Yıl: 2021 Cilt: 51 Sayı: 6 Sayfa Aralığı: 3098 - 3107 Metin Dili: İngilizce DOI: 10.3906/sag-2101-224 İndeks Tarihi: 05-01-2022

Protective effects of anandamide against cisplatin-induced peripheral neuropathy in rats

Öz:
Background/aim: Cisplatin (CIS) is an effective antineoplastic agent used in the treatment of several cancer types. Peripheral neuropathy is a major dose-limiting side-effect in CIS therapy. Cannabinoids may alleviate this painful side effect. This study investigated the analgesic effects of anandamide (AN) on CIS-induced peripheral neuropathy, in vitro effects of AN in CIS neurotoxicity, and the contribution of nitric oxide (NO) in this effect. Materials and methods: This is an experimental animal study. Primary dorsal root ganglion (DRG) cultures were prepared from oneday-old rats for in vitro investigations. DRG cells were incubated with CIS (100–300 μM), and AN (10, 50, 100, and 500 μM) was administered with the submaximal concentration of CIS. Female Sprague Dawley rats were divided into control, CIS, CIS+AN, CIS+AN+ L-NG-nitro arginine methyl ester (LNAME). CIS was administered 3 mg/kg i.p once weekly for 5 weeks. AN (1 mg/kg i.p) or in combination with 10 mg/kg i.p LNAME was administrated 30 min before CIS injection. Mechanical allodynia, thermal hyperalgesia, and tail clip tests were performed. After intracardiac perfusion, sciatic nerves (SN), and DRGs were isolated and semi-thin sections were stained with toluidine blue and investigated histologically. SPSS v. 21.0 and Sigma STAT 3.5 were used for statistical analysis. One/two way ANOVA, Kruskal–Wallis, and Wilcoxon signed ranks tests were used. A p-value of 0.05 was accepted as significant. Results: CIS caused significant mechanical allodynia. AN and AN+LNAME significantly increased hind paw withdrawal latency in mechanical allodynia test. The degenerated axons significantly increased in CIS group, while decreased in AN group. The frequency of larger neurons seemed to be higher in CIS+AN group. Conclusion: AN may be a therapeutic alternative for the treatment of CIS-induced peripheral neuropathy. However, its central adverse effects must be considered.Key words: Cis-diamminedichloroplatinum(II), n-arachidonoylethanolamide, ng nitroarginine methyl ester, nitric oxide, peripheral neuropathy
Anahtar Kelime:

Belge Türü: Makale Makale Türü: Araştırma Makalesi Erişim Türü: Erişime Açık
  • 1. Banach M, Juranek JK, Zygulska AL. Chemotherapy-induced neuropathies-a growing problem for patients and health care providers. Brain and Behavior 2017; 7 (1): e00558. doi: 10.1002/brb3.558
  • 2. Grisold W, Cavaletti G, Windebank AJ. Peripheral neuropathies from chemotherapeutics and targeted agents: diagnosis, treatment, and prevention. Neuro-oncology 2012; 14 (Suppl 4): iv45-54. doi: 10.1093/neuonc/nos203
  • 3. Melli G, Taiana M, Camozzi F, Triolo D, Podini P et al. Alphalipoic acid prevents mitochondrial damage and neurotoxicity in experimental chemotherapy neuropathy. Experimental Neurology 2008; 214 (2): 276-284. doi: 10.1016/j.expneurol.2008.08.013
  • 4. Ta LE, Bieber AJ, Carlton SM, Loprinzi CL, Low PA et al. Transient receptor potential vanilloid 1 is essential for cisplatin-induced heat hyperalgesia in mice. Molecular Pain 2010; 6: 15. doi: 10.1186/1744-8069-6-15
  • 5. Scuteri A, Galimberti A, Ravasi M, Pasini S, Donzelli E et al. NGF protects dorsal root ganglion neurons from oxaliplatin by modulating JNK/Sapk and ERK1/2. Neuroscience Letters 2010; 486 (3): 141-145. doi: 10.1016/j.neulet.2010.09.028
  • 6. Carozzi VA, Chiorazzi A, Canta A, Lapidus RG, Slusher BS et al. Glutamate carboxypeptidase inhibition reduces the severity of chemotherapy-induced peripheral neurotoxicity in rat. Neurotoxicity Research 2010; 17 (4): 380-391. doi: 10.1007/s12640-009-9114-1
  • 7. Horvath P, Szilvassy J, Nemeth J, Peitl B, Szilasi M et al. Decreased sensory neuropeptide release in isolated bronchi of rats with cisplatin-induced neuropathy. European Journal of Pharmacology 2005; 507 (1-3): 247-252. doi: 10.1016/j.ejphar.2004.11.053
  • 8. Avan A, Postma TJ, Ceresa C, Avan A, Cavaletti G et al. Platinuminduced neurotoxicity and preventive strategies: past, present, and future. The Oncologist 2015; 20(4): 411-432. doi: 10.1634/theoncologist.2014-0044
  • 9. Maldonado R, Banos JE and Cabanero D. The endocannabinoid system and neuropathic pain. Pain 2016; 157 Suppl 1: S23-32. doi: 10.1097/j.pain.0000000000000428
  • 10. Nadal X, Porta CL, Bura SA, Maldonado R. Involvement of the opioid and cannabinoid systems in pain control: new insights from knockout studies. European Journal of Pharmacology 2013; 716 (1-3): 142-157. doi: 10.1016/j.ejphar.2013.01.077
  • 11. Cravatt BF, Demarest MP, Patricelli MP, Bracey MH, Giang DK et al. Supersensitivity to anandamide and enhanced endogenous cannabinoid signaling in mice lacking fatty acid amide hydrolase. Proceedings of National Academy of Sciences of the United States of America 2001; 98 (16): 9371-9376. doi: 10.1073/pnas.161191698
  • 12. Smith PB, Compton DR, Welch SP, Razdan RK, Mechoulam R et al. The pharmacological activity of anandamide, a putative endogenous cannabinoid, in mice. The Journal of Pharmacology and Experimental Therapeutics 1994; 270 (1): 219-227.
  • 13. Martin BR. Cellular effects of cannabinoids. Pharmacological Reviews 1986; 38 (1): 45-74.
  • 14. Khasabova IA, Khasabov S, Paz J, Harding-Rose C, Simone DA et al. Cannabinoid type-1 receptor reduces pain and neurotoxicity produced by chemotherapy. Journal of Neuroscience 2012; 32 (20): 7091-101. doi: 10.1523/JNEUROSCI.0403-12.2012
  • 15. Perez M, Benitez SU, Cartarozzi LP, Del Bel E, Guimaraes FS et al. Neuroprotection and reduction of glial reaction by cannabidiol treatment after sciatic nerve transection in neonatal rats. The European Journal of Neuroscience 2013; 38(10): 3424-3434. doi: 10.1111/ejn.12341
  • 16. Liu Q, Bhat M, Bowen WD, Cheng J. Signaling pathways from cannabinoid receptor-1 activation to inhibition of N-methyl-Daspartic acid mediated calcium influx and neurotoxicity in dorsal root ganglion neurons. The Journal of Pharmacology and Experimental Therapeutics 2009; 331 (3): 1062-1070. doi: 10.1124/jpet.109.156216
  • 17. Maione S, Bisogno T, Novellis V, Palazzo E, Cristino L et al. Elevation of endocannabinoid levels in the ventrolateral periaqueductal grey through inhibition of fatty acid amide hydrolase affects descending nociceptive pathways via both cannabinoid receptor type 1 and transient receptor potential vanilloid type-1 receptors. The Journal of Pharmacology and Experimental Therapeutics 2006; 316 (3): 969-982. doi: 10.1124/jpet.105.093286
  • 18. Ahluwalia J, Urban L, Capogna M, Bevan S, Nagy I. Cannabinoid 1 receptors are expressed in nociceptive primary sensory neurons. Neuroscience 2000; 100 (4): 685-658. doi: 10.1016/s0306-4522(00)00389-4.
  • 19. Tognetto M, Amadesi S, Harrison S, Creminon C, Trevisani M et al. Anandamide excites central terminals of dorsal root ganglion neurons via vanilloid receptor-1 activation. Journal of Neuroscience 2001; 21 (4): 1104-1109. doi: 10.1523/JNEUROSCI.21-04-01104.2001
  • 20. Levy D, Zochodne DW. NO pain: potential roles of nitric oxide in neuropathic pain. Pain Practice 2004; 4 (1): 11-18. doi: 10.1111/j.1533-2500.2004.04002.x
  • 21. Martucci C, Trovato AE, Costa B, Borsani E, Franchi S et al. The purinergic antagonist PPADS reduces pain related behaviours and interleukin-1 beta, interleukin-6, iNOS and nNOS overproduction in central and peripheral nervous system after peripheral neuropathy in mice. Pain 2008; 137 (1): 81-95. doi: 10.1016/j.pain.2007.08.017
  • 22. Hervera A, Negrete R, Leanez S, Martin-Compos JM, Pol O. Peripheral effects of morphine and expression of mu-opioid receptors in the dorsal root ganglia during neuropathic pain: nitric oxide signaling. Molecular Pain 2011; 7: 25. doi: 10.1186/1744-8069-7-25
  • 23. Stefano GB, Esch T, Cadet P, Zhu W, Mantione K et al. Endocannabinoids as autoregulatory signaling molecules: coupling to nitric oxide and a possible association with the relaxation response. Medical Science Monitor 2003; 9 (4): 63- 75.
  • 24. Donertas B, Unel CC, Aydin S, Ulupinar E, Ozatik O et al. Agmatine co-treatment attenuates allodynia and structural abnormalities in cisplatin-induced neuropathy in rats. Fundamental and Clinical Pharmacology 2018; 32 (3): 288-296. doi: 10.1111/fcp.12351
  • 25. Erol K, Yiğitaslan S, Ünel Ç, Kaygısız B, Yıldırım E. Evaluation of cisplatin neurotoxicity in cultured rat dorsal root ganglia via cytosolic calcium accumulation. Balkan Medical Journal 2016; 33(2): 144-151. doi: 10.5152/balkanmedj.2016.161110
  • 26. Han FY, Wyse BD and Smith MT. Optimization and pharmacological characterization of a refined cisplatininduced rat model of peripheral neuropathic pain. Behavioral Pharmacology 2014; 25 (8): 732-740.
  • 27. Faul F, Erdfelder E, Buchner A, Lang AG. Statistical power analyses using G*Power 3.1: tests for correlation and regression analyses. Behavior Research Methods 2009; 41 (4): 1149-1160. doi: 10.3758/BRM.41.4.1149
  • 28. Wongtawatchai T, Agthong S, Kaewsema A, Chentanez V. Altered phosphorylation of mitogen-activated protein kinases in dorsal root ganglia and sciatic nerve of rats with cisplatininduced neuropathy. Asian Biomedicine 2012; 6 (3): 397-411. doi: 10.5372/1905-7415.0603.070
  • 29. Compton DR, Rice KC, Costa BR, Razdan RK, Melvin LS et al. Cannabinoid structure-activity relationships: correlation of receptor binding and in vivo activities. The Journal of Pharmacology and Experimental Therapeutics 1993; 265 (1): 218-226.
  • 30. Özatik O, Koçman AE, Dağ İ, Köse AA, Musmul A et al. The effect of decompression on the treatment of chronic constriction injury in peripheral nerve. Kafkas Universitesi Veterinerlik Fakültesi Dergisi 2016; 22 (4): 597-604.
  • 31. Jimenez-Andrade, J.M, Herrera MB, Ghilardi JR, Vardanyan M, Melemedjian O et al. Vascularization of the dorsal root ganglia and peripheral nerve of the mouse: implications for chemicalinduced peripheral sensory neuropathies. Molecular Pain 2008; 4: 10. doi: 10.1186/1744-8069-4-10
  • 32. Seto Y, Takase M, Tsuji Y, To H. Pregabalin reduces cisplatininduced mechanical allodynia in rats. Journal of Pharmacological Sciences 2017; 134 (3): 175-180. doi: 10.1016/j.jphs.2017.06.003
  • 33. Guindon J, Lai Y, Takacs SM, Bradshaw HB, Hohmann AG. Alterations in endocannabinoid tone following chemotherapyinduced peripheral neuropathy: effects of endocannabinoid deactivation inhibitors targeting fatty-acid amide hydrolase and monoacylglycerol lipase in comparison to reference analgesics following cisplatin treatment. Pharmacological Research 2013; 67 (1): 94-109. doi:10.1016/j.phrs.2012.10.013
  • 34. Bianchi C and Franceschini J. Experimental observations on Haffner's method for testing analgesic drugs. British Journal of Pharmacology and Chemotherapy 1954; 9 (3): 280-284. doi: 10.1111/j.1476-5381.1954.tb01681.x
  • 35. Desroches J, Charron S, Bouchard J, Beaulieu P. Endocannabinoids decrease neuropathic pain-related behavior in mice through the activation of one or both peripheral CB(1) and CB(2) receptors. Neuropharmacology 2014; 77: 441-452.
  • 36. Richardson JD, Kilo S, Hargreaves KM. Cannabinoids reduce hyperalgesia and inflammation via interaction with peripheral CB1 receptors. Pain 1998; 75 (1): 111-119. doi: 10.1016/S0304-3959(97)00213-3
  • 37. Cury Y, Picolo G, Gutierrez VP, Ferreira SH. Pain and analgesia: the dual effect of nitric oxide in the nociceptive system. Nitric Oxide 2011; 25 (3): pp. 243-254. doi: 10.1016/j.niox.2011.06.004
  • 38. Yoon YW, Sung B and Chung JM. Nitric oxide mediates behavioral signs of neuropathic pain in an experimental rat model. Neuroreport 1998; 9 (3): 367-372. doi: 10.1097/00001756-199802160-00002
  • 39. Malmberg AB and Yaksh TL. Spinal nitric oxide synthesis inhibition blocks NMDA-induced thermal hyperalgesia and produces antinociception in the formalin test in rats. Pain 1993; 54 (3): 291-300. doi: 10.1016/0304-3959(93)90028-N
  • 40. Duarte ID and Ferreira SH. L-NAME causes antinociception by stimulation of the arginine-NO-cGMP pathway. Mediators of Inflammation 2000; 9 (1): 25-30. doi: 10.1080/09629350050024348
  • 41. Reis GM and Pacheco D. Opioid receptor and NO/cGMP pathway as a mechanism of peripheral antinociceptive action of the cannabinoid receptor agonist anandamide. Life Sciences 2009; 85 (9-10): 351-356. doi: 10.1016/j.lfs.2009.06.012
  • 42. Bridges D, Ahmad K, Rice AS. The synthetic cannabinoid WIN55,212-2 attenuates hyperalgesia and allodynia in a rat model of neuropathic pain. British Journal of Pharmacology 2001; 133 (4): 586-594. doi: 10.1038/sj.bjp.0704110
  • 43. Fox A, Kesingland A, Gentry C, McNair K, Patel S et al. The role of central and peripheral cannabinoid1 receptors in the antihyperalgesic activity of cannabinoids in a model of neuropathic pain. Pain 2001; 92 (1-2): 91-100. doi: 10.1016/s0304-3959(00)00474-7
  • 44. Keilhoff G, Schröder H, Peters B, Becker A. Time-course of neuropathic pain in mice deficient in neuronal or inducible nitric oxide synthase. Neuroscience Research 2013; 77 (4): 215-221. doi: 10.1016/j.neures.2013.08.008
  • 45. Smith LA, Azariah F, Lavender VTC, Stoner NS, Bettiol S. Cannabinoids for nausea and vomiting in adults with cancer receiving chemotherapy. The Cochrane Database of Systematic Reviews 2015; (11). doi: 10.1002/14651858.CD009464.pub2
  • 46. Dewey WL. Cannabinoid pharmacology. Pharmacological Reviews 1986; 38 (2): 151-178.
  • 47. Wongtawatchai T, Agthong S, Atitaya K, Chentanez V. Sexrelated differences in cisplatin-induced neuropathy in rats. Journal of Medical Association of Thailand = Chotmaihet thangphaet 2009; 92 (11): 1485-1491.
  • 48. Tredici G, Braga M, Nicolini G, Marmiroli P, Schenone A et al. Effect of recombinant human nerve growth factor on cisplatin neurotoxicity in rats. Experimental Neurology 1999; 159 (2): 551-558. doi: 10.1006/exnr.1999.7174
  • 49. Lauckner JE, Jensen JB, Chen H, Lu H, Hille B et al. GPR55 is a cannabinoid receptor that increases intracellular calcium and inhibits M current. Proceedings of the National Academy of Sciences of the United States of America 2008; 105 (7): 2699- 2704. doi: 10.1073/pnas.0711278105
APA ÇENGELLI ÜNEL Ç, DONERTAS B, AYDIN S, ULUPINAR E, Özatik O, KAYGISIZ B, Yıldırım E, Erol K (2021). Protective effects of anandamide against cisplatin-induced peripheral neuropathy in rats. , 3098 - 3107. 10.3906/sag-2101-224
Chicago ÇENGELLI ÜNEL ÇIGDEM,DONERTAS BASAK,AYDIN SULE,ULUPINAR EMEL,Özatik Orhan,KAYGISIZ Bilgin,Yıldırım Engin,Erol Kevser Protective effects of anandamide against cisplatin-induced peripheral neuropathy in rats. (2021): 3098 - 3107. 10.3906/sag-2101-224
MLA ÇENGELLI ÜNEL ÇIGDEM,DONERTAS BASAK,AYDIN SULE,ULUPINAR EMEL,Özatik Orhan,KAYGISIZ Bilgin,Yıldırım Engin,Erol Kevser Protective effects of anandamide against cisplatin-induced peripheral neuropathy in rats. , 2021, ss.3098 - 3107. 10.3906/sag-2101-224
AMA ÇENGELLI ÜNEL Ç,DONERTAS B,AYDIN S,ULUPINAR E,Özatik O,KAYGISIZ B,Yıldırım E,Erol K Protective effects of anandamide against cisplatin-induced peripheral neuropathy in rats. . 2021; 3098 - 3107. 10.3906/sag-2101-224
Vancouver ÇENGELLI ÜNEL Ç,DONERTAS B,AYDIN S,ULUPINAR E,Özatik O,KAYGISIZ B,Yıldırım E,Erol K Protective effects of anandamide against cisplatin-induced peripheral neuropathy in rats. . 2021; 3098 - 3107. 10.3906/sag-2101-224
IEEE ÇENGELLI ÜNEL Ç,DONERTAS B,AYDIN S,ULUPINAR E,Özatik O,KAYGISIZ B,Yıldırım E,Erol K "Protective effects of anandamide against cisplatin-induced peripheral neuropathy in rats." , ss.3098 - 3107, 2021. 10.3906/sag-2101-224
ISNAD ÇENGELLI ÜNEL, ÇIGDEM vd. "Protective effects of anandamide against cisplatin-induced peripheral neuropathy in rats". (2021), 3098-3107. https://doi.org/10.3906/sag-2101-224
APA ÇENGELLI ÜNEL Ç, DONERTAS B, AYDIN S, ULUPINAR E, Özatik O, KAYGISIZ B, Yıldırım E, Erol K (2021). Protective effects of anandamide against cisplatin-induced peripheral neuropathy in rats. Turkish Journal of Medical Sciences, 51(6), 3098 - 3107. 10.3906/sag-2101-224
Chicago ÇENGELLI ÜNEL ÇIGDEM,DONERTAS BASAK,AYDIN SULE,ULUPINAR EMEL,Özatik Orhan,KAYGISIZ Bilgin,Yıldırım Engin,Erol Kevser Protective effects of anandamide against cisplatin-induced peripheral neuropathy in rats. Turkish Journal of Medical Sciences 51, no.6 (2021): 3098 - 3107. 10.3906/sag-2101-224
MLA ÇENGELLI ÜNEL ÇIGDEM,DONERTAS BASAK,AYDIN SULE,ULUPINAR EMEL,Özatik Orhan,KAYGISIZ Bilgin,Yıldırım Engin,Erol Kevser Protective effects of anandamide against cisplatin-induced peripheral neuropathy in rats. Turkish Journal of Medical Sciences, vol.51, no.6, 2021, ss.3098 - 3107. 10.3906/sag-2101-224
AMA ÇENGELLI ÜNEL Ç,DONERTAS B,AYDIN S,ULUPINAR E,Özatik O,KAYGISIZ B,Yıldırım E,Erol K Protective effects of anandamide against cisplatin-induced peripheral neuropathy in rats. Turkish Journal of Medical Sciences. 2021; 51(6): 3098 - 3107. 10.3906/sag-2101-224
Vancouver ÇENGELLI ÜNEL Ç,DONERTAS B,AYDIN S,ULUPINAR E,Özatik O,KAYGISIZ B,Yıldırım E,Erol K Protective effects of anandamide against cisplatin-induced peripheral neuropathy in rats. Turkish Journal of Medical Sciences. 2021; 51(6): 3098 - 3107. 10.3906/sag-2101-224
IEEE ÇENGELLI ÜNEL Ç,DONERTAS B,AYDIN S,ULUPINAR E,Özatik O,KAYGISIZ B,Yıldırım E,Erol K "Protective effects of anandamide against cisplatin-induced peripheral neuropathy in rats." Turkish Journal of Medical Sciences, 51, ss.3098 - 3107, 2021. 10.3906/sag-2101-224
ISNAD ÇENGELLI ÜNEL, ÇIGDEM vd. "Protective effects of anandamide against cisplatin-induced peripheral neuropathy in rats". Turkish Journal of Medical Sciences 51/6 (2021), 3098-3107. https://doi.org/10.3906/sag-2101-224