DOI QR코드

DOI QR Code

Antinociceptive effects of oleuropein in experimental models of neuropathic pain in male rats

  • Chen, Huayong (Department of Anesthesiology, Yidu Central Hospital of Weifang) ;
  • Ma, Dandan (Department of Anesthesiology, Yidu Central Hospital of Weifang) ;
  • Zhang, Huapeng (Department of Anesthesiology, Yidu Central Hospital of Weifang) ;
  • Tang, Yanhong (Department of Anesthesiology, Hospital T.C.M Affiliated to Southwest Medical University) ;
  • Wang, Jun (Orbital Disease and Ophthalmoplasty, Department of Ophthalmological Hospital, The Second Hospital of Jilin) ;
  • Li, Renhu (Department of Anesthesiology, The Lu'an Affiliated Hospital of Anhui Medical University) ;
  • Wen, Wen (Department of Anesthesiology, Affiliated Hospital of Guilin Medical University) ;
  • Zhang, Yi (Department of Anesthesiology, Tongji Hospital Affiliated Tongji Medical College, Huazhong Science and Technology University)
  • Received : 2020.09.24
  • Accepted : 2020.11.17
  • Published : 2021.01.01

Abstract

Background: The present investigation explored the therapeutic actions of oleuropein along with the possible signaling pathway involved in attenuating neuropathic pain in chronic constriction injury (CCI) and vincristine-induced neuropathic pain in male rats. Methods: Four loose ligatures were placed around the sciatic nerve to induce CCI, and vincristine (50 ㎍/kg) was injected for 10 days to develop neuropathic pain. The development of cold allodynia, mechanical allodynia, and mechanical hyperalgesia was assessed using different pain-related behavioral tests. The levels of H2S, cystathionine-γ-lyase (CSE), cystathionine-β-synthase (CBS), orexin, and nuclear factor erythroid-2-related factor 2 (Nrf2) were measured in the sciatic nerve. Results: Treatment with oleuropein for 14 days led to significant amelioration of behavioral manifestations of neuropathic pain in two pain models. Moreover, oleuropein restored both CCI and vincristine-induced decreases in H2S, CSE, CBS, orexin, and Nrf2 levels. Co-administration of suvorexant, an orexin receptor antagonist, significantly counteracted the pain-attenuating actions of oleuropein and Nrf2 levels without modulating H2S, CSE and CBS. Conclusions: Oleuropein has therapeutic potential to attenuate the pain manifestations in CCI and vincristine-induced neuropathic pain, possibly by restoring the CSE, CBS, and H2S, which may subsequently increase the expression of orexin and Nrf2 to ameliorate behavioral manifestations of pain.

Keywords

References

  1. Zilliox LA. Neuropathic Pain. Continuum (Minneap Minn) 2017; 23(2, Selected Topics in Outpatient Neurology): 512-32. https://doi.org/10.1212/con.0000000000000462
  2. Badr AM, Attia HA, Al-Rasheed N. Oleuropein reverses repeated corticosterone-induced depressive-like behavior in mice: evidence of modulating effect on biogenic amines. Sci Rep 2020; 10: 3336. https://doi.org/10.1038/s41598-020-60026-1
  3. Mohammad-Beigi H, Aliakbari F, Sahin C, Lomax C, Tawfike A, Schafer NP, et al. Oleuropein derivatives from olive fruit extracts reduce α-synuclein fibrillation and oligomer toxicity. J Biol Chem 2019; 294: 4215-32. https://doi.org/10.1074/jbc.ra118.005723
  4. Fki I, Sayadi S, Mahmoudi A, Daoued I, Marrekchi R, Ghorbel H. Comparative study on beneficial effects of hydroxytyrosol- and oleuropein-rich olive leaf extracts on high-fat diet-induced lipid metabolism disturbance and liver injury in rats. Biomed Res Int 2020; 2020: 1315202.
  5. Czerwinska ME, Gasinska E, Lesniak A, Krawczyk P, Kiss AK, Naruszewicz M, et al. Inhibitory effect of Ligustrum vulgare leaf extract on the development of neuropathic pain in a streptozotocin-induced rat model of diabetes. Phytomedicine 2018; 49: 75-82. https://doi.org/10.1016/j.phymed.2018.06.006
  6. Mao X, Xia B, Zheng M, Zhou Z. Assessment of the anti-inflammatory, analgesic and sedative effects of oleuropein from Olea europaea L. Cell Mol Biol (Noisy-le-grand) 2019; 65: 52-5. https://doi.org/10.14715/cmb/2019.65.1.9
  7. Zare L, Esmaeili-Mahani S, Abbasnejad M, Rasoulian B, Sheibani V, Sahraei H, et al. Oleuropein, chief constituent of olive leaf extract, prevents the development of morphine antinociceptive tolerance through inhibition of morphineinduced L-type calcium channel overexpression. Phytother Res 2012; 26: 1731-7. https://doi.org/10.1002/ptr.4634
  8. Linden DR. Hydrogen sulfide signaling in the gastrointestinal tract. Antioxid Redox Signal 2014; 20: 818-30. https://doi.org/10.1089/ars.2013.5312
  9. Wu D, Hu Q, Zhu D. An update on hydrogen sulfide and nitric oxide interactions in the cardiovascular system. Oxid Med Cell Longev 2018; 2018: 4579140. https://doi.org/10.1155/2018/4579140
  10. Sheibani L, Lechuga TJ, Zhang H, Hameed A, Wing DA, Kumar S, et al. Augmented H2S production via cystathionine-beta-synthase upregulation plays a role in pregnancy-associated uterine vasodilation. Biol Reprod 2017; 96: 664-72. https://doi.org/10.1095/biolreprod.116.143834
  11. Lin JQ, Luo HQ, Lin CZ, Chen JZ, Lin XZ. Sodium hydrosulfide relieves neuropathic pain in chronic constriction injured rats. Evid Based Complement Alternat Med 2014; 2014: 514898.
  12. Chen H, Xie K, Chen Y, Wang Y, Wang Y, Lian N, et al. Nrf2/HO-1 signaling pathway participated in the protection of hydrogen sulfide on neuropathic pain in rats. Int Immunopharmacol 2019; 75: 105746. https://doi.org/10.1016/j.intimp.2019.105746
  13. Lucarini E, Micheli L, Trallori E, Citi V, Martelli A, Testai L, et al. Effect of glucoraphanin and sulforaphane against chemotherapy-induced neuropathic pain: Kv7 potassium channels modulation by H2 S release in vivo. Phytother Res 2018; 32: 2226-34. https://doi.org/10.1002/ptr.6159
  14. Mieda M. The roles of orexins in sleep/wake regulation. Neurosci Res 2017; 118: 56-65. https://doi.org/10.1016/j.neures.2017.03.015
  15. Suyama H, Kawamoto M, Shiraishi S, Gaus S, Kajiyama S, Yuge O. Analgesic effect of intrathecal administration of orexin on neuropathic pain in rats. In Vivo 2004; 18: 119-23.
  16. Toyama S, Shimoyama N, Shimoyama M. The analgesic effect of orexin-A in a murine model of chemotherapy-induced neuropathic pain. Neuropeptides 2017; 61: 95-100. https://doi.org/10.1016/j.npep.2016.12.007
  17. Kajiyama S, Kawamoto M, Shiraishi S, Gaus S, Matsunaga A, Suyama H, et al. Spinal orexin-1 receptors mediate antihyperalgesic effects of intrathecally-administered orexins in diabetic neuropathic pain model rats. Brain Res 2005; 1044: 76-86. https://doi.org/10.1016/j.brainres.2005.03.007
  18. Ma Q. Role of nrf2 in oxidative stress and toxicity. Annu Rev Pharmacol Toxicol 2013; 53: 401-26. https://doi.org/10.1146/annurev-pharmtox-011112-140320
  19. Yetik-Anacak G, Sevin G, Ozzayim O, Dereli MV, Ahmed A. Hydrogen sulfide: a novel mechanism for the vascular protection by resveratrol under oxidative stress in mouse aorta. Vascul Pharmacol 2016; 87: 76-82. https://doi.org/10.1016/j.vph.2016.08.003
  20. Wang Z, Yan Y, Wang Y, Tong F. The interaction between CSE/H2S and the iNOS/NO-mediated resveratrol/poly(ethylene glycol)-poly(phenylalanine) complex alleviates intestinal ischemia/reperfusion injuries in diabetic rats. Biomed Pharmacother 2019; 112: 108736. https://doi.org/10.1016/j.biopha.2019.108736
  21. Vitalone A, Di Sotto A, Mammola CL, Heyn R, Miglietta S, Mariani P, et al. Phytochemical analysis and effects on ingestive behaviour of a Caralluma fimbriata extract. Food Chem Toxicol 2017; 108(Pt A): 63-73. https://doi.org/10.1016/j.fct.2017.07.027
  22. Guo C, Bi J, Li X, Lyu J, Liu X, Wu X, et al. Immunomodulation effects of polyphenols from thinned peach treated by different drying methods on RAW264.7 cells through the NF-κB and Nrf2 pathways. Food Chem 2021; 340: 127931. https://doi.org/10.1016/j.foodchem.2020.127931
  23. Castejon ML, Sanchez-Hidalgo M, Aparicio-Soto M, Montoya T, Martin-LaCave I, Fernandez-Bolanos JG, et al. Dietary oleuropein and its new acyl-derivate attenuate murine lupus nephritis through HO-1/Nrf2 activation and suppressing JAK/STAT, NF-κB, MAPK and NLRP3 inflammasome signaling pathways. J Nutr Biochem 2019; 74: 108229. https://doi.org/10.1016/j.jnutbio.2019.108229
  24. Sanchez-Alavez M, Benedict J, Wills DN, Ehlers CL. Effect of suvorexant on event-related oscillations and EEG sleep in rats exposed to chronic intermittent ethanol vapor and protracted withdrawal. Sleep 2019; 42: zsz020.
  25. Janahmadi Z, Nekooeian AA, Moaref AR, Emamghoreishi M. Oleuropein attenuates the progression of heart failure in rats by antioxidant and antiinflammatory effects. Naunyn Schmiedebergs Arch Pharmacol 2017; 390: 245-52. https://doi.org/10.1007/s00210-016-1323-6
  26. Bennett GJ, Xie YK. A peripheral mononeuropathy in rat that produces disorders of pain sensation like those seen in man. Pain 1988; 33: 87-107. https://doi.org/10.1016/0304-3959(88)90209-6
  27. Ma L, Liu H, Chen G, Chen M, Wang L, Zhang X, et al. Sulfasalazine attenuates chronic constriction injury-induced neuroinflammation and mechanical hypersensitivity in rats. Neurosci Lett 2018; 683: 174-80. https://doi.org/10.1016/j.neulet.2018.07.042
  28. Shibayama M, Kuniyoshi K, Suzuki T, Yamauchi K, Ohtori S, Takahashi K. The effects of locally injected triamcinolone on entrapment neuropathy in a rat chronic constriction injury model. J Hand Surg Am 2014; 39: 1714-21. https://doi.org/10.1016/j.jhsa.2014.05.026
  29. Khangura RK, Bali A, Kaur G, Singh N, Jaggi AS. Neuropathic pain attenuating effects of perampanel in an experimental model of chronic constriction injury in rats. Biomed Pharmacother 2017; 94: 557-63. https://doi.org/10.1016/j.biopha.2017.07.137
  30. Siau C, Bennett GJ. Dysregulation of cellular calcium homeostasis in chemotherapy-evoked painful peripheral neuropathy. Anesth Analg 2006; 102: 1485-90. https://doi.org/10.1213/01.ane.0000204318.35194.ed
  31. Selawry OS, Hananian J. Vincristine treatment of cancer in children. JAMA 1963; 183: 741-6.
  32. Gilchrist L, Tanner L. Gait patterns in children with cancer and vincristine neuropathy. Pediatr Phys Ther 2016; 28: 16-22. https://doi.org/10.1097/PEP.0000000000000208
  33. Vashistha B, Sharma A, Jain V. Ameliorative potential of ferulic acid in vincristine-induced painful neuropathy in rats: an evidence of behavioral and biochemical examination. Nutr Neurosci 2017; 20: 60-70. https://doi.org/10.1179/1476830514y.0000000165
  34. Choi Y, Yoon YW, Na HS, Kim SH, Chung JM. Behavioral signs of ongoing pain and cold allodynia in a rat model of neuropathic pain. Pain 1994; 59: 369-76. https://doi.org/10.1016/0304-3959(94)90023-X
  35. 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. https://doi.org/10.1016/0165-0270(94)90144-9
  36. Wang G, Yang Y, Wang C, Huang J, Wang X, Liu Y, et al. Exploring the role and mechanisms of diallyl trisulfide and diallyl disulfide in chronic constriction-induced neuropathic pain in rats. Korean J Pain 2020; 33: 216-25. https://doi.org/10.3344/kjp.2020.33.3.216
  37. Xie T, Zhang J, Kang Z, Liu F, Lin Z. miR-101 down-regulates mTOR expression and attenuates neuropathic pain in chronic constriction injury rat models. Neurosci Res 2020; 158: 30-6. https://doi.org/10.1016/j.neures.2019.09.002
  38. Yamamoto S, Suzuki Y, Ono H, Kume K, Ohsawa M. N- and L-type calcium channels blocker cilnidipine ameliorates neuropathic pain. Eur J Pharmacol 2016; 793: 66-75. https://doi.org/10.1016/j.ejphar.2016.11.001
  39. Shen X, Chakraborty S, Dugas TR, Kevil CG. Hydrogen sulfide measurement using sulfide dibimane: critical evaluation with electrospray ion trap mass spectrometry. Nitric Oxide 2014; 41: 97-104. https://doi.org/10.1016/j.niox.2014.06.002
  40. Lowry OH, Rosebrough NJ, Farr AL, Randall RJ. Protein measurement with the Folin phenol reagent. J Biol Chem 1951; 193: 265-75. https://doi.org/10.1016/S0021-9258(19)52451-6
  41. Kim YH, Choi YJ, Kang MK, Lee EJ, Kim DY, Oh H, et al. Oleuropein curtails pulmonary inflammation and tissue destruction in models of experimental asthma and emphysema. J Agric Food Chem 2018; 66: 7643-54. https://doi.org/10.1021/acs.jafc.8b01808
  42. Lechuga TJ, Qi QR, Kim T, Magness RR, Chen DB. E2β stimulates ovine uterine artery endothelial cell H2S production in vitro by estrogen receptor-dependent upregulation of cystathionine β-synthase and cystathionine γ-lyase expression†. Biol Reprod 2019; 100: 514-22. https://doi.org/10.1093/biolre/ioy207
  43. Di Cesare Mannelli L, Lucarini E, Micheli L, Mosca I, Ambrosino P, Soldovieri MV, et al. Effects of natural and synthetic isothiocyanate-based H2S-releasers against chemotherapy-induced neuropathic pain: role of Kv7 potassium channels. Neuropharmacology 2017; 121: 49-59. https://doi.org/10.1016/j.neuropharm.2017.04.029
  44. Wu G, Ringkamp M, Hartke TV, Murinson BB, Campbell JN, Griffin JW, et al. Early onset of spontaneous activity in uninjured C-fiber nociceptors after injury to neighboring nerve fibers. J Neurosci 2001; 21: RC140. https://doi.org/10.1523/jneurosci.21-08-j0002.2001
  45. Djouhri L, Koutsikou S, Fang X, McMullan S, Lawson SN. Spontaneous pain, both neuropathic and inflammatory, is related to frequency of spontaneous firing in intact C-fiber nociceptors. J Neurosci 2006; 26: 1281-92. https://doi.org/10.1523/JNEUROSCI.3388-05.2006
  46. Meacham K, Shepherd A, Mohapatra DP, Haroutounian S. Neuropathic pain: central vs. peripheral mechanisms. Curr Pain Headache Rep 2017; 21: 28. https://doi.org/10.1007/s11916-017-0629-5
  47. Razavi BM, Hosseinzadeh H. A review of the role of orexin system in pain modulation. Biomed Pharmacother 2017; 90: 187-93. https://doi.org/10.1016/j.biopha.2017.03.053
  48. Sorge RE, Mapplebeck JC, Rosen S, Beggs S, Taves S, Alexander JK, et al. Different immune cells mediate mechanical pain hypersensitivity in male and female mice. Nat Neurosci 2015; 18: 1081-3. https://doi.org/10.1038/nn.4053
  49. Castejon ML, Rosillo MA, Montoya T, Gonzalez-Benjumea A, Fernandez-Bolanos JG, Alarcon-de-la-Lastra C. Oleuropein down-regulated IL-1β-induced inflammation and oxidative stress in human synovial fibroblast cell line SW982. Food Funct 2017; 8: 1890-8. https://doi.org/10.1039/C7FO00210F
  50. Dubey AK, Handu SS, Mediratta PK. Suvorexant: the first orexin receptor antagonist to treat insomnia. J Pharmacol Pharmacother 2015; 6: 118-21. https://doi.org/10.4103/0976-500X.155496