Neuroprotective effects of ellagic acid on cuprizone-induced acute demyelination through limitation of microgliosis, adjustment of CXCL12/IL-17/IL-11 axis and restriction of mature oligodendrocytes apoptosis

References

• Abakumova TO, Kuz'kina AA, Zharova ME, Pozdeeva DA, Gubskii IL, Shepeleva II, Antonova OM, Nukolova NV, Kekelidze ZI, Chekhonin VP. 2015. Cuprizone model as a tool for preclinical studies of the efficacy of multiple sclerosis diagnosis and therapy. Bull Exp Biol Med. 159:111–115.
   PubMed Web of Science ®Google Scholar
• Abdul-Wahab RH, Waleed MAM, Janakat S, Sawsan AO. 2009. Bioavailability of ellagic acid after single dose administration using HPLC. Pakistan J Nutr. 8:1661–1664.
   Google Scholar
• Amakura Y, Okada M, Tsuji A, Tonogai Y. 2000. High-performance liquid chromatography determination with photodiode array detection of ellagic acid in fresh and processed fruits. J Chromatog B. 896:87–93.
   Google Scholar
• Baeeri M, Momtaz S, Navaei-Nigjeh M, Niaz K, Rahimifard M, Ghasemi-Niri SF, Sanadgol N, Hodjat M, Sharifzadeh M, Abdollahi M. 2017. Molecular evidence on the protective effect of ellagic acid on phosalone-induced senescence in rat embryonic fibroblast cells. Food Chem Toxicol. 100:8–23.
   PubMed Web of Science ®Google Scholar
• Baxi EG, DeBruin J, Tosi DM, Grishkan IV, Smith MD, Kirby LA, Strasburger HJ, Fairchild AN, Calabresi PA, Gocke AR. 2015. Transfer of myelin-reactive Th17 cells impairs endogenous remyelination in the central nervous system of cuprizone-fed mice. J Neurosci. 35:8626–8639.
   PubMed Web of Science ®Google Scholar
• Buschmann JP, Berger K, Awad H, Clarner T, Beyer C, Kipp M. 2012. Inflammatory response and chemokine expression in the white matter corpus callosum and gray matter cortex region during cuprizone-induced demyelination. J Mol Neurosci. 48:66–76.
   PubMed Web of Science ®Google Scholar
• Chen SY, Zheng K, Wang ZQ. 2016. Neuroprotective effects of ellagic acid on neonatal hypoxic brain injury via inhibition of inflammatory mediators and down-regulation of JNK/p38 MAPK activation. Trop J Pharm Res. 15:241–251.
   Web of Science ®Google Scholar
• Clifford MN, Scalbert A. 2000. Ellagitannins-nature, occurrence and dietary burden. J Sci Food Agric. 80:1118–1125.
   Web of Science ®Google Scholar
• Cruz-Orengo L, Chen YJ, Kim JH, Dorsey D, Song SK, Klein RS. 2011. CXCR7 antagonism prevents axonal injury during experimental autoimmune encephalomyelitis as revealed by in vivo axial diffusivity. J Neuroinflamm. 8:170–184.
   PubMed Web of Science ®Google Scholar
• Doan V, Kleindienst AM, McMahon EJ, Long BR, Matsushima GK, Taylor LC. 2013. Abbreviated exposure to cuprizone is sufficient to induce demyelination and oligodendrocyte loss. J Neurosci Res. 91:363–373.
   PubMed Web of Science ®Google Scholar
• Dolatshahi M, Farbood Y, Sarkaki A, Mansouri SMT, Khodadadi A. 2015. Ellagic acid improves hyperalgesia and cognitive deficiency in 6-hydroxidopamine induced rat model of Parkinson's disease. Iran J Basic Med Sci. 18:38–46.
   PubMed Web of Science ®Google Scholar
• Favarin CD, Teixeira MM, Andrade LE, Alves FC, Chica LJE, Sorgi AC, Faccioli LH, Rogerio PA. 2013. Anti-inflammatory effects of ellagic acid on acute lung injury induced by acid in mice. Mediators Inflamm. 2013:164202.
   PubMed Web of Science ®Google Scholar
• Feng Y, Yang SG, Du XT, Zhang X, Sun XX, Zhao M, Sun GY, Liu RT. 2009. Ellagic acid promotes Abeta42 fibrillization and inhibits Abeta42-induced neurotoxicity. Biochem Biophys Res Commun. 390:1250–1254.
   PubMed Web of Science ®Google Scholar
• Goodin DS. 2014. The epidemiology of multiple sclerosis: insights to disease pathogenesis. Handb Clin Neurol. 122:231–266.
   PubMedGoogle Scholar
• Gudi V, Gingele S, Skripuletz T, Stangel M. 2014. Glial response during cuprizone-induced de- and remyelination in the CNS: lessons learned. Front Cell Neurosci. 8:73.
   PubMed Web of Science ®Google Scholar
• Hall ED, Vaishnav RA, Mustafa AG. 2010. Antioxidant therapies for traumatic brain injury. Neurotherapeutics. 7:51–61.
   PubMed Web of Science ®Google Scholar
• Han DH, Lee MJ, Kim JH. 2006. Antioxidant and apoptosis-inducing activities of ellagic acid. Anticancer Res. 26:3601–3606.
   PubMed Web of Science ®Google Scholar
• Heidary M, Rakhshi N, Pahlevan Kakhki M, Behmanesh M, Sanati MH, Sanadgol N, Kamaladini H, Nikravesh A. 2014. The analysis of correlation between IL-1B gene expression and genotyping in multiple sclerosis patients. J Neuro Sci. 343:41–45.
   PubMed Web of Science ®Google Scholar
• Hibbits N, Yoshino J, Le TQ, Armstrong RC. 2012. Astrogliosis during acute and chronic cuprizone demyelination and implications for remyelination. ASN Neuro. 4:e00100.
   PubMed Web of Science ®Google Scholar
• Kang Z, Liu L, Spangler R, Spear C, Wang C, Gulen MF, Veenstra M, Ouyang W, Ransohoff RM, Li X. 2012. IL-17-induced Act1-mediated signaling is critical for cuprizone-induced demyelination. J Neurosci. 32:8284–8292.
   PubMed Web of Science ®Google Scholar
• Krumbholz M, Theil D, Cepok S, Hemmer B, Kivisäkk P, Ransohoff RM, Hofbauer M, Farina C, Derfuss T, Hartle C, et al. 2006. Chemokines in multiple sclerosis: CXCL12 and CXCL13 up-regulation is differentially linked to CNS immune cell recruitment. Brain. 129:200–211.
   PubMed Web of Science ®Google Scholar
• Lau FC, Shukitt-Hale B, Joseph JA. 2007. Nutritional intervention in brain aging: reducing the effects of inflammation and oxidative stress. Subcell Biochem. 42:299–318.
   PubMedGoogle Scholar
• Lei F, Xing DM, Xiang L, Zhao YN, Wang W, Zhang LJ, Du LJ. 2003. Pharmacokinetic study of ellagic acid in rat after oral administration of pomegranate leaf extract. J Chromatogr B Analyt Technol Biomed Life Sci. 796:189–194.
   PubMed Web of Science ®Google Scholar
• Maheshwari A, Janssens K, Bogie J, Van Den Haute C, Struys T, Lambrichts I, Baekelandt V, Stinissen P, Hendriks JJ, Slaets H, et al. 2013. Local overexpression of IL-11 in the CNS limits demyelination and enhances remyelination. Mediators Inflamm. 2013:685317.
   PubMed Web of Science ®Google Scholar
• Mansouri MT, Farbood Y, Naghizadeh B, Shabani S, Mirshekar MA, Sarkaki A. 2016. Beneficial effects of ellagic acid against animal models of scopolamine- and diazepam-induced cognitive impairments. Pharm Biol. 54:1947–1953.
   PubMed Web of Science ®Google Scholar
• McCandless EE, Wang Q, Woerner BM, Harper JM, Klein RS. 2006. CXCL12 limits inflammation by localizing mononuclear infiltrates to the perivascular space during experimental autoimmune encephalomyelitis. J Immunol. 177:8053–8064.
   PubMed Web of Science ®Google Scholar
• Mishra S, Vinayak M. 2015. Role of ellagic acid in regulation of apoptosis by modulating novel and atypical PKC in lymphoma bearing mice. BMC Complement Altern Med. 15:281.
   PubMed Web of Science ®Google Scholar
• Nadeem M, Sklover L, Sloane JA. 2015. Targeting remyelination treatment for multiple sclerosis. World J Neurol. 5:5–16.
   Google Scholar
• Nagla AES, Eman AEB, Karema ED. 2014. Ellagic acid protects against carrageenan-induced acute inflammation through inhibition of nuclear factor kappa B, inducible cyclooxygenase and proinflammatory cytokines and enhancement of interleukin-10 via an antioxidant mechanism. Int Immunopharmacol. 19:290–299.
   PubMed Web of Science ®Google Scholar
• Navindra PS, Lee R, Heber D. 2004. Bioavailability of ellagic acid in human plasma after consumption of ellagitannins from pomegranate (Punica granatum L.) juice. Clin Chim Acta. 348:63–68.
   PubMed Web of Science ®Google Scholar
• Pasquini LA, Calatayud CA, Bertone Uña AL, Millet V, Pasquini JM, Soto EF. 2007. The neurotoxic effect of cuprizone on oligodendrocytes depends on the presence of pro-inflammatory cytokines secreted by microglia. Neurochem Res. 32:279–292.
   PubMed Web of Science ®Google Scholar
• Patel JR, Mc Candless EE, Dorsey D, Klein RS. 2010. CXCR4 promotes differentiation of oligodendrocyte progenitors and remyelination. Proc Natl Acad Sci USA. 107:11062–11067.
   PubMed Web of Science ®Google Scholar
• Patel JR, Williams JL, Muccigrosso MM, Liu L, Sun T, Rubin JB, Klein RS. 2012. Astrocyte TNFR2 is required for CXCL12-mediated regulation of oligodendrocyte progenitor proliferation and differentiation within the adult CNS. Acta Neuropathol. 124:847–860.
   PubMed Web of Science ®Google Scholar
• Peng H, Erdmann N, Whitney N, Dou H, Gorantla S, Gendelman HE, Ghorpade A, Zheng J. 2006. HIV-1-infected and/or immune activated macrophages regulate astrocyte SDF-1 production through IL-1beta. Glia. 54:619–629.
   PubMed Web of Science ®Google Scholar
• Peng H, Huang Y, Rose J, Erichsen D, Herek S, Fujii N, Tamamura H, Zheng J. 2004. Stromal cell-derived factor 1-mediated CXCR4 signaling in rat and human cortical neural progenitor cells. J Neurosci Res. 76:35–50.
   PubMed Web of Science ®Google Scholar
• Prae J, Guglielmetti C, Berneman Z, Van der Linden A, Ponsaerts P. 2014. Cellular and molecular neuropathology of the cuprizone mouse model: clinical relevance for multiple sclerosis. Neurosci Biobehav Rev. 47:485–505.
   PubMed Web of Science ®Google Scholar
• Ramroodi N, Khani M, Ganjali Z, Javan MR, Sanadgol N, Khalseh R, Abdollahi M. 2015. Prophylactic effect of BIO-1211 small-molecule antagonist of VLA-4 in the EAE mouse model of multiple sclerosis. Immunol Invest. 44:694–712.
   PubMed Web of Science ®Google Scholar
• Reich M, Liefeld T, Gould J, Lerner J, Tamayo P, Mesirov JP. 2006. GenePattern 2.0. Nat Genet. 38:500–501.
   PubMed Web of Science ®Google Scholar
• Rogerio AP, Fontanari C, Borducchi E, Keller AC, Russo M, Soares EG, Albuquerque DA, Faccioli LH. 2008. Anti-inflammatory effects of Lafoensia pacari and ellagic acid in a murine model of asthma. Eur J Pharmacol. 580:262–270.
   PubMed Web of Science ®Google Scholar
• Rojanathammanee L, Puig KL, Combs CK. 2013. Pomegranate polyphenols and extract inhibit nuclear factor of activated T cell activity and microglial activation in vitro and in a transgenic mouse model of Alzheimer disease. J Nutr. 143:597–605.
   PubMed Web of Science ®Google Scholar
• Romo-González T, Chavarría A, Pérez HJ. 2012. Central nervous system: a modified immune surveillance circuit? Brain Behav Immun. 26:823–829.
   PubMed Web of Science ®Google Scholar
• Rosillo MA, Sánchez-Hidalgo M, Cárdeno A, Aparicio-Soto M, Sánchez-Fidalgo S, Villegas I, de la Lastra CA. 2012. Dietary supplementation of an ellagic acid-enriched pomegranate extract attenuates chronic colonic inflammation in rats. Pharmacol Res. 66:235–242.
   PubMed Web of Science ®Google Scholar
• Sanadgol N, Mostafaie A, Bahrami G, Mansouri K, Ghanbari F, Bidmeshkipour A. 2010. Elaidic acid sustains LPS and TNF-alpha induced ICAM-1 and VCAM-I expression on human bone marrow endothelial cells (HBMEC). Clin Biochem. 43:968–972.
   PubMed Web of Science ®Google Scholar
• Sanadgol N, Mostafaie A, Mansouri K, Bahrami GH. 2012. Effect of palmitic acid and linoleic acid on expression of ICAM-1 and VCAM-1 in human bone marrow endothelial cells. Arch Med Sci. 8:192–198.
   PubMed Web of Science ®Google Scholar
• Sanadgol N, Golab F, Mostafaie A, Mehdizadeh M, Abdollahi M, Sharifzadeh M, Ravan H. 2016. Ellagic acid ameliorates cuprizone-induced acute CNS inflammation via restriction of microgliosis and down-regulation of CCL2 and CCL3 pro-inflammatory chemokines. Cell Mol Biol (Noisy-Le-Grand). 62:24–30.
   PubMed Web of Science ®Google Scholar
• Sanadgol N, Zahedani SS, Sharifzadeh M, Khalseh R, Barbari GR, Abdollahi M. Forthcoming 2017. Recent updates in imperative natural compounds for healthy brain and nerve function: a systematic review of implications for multiple sclerosis. Curr Drug Targets.
   PubMed Web of Science ®Google Scholar
• Sanchooli J, Ramroodi N, Sanadgol N, Sarabandi V, Ravan H, Saebi Rad R. 2014. Relationship between metalloproteinase 2 and 9 concentrations and soluble CD154 expression in Iranian patients with multiple sclerosis. Kaohsiung J Med Sci. 30:235–242.
   PubMed Web of Science ®Google Scholar
• Skripuletz T, Hackstette D, Bauer K, Gudi V, Pul R, Voss E, Berger K, Kipp M, Baumgärtner W, Stangel M. 2013. Astrocytes regulate myelin clearance through recruitment of microglia during cuprizone-induced demyelination. Brain. 136:147–167.
   PubMed Web of Science ®Google Scholar
• Stasiolek M, Bayas A, Kruse N, Wieczarkowiecz A, Toyka KV. 2006. Impaired maturation and altered regulatory function of plasmacytoid dendritic cells in multiple sclerosis. Brain. 129:1293–1305.
   PubMed Web of Science ®Google Scholar
• Tanaka T, Yoshida S. 2014. Mechanisms of remyelination: recent insight from experimental models. Biomol Concepts. 5:289–298.
   PubMedGoogle Scholar
• Touqeer A, William SN, Nabavi SF, Ilkay EO, Nady B, Eduardo S, Nabavi SM. 2016. Insights into effects of ellagic acid on the nervous system: a mini review. Curr Pharm Des. 22:1350–1360.
   PubMed Web of Science ®Google Scholar
• Trapp BD, Nave KA. 2008. Multiple sclerosis: an immune or neurodegenerative disorder. Annu Rev Neurosci. 31:247–269.
   PubMed Web of Science ®Google Scholar
• Umesalma S, Sudhandiran G. 2010. 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. 107:650–655.
   PubMed Web of Science ®Google Scholar
• Uzar E, Alp H, Cevik MU, Fýrat U, Evliyaoglu O, Tufek A, Altun Y. 2012. Ellagic acid attenuates oxidative stress on brain and sciatic nerve and improves histopathology of brain in streptozotocin-induced diabetic rats. Neurol Sci. 33:567–574.
   PubMed Web of Science ®Google Scholar
• Williams JL, Patel JR, Daniels BP, Klein RS. 2014. Targeting CXCR7/ACKR3 as a therapeutic strategy to promote remyelination in the adult central nervous system. J Exp Med. 211:791–799.
   PubMed Web of Science ®Google Scholar
• Yoshikawa K, Palumbo S, Toscano CD, Bosetti F. 2011. Inhibition of 5-lipoxygenase activity in mice during cuprizone-induced demyelination attenuates neuroinflammation, motor dysfunction and axonal damage. Prost Leukot Essent Fat Acids. 85:43–52.
   PubMed Web of Science ®Google Scholar
• Zeisel SH. 2004. Antioxidants suppress apoptosis. J Nutr. 134:3179S–3180S.
   PubMed Web of Science ®Google Scholar
• Zhang J, Zhang Y, Dutta DJ, Argaw AT, Bonnamain V, Seto J, Braun DA, Zameer A, Hayot F, Lòpez CB, et al. 2011. Proapoptotic and antiapoptotic actions of stat1 versus stat3 underlie neuroprotective and immunoregulatory functions of IL-11. J Immunol. 187:1129–1141.
   PubMed Web of Science ®Google Scholar
• Zhang Y, Taveggia C, Melendez-Vasquez C, Einheber S, Raine CS, Salzer JL, Brosnan CF, John GR. 2006. Interleukin-11 potentiates oligodendrocyte survival and maturation, and myelin formation. J Neurosci. 26:12174–12185.
   PubMed Web of Science ®Google Scholar
• Zilkha-Falb R, Kaushansky N, Kawakami N, Ben-Nun A. 2016. Post-CNS-inflammation expression of CXCL12 promotes the endogenous myelin/neuronal repair capacity following spontaneous recovery from multiple sclerosis-like disease. J Neuroinflam. 13:7.
   PubMed Web of Science ®Google Scholar