262
Views
15
CrossRef citations to date
0
Altmetric
Original Research

Liposomal Encapsulated Curcumin Effectively Attenuates Neuroinflammatory and Reactive Astrogliosis Reactions in Glia Cells and Organotypic Brain Slices

ORCID Icon, , , , ORCID Icon, , , & show all
Pages 3649-3667 | Published online: 25 May 2020

References

  • Linnaeus C. Species Plantarum. Stockholm: Lars Salvius; 1753.
  • Adiwidjaja J, McLachlan AJ, Boddy AV. Curcumin as a clinically-promising anti-cancer agent: pharmacokinetics and drug interactions. Expert Opin Drug Metab Toxicol. 2017;13(9):953–972. doi:10.1080/17425255.2017.136027928776444
  • Deguchi A. Curcumin targets in inflammation and cancer. Endocr Metab Immune Disord Drug Targets. 2015;15(2):88–96. doi:10.2174/187153031566615031612045825772169
  • Naksuriya O, Okonogi S, Schiffelers RM, Hennink WE. Curcumin nanoformulations: a review of pharmaceutical properties and preclinical studies and clinical data related to cancer treatment. Biomaterials. 2014;35(10):3365–3383. doi:10.1016/j.biomaterials.2013.12.09024439402
  • Wong KE, Ngai SC, Chan KG, Lee LH, Goh BH, Chuah LH. Curcumin nanoformulations for colorectal cancer: a review. Front Pharmacol. 2019;10:152. doi:10.3389/fphar.2019.0015230890933
  • Gupta SC, Patchva S, Aggarwal BB. Therapeutic roles of curcumin: lessons learned from clinical trials. AAPS J. 2013;15(1):195–218. doi:10.1208/s12248-012-9432-823143785
  • Yang M, Akbar U, Mohan C. Curcumin in autoimmune and rheumatic diseases. Nutrients. 2019;11(5):E1004. doi:10.3390/nu1105100431052496
  • Farkhondeh T, Samarghandian S, Pourbagher-Shahri AM, Sedaghat M. The impact of curcumin and its modified formulations on Alzheimer’s disease. J Cell Physiol. 2019;234(10):16953–16965. doi:10.1002/jcp.2841130847942
  • Lim GP, Chu T, Yang F, Beech W, Frautschy SA, Cole GM. The curry spice curcumin reduces oxidative damage and amyloid pathology in an Alzheimer transgenic mouse. J Neurosci. 2001;21(21):8370–8377. doi:10.1523/JNEUROSCI.21-21-08370.200111606625
  • Ramkumar M, Rajasankar S, Gobi VV, et al. Demethoxycurcumin, a natural derivative of curcumin abrogates rotenone-induced dopamine depletion and motor deficits by its antioxidative and anti-inflammatory properties in parkinsonian rats. Pharmacogn Mag. 2018;14(53):9–16. doi:10.4103/pm.pm_113_1729576695
  • Tripanichkul W, Jaroensuppaperch EO. Ameliorating effects of curcumin on 6-OHDA-induced dopaminergic denervation, glial response, and SOD1 reduction in the striatum of hemiparkinsonian mice. Eur Rev Med Pharmacol Sci. 2013;17(10):1360–1368.23740450
  • Arora V, Kuhad A, Tiwari V, Chopra K. Curcumin ameliorates reserpine-induced pain-depression dyad: behavioural, biochemical, neurochemical and molecular evidences. Psychoneuroendocrinology. 2011;36(10):1570–1581. doi:10.1016/j.psyneuen.2011.04.01221612876
  • Sun J, Chen F, Braun C, et al. Role of curcumin in the management of pathological pain. Phytomedicine. 2018;48:129–140. doi:10.1016/j.phymed.2018.04.04530195871
  • Drion CM, Borm LE, Kooijman L, et al. Effects of rapamycin and curcumin treatment on the development of epilepsy after electrically induced status epilepticus in rats. Epilepsia. 2016;57(5):688–697. doi:10.1111/epi.1334526924447
  • Bavarsad K, Barreto GE, Hadjzadeh MA, Sahebkar A. Protective effects of curcumin against ischemia-reperfusion injury in the nervous system. Mol Neurobiol. 2018.
  • Zhang Y, Fang M, Sun Y, et al. Curcumin attenuates cerebral ischemia injury in Sprague-Dawley rats and PC12 cells by suppressing overactivated autophagy. J Photochem Photobiol B. 2018;184:1–6. doi:10.1016/j.jphotobiol.2018.05.01029777940
  • Deng Y, Lu X, Wang L, et al. Curcumin inhibits the AKT/NF-kappaB signaling via CpG demethylation of the promoter and restoration of NEP in the N2a cell line. AAPS J. 2014;16(4):649–657. doi:10.1208/s12248-014-9605-824756894
  • Dong W, Yang B, Wang L, et al. Curcumin plays neuroprotective roles against traumatic brain injury partly via Nrf2 signaling. Toxicol Appl Pharmacol. 2018;346:28–36. doi:10.1016/j.taap.2018.03.02029571711
  • Kim HY, Park EJ, Joe EH, Jou I. Curcumin suppresses Janus kinase-STAT inflammatory signaling through activation of Src homology 2 domain-containing tyrosine phosphatase 2 in brain microglia. J Immunol. 2003;171(11):6072–6079. doi:10.4049/jimmunol.171.11.607214634121
  • Shi X, Zheng Z, Li J, et al. Curcumin inhibits Abeta-induced microglial inflammatory responses in vitro: involvement of ERK1/2 and p38 signaling pathways. Neurosci Lett. 2015;594:105–110. doi:10.1016/j.neulet.2015.03.04525818332
  • Tu XK, Yang WZ, Chen JP, et al. Curcumin inhibits TLR2/4-NF-kappaB signaling pathway and attenuates brain damage in permanent focal cerebral ischemia in rats. Inflammation. 2014;37(5):1544–1551. doi:10.1007/s10753-014-9881-624723245
  • Mhillaj E, Tarozzi A, Pruccoli L, Cuomo V, Trabace L, Mancuso C. Curcumin and heme oxygenase: neuroprotection and beyond. Int J Mol Sci. 2019;20:10. doi:10.3390/ijms20102419
  • Yang Z, Zhao T, Zou Y, Zhang JH, Feng H. Curcumin inhibits microglia inflammation and confers neuroprotection in intracerebral hemorrhage. Immunol Lett. 2014;160(1):89–95. doi:10.1016/j.imlet.2014.03.00524680995
  • Ghasemi F, Bagheri H, Barreto GE, Read MI, Sahebkar A. Effects of curcumin on microglial cells. Neurotox Res. 2019;36(1):12–26. doi:10.1007/s12640-019-00030-030949950
  • Parada E, Buendia I, Navarro E, Avendano C, Egea J, Lopez MG. Microglial HO-1 induction by curcumin provides antioxidant, antineuroinflammatory, and glioprotective effects. Mol Nutr Food Res. 2015;59(9):1690–1700. doi:10.1002/mnfr.20150027926047311
  • Bondan E, Cardoso C, Martins MF. Curcumin decreases astrocytic reaction after gliotoxic injury in the rat brainstem. Arq Neuropsiquiatr. 2017;75(8):546–552. doi:10.1590/0004-282x2017009228813085
  • Wang YF, Zu JN, Li J, Chen C, Xi CY, Yan JL. Curcumin promotes the spinal cord repair via inhibition of glial scar formation and inflammation. Neurosci Lett. 2014;560:51–56. doi:10.1016/j.neulet.2013.11.05024316441
  • Yuan J, Liu W, Zhu H, et al. Curcumin inhibits glial scar formation by suppressing astrocyte-induced inflammation and fibrosis in vitro and in vivo. Brain Res. 2017;1655:90–103. doi:10.1016/j.brainres.2016.11.00227865778
  • Yuan J, Zou M, Xiang X, et al. Curcumin improves neural function after spinal cord injury by the joint inhibition of the intracellular and extracellular components of glial scar. J Surg Res. 2015;195(1):235–245. doi:10.1016/j.jss.2014.12.05525661742
  • Machova Urdzikova L, Karova K, Ruzicka J, et al. The anti-inflammatory compound curcumin enhances locomotor and sensory recovery after spinal cord injury in rats by immunomodulation. Int J Mol Sci. 2015;17:1. doi:10.3390/ijms17010049
  • Lestari ML, Indrayanto G. Curcumin. Profiles Drug Subst Excip Relat Methodol. 2014;39:113–204.24794906
  • Yang KY, Lin LC, Tseng TY, Wang SC, Tsai TH. Oral bioavailability of curcumin in rat and the herbal analysis from Curcuma longa by LC-MS/MS. J Chromatogr B Analyt Technol Biomed Life Sci. 2007;853(1–2):183–189. doi:10.1016/j.jchromb.2007.03.010
  • Liu W, Zhai Y, Heng X, et al. Oral bioavailability of curcumin: problems and advancements. J Drug Target. 2016;24(8):694–702. doi:10.3109/1061186X.2016.115788326942997
  • Del Prado-Audelo ML, Caballero-Floran IH, Meza-Toledo JA, et al. Formulations of curcumin nanoparticles for brain diseases. Biomolecules. 2019;9:2. doi:10.3390/biom9020056
  • Fereydouni N, Darroudi M, Movaffagh J, et al. Curcumin nanofibers for the purpose of wound healing. J Cell Physiol. 2019;234(5):5537–5554. doi:10.1002/jcp.2736230370528
  • Jamwal R. Bioavailable curcumin formulations: A review of pharmacokinetic studies in healthy volunteers. J Integr Med. 2018;16(6):367–374. doi:10.1016/j.joim.2018.07.00130006023
  • Khan I, Saeed K, Khan I. Nanoparticles: properties, applications and toxicities. Arab J Chem. 2019;12(7):908–931. doi:10.1016/j.arabjc.2017.05.011
  • Hoshyar N, Gray S, Han H, Bao G. The effect of nanoparticle size on in vivo pharmacokinetics and cellular interaction. Nanomedicine. 2016;11(6):673–692. doi:10.2217/nnm.16.527003448
  • Choi YH, Han HK. Correction to: nanomedicines: current status and future perspectives in aspect of drug delivery and pharmacokinetics. J Pharm Invest. 2019;49(1):201. doi:10.1007/s40005-018-00412-0
  • Bulbake U, Doppalapudi S, Kommineni N, Khan W. Liposomal formulations in clinical use: an updated review. Pharmaceutics. 2017;9:2. doi:10.3390/pharmaceutics9020012
  • Johnston MJ, Semple SC, Klimuk SK, Ansell S, Maurer N, Cullis PR. Characterization of the drug retention and pharmacokinetic properties of liposomal nanoparticles containing dihydrosphingomyelin. Biochim Biophys Acta. 2007;1768(5):1121–1127. doi:10.1016/j.bbamem.2007.01.01917321495
  • Akbarzadeh A, Rezaei-Sadabady R, Davaran S, et al. Liposome: classification, preparation, and applications. Nanoscale Res Lett. 2013;8(1):102. doi:10.1186/1556-276X-8-10223432972
  • Sabin J, Prieto G, Ruso JM, Hidalgo-Alvarez R, Sarmiento F. Size and stability of liposomes: a possible role of hydration and osmotic forces. Eur Phys J E Soft Matter. 2006;20(4):401–408. doi:10.1140/epje/i2006-10029-916957831
  • Al-Jamal WT, Kostarelos K. Liposome–nanoparticle hybrids for multimodal diagnostic and therapeutic applications. Nanomedicine. 2007;2(1):85–98. doi:10.2217/17435889.2.1.8517716195
  • Basnet P, Hussain H, Tho I, Skalko-Basnet N. Liposomal delivery system enhances anti-inflammatory properties of curcumin. J Pharm Sci. 2012;101(2):598–609. doi:10.1002/jps.2278521989712
  • Chen Y, Wu Q, Zhang Z, Yuan L, Liu X, Zhou L. Preparation of curcumin-loaded liposomes and evaluation of their skin permeation and pharmacodynamics. Molecules. 2012;17(5):5972–5987. doi:10.3390/molecules1705597222609787
  • Cheng C, Peng S, Li Z, Zou L, Liu W, Liu C. Improved bioavailability of curcumin in liposomes prepared using a pH-driven, organic solvent-free, easily scalable process. RSC Adv. 2017;7(42):25978–25986. doi:10.1039/C7RA02861J
  • Feng T, Wei Y, Lee RJ, Zhao L. Liposomal curcumin and its application in cancer. Int J Nanomedicine. 2017;12:6027–6044. doi:10.2147/IJN.S13243428860764
  • Roy A, Saha S, Choudhury A, Bahadur S. Bioenhancement of curcumin by combined approaches of adjuvants and liposomal fabrication. Asian J Pharm. 2016;10:4.
  • Mercanti G, Ragazzi E, Toffano G, Giusti P, Zusso M. Phosphatidylserine and curcumin act synergistically to down-regulate release of interleukin-1beta from lipopolysaccharide-stimulated cortical primary microglial cells. CNS Neurol Disord Drug Targets. 2014;13(5):792–800. doi:10.2174/187152731366614041412172324725086
  • Wang Y, Luo J, Li SY. Nano-curcumin simultaneously protects the blood-brain barrier and reduces M1 microglial activation during cerebral ischemia-reperfusion injury. 2.
  • Marin C, Fernandez E. Biocompatibility of intracortical microelectrodes: current status and future prospects. Front Neuroeng. 2010;3:8. doi:10.3389/fneng.2010.0000820577634
  • Polikov VS, Tresco PA, Reichert WM. Response of brain tissue to chronically implanted neural electrodes. J Neurosci Methods. 2005;148(1):1–18. doi:10.1016/j.jneumeth.2005.08.01516198003
  • Arnold P, Himmels P, Weiss S, et al. Antigenic and 3D structural characterization of soluble X4 and hybrid X4-R5 HIV-1 Env trimers. Retrovirology. 2014;11(1):42. doi:10.1186/1742-4690-11-4224884925
  • Henriksen S, Tylden GD, Dumoulin A, Sharma BN, Hirsch HH, Rinaldo CH. The human fetal glial cell line SVG p12 contains infectious BK polyomavirus. J Virol. 2014;88(13):7556–7568. doi:10.1128/JVI.00696-1424760884
  • Schweighardt B, Shieh JT, Atwood WJ. CD4/CXCR4-independent infection of human astrocytes by a T-tropic strain of HIV-1. J Neurovirol. 2001;7(2):155–162. doi:10.1080/1355028015205881611517388
  • Schommer J, Schrag M, Nackenoff A, Marwarha G, Ghribi O. Method for organotypic tissue culture in the aged animal. MethodsX. 2017;4:166–171. doi:10.1016/j.mex.2017.03.00328462173
  • Stoppini L, Buchs PA, Muller D. A simple method for organotypic cultures of nervous tissue. J Neurosci Methods. 1991;37(2):173–182. doi:10.1016/0165-0270(91)90128-M1715499
  • Mewes A, Franke H, Singer D. Organotypic brain slice cultures of adult transgenic P301S mice–a model for tauopathy studies. PLoS One. 2012;7(9):e45017. doi:10.1371/journal.pone.004501722984603
  • Adamski V, Schmitt C, Ceynowa F, et al. Effects of sequentially applied single and combined temozolomide, hydroxychloroquine and AT101 treatment in a long-term stimulation glioblastoma in vitro model. J Cancer Res Clin Oncol. 2018;144(8):1475–1485. doi:10.1007/s00432-018-2680-y29858681
  • Lin MS, Lee YH, Chiu WT, Hung KS. Curcumin provides neuroprotection after spinal cord injury. J Surg Res. 2011;166(2):280–289. doi:10.1016/j.jss.2009.07.00120018302
  • Zhang N, Wei G, Ye J, et al. Effect of curcumin on acute spinal cord injury in mice via inhibition of inflammation and TAK1 pathway. Pharmacol Rep. 2017;69(5):1001–1006. doi:10.1016/j.pharep.2017.02.01228941865
  • Nelson KM, Dahlin JL, Bisson J, Graham J, Pauli GF, Walters MA. The essential medicinal chemistry of curcumin. J Med Chem. 2017;60(5):1620–1637. doi:10.1021/acs.jmedchem.6b0097528074653
  • Potter KA, Jorfi M, Householder KT, Foster EJ, Weder C, Capadona JR. Curcumin-releasing mechanically adaptive intracortical implants improve the proximal neuronal density and blood-brain barrier stability. Acta Biomater. 2014;10(5):2209–2222. doi:10.1016/j.actbio.2014.01.01824468582
  • Raza F, Zafar H, You X, Khan A, Wu J, Ge L. Cancer nanomedicine: focus on recent developments and self-assembled peptide nanocarriers. J Mater Chem B. 2019;7(48):7639–7655. doi:10.1039/C9TB01842E31746934
  • Roy B, Guha P, Bhattarai R, et al. Influence of lipid composition, pH, and temperature on physicochemical properties of liposomes with curcumin as model drug. J Oleo Sci. 2016;65(5):399–411. doi:10.5650/jos.ess1522927150333
  • Franze S, Selmin F, Samaritani E, Minghetti P, Cilurzo F. Lyophilization of liposomal formulations: still necessary, still challenging. Pharmaceutics. 2018;10:3. doi:10.3390/pharmaceutics10030139
  • van Winden ECA, Crommelin DJ. Long term stability of freeze-dried, lyoprotected doxorubicin liposomes. Eur J Pharm Biopharm. 1997;43(3):295–307. doi:10.1016/S0939-6411(97)00058-1
  • Mohammed AR, Coombes AG, Perrie Y. Amino acids as cryoprotectants for liposomal delivery systems. Eur J Pharm Sci. 2007;30(5):406–413. doi:10.1016/j.ejps.2007.01.00117317117
  • Zhao M, Zhao M, Fu C, Yu Y, Fu A. Targeted therapy of intracranial glioma model mice with curcumin nanoliposomes. Int J Nanomedicine. 2018;13:1601–1610.29588587
  • Sofroniew MV. Molecular dissection of reactive astrogliosis and glial scar formation. Trends Neurosci. 2009;32(12):638–647. doi:10.1016/j.tins.2009.08.00219782411
  • Jin CY, Lee JD, Park C, Choi YH, Kim GY. Curcumin attenuates the release of pro-inflammatory cytokines in lipopolysaccharide-stimulated BV2 microglia. Acta Pharmacol Sin. 2007;28(10):1645–1651. doi:10.1111/j.1745-7254.2007.00651.x17883952
  • Karlstetter M, Lippe E, Walczak Y, et al. Curcumin is a potent modulator of microglial gene expression and migration. J Neuroinflammation. 2011;8(1):125. doi:10.1186/1742-2094-8-12521958395
  • Guo L, Xing Y, Pan R, et al. Curcumin protects microglia and primary rat cortical neurons against HIV-1 gp120-mediated inflammation and apoptosis. PLoS One. 2013;8(8):e70565. doi:10.1371/journal.pone.007056523936448
  • Cianciulli A, Calvello R, Porro C, Trotta T, Salvatore R, Panaro MA. PI3k/Akt signalling pathway plays a crucial role in the anti-inflammatory effects of curcumin in LPS-activated microglia. Int Immunopharmacol. 2016;36:282–290. doi:10.1016/j.intimp.2016.05.00727208432
  • Ding F, Li F, Li Y, et al. HSP60 mediates the neuroprotective effects of curcumin by suppressing microglial activation. Exp Ther Med. 2016;12(2):823–828. doi:10.3892/etm.2016.341327446282
  • Qin X, Qiao H, Wu S, Cheng J, Wan Q, Liu R. Curcumin inhibits monocyte chemoattractant Protein-1 expression in TNF-alpha induced astrocytes through AMPK pathway. Neurochem Res. 2018;43(4):775–784. doi:10.1007/s11064-018-2479-x29460119
  • Seyedzadeh MH, Safari Z, Zare A, et al. Study of curcumin immunomodulatory effects on reactive astrocyte cell function. Int Immunopharmacol. 2014;22(1):230–235. doi:10.1016/j.intimp.2014.06.03524998635
  • Daverey A, Agrawal SK. Curcumin alleviates oxidative stress and mitochondrial dysfunction in astrocytes. Neuroscience. 2016;333:92–103. doi:10.1016/j.neuroscience.2016.07.01227423629
  • Kolter M, Wittmann M, Koll-Weber M, Suss R. The suitability of liposomes for the delivery of hydrophobic drugs - a case study with curcumin. Eur J Pharm Biopharm. 2019;140:20–28. doi:10.1016/j.ejpb.2019.04.01331015019
  • Bollimpelli VS, Kumar P, Kumari S, Kondapi AK. Neuroprotective effect of curcumin-loaded lactoferrin nano particles against rotenone induced neurotoxicity. Neurochem Int. 2016;95:37–45. doi:10.1016/j.neuint.2016.01.00626826319
  • Krupa P, Svobodova B, Dubisova J, Kubinova S, Jendelova P, Machova Urdzikova L. Nano-formulated curcumin (Lipodisq) modulates the local inflammatory response, reduces glial scar and preserves the white matter after spinal cord injury in rats. Neuropharmacology. 2019;155:54–64. doi:10.1016/j.neuropharm.2019.05.01831108112
  • Naeimi R, Safarpour F, Hashemian M, et al. Curcumin-loaded nanoparticles ameliorate glial activation and improve myelin repair in lysolecithin-induced focal demyelination model of rat corpus callosum. Neurosci Lett. 2018;674:1–10. doi:10.1016/j.neulet.2018.03.01829530814
  • Hoppe JB, Haag M, Whalley BJ, Salbego CG, Cimarosti H. Curcumin protects organotypic hippocampal slice cultures from Abeta1-42-induced synaptic toxicity. Toxicol in Vitro. 2013;27(8):2325–2330. doi:10.1016/j.tiv.2013.10.00224134851
  • Hoppe JB, Frozza RL, Pires EN, Meneghetti AB, Salbego C. The curry spice curcumin attenuates beta-amyloid-induced toxicity through beta-catenin and PI3K signaling in rat organotypic hippocampal slice culture. Neurol Res. 2013;35(8):857–866. doi:10.1179/1743132813Y.000000022523816368
  • Choi GY, Kim HB, Hwang ES, et al. Curcumin alters neural plasticity and viability of intact hippocampal circuits and attenuates behavioral despair and COX-2 expression in chronically stressed rats. Mediators Inflamm. 2017;2017:6280925. doi:10.1155/2017/628092528167853
  • Dal Ben M, Bottin C, Zanconati F, Tiribelli C, Gazzin S. Evaluation of region selective bilirubin-induced brain damage as a basis for a pharmacological treatment. Sci Rep. 2017;7:41032. doi:10.1038/srep4103228102362
  • Drion CM, Kooijman L, Aronica E, et al. Curcumin reduces development of seizurelike events in the hippocampal-entorhinal cortex slice culture model for epileptogenesis. Epilepsia. 2019;60(4):605–614. doi:10.1111/epi.1466730747999