Punicalagin and ellagic acid containing Punica granatum L. fruit rind extract prevents vincristine-induced neuropathic pain in rats: an in silico and in vivo evidence of GABAergic action and cytokine inhibition

References

• Jaggi AS, Singh N. Mechanisms in cancer-chemotherapeutic drugs-induced peripheral neuropathy. Toxicology. 2012;291(1–3):1–9.
   PubMed Web of Science ®Google Scholar
• Verstappen CC, Heimans JJ, Hoekman K, Postma TJ. Neurotoxic complications of chemotherapy in patients with cancer: clinical signs and optimal management. Drugs. 2003;63(15):1549–63.
   PubMed Web of Science ®Google Scholar
• Zajaczkowska R, Kocot-Kepska M, Leppert W, Wrzosek A, Mika J, Wordliczek J. Mechanisms of chemotherapy-induced peripheral neuropathy. Int J Mol Sci. 2019;20(6):1451.
   PubMed Web of Science ®Google Scholar
• Ebersberger A. The analgesic potential of cytokine neutralization with biologicals. Eur J Pharmacol. 2018;835:19–30.
   PubMed Web of Science ®Google Scholar
• Marchand F, Tsantoulas C, Singh D, Grist J, Clark AK, Bradbury EJ, McMahon SB. Effects of etanercept and minocycline in a rat model of spinal cord injury. Eur J Pain. 2009;13(7):673–81.
   PubMed Web of Science ®Google Scholar
• Milligan ED, O'Connor KA, Nguyen KT, Armstrong CB, Twining C, Gaykema RP, et al. Intrathecal HIV-1 envelope glycoprotein gp120 induces enhanced pain states mediated by spinal cord proinflammatory cytokines. J Neurosci. 2001;21(8):2808–19.
   PubMed Web of Science ®Google Scholar
• Svensson CI, Schafers M, Jones TL, Powell H, Sorkin LS. Spinal blockade of TNF blocks spinal nerve ligation-induced increases in spinal P-p38. Neurosci Lett. 2005;379(3):209–13.
   PubMed Web of Science ®Google Scholar
• Kiguchi N, Maeda T, Kobayashi Y, Saika F, Kishioka S. Involvement of inflammatory mediators in neuropathic pain caused by vincristine. Int Rev Neurobiol. 2009;85:179–90.
   PubMed Web of Science ®Google Scholar
• Mangiacavalli S, Corso A, De Amici M, Varettoni M, Alfonsi E, Lozza A, Lazzarino M. Emergent T-helper 2 profile with high interleukin-6 levels correlates with the appearance of bortezomib-induced neuropathic pain. Br J Haematol. 2010;149(6):916–8.
   PubMed Web of Science ®Google Scholar
• Siau C, Xiao W, Bennett GJ. Paclitaxel- and vincristine-evoked painful peripheral neuropathies: loss of epidermal innervation and activation of Langerhans cells. Exp Neurol. 2006;201(2):507–14.
   PubMed Web of Science ®Google Scholar
• Masocha W. Comprehensive analysis of the GABAergic system gene expression profile in the anterior cingulate cortex of mice with paclitaxel-induced neuropathic pain. Gene Expr. 2015;16(3):145–53.
   PubMed Web of Science ®Google Scholar
• Xu D, Zhao H, Gao H, Zhao H, Liu D, Li J. Participation of pro-inflammatory cytokines in neuropathic pain evoked by chemotherapeutic oxaliplatin via central GABAergic pathway. Mol Pain. 2018;14:1744806918783535.
   Web of Science ®Google Scholar
• Ghoreishi Z, Esfahani A, Djazayeri A, Djalali M, Golestan B, Ayromlou H, et al. Omega-3 fatty acids are protective against paclitaxel-induced peripheral neuropathy: a randomized double-blind placebo controlled trial. BMC Cancer. 2012;12:355.
   PubMed Web of Science ®Google Scholar
• Maestri A, De Pasquale Ceratti A, Cundari S, Zanna C, Cortesi E, Crino L. A pilot study on the effect of acetyl-L-carnitine in paclitaxel- and cisplatin-induced peripheral neuropathy. Tumori. 2005;91(2):135–38.
   PubMed Web of Science ®Google Scholar
• Schroder S, Beckmann K, Franconi G, Meyer-Hamme G, Friedemann T, Greten HJ, et al. Can medical herbs stimulate regeneration or neuroprotection and treat neuropathic pain in chemotherapy-induced peripheral neuropathy? Evid Based Complement Alternat Med. 2013;2013:423713.
   PubMed Web of Science ®Google Scholar
• Singh AP, Singh AJ, Singh N. Pharmacological investigations of Punica granatum in glycerol-induced acute renal failure in rats. Indian J Pharmacol. 2011;43(5):551–56.
   PubMed Web of Science ®Google Scholar
• Singh K, Jaggi AS, Singh N. Exploring the ameliorative potential of Punica granatum in dextran sulfate sodium induced ulcerative colitis in mice. Phytother Res. 2009;23(11):1565–74.
   PubMed Web of Science ®Google Scholar
• Jain V, Pareek A, Bhardwaj YR, Singh N. Attenuating effect of standardized fruit extract of Punica granatum L in rat model of tibial and sural nerve transection induced neuropathic pain. BMC Complement Altern Med. 2013;13:274.
   PubMed Web of Science ®Google Scholar
• Girish C, Raj V, Arya J, Balakrishnan S. Involvement of the GABAergic system in the anxiolytic-like effect of the flavonoid ellagic acid in mice. Eur J Pharmacol. 2013;710(1–3):49–58.
   PubMed Web of Science ®Google Scholar
• Dworkin RH, O'Connor AB, Audette J, Baron R, Gourlay GK, Haanpaa ML, et al. Recommendations for the pharmacological management of neuropathic pain: an overview and literature update. Mayo Clin Proc. 2010;85(3 Suppl):S3–14.
   PubMed Web of Science ®Google Scholar
• Bourquin AF, Suveges M, Pertin M, Gilliard N, Sardy S, Davison AC, et al. Assessment and analysis of mechanical allodynia-like behavior induced by spared nerve injury (SNI) in the mouse. Pain. 2006;122(1–2):14 e1–14.
   Web of Science ®Google Scholar
• Banik RK, Woo YC, Park SS, Brennan TJ. Strain and sex influence on pain sensitivity after plantar incision in the mouse. Anesthesiology. 2006;105(6):1246–53.
   PubMed Web of Science ®Google Scholar
• Tall JM, Stuesse SL, Cruce WL, Crisp T. Gender and the behavioral manifestations of neuropathic pain. Pharmacol Biochem Behav. 2001;68(1):99–104.
   PubMed Web of Science ®Google Scholar
• Authier N, Coudore F, Eschalier A, Fialip J. Pain related behaviour during vincristine-induced neuropathy in rats. Neuroreport. 1999;10(5):965–68.
   PubMed Web of Science ®Google Scholar
• Flatters SJ, Bennett GJ. Ethosuximide reverses paclitaxel- and vincristine-induced painful peripheral neuropathy. Pain. 2004;109(1–2):150–61.
   PubMed Web of Science ®Google Scholar
• Erichsen HK, Blackburn-Munro G. Pharmacological characterisation of the spared nerve injury model of neuropathic pain. Pain. 2002;98(1–2):151–61.
   PubMed Web of Science ®Google Scholar
• de Medinaceli L, Freed WJ, Wyatt RJ. An index of the functional condition of rat sciatic nerve based on measurements made from walking tracks. Exp Neurol. 1982;77(3):634–43.
   PubMed Web of Science ®Google Scholar
• Lowry OH, Rosebrough NJ, Farr AL, Randall RJ. Protein measurement with the folin phenol reagent. J Biol Chem. 1951;193(1):265–75.
   PubMed Web of Science ®Google Scholar
• Martucci C, Trovato AE, Costa B, Borsani E, Franchi S, Magnaghi V, 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.
   PubMed Web of Science ®Google Scholar
• Grisham MB, Benoit JN, Granger DN. Assessment of leukocyte involvement during ischemia and reperfusion of intestine. Methods Enzymol. 1990;186:729–42.
   PubMed Web of Science ®Google Scholar
• Xavier AM, Serafim KG, Higashi DT, Vanat N, Flaiban KK, Siqueira CP, et al. Simvastatin improves morphological and functional recovery of sciatic nerve injury in Wistar rats. Injury. 2012;43(3):284–9.
   PubMed Web of Science ®Google Scholar
• Sudoh Y, Desai SP, Haderer AE, Sudoh S, Gerner P, Anthony DC, et al. Neurologic and histopathologic evaluation after high-volume intrathecal amitriptyline. Reg Anesth Pain Med. 2004;29(5):434–40.
   PubMed Web of Science ®Google Scholar
• Ito Y. [Neurochemical and pharmacological studies on brain GABA receptors]. Nippon Yakurigaku Zasshi. 1994;103(1):1–10.
   PubMedGoogle Scholar
• Patel C, Dadhaniya P, Hingorani L, Soni MG. Safety assessment of pomegranate fruit extract: acute and subchronic toxicity studies. Food Chem Toxicol. 2008;46(8):2728–35.
   PubMed Web of Science ®Google Scholar
• Masiulis S, Desai R, Uchanski T, Serna Martin I, Laverty D, Karia D, et al. GABAA receptor signalling mechanisms revealed by structural pharmacology. Nature. 2019;565(7740):454–459.
   PubMed Web of Science ®Google Scholar
• Jaggi AS, Singh N. Analgesic potential of intrathecal farnesyl thiosalicylic acid and GW 5074 in vincristine-induced neuropathic pain in rats. Food Chem Toxicol. 2012;50(5):1295–301.
   PubMed Web of Science ®Google Scholar
• Kaur G, Jaggi AS, Singh N. Exploring the potential effect of Ocimum sanctum in vincristine-induced neuropathic pain in rats. J Brachial Plex Peripher Nerve Inj. 2010;5:3.
   PubMedGoogle Scholar
• Jain V, Pareek A, Ratan Y, Singh N. Standardized fruit extract of Momordica charantia L protect against vincristine induced neuropathic pain in rats by modulating GABAergic action, antimitotoxic, NOS inhibition, anti-inflammatory and antioxidative activity. S Afr J Bot. 2015;97:123–132.
   Web of Science ®Google Scholar
• Jung KH, Kim MJ, Ha E, Uhm YK, Kim HK, Chung JH, Yim SV. Suppressive effect of Punica granatum on the production of tumor necrosis factor (Tnf) in BV2 microglial cells. Biol Pharm Bull. 2006;29(6):1258–61.
   PubMed Web of Science ®Google Scholar
• Lee HG, Kim WM, Yoon MH, Park AR, Choi JI. Synergistic anti-allodynic effect between intraperitoneal thalidomide and morphine on rat spinal nerve ligation-induced neuropathic pain. Korean J Anesthesiol. 2013;65(4):331–6.
   PubMedGoogle Scholar
• Carrilho PE, Araujo AC, Alves O, Kotze PG. Motor neuropathy with multiple conduction blocks associated with TNF-alpha antagonist. Arq Neuropsiquiatr. 2010;68(3):452–4.
   PubMed Web of Science ®Google Scholar
• Umesalma S, Sudhandiran G. Differential inhibitory effects of the polyphenol ellagic acid on inflammatory mediators NF-kappaB, iNOS, COX-2, TNF-alpha, and IL-6 in 1,2-dimethylhydrazine-induced rat colon carcinogenesis. Basic Clin Pharmacol Toxicol. 2010;107(2):650–5.
   PubMed Web of Science ®Google Scholar
• Hartman RE, Shah A, Fagan AM, Schwetye KE, Parsadanian M, Schulman RN, et al. Pomegranate juice decreases amyloid load and improves behavior in a mouse model of Alzheimer's disease. Neurobiol Dis. 2006;24(3):506–15.
   PubMed Web of Science ®Google Scholar
• Lee C-J, Chen L-G, Liang W-L, Wang C-C. Anti-inflammatory effects of Punica granatum Linne invitro and in vivo. Food Chem. 2010;118(2):315–322.
   Web of Science ®Google Scholar
• Eaton MJ, Plunkett JA, Karmally S, Martinez MA, Montanez K. Changes in GAD- and GABA- immunoreactivity in the spinal dorsal horn after peripheral nerve injury and promotion of recovery by lumbar transplant of immortalized serotonergic precursors. J Chem Neuroanat. 1998;16(1):57–72.
   PubMed Web of Science ®Google Scholar
• Lee J, Back SK, Lim EJ, Cho GC, Kim MA, Kim HJ, et al. Are spinal GABAergic elements related to the manifestation of neuropathic pain in rat? Korean J Physiol Pharmacol. 2010;14(2):59–69.
   PubMed Web of Science ®Google Scholar
• Mueller M, Jungbauer A. Culinary plants, herbs and spices – a rich source of PPARγ ligands. Food Chem. 2009;117(4):660–667.
   Web of Science ®Google Scholar
• Moreno S, Farioli-Vecchioli S, Ceru MP. Immunolocalization of peroxisome proliferator-activated receptors and retinoid X receptors in the adult rat CNS. Neuroscience. 2004;123(1):131–45.
   PubMed Web of Science ®Google Scholar
• Park SW, Yi JH, Miranpuri G, Satriotomo I, Bowen K, Resnick DK, Vemuganti R. Thiazolidinedione class of peroxisome proliferator-activated receptor gamma agonists prevents neuronal damage, motor dysfunction, myelin loss, neuropathic pain, and inflammation after spinal cord injury in adult rats. J. Pharmacol. Exp. Ther. 2007;320(3):1002–12.
   PubMed Web of Science ®Google Scholar
• Baradaran Rahimi V, Askari VR, Mousavi SH. Ellagic acid dose and time-dependently abrogates d-galactose-induced animal model of aging: investigating the role of PPAR-gamma. Life Sci. 2019;232:116595.
   PubMed Web of Science ®Google Scholar
• Chen J, Yang H, Sheng Z. Ellagic acid activated PPAR signaling pathway to protect ileums against castor oil-induced diarrhea in mice: application of transcriptome analysis in drug screening. Front Pharmacol. 2019;10:1681.
   PubMed Web of Science ®Google Scholar
• Vivek Jain ASJ, Singh, N. Non-beneficial effects of rosiglitazone in oxaliplatin-induced cold hyperalgesia in rats. J. Pharm. Negat. Results . 2011;2 (1):28–34.
   Google Scholar
• Morteza-Semnani K, Saeedi M, Hamidian M. Anti-inflammatory and analgesic activity of the topical preparation of Glaucium grandiflorum. Fitoterapia. 2004;75(2):123–9.
   PubMed Web of Science ®Google Scholar
• Wagner H, Ulrich-Merzenich G. Synergy research: approaching a new generation of phytopharmaceuticals. Phytomedicine. 2009;16(2–3):97–110.
   PubMed Web of Science ®Google Scholar
• Lee C-J, Chen L-G, Liang W-L, Hsieh M-S, Wang C-C. Inhibitory effects of punicalagin from Punica granatum against type II collagenase-induced osteoarthritis. J Funct Foods. 2018;41:216–222.
   Web of Science ®Google Scholar
• Larrosa M, Tomás-Barberán FA, Espín JC. The dietary hydrolysable tannin punicalagin releases ellagic acid that induces apoptosis in human colon adenocarcinoma Caco-2 cells by using the mitochondrial pathway. J Nutr Biochem. 2006;17(9):611–625.
   PubMed Web of Science ®Google Scholar
• Kumar P, Kalonia H, Kumar A. Possible GABAergic mechanism in the neuroprotective effect of gabapentin and lamotrigine against 3-nitropropionic acid induced neurotoxicity. Eur J Pharmacol. 2012;674(2–3):265–74.
   PubMed Web of Science ®Google Scholar
• Li C, Lei Y, Tian Y, Xu S, Shen X, Wu H, et al. The etiological contribution of GABAergic plasticity to the pathogenesis of neuropathic pain. Mol Pain. 2019;15:1744806919847366.
   Web of Science ®Google Scholar
• Alles SRA, Smith PA. Etiology and pharmacology of neuropathic pain. Pharmacol Rev. 2018;70(2):315–347.
   PubMed Web of Science ®Google Scholar
• Alves JM, Lin K. Neuropathic pain: a review of interneuronal disinhibition. Arch Neurosci. 2018;5(1):e12290.
   Web of Science ®Google Scholar
• Jasmin L, Wu MV, Ohara PT. GABA puts a stop to pain. Curr Drug Targets CNS Neurol Disord. 2004;3(6):487–505.
   PubMedGoogle Scholar
• Puhl AC MF, Cvoro A, Sieglaff DH, Campos JC, Bernardes A, Filgueira CS, et al. Mechanisms of peroxisome proliferator activated receptor γ regulation by non-steroidal anti-inflammatory drugs. Nucl Recept Signal. 2015;5(13):e004.
   Google Scholar
• Raafat K, Samy W. Amelioration of diabetes and painful diabetic neuropathy by Punica granatum L. extract and its spray dried biopolymeric dispersions. Evid -Based Complement Altern Med. 2014;2014:180495.
   PubMed Web of Science ®Google Scholar
• Koolhaas JM. The laboratory Rat. In: R Hubrecht, J Kirkwood, editors. The UFAW handbook on the care and management of laboratory and other research animals. Hoboken (NJ): Wiley-Blackwell; 2010. doi:10.1002/9781444318777.ch22 
   Google Scholar
• Hestehave S, Abelson KSP, Brønnum Pedersen T, et al. The influence of rat strain on the development of neuropathic pain and comorbid anxio-depressive behaviour after nerve injury. Sci Rep. 2020;10:20981, doi:10.1038/s41598-020-77640-8.
   PubMed Web of Science ®Google Scholar
• Kim YE, Hwang CJ, Lee HP, Kim CS, Son DJ, Ham YW, et al. Inhibitory effect of punicalagin on lipopolysaccharide-induced neuroinflammation, oxidative stress and memory impairment via inhibition of nuclear factor-kappaB. Neuropharmacology. 2017;117:21–32. doi:10.1016/j.neuropharm.2017.01.025.
   PubMed Web of Science ®Google Scholar
• Varghese JN, Moritz RL, Lou M-Z, et al. Structure of the extracellular domains of the human interleukin-6 receptor α-chain. Proc Natl Acad Sci USA. 2002;99:15959–15964. doi:10.1073/pnas.232432399.
   PubMed Web of Science ®Google Scholar
• Hirudkar JR, Parmar KM, Prasad RS, Sinha SK, Lomte AD, Itankar PR, Prasad SK. The antidiarrhoeal evaluation of Psidium guajava L. against enteropathogenic Escherichia coli induced infectious diarrhoea. J Ethnopharmacol. 2020;6(251):112561. doi:10.1016/j.jep.2020.112561.
   Google Scholar
• Bazan JF. Structural design and molecular evolution of a cytokine receptor superfamily. Proc Natl Acad Sci USA. 1990;87:6934–6938. doi:10.1073/pnas.87.18.6934.
   PubMed Web of Science ®Google Scholar