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Review

Novel drug delivery systems of β2 adrenoreceptor agonists to suppress SNCA gene expression and mitochondrial oxidative stress in Parkinson’s disease management

, ORCID Icon, ORCID Icon, ORCID Icon &
Pages 1119-1132 | Received 06 Mar 2020, Accepted 03 Jun 2020, Published online: 22 Jun 2020

References

  • Tysnes O-B, Storstein A. Epidemiology of Parkinson’s disease. J Neural Transm. 2017;124(8):901–905.
  • Jankovic J, Aguilar LG. Current approaches to the treatment of Parkinson’s disease. Neuropsychiatr Dis Treat. 2008;4(4):743.
  • Rascol O, Payoux P, Ory F, et al. Limitations of current Parkinson’s disease therapy. Ann Neurol. 2003;53(S3):S3–S15.
  • Dehay B, Bourdenx M, Gorry P, et al. Targeting α-synuclein for treatment of Parkinson’s disease: mechanistic and therapeutic considerations.Lancet Neurol. 2015;14(8):855–866.
  • McGeer PL, Itagaki S, Akiyama H, et al. Rate of cell death in parkinsonism indicates active neuropathological process. Ann Neurol. 1988;24(4):574–576.
  • Poewe W, Seppi K, Tanner CM, et al., Parkinson disease. Nat Rev Dis Primers. 2017;3(1):17013.
  • Lee VM-Y, Trojanowski JQ. Mechanisms of Parkinson’s disease linked to pathological α-synuclein: new targets for drug discovery. Neuron. 2006;52(1):33–38.
  • Gosavi N, Lee H-J, Lee JS, et al. Golgi fragmentation occurs in the cells with prefibrillar α-synuclein aggregates and precedes the formation of fibrillar inclusion. J Biol Chem. 2002;277(50):48984–48992.
  • Cooper AA, Gitler AD, Cashikar A, et al. α-synuclein blocks ER-golgi traffic and rab1 rescues neuron loss in Parkinson’s models. Science. 2006;313(5785):324–328.
  • Smith WW, Jiang H, Pei Z, et al. Endoplasmic reticulum stress and mitochondrial cell death pathways mediate A53T mutant alpha-synuclein-induced toxicity. Hum Mol Genet. 2005;14(24):3801–3811.
  • Cookson MR. α-Synuclein and neuronal cell death. Mol Neurodegener. 2009;4(1):9.
  • Cuervo AM, Stefanis L, Fredenburg R, et al. Impaired degradation of mutant α-synuclein by chaperone-mediated autophagy. Science. 2004;305(5688):1292–1295.
  • Stefanis L, Larsen KE, Rideout HJ, et al. Expression of A53T mutant but not wild-type α-synuclein in PC12 cells induces alterations of the ubiquitin-dependent degradation system, loss of dopamine release, and autophagic cell death. J Neurosci. 2001;21(24):9549–9560.
  • Chiba-Falek O, Nussbaum RL. Effect of allelic variation at the NACP–rep1 repeat upstream of the α-synuclein gene (SNCA) on transcription in a cell culture luciferase reporter system. Hum Mol Genet. 2001;10(26):3101–3109.
  • Corrado L, De Marchi F, Tunesi S, et al. The length of SNCA Rep1 microsatellite may influence cognitive evolution in Parkinson’s disease. Front Neurol. 2018;9:213.
  • George S, Brundin P. Immunotherapy in Parkinson’s disease: micromanaging alpha-synuclein aggregation. J Parkinsons Dis. 2015;5(3):413–424.
  • Xu L, Pu J. Alpha-synuclein in Parkinson’s disease: from pathogenetic dysfunction to potential clinical application. Parkinson’s Dis. 2016;2016:1–10.
  • Karmacharya MB, Hada B, Park SR, et al. Low-intensity ultrasound decreases α-synuclein aggregation via attenuation of mitochondrial reactive oxygen species in MPP (+)-treated PC12 cells. Mol Neurobiol. 2017;54(8):6235–6244.
  • Niu S, Zhang L-K, Zhang L, et al. Inhibition by multifunctional magnetic nanoparticles loaded with alpha-synuclein RNAi plasmid in a Parkinson’s disease model. Theranostics. 2017;7(2):344.
  • Alexander G, Schwartzman R, Nukes T, et al. β2‐adrenergic agonist as adjunct therapy to levodopa in Parkinson’s disease. Neurology. 1994;44(8):1511.
  • Hishida R, Kurahashi K, Narita S, et al. Wearing-off” and β2-adrenoceptor agonist in Parkinson’s disease. Lancet. 1992;339(8797):870. .
  • Uc EY, Lambert CP, Harik SI, et al. Albuterol improves response to levodopa and increases skeletal muscle mass in patients with fluctuating Parkinson disease. Clin Neuropharmacol. 2003;26(4):207–212.
  • Mittal S, Bjørnevik K, Im DS, et al., β2-adrenoreceptor is a regulator of the α-synuclein gene driving risk of Parkinson’s disease. Science. 2017;357(6354):891–898.
  • Choucair-Jaafar N, Beetz N, Gilsbach R, et al. Cardiovascular effects of chronic treatment with a β2-adrenoceptor agonist relieving neuropathic pain in mice. Neuropharmacology. 2011;61(1–2):51–60.
  • Khan AR, Yang X, Fu M, et al. Recent progress of drug nanoformulations targeting to brain. J Control Release. 2018;291:37–64.
  • Loureiro JA, Gomes B, Coelho MA, et al. Immunoliposomes doubly targeted to transferrin receptor and to α-synuclein. Future Sci OA. 2015;1(4):4.
  • Stefanis L. α-synuclein in Parkinson’s disease. Cold Spring Harb Perspect Med. 2012;2(2):a009399.
  • Jakes R, Spillantini MG, Goedert M. Identification of two distinct synucleins from human brain. FEBS Lett. 1994;345(1):27–32.
  • Polymeropoulos MH, Lavedan C, Leroy E, et al. Mutation in the α-synuclein gene identified in families with Parkinson’s disease. science. 1997;276(5321):2045–2047.
  • Krüger R, Kuhn W, Müller T, et al. AlaSOPro mutation in the gene encoding α-synuclein in Parkinson’s disease. Nat Genet. 1998;18(2):106.
  • Zarranz JJ, Alegre J, Gómez‐Esteban JC, et al. The new mutation, E46K, of α‐synuclein causes Parkinson and lewy body dementia. Ann Neurol. 2004;55(2):164–173.
  • Appel‐Cresswell S, Vilarino‐Guell C, Encarnacion M, et al. Alpha‐synuclein p. H50Q, a novel pathogenic mutation for Parkinson’s disease. Mov Disord. 2013;28(6):811–813.
  • Lesage S, Anheim M, Letournel F, et al. G51D α‐synuclein mutation causes a novel Parkinsonian–pyramidal syndrome. Ann Neurol. 2013;73(4):459–471.
  • Pasanen P, Myllykangas L, Siitonen M, et al. A novel α-synuclein mutation A53E associated with atypical multiple system atrophy and Parkinson’s disease-type pathology. Neurobiol Aging. 2014;35(9):2180.e1-2180. e5.
  • Chung CY, Koprich JB, Siddiqi H, et al. Dynamic changes in presynaptic and axonal transport proteins combined with striatal neuroinflammation precede dopaminergic neuronal loss in a rat model of AAV α-synucleinopathy. J Neurosci. 2009;29(11):3365–3373.
  • Garcia-Reitböck P, Anichtchik O, Bellucci A, et al. SNARE protein redistribution and synaptic failure in a transgenic mouse model of Parkinson’s disease. Brain. 2010;133(7):2032–2044.
  • Nemani VM, Lu W, Berge V, et al. Increased expression of α-synuclein reduces neurotransmitter release by inhibiting synaptic vesicle reclustering after endocytosis. Neuron. 2010;65(1):66–79.
  • Scott DA, Tabarean I, Tang Y, et al. A pathologic cascade leading to synaptic dysfunction in α-synuclein-induced neurodegeneration. J Neurosci. 2010;30(24):8083–8095.
  • Yang Q, She H, Gearing M, et al. Regulation of neuronal survival factor MEF2D by chaperone-mediated autophagy. Science. 2009;323(5910):124–127.
  • Martin LJ, Pan Y, Price AC, et al. Parkinson’s disease α-synuclein transgenic mice develop neuronal mitochondrial degeneration and cell death. J Neurosci. 2006;26(1):41–50.
  • Li -W-W, Yang R, Guo J-C, et al. Localization of α-synuclein to mitochondria within midbrain of mice. Neuroreport. 2007;18(15):1543–1546.
  • Devi L, Raghavendran V, Prabhu BM, et al. Mitochondrial import and accumulation of α-synuclein impair complex I in human dopaminergic neuronal cultures and Parkinson disease brain. J Biol Chem. 2008;283(14):9089–9100.
  • Nakamura K, Nemani VM, Wallender EK, et al. Optical reporters for the conformation of α-synuclein reveal a specific interaction with mitochondria. J Neurosci. 2008;28(47):12305–12317.
  • Liu G, Zhang C, Yin J, et al. α-Synuclein is differentially expressed in mitochondria from different rat brain regions and dose-dependently down-regulates complex I activity. Neurosci Lett. 2009;454(3):187–192.
  • Loeb V, Yakunin E, Saada A, et al. The transgenic overexpression of α-synuclein and not its related pathology associates with complex I inhibition. J Biol Chem. 2010;285(10):7334–7343.
  • Choubey V, Safiulina D, Vaarmann A, et al. Mutant A53T α-synuclein induces neuronal death by increasing mitochondrial autophagy. J Biol Chem. 2011;286(12):10814–10824.
  • Edwards DJ, Sorisio DA, Knopf S. Effects of the β2-adrenoceptor agonist clenbuterol on tyrosine and tryptophan in plasma and brain of the rat. Biochem Pharmacol. 1989;38(18):2957–2965.
  • Alexander GM, Schwartzman RJ, Grothusen JR, et al. Effect of plasma levels of large neutral amino acids and degree of parkinsonism on the blood‐to‐brain transport of levodopa in naive and MPTP parkinsonian monkeys. Neurology. 1994;44(8):1491.
  • Magistrelli L, Comi C. Beta2-Adrenoceptor Agonists in Parkinson’s Disease and Other Synucleinopathies. J Neuroimmune Pharmacol. 2020;15(1):74–81.
  • Goetz CG, Tilley BC, Shaftman SR, et al. Movement disorder society‐sponsored revision of the Unified Parkinson’s Disease Rating Scale (MDS‐UPDRS): scale presentation and clinimetric testing results. Mov Disord. 2008;23(15):2129–2170.
  • Gronich N, Abernethy DR, Auriel E, et al. β2‐adrenoceptor agonists and antagonists and risk of Parkinson’s disease. Mov Disord. 2018;33(9):1465–1471.
  • Sears MR. Adverse effects of β-agonists. J Allergy Clin Immunol. 2002;110(6):S322–S328.
  • Bristow MR. β-Adrenergic receptor blockade in chronic heart failure. Circulation. 2000;101(5):558–569.
  • Robin ED, McCauley R. Sudden cardiac death in bronchial asthma, inhaled beta-adrenergic agents. Chest. 1992;101(6):1699–1703.
  • Salpeter SR, Ormiston TM, Salpeter EE. Cardiovascular effects of β-agonists in patients with asthma and COPD: a meta-analysis. Chest. 2004;125(6):2309–2321.
  • Au DH, Lemaitre RN, Randall Curtis J, et al. The risk of myocardial infarction associated with inhaled β-adrenoceptor agonists. Am J Respir Crit Care Med. 2000;161(3):827–830.
  • Singh N, Joshi A, Toor AP. et al. Drug delivery: advancements and challenges. In: Nanostructures for Drug Delivery. Volume 2. Ecaterina Andronescu, editor. Amsterdam: Elsevier Inc; 2017; 865–886.
  • Juillerat-Jeanneret L. Critical analysis of cancer therapy using nanomaterials. In: Nanotechnologies for the Life Sciences Volume 6. Challa S. S. R. Kumar, editor. Weinheim: WILEY-VCH Verlag GmbH & Co. KGaA; 2007;199–241.
  • Wilczewska AZ, Niemirowicz K, Markiewicz KH, et al. Nanoparticles as drug delivery systems. Pharmacol Rep. 2012;64(5):1020–1037.
  • Patel T, Zhou J, Piepmeier JM, et al. Polymeric nanoparticles for drug delivery to the central nervous system. Adv Drug Deliv Rev. 2012;64(7):701–705.
  • Danhier F, Ansorena E, Silva JM, et al. PLGA-based nanoparticles: an overview of biomedical applications. J Control Release. 2012;161(2):505–522.
  • Sophia GA, Paraskevi K,  Dimitrios GF.Liposomes and drug deliver. In: Pharmaceutical manufacturing handbook production and processes. Gad SC, editor. Hoboken, NJ: Wiley-Interscience; 2008; 443–534. Available from: http://site.ebrary.com/lib/ascc/Doc?id=10226725
  • Olusanya T, Haj Ahmad R, Ibegbu D, et al. Liposomal drug delivery systems and anticancer drugs. Molecules. 2018;23(4):4.
  • Sunderland CJ, Steiert M, Talmadge JE, et al. Targeted nanoparticles for detecting and treating cancer. Drug Dev Res. 2006;67(1):70–93.
  • Milla P, Dosio F, Cattel L. PEGylation of proteins and liposomes: a powerful and flexible strategy to improve the drug delivery. Curr Drug Metab. 2012;13(1):105–119.
  • Vlieghe P, Khrestchatisky M. Medicinal chemistry based approaches and nanotechnology-based systems to improve CNS drug targeting and delivery. Med Res Rev. 2013;33(3):457–516.
  • Schnyder A, Huwyler J. Drug transport to brain with targeted liposomes. NeuroRX. 2005;2(1):99–107.
  • Yue P-J, He L, Qiu S-W, et al. OX26/CTX-conjugated PEGylated liposome as a dual-targeting gene delivery system for brain glioma. Mol Cancer. 2014;13(1):1.
  • Soni V, Kohli DV, Jain SK. Transferrin coupled liposomes as drug delivery carriers for brain targeting of 5-florouracil. J Drug Target. 2008;13(4):245–250.
  • Qin Y, Fan W, Chen H, et al. In vitro and in vivo investigation of glucose-mediated brain-targeting liposomes. J Drug Target. 2010;18(7):536–549.
  • Gurturk Z, Tezcaner A, Dalgic AD, et al. Maltodextrin modified liposomes for drug delivery through the blood–brain barrier. MedChemComm. 2017;8(6):1337–1345.
  • Akbarzadeh A, Rezaei-Sadabady R, Davaran S, et al. Liposome: classification, preparation, and applications. Nanoscale Res Lett. 2013;8(1):1.
  • Geszke-Moritz M, Moritz M. Solid lipid nanoparticles as attractive drug vehicles: composition, properties and therapeutic strategies. Mater Sci Eng C. 2016;68:982–994.
  • Paliwal R, Paliwal SR, Kenwat R, et al. Solid lipid nanoparticles: a review on recent perspectives and patents. Expert Opin Ther Pat. 2020 Mar;30(3):179–194. PubMed PMID: 32003260.
  • He H, Yao J, Zhang Y, et al. Solid lipid nanoparticles as a drug delivery system to across the blood-brain barrier. Biochem Biophys Res Commun. 2019;519(2):385–390.
  • Cacciatore I, Ciulla M, Fornasari E, et al. Solid lipid nanoparticles as a drug delivery system for the treatment of neurodegenerative diseases. Expert Opin Drug Deliv. 2016;13(8):1121–1131.
  • Blasi P, Giovagnoli S, Schoubben A, et al. Solid lipid nanoparticles for targeted brain drug delivery. Adv Drug Deliv Rev. 2007 Jul 10;59(6):454–477. PubMed PMID: 17570559.
  • Kaur IP, Bhandari R, Bhandari S, et al. Potential of solid lipid nanoparticles in brain targeting. J Control Release. 2008;127(2):97–109.
  • Patel M, Souto EB, Singh KK. Advances in brain drug targeting and delivery: limitations and challenges of solid lipid nanoparticles. Expert Opin Drug Deliv. 2013 Jul;10(7):889–905. PubMed PMID: 23550609.
  • Mulik RS, Mönkkönen J, Juvonen RO, et al. Apoptosis-induced anticancer effect of transferrin-conjugated solid lipid nanoparticles of curcumin. Cancer nanotechnol. 2012;3(1):65.
  • Dal Magro R, Ornaghi F, Cambianica I, et al. ApoE-modified solid lipid nanoparticles: A feasible strategy to cross the blood-brain barrier. J Control Release. 2017;249:103–110.
  • Neves AR, Queiroz JF, Lima SAC, et al. Apo E-functionalization of solid lipid nanoparticles enhances brain drug delivery: uptake mechanism and transport pathways. Bioconjug Chem. 2017 Apr 19;28(4):995–1004. PubMed PMID: 28355061.
  • Singh I, Swami R, Pooja D, et al. Lactoferrin bioconjugated solid lipid nanoparticles: a new drug delivery system for potential brain targeting. J Drug Target. 2016;24(3):212–223. PubMed PMID: 26219519.
  • Neves AR, Queiroz JF, Reis S. Brain-targeted delivery of resveratrol using solid lipid nanoparticles functionalized with apolipoprotein E. J Nanobiotechnology. 2016;14(1):27.
  • Liu Z, Zhao H, Shu L, et al. Preparation and evaluation of Baicalin-loaded cationic solid lipid nanoparticles conjugated with OX26 for improved delivery across the BBB. Drug Dev Ind Pharm. 2015;41(3):353–361.
  • Gandomi N, Varshochian R, Atyabi F, et al. Solid lipid nanoparticles surface modified with anti-Contactin-2 or anti-Neurofascin for brain-targeted delivery of medicines. Pharm Dev Technol. 2017;22(3):426–435.
  • Olbrich C, Gessner A, Kayser O, et al. Lipid-drug-conjugate (LDC) nanoparticles as novel carrier system for the hydrophilic antitrypanosomal drug diminazenediaceturate. J Drug Target. 2008;10(5):387–396.
  • Mishra V, Bansal K, Verma A, et al. Solid lipid nanoparticles: emerging colloidal nano drug delivery systems. Pharmaceutics. 2018;10:4.
  • Guo Q, Shen XT, Li YY, et al. Carbon nanotubes-based drug delivery to cancer and brain. J Huazhong Univ Sci Technolog Med Sci. 2017 Oct;37(5):635–641. PubMed PMID: 29058274.
  • Tan JM, Saifullah B, Kura AU, et al. Incorporation of levodopa into biopolymer coatings based on carboxylated carbon nanotubes for PH-dependent sustained release drug delivery. Nanomaterials (Basel). 2018 May 31;8(6):389. PubMed PMID: 29857532; PubMed Central PMCID: PMCPMC6027427.
  • Alexander P. Moravsky, Eugene M. Wexler, Raouf O. Loutfy. Growth of carbon nanotubes by Arc discharge and Laser ablation method. In: Carbon nanotubes: science and applications. Meyyappan M, editor. Boca Raton, FL: CRC Press; 2005;65–94.
  • Bethune D, Kiang CH, De Vries M, et al. Cobalt-catalysed growth of carbon nanotubes with single-atomic-layer walls. Nature. 1993;363(6430):605–607.
  • Cassell AM, Raymakers JA, Kong J, et al. Large scale CVD synthesis of single-walled carbon nanotubes. The Journal of Physical Chemistry B. 1999;103(31):6484–6492.
  • Prato M, Kostarelos K, Bianco A. Functionalized carbon nanotubes in drug design and discovery. Acc Chem Res. 2008;41(1):60–68.
  • Pardo J, Peng Z, Leblanc RM. Cancer targeting and drug delivery using carbon-based quantum dots and nanotubes. Molecules. 2018 Feb 10;23(2):378. PubMed PMID: 29439409; PubMed Central PMCID: PMCPMC6017112.
  • Wang JT, Al-Jamal KT. Functionalized carbon nanotubes: revolution in brain delivery. Nanomedicine (Lond). 2015;10(17):2639–2642. PubMed PMID: 26328513.
  • Ren J, Shen S, Wang D, et al. The targeted delivery of anticancer drugs to brain glioma by PEGylated oxidized multi-walled carbon nanotubes modified with angiopep-2. Biomaterials. 2012 Apr;33(11):3324–3333. PubMed PMID: 22281423.
  • Guo Q, You H, Yang X, et al. Functional single-walled carbon nanotubes ‘CAR’ for targeting dopamine delivery into the brain of parkinsonian mice. Nanoscale. 2017 Aug 3;9(30):10832–10845. PubMed PMID: 28726961.
  • Wakaskar RR. General overview of lipid–polymer hybrid nanoparticles, dendrimers, micelles, liposomes, spongosomes and cubosomes. J Drug Target. 2018;26(4):311–318.
  • Elezaby RS, Gad HA, Metwally AA, et al. Self-assembled amphiphilic core-shell nanocarriers in line with the modern strategies for brain delivery. J Control Release. 2017;261:43–61.
  • Ruan H, Chai Z, Shen Q, et al. A novel peptide ligand RAP12 of LRP1 for glioma targeted drug delivery. J Control Release. 2018;279:306–315.
  • Croy S, Kwon G. Polymeric micelles for drug delivery. Curr Pharm Des. 2006;12(36):4669–4684.
  • Gu PF, Xu H, Sui BW, et al. Polymeric micelles based on poly (ethylene glycol) block poly (racemic amino acids) hybrid polypeptides: conformation-facilitated drug-loading behavior and potential application as effective anticancer drug carriers. Int J Nanomedicine. 2012;7:109.
  • Allen C, Yu Y, Maysinger D, et al. Polycaprolactone-b-poly (ethylene oxide) block copolymer micelles as a novel drug delivery vehicle for neurotrophic agents FK506 and L-685,818. Bioconjug Chem. 1998;9(5):564–572.
  • Nance E, Zhang F, Mishra MK, et al. Nanoscale effects in dendrimer-mediated targeting of neuroinflammation. Biomaterials. 2016;101:96–107.
  • Kuang Y, An S, Guo Y, et al. T7 peptide-functionalized nanoparticles utilizing RNA interference for glioma dual targeting. Int J Pharm. 2013;454(1):11–20.
  • Safari J, Zarnegar Z. Advanced drug delivery systems: nanotechnology of health design A review. J Saudi Chem Soc. 2014;18(2):85–99.
  • Li Y, He H, Jia X, et al. A dual-targeting nanocarrier based on poly (amidoamine) dendrimers conjugated with transferrin and tamoxifen for treating brain gliomas. Biomaterials. 2012;33(15):3899–3908.
  • Mangraviti A, Gullotti D, Tyler B, et al. Nanobiotechnology-based delivery strategies: new frontiers in brain tumor targeted therapies. J Control Release. 2016;240:443–453.
  • Zhu Y, Liu C, Pang Z. Dendrimer-Based Drug Delivery Systems for Brain Targeting. Biomolecules. 2019;9(12):790.
  • Mignani S, Bryszewska M, Zablocka M, et al. Can dendrimer based nanoparticles fight neurodegenerative diseases? Current situation versus other established approaches. Prog Polym Sci. 2017;64:23–51.
  • Lyu Z, Ding L, Huang A-T, et al. Poly (amidoamine) dendrimers: covalent and supramolecular synthesis. Mater Today Chem. 2019;13:34–48.
  • Kesharwani P, Iyer AK. Recent advances in dendrimer-based nanovectors for tumor-targeted drug and gene delivery. Drug Discov Today. 2015;20(5):536–547.
  • Sun T, Wu H, Li Y, et al. Targeting transferrin receptor delivery of temozolomide for a potential glioma stem cell-mediated therapy. Oncotarget. 2017;8(43):74451.
  • Aly AE, Waszczak BL. Intranasal gene delivery for treating Parkinson’s disease: overcoming the blood–brain barrier. Expert Opin Drug Deliv. 2015;12(12):1923–1941.
  • Migliore M, Ortiz R, Dye S, et al. Neurotrophic and neuroprotective efficacy of intranasal GDNF in a rat model of Parkinson’s disease. Neuroscience. 2014;274:11–23.
  • Sonvico F, Clementino A, Buttini F, et al. Surface-modified nanocarriers for nose-to-brain delivery: from bioadhesion to targeting. Pharmaceutics. 2018;10(1):34.
  • Mandal A, Bisht R, Pal D, et al. Diagnosis and Drug Delivery to the Brain: novel Strategies. In: Emerging Nanotechnologies for Diagnostics, Drug Delivery and Medical Devices. Ashim KM, Kishore C, Abhirup M, editors. Amsterdam: Elsevier Inc; 2017. p. 59–83.
  • Md S, Haque S, Sahni JK, et al. New non-oral drug delivery systems for Parkinson’s disease treatment. Expert Opin Drug Deliv. 2011;8(3):359–374.
  • Illum L. Transport of drugs from the nasal cavity to the central nervous system. Eur J Pharm Sci. 2000;11(1):1–18.
  • Ying W. The nose may help the brain: intranasal drug delivery for treating neurological diseases. Future Neurology. 2008; 3(1):1–4.
  • Dhuria SV, Hanson LR, Frey WH II. Intranasal delivery to the central nervous system: mechanisms and experimental considerations. J Pharm Sci. 2010;99(4):1654–1673.
  • Gao H. Progress and perspectives on targeting nanoparticles for brain drug delivery. Acta Pharm Sin B. 2016;6(4):268–286.
  • Md S, Haque S, Fazil M, et al. Optimised nanoformulation of bromocriptine for direct nose-to-brain delivery: biodistribution, pharmacokinetic and dopamine estimation by ultra-HPLC/mass spectrometry method. Expert Opin Drug Deliv. 2014;11(6):827–842.
  • Jafarieh O, Md S, Ali M, et al. Design, characterization, and evaluation of intranasal delivery of ropinirole-loaded mucoadhesive nanoparticles for brain targeting. Drug Dev Ind Pharm. 2015;41(10):1674–1681.
  • Sharma S, Lohan S, Murthy R. Formulation and characterization of intranasal mucoadhesive nanoparticulates and thermo-reversible gel of levodopa for brain delivery. Drug Dev Ind Pharm. 2014;40(7):869–878.
  • Mittal D, Md S, Hasan Q, et al. Brain targeted nanoparticulate drug delivery system of rasagiline via intranasal route. Drug Deliv. 2016;23(1):130–139. .
  • Wen Z, Yan Z, Hu K, et al. Odorranalectin-conjugated nanoparticles: preparation, brain delivery and pharmacodynamic study on Parkinson’s disease following intranasal administration. J Control Release. 2011;151(2):131–138.
  • Gambaryan P, Kondrasheva I, Severin E, et al. Increasing the efficiency of parkinson’s disease treatment using a poly (lactic-co-glycolic acid)(PLGA) based L-DOPA delivery system. Exp Neurobiol. 2014;23(3):246–252.
  • Pardeshi CV, Rajput PV, Belgamwar VS, et al. Novel surface modified solid lipid nanoparticles as intranasal carriers for ropinirole hydrochloride: application of factorial design approach. Drug Deliv. 2013;20(1):47–56.
  • Pardeshi CV, Belgamwar VS, Tekade AR, et al. Novel surface modified polymer–lipid hybrid nanoparticles as intranasal carriers for ropinirole hydrochloride: in vitro, ex vivo and in vivo pharmacodynamic evaluation. J Mater Sci. 2013;24(9):2101–2115.
  • Mustafa G, Baboota S, Ahuja A, et al. Formulation development of chitosan coated intra nasal ropinirole nanoemulsion for better management option of Parkinson: an in vitro ex vivo evaluation. Curr Nanosci. 2012;8(3):348–360.
  • Zhao Y-Z, Li X, Lu C-T, et al. Gelatin nanostructured lipid carriers-mediated intranasal delivery of basic fibroblast growth factor enhances functional recovery in hemiparkinsonian rats. Nanomedicine. 2014;10(4):755–764.
  • Zhao Y-Z, Jin -R-R, Yang W, et al. Using gelatin nanoparticle mediated intranasal delivery of neuropeptide substance P to enhance neuro-recovery in hemiparkinsonian rats. PloS One. 2016;11:2.
  • Hernando S, Herran E, Figueiro-Silva J, et al. Intranasal administration of TAT-conjugated lipid nanocarriers loading GDNF for Parkinson’s disease. Mol Neurobiol. 2018;55(1):145–155.

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