristic strategies based on these targets. Int J Endocrinol. 2014; 2014: 674987, doi: 10.1155/2014/674987, indexed in Pubmed: 24883061.
• 49. Seto Y, Okazaki F, Horikawa K, et al. Influence of dosing times on cisplatin-induced peripheral neuropathy in rats. BMC Cancer. 2016; 16(1): 756, doi: 10.1186/s12885-016-2777-0, indexed in Pubmed: 27678475.
• 50. Stein DG. Progesterone exerts neuroprotective effects after brain injury. Brain Res Rev. 2008; 57(2): 386–397, doi: 10.1016/j.brainresrev.2007.06.012, indexed in Pubmed: 17826842.
• 51. VanLandingham JW, Cekic M, Cutler S, et al. Neurosteroids reduce inflammation after TBI through CD55 induction. Neurosci Lett. 2007; 425(2): 94–98, doi: 10.1016/j.neulet.2007.08.045, indexed in Pubmed: 17826908.
• 52. Wang XM, Lehky TJ, Brell JM, et al. Discovering cytokines as targets for chemotherapy-induced painful peripheral neuropathy. Cytokine. 2012; 59(1): 3–9, doi: 10.1016/j.cyto.2012.03.027, indexed in Pubmed: 22537849.
• 53. 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(2): 424–431, doi: 10.1124/jpet.104.075119, indexed in Pubmed: 15496615.
• 54. Yang X, Fraser M, Moll UM, et al. Akt-mediated cisplatin resistance in ovarian cancer: modulation of p53 action on caspase-dependent mitochondrial death pathway. Cancer Res. 2006; 66(6): 3126–3136, doi: 10.1158/0008-5472. CAN-05-0425, indexed in Pubmed: 16540663.
• 55. Zhu J, Carozzi VA, Reed N, et al. Ethoxyquin provides neuroprotection against cisplatin-induced neurotoxicity. Sci Rep. 2016; 6: 28861, doi: 10.1038/srep28861, indexed in Pubmed: 27350330.

Identyfikatory

DOI

10.5603/FM.a2017.0090