Delivery of Dual Drug Loaded Lipid Based Nanoparticles across the Blood-Brain Barrier Impart Enhanced Neuroprotection in a Rotenone Induced Mouse Model of Parkinson's Disease

ACS Chemical Neuroscience

Volumn 7, Issue 12, 2016, Pages 1658-1670

  Kundu, Paromita ^a   Das, Manasi ^a   Tripathy, Kalpalata ^b   Sahoo, Sanjeeb K ^a  

^a INSTITUTE OF LIFE SCIENCES   (India)

^b Shri Ramachandra Bhanj Medical College   (India)

Author keywords

blood brain barrier; curcumin; lipid based nanoparticles; Parkinson's disease; piperine; synuclein

Indexed keywords

ALPHA SYNUCLEIN; ANTIPARKINSON AGENT; CURCUMIN; GLYCEROL MONOOLEATE NANOPARTICLE; LIPID; NANOCARRIER; NANOPARTICLE; OLIGOMER; PIPERINE; ROTENONE; S PROTEIN ALPHA; SURFACTANT; UNCLASSIFIED DRUG; VITRONECTIN; 1,3 BENZODIOXOLE DERIVATIVE; ALKALOID; AMIDE; LIPOSOME; NEUROPROTECTIVE AGENT; PIPERIDINE DERIVATIVE;

ANIMAL CELL; ANIMAL EXPERIMENT; ANIMAL MODEL; ANIMAL TISSUE; APOPTOSIS; ARTICLE; AUTOPHAGY; BLOOD BRAIN BARRIER; BRAIN TISSUE; CELL ACTIVATION; CELL FUNCTION; COMPARATIVE STUDY; CONTROLLED STUDY; DRUG BIOAVAILABILITY; DRUG DELIVERY SYSTEM; DRUG DETERMINATION; DRUG FORMULATION; DRUG PENETRATION; DRUG SYNTHESIS; DRUG TISSUE LEVEL; IMMUNOHISTOCHEMISTRY; IN VITRO STUDY; INTERNALIZATION; LYSOSOME; MALE; MOUSE; MOUSE MODEL; NEUROPROTECTION; NONHUMAN; OXIDATIVE STRESS; PARKINSON DISEASE; PRIORITY JOURNAL; PROTEIN AGGREGATION; RAT; ROTAROD TEST; ROTENONE INDUCED PARKINSON DISEASE; ANIMAL; BAGG ALBINO MOUSE; C57BL MOUSE; CAPILLARY PERMEABILITY; COMBINATION DRUG THERAPY; DRUG EFFECTS; METABOLISM; PARKINSONIAN DISORDERS; PC12 CELL LINE; PHYSIOLOGY; PROTEIN AGGREGATION, PATHOLOGICAL; RANDOMIZATION;

ALKALOIDS; ALPHA-SYNUCLEIN; ANIMALS; ANTIPARKINSON AGENTS; BENZODIOXOLES; BLOOD-BRAIN BARRIER; CAPILLARY PERMEABILITY; CURCUMIN; DRUG DELIVERY SYSTEMS; DRUG THERAPY, COMBINATION; LIPOSOMES; MALE; MICE, INBRED BALB C; MICE, INBRED C57BL; NANOPARTICLES; NEUROPROTECTIVE AGENTS; PARKINSONIAN DISORDERS; PC12 CELLS; PIPERIDINES; POLYUNSATURATED ALKAMIDES; PROTEIN AGGREGATION, PATHOLOGICAL; RANDOM ALLOCATION; RATS; ROTENONE; SURFACE-ACTIVE AGENTS;

EID: 85006931068     PISSN: None     EISSN: 19487193     Source Type: Journal    
DOI: 10.1021/acschemneuro.6b00207     Document Type: Article

References (70)

1. Moore, D. J., West, A. B., Dawson, V. L., and Dawson, T. M. (2005) Molecular pathophysiology of Parkinson's disease Annu. Rev. Neurosci. 28, 57-87 10.1146/annurev.neuro.28.061604.135718
2. Gandhi, S. and Wood, N. W. (2005) Molecular pathogenesis of Parkinson's disease Hum. Mol. Genet. 14, 2749-2755 10.1093/hmg/ddi308
3. Dauer, W. and Przedborski, S. (2003) Parkinson's disease: mechanisms and models Neuron 39, 889-909 10.1016/S0896-6273(03)00568-3
4. Connolly, B. S. and Lang, A. E. (2014) Pharmacological treatment of Parkinson disease: a review Jama 311, 1670-1683 10.1001/jama.2014.3654
5. Meissner, W. G., Frasier, M., Gasser, T., Goetz, C. G., Lozano, A., Piccini, P., Obeso, J. A., Rascol, O., Schapira, A., Voon, V., Weiner, D. M., Tison, F., and Bezard, E. (2011) Priorities in Parkinson's disease research Nat. Rev. Drug Discovery 10, 377-393 10.1038/nrd3430
6. Chaudhuri, K. R., Rizos, A., and Sethi, K. D. (2013) Motor and nonmotor complications in Parkinson's disease: an argument for continuous drug delivery? J. Neural Transm. 120, 1305-1320 10.1007/s00702-013-0981-5
7. Rajeswari, A. and Sabesan, M. (2008) Inhibition of monoamine oxidase-B by the polyphenolic compound, curcumin and its metabolite tetrahydrocurcumin, in a model of Parkinson's disease induced by MPTP neurodegeneration in mice Inflammopharmacology 16, 96-99 10.1007/s10787-007-1614-0
8. Rajeswari, A. (2006) Curcumin protects mouse brain from oxidative stress caused by 1-methyl-4-phenyl-1,2,3,6-tetrahydropyridine Eur. Rev. Med. Pharmacol. Sci. 10, 157-161
9. Zbarsky, V., Datla, K. P., Parkar, S., Rai, D. K., Aruoma, O. I., and Dexter, D. T. (2005) Neuroprotective properties of the natural phenolic antioxidants curcumin and naringenin but not quercetin and fisetin in a 6-OHDA model of Parkinson's disease Free Radical Res. 39, 1119-1125 10.1080/10715760500233113
10. Anand, P., Kunnumakkara, A. B., Newman, R. A., and Aggarwal, B. B. (2007) Bioavailability of curcumin: problems and promises Mol. Pharmaceutics 4, 807-818 10.1021/mp700113r
11. Singh, S., Jamwal, S., and Kumar, P. (2015) Piperine Enhances the Protective Effect of Curcumin Against 3-NP Induced Neurotoxicity: Possible Neurotransmitters Modulation Mechanism Neurochem. Res. 40, 1758-1766 10.1007/s11064-015-1658-2
12. Panahi, Y., Khalili, N., Hosseini, M. S., Abbasinazari, M., and Sahebkar, A. (2014) Lipid-modifying effects of adjunctive therapy with curcuminoids-piperine combination in patients with metabolic syndrome: results of a randomized controlled trial Complement. Ther. Med. 22, 851-857 10.1016/j.ctim.2014.07.006
13. Ucisik, M. H., Kupcu, S., Schuster, B., and Sleytr, U. B. (2013) Characterization of CurcuEmulsomes: nanoformulation for enhanced solubility and delivery of curcumin J. Nanobiotechnol. 11, 37 10.1186/1477-3155-11-37
14. Shoba, G., Joy, D., Joseph, T., Majeed, M., Rajendran, R., and Srinivas, P. S. (1998) Influence of piperine on the pharmacokinetics of curcumin in animals and human volunteers Planta Med. 64, 353-356 10.1055/s-2006-957450
15. Shrivastava, P., Vaibhav, K., Tabassum, R., Khan, A., Ishrat, T., Khan, M. M., Ahmad, A., Islam, F., Safhi, M. M., and Islam, F. (2013) Anti-apoptotic and anti-inflammatory effect of Piperine on 6-OHDA induced Parkinson's rat model J. Nutr. Biochem. 24, 680-687 10.1016/j.jnutbio.2012.03.018
16. Al-Baghdadi, O. B., Prater, N. I., Van der Schyf, C. J., and Geldenhuys, W. J. (2012) Inhibition of monoamine oxidase by derivatives of piperine, an alkaloid from the pepper plant Piper nigrum, for possible use in Parkinson's disease Bioorg. Med. Chem. Lett. 22, 7183-7188 10.1016/j.bmcl.2012.09.056
17. Patel, T. R. (2014) Nanocarrier-based therapies for CNS tumors CNS Oncol. 3, 115-122 10.2217/cns.14.2
18. Dilnawaz, F. and Sahoo, S. K. (2015) Therapeutic approaches of magnetic nanoparticles for the central nervous system Drug Discovery Today 20, 1256-1264 10.1016/j.drudis.2015.06.008
19. Kaur, I. P., Bhandari, R., Bhandari, S., and Kakkar, V. (2008) Potential of solid lipid nanoparticles in brain targeting J. Controlled Release 127, 97-109 10.1016/j.jconrel.2007.12.018
20. Wong, H. L., Chattopadhyay, N., Wu, X. Y., and Bendayan, R. (2010) Nanotechnology applications for improved delivery of antiretroviral drugs to the brain Adv. Drug Delivery Rev. 62, 503-517 10.1016/j.addr.2009.11.020
21. Uner, M. and Yener, G. (2007) Importance of solid lipid nanoparticles (SLN) in various administration routes and future perspectives Int. J. Nanomed. 2, 289-300
22. Lai, J., Lu, Y., Yin, Z., Hu, F., and Wu, W. (2010) Pharmacokinetics and enhanced oral bioavailability in beagle dogs of cyclosporine A encapsulated in glyceryl monooleate/poloxamer 407 cubic nanoparticles Int. J. Nanomed. 5, 13-23
23. Yang, Z., Chen, M., Yang, M., Chen, J., Fang, W., and Xu, P. (2014) Evaluating the potential of cubosomal nanoparticles for oral delivery of amphotericin B in treating fungal infection Int. J. Nanomed. 9, 327-336 10.2147/IJN.S54967
24. Dilnawaz, F., Singh, A., Mewar, S., Sharma, U., Jagannathan, N. R., and Sahoo, S. K. (2012) The transport of non-surfactant based paclitaxel loaded magnetic nanoparticles across the blood brain barrier in a rat model Biomaterials 33, 2936-2951 10.1016/j.biomaterials.2011.12.046
25. Parhi, P. and Sahoo, S. K. (2015) Trastuzumab guided nanotheranostics: A lipid based multifunctional nanoformulation for targeted drug delivery and imaging in breast cancer therapy J. Colloid Interface Sci. 451, 198-211 10.1016/j.jcis.2015.03.049
26. Kreuter, J. (2004) Influence of the surface properties on nanoparticle-mediated transport of drugs to the brain J. Nanosci. Nanotechnol. 4, 484-488 10.1166/jnn.2003.077
27. Kulkarni, S. A. and Feng, S. S. (2013) Effects of particle size and surface modification on cellular uptake and biodistribution of polymeric nanoparticles for drug delivery Pharm. Res. 30, 2512-2522 10.1007/s11095-012-0958-3
28. Gelperina, S., Maksimenko, O., Khalansky, A., Vanchugova, L., Shipulo, E., Abbasova, K., Berdiev, R., Wohlfart, S., Chepurnova, N., and Kreuter, J. (2010) Drug delivery to the brain using surfactant-coated poly(lactide-co-glycolide) nanoparticles: influence of the formulation parameters Eur. J. Pharm. Biopharm. 74, 157-163 10.1016/j.ejpb.2009.09.003
29. Kalia, L. V., Kalia, S. K., and Lang, A. E. (2015) Disease-modifying strategies for Parkinson's disease Mov. Disord. 30, 1442-1450 10.1002/mds.26354
30. Garbayo, E., Ansorena, E., and Blanco-Prieto, M. J. (2013) Drug development in Parkinson's disease: from emerging molecules to innovative drug delivery systems Maturitas 76, 272-278 10.1016/j.maturitas.2013.05.019
31. Jain, K. K. (2012) Nanobiotechnology-based strategies for crossing the blood-brain barrier Nanomedicine (London, U. K.) 7, 1225-1233 10.2217/nnm.12.86
32. Grau, C. M. and Greene, L. A. (2012) Use of PC12 cells and rat superior cervical ganglion sympathetic neurons as models for neuroprotective assays relevant to Parkinson's disease Methods Mol. Biol. 846, 201-211 10.1007/978-1-61779-536-7-18
33. Panyam, J., Zhou, W. Z., Prabha, S., Sahoo, S. K., and Labhasetwar, V. (2002) Rapid endo-lysosomal escape of poly(DL-lactide-co-glycolide) nanoparticles: implications for drug and gene delivery FASEB J. 16, 1217-1226 10.1096/fj.02-0088com
34. Das, M., Duan, W., and Sahoo, S. K. (2015) Multifunctional nanoparticle-EpCAM aptamer bioconjugates: a paradigm for targeted drug delivery and imaging in cancer therapy Nanomedicine 11, 379-389 10.1016/j.nano.2014.09.002
35. Stefanis, L. (2012) alpha-Synuclein in Parkinson's disease Cold Spring Harbor Perspect. Med. 2, a009399 10.1101/cshperspect.a009399
36. Ono, K. and Yamada, M. (2006) Antioxidant compounds have potent anti-fibrillogenic and fibril-destabilizing effects for alpha-synuclein fibrils in vitro J. Neurochem. 97, 105-115 10.1111/j.1471-4159.2006.03707.x
37. Ahsan, N., Mishra, S., Jain, M. K., Surolia, A., and Gupta, S. (2015) Curcumin Pyrazole and its derivative (N-(3-Nitrophenylpyrazole) Curcumin inhibit aggregation, disrupt fibrils and modulate toxicity of Wild type and Mutant alpha-Synuclein Sci. Rep. 5, 9862 10.1038/srep09862
38. Wang, H., Liu, J., Gao, G., Wu, X., Wang, X., and Yang, H. (2016) Protection effect of piperine and piperlonguminine from Piper longum L. alkaloids against rotenone-induced neuronal injury Brain Res. 1639, 214-227 10.1016/j.brainres.2015.07.029
39. Ahmad, B. and Lapidus, L. J. (2012) Curcumin prevents aggregation in alpha-synuclein by increasing reconfiguration rate J. Biol. Chem. 287, 9193-9199 10.1074/jbc.M111.325548
40. Wang, B., Yu, X. C., Xu, S. F., and Xu, M. (2015) Paclitaxel and etoposide co-loaded polymeric nanoparticles for the effective combination therapy against human osteosarcoma J. Nanobiotechnol. 13, 22 10.1186/s12951-015-0086-4
41. Sahoo, S. K. and Labhasetwar, V. (2005) Enhanced antiproliferative activity of transferrin-conjugated paclitaxel-loaded nanoparticles is mediated via sustained intracellular drug retention Mol. Pharmaceutics 2, 373-383 10.1021/mp050032z
42. Panyam, J. and Labhasetwar, V. (2003) Dynamics of endocytosis and exocytosis of poly(D,L-lactide-co-glycolide) nanoparticles in vascular smooth muscle cells Pharm. Res. 20, 212-220 10.1023/A:1022219003551
43. Jayaraj, R. L., Tamilselvam, K., Manivasagam, T., and Elangovan, N. (2013) Neuroprotective effect of CNB-001, a novel pyrazole derivative of curcumin on biochemical and apoptotic markers against rotenone-induced SK-N-SH cellular model of Parkinson's disease J. Mol. Neurosci. 51, 863-870 10.1007/s12031-013-0075-8
44. Schapira, A. H. and Jenner, P. (2011) Etiology and pathogenesis of Parkinson's disease Mov. Disord. 26, 1049-1055 10.1002/mds.23732
45. Zhu, J. and Chu, C. T. (2010) Mitochondrial dysfunction in Parkinson's disease J. Alzheimers Dis. 20 (Suppl 2) S325-334 10.3233/JAD-2010-100363
46. Martin, H. L. and Teismann, P. (2009) Glutathione - a review on its role and significance in Parkinson's disease FASEB J. 23, 3263-3272 10.1096/fj.08-125443
47. Sharma, N. and Nehru, B. (2013) Beneficial Effect of Vitamin E in Rotenone Induced Model of PD: Behavioural, Neurochemical and Biochemical Study Exp. Neurobiol. 22, 214-223 10.5607/en.2013.22.3.214
48. Jagatha, B., Mythri, R. B., Vali, S., and Bharath, M. M. (2008) Curcumin treatment alleviates the effects of glutathione depletion in vitro and in vivo: therapeutic implications for Parkinson's disease explained via in silico studies Free Radical Biol. Med. 44, 907-917 10.1016/j.freeradbiomed.2007.11.011
49. Lee, C. S., Han, E. S., and Kim, Y. K. (2006) Piperine inhibition of 1-methyl-4-phenylpyridinium-induced mitochondrial dysfunction and cell death in PC12 cells Eur. J. Pharmacol. 537, 37-44 10.1016/j.ejphar.2006.03.026
50. Gorrini, C., Harris, I. S., and Mak, T. W. (2013) Modulation of oxidative stress as an anticancer strategy Nat. Rev. Drug Discovery 12, 931-947 10.1038/nrd4002
51. Liu, Z., Dou, W., Zheng, Y., Wen, Q., Qin, M., Wang, X., Tang, H., Zhang, R., Lv, D., Wang, J., and Zhao, S. (2016) Curcumin upregulates Nrf2 nuclear translocation and protects rat hepatic stellate cells against oxidative stress Mol. Med. Rep. 13, 1717-1724 10.3892/mmr.2015.4690
52. Reale, M., Pesce, M., Priyadarshini, M., Kamal, M. A., and Patruno, A. (2012) Mitochondria as an easy target to oxidative stress events in Parkinson's disease CNS Neurol. Disord.: Drug Targets 11, 430-438 10.2174/187152712800792875
53. Dehay, B., Martinez-Vicente, M., Caldwell, G. A., Caldwell, K. A., Yue, Z., Cookson, M. R., Klein, C., Vila, M., and Bezard, E. (2013) Lysosomal impairment in Parkinson's disease Mov. Disord. 28, 725-732 10.1002/mds.25462
54. Wu, F., Xu, H. D., Guan, J. J., Hou, Y. S., Gu, J. H., Zhen, X. C., and Qin, Z. H. (2015) Rotenone impairs autophagic flux and lysosomal functions in Parkinson's disease Neuroscience 284, 900-911 10.1016/j.neuroscience.2014.11.004
55. Jiang, T. F., Zhang, Y. J., Zhou, H. Y., Wang, H. M., Tian, L. P., Liu, J., Ding, J. Q., and Chen, S. D. (2013) Curcumin ameliorates the neurodegenerative pathology in A53T alpha-synuclein cell model of Parkinson's disease through the downregulation of mTOR/p70S6K signaling and the recovery of macroautophagy J. Neuroimmune Pharmacol. 8, 356-369 10.1007/s11481-012-9431-7
56. Naponelli, V., Modernelli, A., Bettuzzi, S., and Rizzi, F. (2015) Roles of autophagy induced by natural compounds in prostate cancer BioMed Res. Int. 2015, 121826 10.1155/2015/121826
57. Rekha, K. R. and Selvakumar, G. P. (2014) Gene expression regulation of Bcl2, Bax and cytochrome-C by geraniol on chronic MPTP/probenecid induced C57BL/6 mice model of Parkinson's disease Chem.-Biol. Interact. 217, 57-66 10.1016/j.cbi.2014.04.010
58. Shakeri, A. and Sahebkar, A. (2016) Nanotechnology: A Successful Approach to Improve Oral Bioavailability of Phytochemicals Recent Pat. Drug Delivery Formulation 10, 4-6 10.2174/1872211309666150611120724
59. Yang, K. Y., Lin, L. C., Tseng, T. Y., Wang, S. C., and Tsai, T. H. (2007) Oral bioavailability of curcumin in rat and the herbal analysis from Curcuma longa by LC-MS/MS J. Chromatogr. B: Anal. Technol. Biomed. Life Sci. 853, 183-189 10.1016/j.jchromb.2007.03.010
60. Ramalingam, P. and Ko, Y. T. (2015) Enhanced oral delivery of curcumin from N-trimethyl chitosan surface-modified solid lipid nanoparticles: pharmacokinetic and brain distribution evaluations Pharm. Res. 32, 389-402 10.1007/s11095-014-1469-1
61. Kakkar, V., Mishra, A. K., Chuttani, K., and Kaur, I. P. (2013) Proof of concept studies to confirm the delivery of curcumin loaded solid lipid nanoparticles (C-SLNs) to brain Int. J. Pharm. 448, 354-359 10.1016/j.ijpharm.2013.03.046
62. Inden, M., Kitamura, Y., Tamaki, A., Yanagida, T., Shibaike, T., Yamamoto, A., Takata, K., Yasui, H., Taira, T., Ariga, H., and Taniguchi, T. (2009) Neuroprotective effect of the antiparkinsonian drug pramipexole against nigrostriatal dopaminergic degeneration in rotenone-treated mice Neurochem. Int. 55, 760-767 10.1016/j.neuint.2009.07.009
63. da Rocha Lindner, G., Bonfanti Santos, D., Colle, D., Gasnhar Moreira, E. L., Daniel Prediger, R., Farina, M., Khalil, N. M., and Mara Mainardes, R. (2015) Improved neuroprotective effects of resveratrol-loaded polysorbate 80-coated poly(lactide) nanoparticles in MPTP-induced Parkinsonism Nanomedicine (London, U. K.) 10, 1127-1138 10.2217/nnm.14.165
64. Vandana, M. and Sahoo, S. K. (2009) Optimization of physicochemical parameters influencing the fabrication of protein-loaded chitosan nanoparticles Nanomedicine (London, U. K.) 4, 773-785 10.2217/nnm.09.54
65. Misra, R., Das, M., Sahoo, B. S., and Sahoo, S. K. (2014) Reversal of multidrug resistance in vitro by co-delivery of MDR1 targeting siRNA and doxorubicin using a novel cationic poly(lactide-co-glycolide) nanoformulation Int. J. Pharm. 475, 372-384 10.1016/j.ijpharm.2014.08.056
66. Suresh, D. and Srinivasan, K. (2010) Tissue distribution & elimination of capsaicin, piperine & curcumin following oral intake in rats Indian J. Med. Res. 131, 682-691
67. Shaikh, J., Ankola, D. D., Beniwal, V., Singh, D., and Kumar, M. N. (2009) Nanoparticle encapsulation improves oral bioavailability of curcumin by at least 9-fold when compared to curcumin administered with piperine as absorption enhancer Eur. J. Pharm. Sci. 37, 223-230 10.1016/j.ejps.2009.02.019
68. Danzer, K. M., Haasen, D., Karow, A. R., Moussaud, S., Habeck, M., Giese, A., Kretzschmar, H., Hengerer, B., and Kostka, M. (2007) Different species of alpha-synuclein oligomers induce calcium influx and seeding J. Neurosci. 27, 9220-9232 10.1523/JNEUROSCI.2617-07.2007
69. Vandana, M. and Sahoo, S. K. (2015) Synergistic activity of combination therapy with PEGylated pemetrexed and gemcitabine for an effective cancer treatment Eur. J. Pharm. Biopharm. 94, 83-93 10.1016/j.ejpb.2015.04.017
70. Kimura, S., Noda, T., and Yoshimori, T. (2007) Dissection of the autophagosome maturation process by a novel reporter protein, tandem fluorescent-tagged LC3 Autophagy 3, 452-460 10.4161/auto.4451