Anti-inflammatory and anti-apoptotic effects of hyperbaric oxygen preconditioning in a rat model of cisplatin-induced peripheral neuropathy

Document Type: Original Article

Authors

1 Molecular and Cell Biology Research Center, Department of Anatomy, Faculty of Medicine, Mazandaran University of Medical Sciences, Sari, Iran

2 Cellular and Molecular Research Center, Iran University of Medical Sciences, Tehran, Iran

3 Neuroscience Research Center, Iran University of Medical Sciences, Tehran, Iran

4 Department of Biochemistry, Faculty of Medicine, Lorestan University of Medical Sciences, Khorramabad, Iran

5 Razi Herbal Researches Center, Lorestan University of Medical Sciences, Khorramabad, Iran

6 Immunogenetic Research Center and Department of Physiology and Pharmacology, Faculty of Medicine, Mazandaran University of Medical Sciences, Sari, Iran

Abstract

Objective(s): Cisplatin-induced peripheral neuropathy is a debilitating side effect in patients receiving this drug.  Recent studies suggest hyperbaric oxygen (HBO) therapy as a new treatment approach for models of neural injury. The aim of the current study was to determine the protective effects of HBO preconditioning against peripheral neuropathy induced by Cisplatin (CDDP).
Materials and Methods: The present study was conducted on 4 groups of rats: Sham group; HBO group (60 min/d); Control group (CDDP 2 mg/kg/d); Precondition group (HBO+CDDP). Mechanical threshold testing was weekly carried out using von Frey filament. Sciatic nerve and associated ganglia were removed  five weeks after the first CDDP injection for biochemical evaluation of malondialdehyde (MDA) content and myeloperoxidase (MPO) activity, immunohistochemistry of terminal deoxynucleotidyl transferase dUTP nick end labeling (TUNEL), TNF-α, caspase-3 and  iNOS, and transmission electron microscopic (TEM) assessments.
Results: MDA levels and MPO activities were significantly decreased in preconditioned rats. Attenuated TUNEL reaction along with attenuated caspase-3, TNF-α, and iNOS expression could be significantly detected in preconditioned rats. Also, HBO preconditioning improved the nociceptive threshold.
Conclusion: The results suggest that HBO preconditioning can attenuate peripheral neuropathy caused by cisplatin in rats.

Keywords


1. Quasthoff S, Hartung HP. Chemotherapy-induced peripheral neuropathy. J Neurol 2002; 249:9-17.
2. Starobova H, Vetter I. Pathophysiology of chemotherapy-induced peripheral neuropathy. Front Mol Neurosci 2017; 10:174.
3. Cavaletti G, Tredici G, Marmiroli P,  Petruccioli MG, Barajon I, Fabbrica D. Morphometric study of the sensory neuron and peripheral nerve changes induced by chronic cisplatin (DDP) administration in rats. Acta Neuropathol 1992; 84:364-371.
4. McDonald ES, Randon KR, Knight A, Windebank AJ. Cisplatin preferentially binds to DNA in dorsal root ganglion neurons in vitro and in vivo: a potential mechanism for neurotoxicity. Neurobiol Dis 2005; 18:305-313.
5. Sugimoto T, Takeyama A, Fujita M, Ichikawa H, Takano-Yamamoto  T. Peripheral neuroglial death induced by cisplatin administration in newborn rats. Neuroreport 2001; 12:137-140.
6. Podratz JL, Knight AM, Ta LE, Staff NP, Gass JM, Genelin K, at al. Cisplatin induced mitochondrial DNA damage in dorsal root ganglion neurons. Neurobiol Dis 2011; 41:661–668.
7. Marullo R, Werner E, Degtyareva N, Moore B, Altavilla G, Ramalingam SS, et al. Cisplatin induces a mitochondrial-ROS response that contributes to cytotoxicity depending on mitochondrial redox status and bioenergetic functions. PLoS One 2013; 8:e81162.
8. Agthong S, Kaewsema A, Charoensub T. Curcumin ameliorates functional and structural abnormalities in cisplatin-induced neuropathy. Exp Neurobiol 2015; 24:139-145.
9. Melli G, Taiana M, Camozzi  F, Triolo D, Podini P, Quattrini A, et al. Alpha-lipoic acid prevents mitochondrial damage and neurotoxicity in experimental chemotherapy neuropathy. Exp Neurol 2008; 214:276-284.
10. Zhou BC, Liu LJ, Liu B.  Neuroprotection of hyperbaric oxygen therapy in sub-acute traumatic brain injury: not by immediately improving cerebral oxygen saturation and oxygen partial pressure. Neural Regen Res 2016; 11:1445-1449.
11. Huang H, Xue L, Zhang X, Weng Q, Chen H, Gu J, et al. Hyperbaric oxygen therapy provides neuroprotection following spinal cord injury in a rat model. Int J Clin Exp Pathol 2013; 6:1337-1342.
12. Chazalviel L, Haelewyn B, Degoulet M, Blatteau JE, Vallée N, Risso JJ, et al. Hyperbaric oxygen increases tissue-plasminogen activator-induced thrombolysis in vitro, and reduces ischemic brain damage and edema in rats subjected to thromboembolic brain ischemia. Med Gas Res 2016; 6:64-69.
13. Xu J, Huang G, Zhang K, Sun J, Xu T, Li R, et al. Nrf2 activation in astrocytes contributes to spinal cord ischemic tolerance induced by hyperbaric oxygen preconditioning. J Neurotrauma 2014; 31:1343-1353.
14. Chen X, Li Y, Chen W, Nong Z, Huang J, Chen C. Protective effect of hyperbaric oxygen on cognitive impairment induced by D-Galactose in mice. Neurochem Res 2016; 41:3032-3041.
15. Pan X, Chen C, Huang J, Wei H, Fan Q. Neuroprotective effect of combined therapy with hyperbaric oxygen and madopar on 6-hydroxydopamine-induced Parkinson’s disease in rats. Neurosci Lett 2015; 600:220-225.
16. Han G, Li L, Meng LX. Effects of hyperbaric oxygen on pain-related behaviors and nitric oxide synthase in a rat model of neuropathic pain. Pain Res Manag 2013; 18:137-141.
17. Shams Z, Khalatbary AR, Ahmadvand H, Zare Z, Kian K. Neuroprotective effects of hyperbaric oxygen (HBO) therapy on neuronal death induced by sciatic nerve transection in rat. BMC Neurol 2017; 17: 220.
18. Li J, Liu W, Ding S, Xu W, Guan Y, Zhang JH, et al. Hyperbaric oxygen preconditioning induces tolerance against brain ischemia-reperfusion injury by upregulation of antioxidant enzymes in rats. Brain Res 2008; 1210:223-229.
19. Yang ZJ, Xie Y, Bosco GM, Chen C, Camporesi EM. Hyperbaric oxygenation alleviates MCAO-induced brain injury and reduces hydroxyl radical formation and glutamate release. Eur J Appl Physiol 2010; 108:513-522.
20. Yang L, Tang J, Chen Q, Jiang B, Zhang B, Tao Y, et al. Hyperbaric oxygen preconditioning attenuates neuroinflammation after intracerebral hemorrhage in rats by regulating microglia characteristics. Brain Res 2015; 1627:21-30.
21. Lin KC, Niu KC, Tsai KJ, Kuo JR, Wang LC, Chio CC, et al. Attenuating inflammation but stimulating both angiogenesis and neurogenesis using hyperbaric oxygen in rats with traumatic brain injury. J Trauma Acute Care Surg 2012; 72:650-659.
22. Wee HY, Lim SW, Chio CC, Niu KC, Wang CC, Kuo JR. Hyperbaric oxygen effects on neuronal apoptosis associations in a traumatic brain injury rat model. J Surg Res 2015; 197:382-389.
23. Lu PG, Feng H, Yuan SJ, Zhang RW, Li M, Hu R, et al. Effect of preconditioning with hyperbaric oxygen on neural cell apoptosis after spinal cord injury in rats. J Neurosurg Sci 2013; 57:253-258.
24. Sunami K, Takeda Y, Hashimoto M, Hirakawa M. Hyperbaric oxygen reduces infarct volume in rats by increasing oxygen supply to the ischemic periphery. Crit Care Med 2000; 28:2831-2836.
25. Calvert JW, Cahill J, Zhang JH. Hyperbaric oxygen and cerebral physiology. Neurol Res 2007; 29:132-141.
26. Aydinoz S, Uzun G, Cermik H, Atasoyu EM, Yildiz S, Karagoz B, et al. Effects of different doses of hyperbaric oxygen on cisplatin-induced nephrotoxicity. Ren Fail 2007; 29:257-263.
27. Atasoyu EM, Yildiz S, Bilgi O, Cermik H, Evrenkaya R, Aktas S, et al. Investigation of the role of hyperbaric oxygen therapy in cisplatin-induced nephrotoxicity in rats. Arch Toxicol 2005; 79:289-293.
28. Yassuda CC, Righetti  AE, Cury MC, Hyppolito MA, Oliveira JA, Féres O. The role of hyperbaric oxygen therapy (hot) as an otoprotection agent against cisplatin ototoxicity. Acta Cir Bras 2008; 23:72-76.
29. Cobanoglu HB, Vuralkan E, Arslan A, Mirasoglu B, Toklu AS. Is hyperbaric oxygen therapy effective in cisplatin-induced ototoxicity in rats?.  Clin Exp Otorhinolaryngol 2019; 12:66-71.
30. Bianchi R, Gilardini A, Rodriguez-Menendez V, Oggioni N, Canta A, Colombo T, et al. Cisplatin-induced peripheral neuropathy: neuroprotection by erythropoietin without affecting tumour growth. Eur J Cancer 2007; 43:710-717.
31. Bianchi R, Brines M, Lauria G, Savino C, Gilardini A, Nicolini G, et al. Protective effect of erythropoietin and its carbamylated derivative in experimental Cisplatin peripheral neurotoxicity. Clin Cancer Res 2006; 12:2607-2612.
32. Zhao BS, Song XR, Hu PY, Meng LX, Tan YH, She YJ, et al. Hyperbaric oxygen treatment at various stages following chronic constriction injury produces different antinociceptive effects via regulation of P2X4R expression and apoptosis. PLoS One 2015; 10:e0120122.
33. Chaplan SR, Bach FW, Pogrel JW, Chung JM, Yaksh TL.  Quantitative assessment of tactile allodynia in the rat paw. J Neurosci Methods. 1994; 53:55-63.
34. Mihara M, Uchiyama M. Determination of malonaldehyde precursor in tissues by thiobarbituric acid test. Anal Biochem 1978; 86:271-278.
35. Mullane K. Neutrophil-platelet interactions and post-ischemic myocardial injury. Prog Clin Biol Res 1989; 301:39-51.
36. Kato N, Matsumoto M, Kogawa M, Atkins GJ, Findlay DM, Fujikawa T, et al. Critical role of p38 MAPK for regeneration of the sciatic nerve following crush injury in vivo. J Neuroinflammation 2013; 10:1.
37. Kanat O, Ertas H, Caner B. Platinum-induced neurotoxicity: A review of possible mechanisms. World J Clin Oncol 2017; 8:329-335.
38. Gill JS, Windebank AJ. Cisplatin-induced apoptosis in rat dorsal root ganglion neurons is associated with attempted entry into the cell cycle. J Clin Invest 1998; 101:2842-2850.
39. Li JS, Zhang W, Kang ZM, Ding SJ, Liu WW, Zhang JH, et al. Hyperbaric oxygen preconditioning reduces ischemia-reperfusion injury by inhibition of apoptosis via mitochondrial pathway in rat brain. Neuroscience 2009; 159:1309-1315.
40. Ostrowski RP, Graupner G, Titova E, Zhang J, Chiu J, Dach N, et al. The hyperbaric oxygen preconditioning-induced brain protection is mediated by a reduction of early apoptosis after transient global cerebral ischemia. Neurobiol Dis 2008; 29:1-13.
41. Lou M, Chen Y, Ding M, Eschenfelder CC, Deuschl G. Involvement of the mitochondrial ATP-sensitive potassium channel in the neuroprotective effect of hyperbaric oxygenation after cerebral ischemia. Brain Res Bull 2006; 69:109-116.
42. Long Y, Liang F, Gao C, Li Z, Yang J. Hyperbaric oxygen therapy reduces apoptosis after spinal cord injury in rats. Int J Clin Exp Med 2014; 7:4073-4081.
43. Liu X, Yang J, Li Z, Liang F, Wang Y, Su Q, et al. Hyperbaric oxygen treatment protects against spinal cord injury by inhibiting endoplasmic reticulum stress in rats. Spine 2015; 40:E1276-1283.
44. Zhou Y, Liu XH, Qu SD, Yang J, Wang ZW, Gao CJ, et al. Hyperbaric oxygen intervention on expression of hypoxia-inducible factor-1α and vascular endothelial growth factor in spinal cord injury models in rats. Chin Med J 2013; 126:3897-3903.
45. Fu H, Li F, Thomas S, Yang Z. Hyperbaric oxygenation alleviates chronic constriction injury (CCI)-induced neuropathic pain and inhibits GABAergic neuron apoptosis in the spinal cord. Scand J Pain 2017; 17:330-338.
46. Hu Q, Fang L, Li F, Thomas S, Yang Z. Hyperbaric oxygenation treatment alleviates CCI-induced neuropathic pain and decreases spinal apoptosis. Eur J Pain 2015; 19:920-928.
47. Areti A, Yerra VG, Naidu V, Kumar A.  Oxidative stress and nerve damage: role in chemotherapy induced peripheral neuropathy. Redox Biol 2014; 2:289-295.
48. Low PA, Nickander KK, Tritschler HJ.  The roles of oxidative stress and antioxidant treatment in experimental diabetic neuropathy. Diabetes 1997; 46:S38-42.
49. Khalil Z, Khodr B. A role for free radicals and nitric oxide in delayed recovery in aged rats with chronic constriction nerve injury. Free Radic Biol Med 2001; 31:430–439.
50. Xiao WH, Bennett GJ. Effects of mitochondrial poisons on the neuropathic pain produced by the chemotherapeutic agents, paclitaxel and oxaliplatin. Pain 2012; 153:704-709.
51. Gilardini A, Avila RL, Oggioni N, Rodriguez-Menendez V, Bossi M, Canta A, et al. Myelin structure is unaltered in chemotherapy-induced peripheral neuropathy. Neurotoxicology 2012; 33:1-7.
52. Zhao B, Meng LX, Ding YY, Cao YY. Hyperbaric oxygen treatment produces an antinociceptive response phase and inhibits astrocyte activation and inflammatory response in a rat model of neuropathic pain. J Mol Neurosc 2014; 53:251–261.
53. Cámara-Lemarroy CR, Guzmán-de la Garza FJ, Fernández-Garza NE. Molecular inflammatory mediators in peripheral nerve degeneration and regeneration. Neuroimmunomodulation 2010; 17:314-324.
54. Ding Y, Yao P, Hong T, Li H, Zhu Y, Han Z, et al. The analgesic effect of early hyperbaric oxygen treatment in chronic constriction injury rats and its influence on nNOS and iNOS expression and inflammatory factor production. Mol Pain 2018; 14:1744806918765837.
55. Li F, Fang L, Huang S, Yang Z, Nandi J, Thomas S, et al. Hyperbaric oxygenation therapy alleviates chronic constrictive injury-induced neuropathic pain and reduces tumor necrosis factor-alpha production. Anesth Analg 2011; 113:626-633.
56. Cheng O, Ostrowski RP, Wu B, Liu W, Chen C, Zhang JH. Cyclooxygenase-2 mediates hyperbaric oxygen preconditioning in the rat model of transient global cerebral ischemia. Stroke 2011; 42:484-490.
57. Miao T, Meng X, He H, Ji X. Antiallodynic effect of hyperbaric oxygen on paclitaxel-induced peripheral neuropathy in a model of rat and its mechanism. Open Access Library Journal 2019; 6:e5339.
58. Jensen TS, Baron R. Translation of symptoms and signs into mechanisms in neuropathic pain. Pain 2003; 102:1-8.
59. Hu Q, Manaenko A, Matei N, Guo Z, Xu T, Tang J, et al. Hyperbaric oxygen preconditioning: a reliable option for neuroprotection. Med Gas Res 2016; 6:20-32.
60. Liu YD, Wang ZB, Han G, Jin L, Zhao P. Hyperbaric oxygen relieves neuropathic pain through AKT/TSC2/mTOR pathway activity to induce autophagy. J Pain Res 2019; 12:443–451.
61. Ding Y, Yao P, Hong T, Han Z, Zhao B, Chen W. The NO-cGMP-PKG signal transduction pathway is involved in the analgesic effect of early hyperbaric oxygen treatment of neuropathic pain. J Headache Pain 2017; 18:51.
62. Zhao B, Pan Y, Xu H, Song X.  Hyperbaric oxygen attenuates neuropathic pain and reverses inflammatory signaling likely via the Kindlin-1/Wnt-10a signaling pathway in the chronic pain injury model in rats. J Headache Pain 2017; 18:1.