Generic placeholder image

Mini-Reviews in Medicinal Chemistry

Editor-in-Chief

ISSN (Print): 1389-5575
ISSN (Online): 1875-5607

Mini-Review Article

Recent Developments on the Use of Nanomaterials for the Treatment of Epilepsy

Author(s): Sara G. Pedrero, Davide Staedler and Sandrine Gerber-Lemaire*

Volume 22, Issue 11, 2022

Published on: 06 January, 2022

Page: [1460 - 1475] Pages: 16

DOI: 10.2174/1389557521666210805113647

Price: $65

Abstract

Epilepsy affects more than 40 million people worldwide, constituting one of the most debilitating disorders of the Central Nervous System (CNS). It results from an imbalance in the electrical activity of neurons, which is primarily mediated by calcium ions. In many cases, treatment with Antiepileptic Drugs (AEDs) that regulate calcium channel activity results in successful seizure control. However, AEDs frequently cause adverse effects that range in severity from minimal impairment of the CNS to death from aplastic anemia or hepatic failure. Moreover, 30% of epileptic patients show drug-resistant epilepsy and do not respond to any form of medical treatment. In this context, nanotechnology has emerged as an excellent tool to overcome AEDs limitations. Numerous nano-strategies have been proposed as therapeutics and diagnostics for epilepsy through inhibition of different calcium channel types in the brain. In addition, limited brain access of classical AEDs in patients showing refractory epilepsy could be improved through the design of targeted drug delivery nanosystems. This report presents a review of the nanocarriers developed so far that could facilitate the interaction with calcium channels in the brain and the transport of AEDs through the blood-brain-barrier, mapping out a potential future direction in the research of epilepsy treatment.

Keywords: Epilepsy, nanomaterials, calcium channels, central nervous system, blood-brain barrier, drug delivery, antiepileptic drugs.

Graphical Abstract
[1]
Du, W.; Bautista, J.F.; Yang, H.; Diez-Sampedro, A.; You, S-A.; Wang, L.; Kotagal, P.; Lüders, H.O.; Shi, J.; Cui, J.; Richerson, G.B.; Wang, Q.K. Calcium-sensitive potassium channelopathy in human epilepsy and paroxysmal movement disorder. Nat. Genet., 2005, 37(7), 733-738.
[http://dx.doi.org/10.1038/ng1585] [PMID: 15937479]
[2]
Fletcher, C.F.; Lutz, C.M.; O’Sullivan, T.N.; Shaughnessy, J.D.; Hawkes, R.; Frankel, W.N.; Copeland, N.G.; Jenkins, N.A. Absence epilepsy in tottering mutant mice is associated with calcium channel defects. 11
[3]
Cano, A.; Ettcheto, M.; Espina, M.; Auladell, C.; Calpena, A.C.; Folch, J.; Barenys, M.; Sánchez-López, E.; Camins, A.; García, M.L. Epi-gallocatechin-3-gallate loaded PEGylated-PLGA nanoparticles: A new anti-seizure strategy for temporal lobe epilepsy. Nanomedicine (Lond.), 2018, 14(4), 1073-1085.
[http://dx.doi.org/10.1016/j.nano.2018.01.019] [PMID: 29454994]
[4]
Pedram, M.Z.; Shamloo, A.; Alasty, A.; Ghafar-Zadeh, E. Toward epileptic brain region detection based on magnetic nanoparticle patter-ning., 2015 19.
[http://dx.doi.org/10.3390/s150924409]
[5]
Goldenberg, M.M. Overview of drugs used for epilepsy and seizures. 24,
[6]
Zamponi, G.W.; Lory, P.; Perez-Reyes, E. Role of voltage-gated calcium channels in epilepsy. Pflugers Arch., 2010, 460(2), 395-403.
[http://dx.doi.org/10.1007/s00424-009-0772-x] [PMID: 20091047]
[7]
Khosravani, H.; Zamponi, G.W. Voltage-gated calcium channels and idiopathic generalized epilepsies. Physiol. Rev., 2006, 86(3), 941-966.
[http://dx.doi.org/10.1152/physrev.00002.2006] [PMID: 16816142]
[8]
Weiergräber, M.; Stephani, U.; Köhling, R. Voltage-gated calcium channels in the etiopathogenesis and treatment of absence epilepsy. Brain Res. Brain Res. Rev., 2010, 62(2), 245-271.
[http://dx.doi.org/10.1016/j.brainresrev.2009.12.005] [PMID: 20026356]
[9]
Belardetti, F.; Zamponi, G.W. Calcium channels as therapeutic targets., 2012. 1, 19.
[10]
Pietrobon, D. Calcium channels and channelopathies of the central nervous system. Mol. Neurobiol., 2002, 25(1), 31-50.
[http://dx.doi.org/10.1385/MN:25:1:031] [PMID: 11890456]
[11]
Yin, S.; Liu, J.; Kang, Y.; Lin, Y.; Li, D.; Shao, L. Interactions of nanomaterials with ion channels and related mechanisms. Br. J. Pharmacol., 2019, 176(19), 3754-3774.
[12]
Joksimovic, S.Lj.; Donald, R.R.; Park, J-Y.; Todorovic, S.M. Inhibition of multiple voltage-gated calcium channels may contribute to spi-nally mediated analgesia by epipregnanolone in a rat model of surgical paw incision. Channels (Austin), 2019, 13(1), 48-61.
[http://dx.doi.org/10.1080/19336950.2018.1564420] [PMID: 30672394]
[13]
Rajakulendran, S.; Hanna, M.G. The role of calcium channels in epilepsy. 21
[14]
Neumaier, F.; Dibué-Adjei, M.; Hescheler, J.; Schneider, T. Voltage-gated calcium channels: Determinants of channel function and modu-lation by inorganic cations. Prog. Neurobiol., 2015, 129, 1-36.
[http://dx.doi.org/10.1016/j.pneurobio.2014.12.003] [PMID: 25817891]
[15]
Huang, J.; Zamponi, G.W. Regulation of voltage gated calcium channels by GPCRs and post-translational modification. Curr. Opin. Pharmacol., 2017, 32, 1-8.
[http://dx.doi.org/10.1016/j.coph.2016.10.001] [PMID: 27768908]
[16]
Catterall, W.A. Structure and regulation of voltage-gated Ca2+ channels. Annu. Rev. Cell Dev. Biol., 2000, 16, 521-555.
[http://dx.doi.org/10.1146/annurev.cellbio.16.1.521] [PMID: 11031246]
[17]
Bünemann, M.; Gerhardstein, B.L.; Gao, T.; Hosey, M.M. Functional regulation of L-type calcium channels via protein kinase A-mediated phosphorylation of the beta(2) subunit. J. Biol. Chem., 1999, 274(48), 33851-33854.
[http://dx.doi.org/10.1074/jbc.274.48.33851] [PMID: 10567342]
[18]
Lei, M.; Xu, J.; Gao, Q.; Minobe, E.; Kameyama, M.; Hao, L. PKA phosphorylation of Cav1.2 channel modulates the interaction of cal-modulin with the C terminal tail of the channel. J. Pharmacol. Sci., 2018, 137(2), 187-194.
[http://dx.doi.org/10.1016/j.jphs.2018.05.010] [PMID: 30042022]
[19]
Oldham, W.M.; Hamm, H.E.; Heterotrimeric, G. Heterotrimeric G protein activation by G-protein-coupled receptors. Nat. Rev. Mol. Cell Biol., 2008, 9(1), 60-71.
[http://dx.doi.org/10.1038/nrm2299] [PMID: 18043707]
[20]
Dolphin, A.C. A short history of voltage‐gated calcium channels. 147(7)
[21]
Stotz, S.C.; Jarvis, S.E.; Zamponi, G.W. Functional roles of cytoplasmic loops and pore lining transmembrane helices in the voltage-dependent inactivation of HVA calcium channels. J. Physiol., 2004, 554(Pt 2), 263-273.
[http://dx.doi.org/10.1113/jphysiol.2003.047068] [PMID: 12815185]
[22]
Berrou, L.; Bernatchez, G.; Parent, L. Molecular determinants of inactivation within the I-II linker of alpha1E (CaV2.3) calcium channels. Biophys. J., 80(1), 215-228.
[23]
Halling, D.B.; Aracena-Parks, P.; Hamilton, S.L. Regulation of voltage-gated Ca2+ channels by calmodulin. Sci. STKE, 2005, 2005(315), re15.
[PMID: 16369047]
[24]
Shah, V.N.; Chagot, B.; Chazin, W.J. Calcium-dependent regulation of ion channels. Cal. Bind Prot., 2017, 1(4), 203-212.
[25]
Cazade, M.; Bidaud, I.; Lory, P.; Chemin, J. Activity-dependent regulation of T-type calcium channels by submembrane calcium ions. eLife, 2017, 6, e22331.
[http://dx.doi.org/10.7554/eLife.22331] [PMID: 28109159]
[26]
Simms, B.A.; Zamponi, G.W. Neuronal voltage-gated calcium channels: Structure, function, and dysfunction. Neuron, 2014, 82(1), 24-45.
[http://dx.doi.org/10.1016/j.neuron.2014.03.016] [PMID: 24698266]
[27]
Martin, C.R.; Preedy, V.R. Nanomedicine and the nervous system.2012 426.,
[http://dx.doi.org/10.1201/b11835]
[28]
Elinder, F.; Århem, P. Metal ion effects on ion channel gating. Q. Rev. Biophys., 2003, 36(4), 373-427.
[http://dx.doi.org/10.1017/S0033583504003932] [PMID: 15267168]
[29]
Guo, D.; Bi, H.; Wang, D.; Wu, Q. Zinc oxide nanoparticles decrease the expression and activity of plasma membrane calcium ATPase, disrupt the intracellular calcium homeostasis in rat retinal ganglion cells. Int. J. Biochem. Cell Biol., 2013, 45(8), 1849-1859.
[http://dx.doi.org/10.1016/j.biocel.2013.06.002] [PMID: 23764618]
[30]
Tang, M.; Wang, M.; Xing, T.; Zeng, J.; Wang, H.; Ruan, D-Y. Mechanisms of unmodified CdSe quantum dot-induced elevation of cyto-plasmic calcium levels in primary cultures of rat hippocampal neurons. Biomaterials, 2008, 29(33), 4383-4391.
[http://dx.doi.org/10.1016/j.biomaterials.2008.08.001] [PMID: 18752844]
[31]
Park, K.H.; Chhowalla, M.; Iqbal, Z.; Sesti, F. Single-walled carbon nanotubes are a new class of ion channel blockers. J. Biol. Chem., 2003, 278(50), 50212-50216.
[http://dx.doi.org/10.1074/jbc.M310216200] [PMID: 14522977]
[32]
Ni, Y.; Hu, H.; Malarkey, E.B.; Zhao, B.; Montana, V.; Haddon, R.C.; Parpura, V. Chemically functionalized water soluble single-walled carbon nanotubes modulate neurite outgrowth.2005, 5(10), 1707-1712.,
[http://dx.doi.org/10.1166/jnn.2005.189]
[33]
Chhowalla, M.; Unalan, H.E.; Wang, Y.; Iqbal, Z.; Park, K.; Sesti, F. Irreversible blocking of ion channels using functionalized single-walled carbon nanotubes. Nanotechnology, 2005, 16, 2982-2986.
[http://dx.doi.org/10.1088/0957-4484/16/12/042]
[34]
Xu, H.; Bai, J.; Meng, J.; Hao, W.; Xu, H.; Cao, J.-M. Multi-walled carbon nanotubes suppress potassium channel activities in pc12 cells.2009, 20(28), 285102.,
[http://dx.doi.org/10.1088/0957-4484/20/28/285102]
[35]
Jakubek, L.M.; Marangoudakis, S.; Raingo, J.; Liu, X.; Lipscombe, D.; Hurt, R.H. The inhibition of neuronal calcium ion channels by trace levels of yttrium released from carbon nanotubes. Biomaterials, 2009, 30(31), 6351-6357.
[http://dx.doi.org/10.1016/j.biomaterials.2009.08.009] [PMID: 19698989]
[36]
Hilder, T.A.; Chung, S-H. Designing a C84 fullerene as a specific voltage-gated sodium channel blocker. Nanoscale Res. Lett., 2013, 8(1), 323.
[http://dx.doi.org/10.1186/1556-276X-8-323] [PMID: 23855749]
[37]
Lee, D.; Hong, J.H. Physiological application of nanoparticles in calcium-related proteins and channels. Nanomedicine (Lond.), 2019, 14(18), 2479-2486.
[http://dx.doi.org/10.2217/nnm-2019-0004] [PMID: 31456482]
[38]
Bryant, S.L.; Eixenberger, J.E.; Rossland, S.; Apsley, H.; Hoffmann, C.; Shrestha, N.; McHugh, M.; Punnoose, A.; Fologea, D. ZnO nano-particles modulate the ionic transport and voltage regulation of lysenin nanochannels. J. Nanobiotechnology, 2017, 15(1), 90.
[http://dx.doi.org/10.1186/s12951-017-0327-9] [PMID: 29246155]
[39]
Jingxia, Z.; Lanju, X.; Tao, Z.; Guogang, R.; Zhuo, Y. Influences of nanoparticle zinc oxide on acutely isolated rat hippocampal ca3 pyra-midal neurons. Neurotoxicology, 2009, 30(2), 220-230.
[40]
Piscopo, S.; Brown, E.R. Zinc oxide nanoparticles and voltagegated human kv11.1 potassium channels interact through a novel mecha-nism. Small, 2018, 14(15), e1703403.
[41]
Gu, Z.; Plant, L.D.; Meng, X-Y.; Perez-Aguilar, J.M.; Wang, Z.; Dong, M.; Logothetis, D.E.; Zhou, R. Exploring the nanotoxicology of mos2: A study on the interaction of mos2 nanoflakes and k+ channels. ACS Nano, 2018, 12(1), 705-717.
[http://dx.doi.org/10.1021/acsnano.7b07871] [PMID: 29236481]
[42]
Strauss, D.J.; Busse, M. Stevens, ; Kraegeloh, ; Cavelius, C.; Vukelic, M.; Arzt, Estimating the modulatory effects of nanoparticles on neuronal circuits using computational upscaling. Int. J. Nanomed., 2013, 3559.
[http://dx.doi.org/10.2147/IJN.S43663]
[43]
Zhao, J.; Yao, Y.; Liu, S.; Zhang, T.; Ren, G.; Yang, Z. Involvement of reactive oxygen species and high-voltage-activated calcium cu-rrents in nanoparticle zinc oxide-induced cytotoxicity in vitro. J. Nanopart. Res., 2012, 14.
[http://dx.doi.org/10.1007/s11051-012-1238-1]
[44]
Nazroğlu, M. Nanoparticles as potential clinical therapeutic agents in alzheimers disease: Focus on selenium nanoparticles. Expert Rev. Clin. Pharmacol., 2017, 10(7), 773-782.
[45]
Furtado, D.; Björnmalm, M.; Ayton, S.; Bush, A.I.; Kempe, K.; Caruso, F. Overcoming the blood-brain barrier: The role of nanomaterials in treating neurological diseases. Adv. Mater., 2018, 30(46), e1801362.
[http://dx.doi.org/10.1002/adma.201801362] [PMID: 30066406]
[46]
Singh, R.; Lillard, J.W. Jr Nanoparticle-based targeted drug delivery. Exp. Mol. Pathol., 2009, 86(3), 215-223.
[http://dx.doi.org/10.1016/j.yexmp.2008.12.004] [PMID: 19186176]
[47]
Kumar, R. Chapter 8 - lipid-based nanoparticles for drug-delivery systems.
[48]
Gilmore, J.L.; Yi, X.; Quan, L.; Kabanov, A.V. Novel nanomaterials for clinical neuroscience. J. Neuroimmune Pharmacol., 2008, 3(2), 83-94.
[http://dx.doi.org/10.1007/s11481-007-9099-6] [PMID: 18210200]
[49]
Bennewitz, M.F.; Saltzman, W.M. Nanotechnology for delivery of drugs to the brain for epilepsy. Neurotherapeutics, 2009, 6(2), 323-336.
[50]
Lombardo, S.M.; Schneider, M.; Türeli, A.E.; Günday Türeli, N. Key for crossing the BBB with nanoparticles: The rational design. Beilstein J. Nanotechnol., 2020, 11, 866-883.
[http://dx.doi.org/10.3762/bjnano.11.72] [PMID: 32551212]
[51]
Masserini, M. Nanoparticles for brain drug delivery. ISRN Biochem., 2013, 6
[http://dx.doi.org/10.1155/2013/238428]
[52]
Tsou, Y-H.; Zhang, X-Q.; Zhu, H.; Syed, S.; Xu, X. Drug delivery to the brain across the blood-brain barrier using nanomaterials. Small, 2017, 13(43), 1701921.
[http://dx.doi.org/10.1002/smll.201701921] [PMID: 29045030]
[53]
Rollerova, E.; Scsukova, S.; Jurcovicova, J. Alzbeta Bujnakova, Mlynarcikova; Elena, Szabova; Kovriznych, J.; Zeljenkova, D.Polymeric nanoparticles - targeted drug delivery systems.Pdf. Endocr. Regul.2011, 49-60.
[PMID: 21314211]
[54]
Paul, W. Inorganic nanoparticles for targeted drug delivery. Sci. Design, 2010, 32, 204-235.
[http://dx.doi.org/10.1533/9781845699802.2.204]
[55]
Palanisamy, S.; Wang, Y-M. Superparamagnetic iron oxide nanoparticulate system: Synthesis, targeting, drug delivery and therapy in can-cer. Dalton Trans., 2019, 48(26), 9490-9515.
[http://dx.doi.org/10.1039/C9DT00459A] [PMID: 31211303]
[56]
Kaur, J.; Gill, G.S.; Jeet, K. Applications of carbon nanotubes in drug delivery. Characterization and biology of nanomaterials for drug delivery; Elsevier, 2019, pp. 113-135.
[http://dx.doi.org/10.1016/B978-0-12-814031-4.00005-2]
[57]
Foldvari, M.; Bagonluri, M. Carbon nanotubes as functional excipients for nanomedicines: II. Drug delivery and biocompatibility issues. Nanomedicine (Lond.), 2008, 4(3), 183-200.
[http://dx.doi.org/10.1016/j.nano.2008.04.003] [PMID: 18550450]
[58]
Bianco, A.; Kostarelos, K.; Prato, M. Applications of carbon nanotubes in drug delivery. Curr. Opin. Chem. Biol., 2005, 9(6), 674-679.
[http://dx.doi.org/10.1016/j.cbpa.2005.10.005] [PMID: 16233988]
[59]
Pastorin, G.; Wu, W.; Wieckowski, S.; Briand, J-P.; Kostarelos, K.; Prato, M.; Bianco, A. Double functionalization of carbon nanotubes for multimodal drug delivery. Chem. Commun. (Camb.), 2006, (11), 1182-1184.
[http://dx.doi.org/10.1039/b516309a] [PMID: 16518484]
[60]
Banks, W.A. From blood–brain barrier to blood–brain interface: New opportunities for cns drug delivery. DRUG Discov., 18
[61]
Dong, X. Current strategies for brain drug delivery. Theranostics, 2018, 8(6), 1481-1493.
[http://dx.doi.org/10.7150/thno.21254] [PMID: 29556336]
[62]
Zhang, C.; Kwan, P.; Zuo, Z.; Baum, L. The transport of antiepileptic drugs by P-glycoprotein. Adv. Drug Deliv. Rev., 2012, 64(10), 930-942.
[http://dx.doi.org/10.1016/j.addr.2011.12.003] [PMID: 22197850]
[63]
Naqvi, S.; Panghal, A.; Flora, S.J.S. Nanotechnology: A promising approach for delivery of neuroprotective drugs. Front. Neurosci., 2020, 14, 494.
[http://dx.doi.org/10.3389/fnins.2020.00494] [PMID: 32581676]
[64]
Betzer, O.; Shilo, M.; Opochinsky, R.; Barnoy, E.; Motiei, M.; Okun, E.; Yadid, G.; Popovtzer, R. The effect of nanoparticle size on the ability to cross the blood-brain barrier: An in vivo study. Nanomedicine (Lond.), 2017, 12(13), 1533-1546.
[http://dx.doi.org/10.2217/nnm-2017-0022] [PMID: 28621578]
[65]
Shilo, M.; Sharon, A.; Baranes, K.; Motiei, M.; Lellouche, J-P.M.; Popovtzer, R. The effect of nanoparticle size on the probability to cross the blood-brain barrier: An in-vitro endothelial cell model. J. Nanobiotechnology, 2015, 13, 19.
[http://dx.doi.org/10.1186/s12951-015-0075-7] [PMID: 25880565]
[66]
Morachis, J.M.; Mahmoud, E.A.; Almutairi, A. Physical and chemical strategies for therapeutic delivery by using polymeric nanoparticles. Pharmacol. Rev., 2012, 64(3), 505-519.
[http://dx.doi.org/10.1124/pr.111.005363] [PMID: 22544864]
[67]
Kolhar, P.; Anselmo, A.C.; Gupta, V.; Pant, K.; Prabhakarpandian, B.; Ruoslahti, E.; Mitragotri, S. Using shape effects to target antibody-coated nanoparticles to lung and brain endothelium. Proc. Natl. Acad. Sci. USA, 2013, 110(26), 10753-10758.
[http://dx.doi.org/10.1073/pnas.1308345110] [PMID: 23754411]
[68]
Saraiva, C.; Praça, C.; Ferreira, R.; Santos, T.; Ferreira, L.; Bernardino, L. Nanoparticle-mediated brain drug delivery: Overcoming blood-brain barrier to treat neurodegenerative diseases. J. Control. Release, 2016, 235, 34-47.
[http://dx.doi.org/10.1016/j.jconrel.2016.05.044] [PMID: 27208862]
[69]
Ceña, V.; Játiva, P. Nanoparticle crossing of blood-brain barrier: A road to new therapeutic approaches to central nervous system diseases. Nanomedicine (Lond.), 2018, 13(13), 1513-1516.
[http://dx.doi.org/10.2217/nnm-2018-0139] [PMID: 29998779]
[70]
Nance, E.A.; Woodworth, G.F.; Sailor, K.A.; Shih, T.-Y.; Xu, Q.; Swaminathan, G.; Xiang, D.; Eberhart, C.; Hanes, J. A dense poly(ethylene glycol) coating improves penetration of large polymeric nanoparticles within brain tissue. Sci. Transl. Med., 2012, 4, 149ra119-149ra119.
[71]
Biddlestone-Thorpe, L.; Marchi, N.; Guo, K.; Ghosh, C.; Janigro, D.; Valerie, K.; Yang, H. Nanomaterial-mediated CNS delivery of diag-nostic and therapeutic agents. Adv. Drug Deliv. Rev., 2012, 64(7), 605-613.
[http://dx.doi.org/10.1016/j.addr.2011.11.014] [PMID: 22178615]
[72]
Mahmood, M.; Mustafa, T.; Xu, Y.; Nima, Z.; Kannarpady, G.; Bourdo, S.; Casciano, D.; Biris, A.S. Calcium-channel blocking and nano-particles-based drug delivery for treatment of drug-resistant human cancers. Ther. Deliv., 2014, 5(7), 763-780.
[http://dx.doi.org/10.4155/tde.14.30] [PMID: 25287384]
[73]
Liu, J. Functionalized nanocarrier combined seizure-specific vector with p-glycoprotein modulation property for antiepileptic drug deli-very. AGRIS, 2016, 74(4), 64-76.
[http://dx.doi.org/10.1016/j.biomaterials.2015.09.041]
[74]
Dycke, A.V. Local delivery strategies in epilepsy; a focus on adenosine. Seizure, 2011, 20(5), 376-382.
[75]
Ji, Y.; Hu, Y.; Ren, J.; Khanna, R.; Yao, Y.; Chen, Y.; Li, Q.; Sun, L. CRMP2-derived peptide ST2-104 (R9-CBD3) protects SH-SY5Y neuroblastoma cells against A 25-35-induced neurotoxicity by inhibiting the pCRMP2/NMDAR2B signaling pathway. Chem. Biol. Interact., 2019, 305, 28-39.
[76]
Chew, L.A.; Khanna, R. CRMP2 and voltage-gated ion channels: Potential roles in neuropathic pain. Neuronal Signal., 2018, 16.
[77]
Chen, X.; Liu, D.; Zhou, D.; Si, Y.; Xu, D.; Stamatkin, C.W.; Ghozayel, M.K.; Ripsch, M.S.; Obukhov, A.G.; White, F.A.; Meroueh, S.O. Small-molecule CaVα1.CaVβ antagonist suppresses neuronal voltage-gated calcium-channel trafficking. Proc. Natl. Acad. Sci. USA, 2018, 115(45), E10566-E10575.
[http://dx.doi.org/10.1073/pnas.1813157115] [PMID: 30355767]
[78]
Ortner, N.J. L-type calcium channels as drug targets in cns disorders. Channels (Austin), 2016, 10(1), 7-13.
[79]
Wagner, J.L.; Mueller, M.; Kellermann, T.; Griffin, M.; Smith, G.; Soliven, M.; Guilfoyle, S.M.; Junger, K.F.; Mucci, G.; Huszti, H.; Ba-rrett, L.; Zupanc, M.; Modi, A.C. Vulnerabilities to antiepileptic drug (AED) side effects in youth with epilepsy. Epilepsy Behav., 2019, 97, 22-28.
[http://dx.doi.org/10.1016/j.yebeh.2019.05.012] [PMID: 31181425]
[80]
Kaeberle, J. Epilepsy disorders and treatment modalities. NASN Sch Nurse, 2018, 33(6), 342-344.
[http://dx.doi.org/10.1177/1942602X18785246] [PMID: 30024820]
[81]
Svalheim, S.; Sveberg, L.; Mochol, M.; Taubøll, E. Interactions between antiepileptic drugs and hormones. Seizure, 2015, 28, 12-17.
[http://dx.doi.org/10.1016/j.seizure.2015.02.022] [PMID: 25797888]
[82]
Samia, O.; Hanan, R.; Kamal, T. Carbamazepine mucoadhesive nanoemulgel (MNEG) as brain targeting delivery system via the olfactory mucosa. Drug Deliv., 2012, 19(1), 58-67.
[http://dx.doi.org/10.3109/10717544.2011.644349] [PMID: 22191715]
[83]
Kohane, D.S.; Holmes, G.L.; Chau, Y.; Zurakowski, D.; Langer, R.; Cha, B.H. Effectiveness of muscimol-containing microparticles against pilocarpine-induced focal seizures. Epilepsia, 2002, 43(12), 1462-1468.
[http://dx.doi.org/10.1046/j.1528-1157.2002.11202.x] [PMID: 12460246]
[84]
Hsiao, M-H.; Larsson, M.; Larsson, A.; Evenbratt, H.; Chen, Y-Y.; Chen, Y-Y.; Liu, D-M. Design and characterization of a novel amphip-hilic chitosan nanocapsule-based thermo-gelling biogel with sustained in vivo release of the hydrophilic anti-epilepsy drug ethosuximide. J. Control. Release, 2012, 161(3), 942-948.
[http://dx.doi.org/10.1016/j.jconrel.2012.05.038] [PMID: 22652548]
[85]
Ali, A.; Kolappa Pillai, K.; Jalees Ahmad, F.; Dua, Y.; Iqbal Khan, Z.; Vohora, D. Comparative efficacy of liposome-entrapped amiloride and free amiloride in animal models of seizures and serum potassium in mice. Eur. Neuropsychopharmacol., 2007, 17(3), 227-229.
[http://dx.doi.org/10.1016/j.euroneuro.2006.05.003] [PMID: 16843647]
[86]
Argelia Rosillo-de, la Torre; Gabriel, Luna-Bárcenas; Sandra, Orozco-Suárez; Hermelinda, Salgado-Ceballos; Perla, García; Alberto, Laza-rowski; Luisa, Rocha. Pharmacoresistant epilepsy and nanotechnology. Front. Biosci., 2014, 1, 329-340.

Rights & Permissions Print Cite
© 2024 Bentham Science Publishers | Privacy Policy