Anti-inflammatory and antioxidative effects of fluoxetine on neuropathic pain responses in a Rat model of chronic constriction injury

authors:

avatar Abolfazl Abbaszadeh , avatar Amin Hasanvand , * , avatar A. li Kharazmkia , avatar Mehdi Goudarzi , avatar Shokoufeh Ahmadipour , avatar Sahar Koushki

Koomesh: Vol.20, issue 4; 731-736
published online: March 29, 2018
article type: issue_documents_importer
received: February 02, 2017
accepted: March 01, 2018

how to cite: Abbaszadeh A, Hasanvand A, Kharazmkia A L, Goudarzi M, Ahmadipour S, et al. Anti-inflammatory and antioxidative effects of fluoxetine on neuropathic pain responses in a Rat model of chronic constriction injury. koomesh. 2018;20(4):e153019. 

Abstract

Introduction: One of the most important side effects after neural injury is neuropathic pain. Increasing levels of inflammatory cytokines and oxidative stress play an important role in causing pain. Fluoxetine is one of the most important drugs used in the treatment of depression, which has been shown to have anti-inflammatory and anti-oxidative effects. In this study, we investigated the anti-inflammatory and antioxidant effects of fluoxetine in a Rat model of chronic constriction injury (CCI). Materials and Methods: 40 male Wistar rats were used in this study (230-250 g, n=10). Animals randomly individual in 4 groups such as: Sham, CCI, CCI + Fluoxetine (2 mg/kg, IP injection, for 14 days) and CCI + Fluoxetine (5 mg/kg, IP injection, for 14 days). Rats were tested behavioural tests (heat hyperalgesia, heat and mechanical Allodynia) on the days of 1, 7 and 14 after induced CCI. After 14 days, spinal cord was collected to measure tissue concentration of anti-inflammatory and antioxidative enzymes including tumor necrosis factor-α (TNF- α) interleukin-6 (IL-6), malonedialdehyde (MDA) and  superoxide (SOD). Results: The results of behavioral tests revealed that administration of fluoxetine reduced the symptoms of neuropathic pain. Fluoxetine administration also decreased levels of TNFα, IL-6 and MDA and increased SOD levels. Conclusion: Findings of this study showed that that fluoxetine has protective effects in an experimental model of neropathic pain and this effect might be mediated via its anti-inflammatory and antioxidant effects.  

References

  • 1.

    Gui Y, Li A, Zhang J, Li G, Ruan X, Guo Q, Zou W. Alpha-asarone alleviated chronic constriction injury-induced neuropathic pain through inhibition of spinal endoplasmic reticulum stress in an liver X receptor-dependent manner. Anesth Analg 2018.

  • 2.

    Zhuo M. Neuronal mechanism for neuropathic pain. Mol Pain 2007; 3: 14.

  • 3.

    Latremoliere A, Woolf CJ. Central sensitization: a generator of pain hypersensitivity by central neural plasticity. J Pain 2009; 10: 895-926.

  • 4.

    Dworkin RH, Backonja M, Rowbotham MC, Allen RR, Argoff CR, Bennett GJ, et al. Advances in neuropathic pain: diagnosis, mechanisms, and treatment recommendations. Arch Neurol 2003; 60: 1524-1534.

  • 5.

    De Jongh RF, Vissers KC, Meert TF, Booij LH, De Deyne CS, Heylen RJ. The role of interleukin-6 in nociception and pain. Anesth Analg 2003; 96: 1096-1103.

  • 6.

    Shi J, Jiang K, Li Z. Involvement of spinal glutamate transporter-1 in the development of mechanical allodynia and hyperalgesia associated with type 2 diabetes. J Pain Res 2016; 9: 1121-1129.

  • 7.

    Aafakhah HA, Bazargani A, Ghanbari A. Effects of forced exercise on neuropathic pain induced by chronic constriction injury of sciatic nerve in male rat. Koomesh 2016; 17: 411-418. (Persian).

  • 8.

    Dubov P, Janlek R, Kubek T. Role of inflammation and cytokines in peripheral nerve regeneration. Int Rev Neurobiol 2013; 108: 173-206.

  • 9.

    Sedeek M, Callera G, Montezano A, Gutsol A, Heitz F, Szyndralewiez C, et al. Critical role of Nox4-based NADPH oxidase in glucose-induced oxidative stress in the kidney: implications in type 2 diabetic nephropathy. Am J Physiol Renal Physiol 2010; 299: F1348-1358.

  • 10.

    Xie ZM, Wang XM, Xu N, Wang J, Pan W, Tang XH, et al. Alterations in the inflammatory cytokines and brain-derived neurotrophic factor contribute to depression-like phenotype after spared nerve injury: improvement by ketamine. Sci Rep 2017; 7: 3124.

  • 11.

    Cerles O, Benoit E, Chereau C, Chouzenoux S, Morin F, Guillaumot MA, et al. Niclosamide inhibits oxaliplatin neurotoxicity while improving colorectal cancer therapeutic response. Mol Cancer Ther 2017; 16: 300-311.

  • 12.

    Savegnago L, Jesse CR, Pinto LG, Rocha JB, Nogueira CW. Diphenyl diselenide attenuates acute thermal hyperalgesia and persistent inflammatory and neuropathic pain behavior in mice. Brain Res 2007; 1175: 54-59.

  • 13.

    Jadidi M, Sameni HR, mirbeygi Z, Jafari M, Taherian Aa. Effects of hydroalchoholic extract of Turmeric (Curcuma longa) Rhizome on the peripheral and visceral pain in mice. Koomesh 2016; 17: 692-700.

  • 14.

    Nickel FT, Seifert F, Lanz S, Maihfner C. Mechanisms of neuropathic pain. Eur Neuropsychopharmacol 2012; 22: 81-91.

  • 15.

    Zhou YQ, Liu Z, Liu ZH, Chen SP, Li M, Shahveranov A, et al. Interleukin-6: an emerging regulator of pathological pain. J Neuroinflammation 2016; 13.

  • 16.

    Valsecchi AE, Franchi S, Panerai AE, Sacerdote P, Trovato AE, Colleoni M. Genistein, a natural phytoestrogen from soy, relieves neuropathic pain following chronic constriction sciatic nerve injury in mice: anti-inflammatory and antioxidant activity. J Neurochem 2008; 107: 230-240.

  • 17.

    Bansode V, Vyawahare N, Munjal N, Gore P, Amrutkar P, Sontakke S. Ameliorative effect of ethyl pyruvate in neuropathic pain induced by chronic constriction injury of sciatic nerve. Indian J Pain 2014; 28: 82-88.

  • 18.

    Vierci G, Pannunzio B, Bornia N, Rossi FM. H3 and H4 lysine acetylation correlates with developmental and experimentally induced adult experience-dependent plasticity in the mouse visual cortex. J Exp Neurosci 2016; 10: 49-64.

  • 19.

    Dupuis A, Wattiez AS, Pinguet J, Richard D, Libert F, Chalus M, et al. Increasing spinal 5-HT2A receptor responsiveness mediates anti-allodynic effect and potentiates fluoxetine efficacy in neuropathic rats. Evidence for GABA release. Pharmacol Res 2017; 118: 93-103.

  • 20.

    Tembhurne SV, Sakarkar DM. Effect of fluoxetine on an experimental model of diabetes-induced neuropathic pain perception in the rat. Indian J Pharm Sci 2011; 73: 621-625.

  • 21.

    Shan H, Bian Y, Shu Z, Zhang L, Zhu J, Ding J, et al. Fluoxetine protects against IL-1beta-induced neuronal apoptosis via downregulation of p53. Neuropharmacology 2016; 107: 68-78.

  • 22.

    Ludka FK, Dal-Cim T, Binder LB, Constantino LC, Massari C, Tasca CI. Atorvastatin and fluoxetine prevent oxidative stress and mitochondrial dysfunction evoked by glutamate toxicity in hippocampal slices. Mol Neurobiol 2017; 54: 3149-3161.

  • 23.

    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.

  • 24.

    Jain V, Jaggi AS, Singh N. Ameliorative potential of rosiglitazone in tibial and sural nerve transection-induced painful neuropathy in rats. Pharmacol Res 2009; 59: 385-392.

  • 25.

    Yamamoto K, Chiba N, Chiba T, Kambe T, Abe K, Kawakami K, et al. Transient receptor potential ankyrin 1 that is induced in dorsal root ganglion neurons contributes to acute cold hypersensitivity after oxaliplatin administration. Mol Pain 2015; 11; 69.

  • 26.

    Seto Y, Okazaki F, Horikawa K, Zhang J, Sasaki H, To H. Influence of dosing times on cisplatin-induced peripheral neuropathy in rats. BMC Cancer 2016; 16: 756.

  • 27.

    Darabi S, Hasanvand A, Nourollahi A. Assessment of the effects of anti-inflammatory of garlic; nettle leaves and olives extracts in STZ-induced diabetic rat. CMJA 2016; 1: 1452-1460.

  • 28.

    Covey WC, Ignatowski TA, Knight PR, Spengler RN. Brain-derived TNFalpha: involvement in neuroplastic changes implicated in the conscious perception of persistent pain. Brain Res 2000; 859: 113-122.

  • 29.

    Lee HL, Lee KM, Son SJ, Hwang SH, Cho HJ. Temporal expression of cytokines and their receptors mRNAs in a neuropathic pain model. Neuroreport 2004; 15: 2807-2811.

  • 30.

    Siniscalco D, Fuccio C, Giordano C, Ferraraccio F, Palazzo E, Luongo L, et al. Role of reactive oxygen species and spinal cord apoptotic genes in the development of neuropathic pain. Pharmacol Res 2007; 55: 158-166.

  • 31.

    Kim HY, Wang J, Lu Y, Chung JM, Chung K. Superoxide signaling in pain is independent from nitric oxide signaling. Neuroreport 2009; 20: 1424.

  • 32.

    Roumestan C, Michel A, Bichon F, Portet K, Detoc M, Henriquet C, et al. Anti-inflammatory properties of desipramine and fluoxetine. Respir Res 2007; 8: 35.

  • 33.

    Carvalho LA, Torre JP, Papadopoulos AS, Poon L, Juruena MF, Markopoulou K, et al. Lack of clinical therapeutic benefit of antidepressants is associated overall activation of the inflammatory system. J Affect Disord 2013; 148: 136-140.

  • 34.

    Blatteau J-E, de Maistre S, Lambrechts K, Abraini J, Risso J-J, Valle N. Fluoxetine stimulates anti-inflammatory IL-10 cytokine production and attenuates sensory deficits in a rat model of decompression sickness. J Appl Physiol 2015; 119: 1393-1399.

  • 35.

    Dinarello CA. Historical insights into cytokines. Eur J Immunol 2007; 37: S34-S45.

  • 36.

    Ohgi Y, Futamura T, Kikuchi T, Hashimoto K. Effects of antidepressants on alternations in serum cytokines and depressive-like behavior in mice after lipopolysaccharide administration. Pharmacol Biochem Behav 2013; 103: 853-859.

  • 37.

    Kim DH, Li H, Yoo KY, Lee BH, Hwang IK, Won MH. Effects of fluoxetine on ischemic cells and expressions in BDNF and some antioxidants in the gerbil hippocampal CA1 region induced by transient ischemia. Exp Neurol 2007; 204: 748-758.

  • 38.

    Lee TH, Kato H, Chen ST, Kogure K, Itoyama Y. Expression disparity of brain-derived neurotrophic factor immunoreactivity and mRNA in ischemic hippocampal neurons. Neuroreport 2002; 13: 2271-2275.

  • 39.

    Caraci F, Tascedda F, Merlo S, Benatti C, Spampinato SF, Munaf A, et al. Fluoxetine prevents A(1-42)-induced toxicity via a paracrine signaling mediated by transforming-growth-factor-1. Front Pharmacol 2016; 7: 389.

  • 40.

    Mundalil Vasu M, Anitha A, Takahashi T, Thanseem I, Iwata K, Asakawa T, et al. Fluoxetine increases the expression of miR-572 and miR-663a in human neuroblastoma cell lines. PLoS One 2016; 11: e0164425.

  • 41.

    Murad H, Ayuob N. Co-Administration of pioglitazone improves fluoxetine's antinociceptive, neuroprotective, and antidepressant effects in chronic constriction injury in rats. Pain Physician 2015; 18: 609-620.##.