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Vol. 14 (2022)

Anti-Parkinsonian Therapy: Strategies for Crossing the Blood–Brain Barrier and Nano-Biological Effects of Nanomaterials

https://doi.org/10.1007/s40820-022-00847-z
Guowang Cheng
Key Laboratory of Modern Preparation of Traditional Chinese Medicine, Ministry of Education, Jiangxi University of Chinese Medicine, Nanchang 330004, People’s Republic of China
Yujing Liu
Science and Technology Innovation Center, Guangzhou University of Chinese Medicine, Guangzhou 510405, People’s Republic of China
Rui Ma
Science and Technology Innovation Center, Guangzhou University of Chinese Medicine, Guangzhou 510405, People’s Republic of China
Guopan Cheng
Science and Technology Innovation Center, Guangzhou University of Chinese Medicine, Guangzhou 510405, People’s Republic of China
Yucheng Guan
Science and Technology Innovation Center, Guangzhou University of Chinese Medicine, Guangzhou 510405, People’s Republic of China
Xiaojia Chen
State Key Laboratory of Quality Research in Chinese Medicine, Institute of Chinese Medical Sciences, University of Macau, Macau 999078, People’s Republic of China
Zhenfeng Wu
Key Laboratory of Modern Preparation of Traditional Chinese Medicine, Ministry of Education, Jiangxi University of Chinese Medicine, Nanchang 330004, People’s Republic of China
Tongkai Chen
Science and Technology Innovation Center, Guangzhou University of Chinese Medicine, Guangzhou 510405, People’s Republic of China

Corresponding Author: Tongkai Chen

chentongkai@gzucm.edu.cn

Nano-Micro Letters, Vol. 14 (2022), Article Number: 105

Abstract

Parkinson’s disease (PD), a neurodegenerative disease that shows a high incidence in older individuals, is becoming increasingly prevalent. Unfortunately, there is no clinical cure for PD, and novel anti-PD drugs are therefore urgently required. However, the selective permeability of the blood–brain barrier (BBB) poses a huge challenge in the development of such drugs. Fortunately, through strategies based on the physiological characteristics of the BBB and other modifications, including enhancement of BBB permeability, nanotechnology can offer a solution to this problem and facilitate drug delivery across the BBB. Although nanomaterials are often used as carriers for PD treatment, their biological activity is ignored. Several studies in recent years have shown that nanomaterials can improve PD symptoms via their own nano-bio effects. In this review, we first summarize the physiological features of the BBB and then discuss the design of appropriate brain-targeted delivery nanoplatforms for PD treatment. Subsequently, we highlight the emerging strategies for crossing the BBB and the development of novel nanomaterials with anti-PD nano-biological effects. Finally, we discuss the current challenges in nanomaterial-based PD treatment and the future trends in this field. Our review emphasizes the clinical value of nanotechnology in PD treatment based on recent patents and could guide researchers working in this area in the future.


Highlights:


1 Strategies for crossing the blood–brain barrier and the nano-biological effects of nanomaterials used for anti-Parkinsonian therapy are summarized.
2 Patents related to nanotechnology-based anti-Parkinsonian therapy are reviewed, and the status of progress in this field are discussed.
3 Current challenges in nanotechnology-based Parkinson’s disease treatment are discussed, with insights into the future trends in this field.

Keywords

Blood–brain barrier Parkinson’s disease Nasal delivery Biomimetic drug delivery Nano-biological effects
Cheng, Guowang, Yujing Liu, Rui Ma, Guopan Cheng, Yucheng Guan, Xiaojia Chen, Zhenfeng Wu, and Tongkai Chen. 2022. “Anti-Parkinsonian Therapy: Strategies for Crossing the Blood–Brain Barrier and Nano-Biological Effects of Nanomaterials”. Nano-Micro Letters 14 (April):105. https://doi.org/10.1007/s40820-022-00847-z.
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References
  1. Y. Hou, X. Dan, M. Babbar, Y. Wei, S.G. Hasselbalch et al., Ageing as a risk factor for neurodegenerative disease. Nat. Rev. Neurol. 15, 565–581 (2019). https://doi.org/10.1038/s41582-019-0244-7
  2. L.V. Kalia, A.E. Lang, Parkinson’s disease. The Lancet 386(9996), 896–912 (2015). https://doi.org/10.1016/s0140-6736(14)61393-3
  3. M. Goedert, A. Compston, Parkinson’s disease - the story of an eponym. Nat. Rev. Neurol. 14, 57–62 (2018). https://doi.org/10.1038/nrneurol.2017.165
  4. W. Poewe, K. Seppi, C.M. Tanner, G.M. Halliday, P. Brundin et al., Parkinson disease. Nat. Rev. Dis. Primers 3, 17013 (2017). https://doi.org/10.1038/nrdp.2017.13
  5. S. Przedborski, The two-century journey of Parkinson disease research. Nat. Rev. Neurosci. 18, 251–259 (2017). https://doi.org/10.1038/nrn.2017.25
  6. J. Kulisevsky, L. Oliveira, S.H. Fox, Update in therapeutic strategies for Parkinson’s disease. Curr. Opin. Neurol. 31(4), 439–447 (2018). https://doi.org/10.1097/WCO.0000000000000579
  7. D. Charvin, R. Medori, R.A. Hauser, O. Rascol, Therapeutic strategies for Parkinson disease: beyond dopaminergic drugs. Nat. Rev. Drug Discov. 17, 804–822 (2018). https://doi.org/10.1038/nrd.2018.136
  8. A. Elkouzi, V. Vedam-Mai, R.S. Eisinger, M.S. Okun, Emerging therapies in Parkinson disease - repurposed drugs and new approaches. Nat. Rev. Neurol. 15, 204–223 (2019). https://doi.org/10.1038/s41582-019-0155-7
  9. H. Homayoun, Parkinson disease. Ann. Int. Med. 169, ITC33–ITC48 (2018). https://doi.org/10.7326/AITC201809040
  10. K. Liaw, Z. Zhang, S. Kannan, Neuronanotechnology for brain regeneration. Adv. Drug Deliv. Rev. 148, 3–18 (2019). https://doi.org/10.1016/j.addr.2019.04.004
  11. N. Bengoa-Vergniory, R.F. Roberts, R. Wade-Martins, J. Alegre-Abarrategui, Alpha-synuclein oligomers: a new hope. Acta Neuropathol. 134, 819–838 (2017). https://doi.org/10.1007/s00401-017-1755-1
  12. D. Eleftheriadou, D. Kesidou, F. Moura, E. Felli, W. Song, Redox-responsive nanobiomaterials-based therapeutics for neurodegenerative diseases. Small 16(43), 1907308 (2020). https://doi.org/10.1002/smll.201907308
  13. J. Bicker, G. Alves, A. Fortuna, A. Falcao, Blood-brain barrier models and their relevance for a successful development of CNS drug delivery systems: a review. Eur. J. Pharm. Biopharm. 87(3), 409–432 (2014). https://doi.org/10.1016/j.ejpb.2014.03.012
  14. W.A. Banks, From blood-brain barrier to blood-brain interface: new opportunities for CNS drug delivery. Nat. Rev. Drug Discov. 15, 275–292 (2016). https://doi.org/10.1038/nrd.2015.21
  15. M.D. Sweeney, Z. Zhao, A. Montagne, A.R. Nelson, B.V. Zlokovic, Blood-brain barrier: from physiology to disease and back. Physiol. Rev. 99, 21–78 (2019). https://doi.org/10.1152/physrev.00050.2017
  16. F. Meng, J. Wang, F. Ding, Y. Xie, Y. Zhang et al., Neuroprotective effect of matrine on MPTP-induced Parkinson’s disease and on Nrf2 expression. Oncol. Lett. 13, 296–300 (2017). https://doi.org/10.3892/ol.2016.5383
  17. A. Bhat, A.M. Mahalakshmi, B. Ray, S. Tuladhar, T.A. Hediyal et al., Benefits of curcumin in brain disorders. BioFactors 45(5), 666–689 (2019). https://doi.org/10.1002/biof.1533
  18. S.C. Cunnane, E. Trushina, C. Morland, A. Prigione, G. Casadesus et al., Brain energy rescue: an emerging therapeutic concept for neurodegenerative disorders of ageing. Nat. Rev. Drug Discov. 19, 609–633 (2020). https://doi.org/10.1038/s41573-020-0072-x
  19. C. Liu, J. Shin, S. Son, Y. Choe, N. Farokhzad et al., Pnictogens in medicinal chemistry: evolution from erstwhile drugs to emerging layered photonic nanomedicine. Chem. Soc. Rev. 50(4), 2260–2279 (2021). https://doi.org/10.1039/d0cs01175d
  20. J. Zhang, K. Hu, L. Di, P. Wang, Z. Liu et al., Traditional herbal medicine and nanomedicine: converging disciplines to improve therapeutic efficacy and human health. Adv. Drug Deliv. Rev. 178, 113964 (2021). https://doi.org/10.1016/j.addr.2021.113964
  21. D. Furtado, M. Björnmalm, S. Ayton, A.I. Bush, K. Kempe et al., Overcoming the blood-brain barrier: the role of nanomaterials in treating neurological diseases. Adv. Mater. 30, e1801362 (2018). https://doi.org/10.1002/adma.201801362
  22. W. Tang, W. Fan, J. Lau, L. Deng, Z. Shen et al., Emerging blood-brain-barrier-crossing nanotechnology for brain cancer theranostics. Chem. Soc. Rev. 48(11), 2967–3014 (2019). https://doi.org/10.1039/c8cs00805a
  23. J. Kreuter, Drug delivery to the central nervous system by polymeric nanops: what do we know? Adv. Drug Deliv. Rev. 71, 2–14 (2014). https://doi.org/10.1016/j.addr.2013.08.008
  24. J.Y. Ljubimova, T. Sun, L. Mashouf, A.V. Ljubimov, L.L. Israel et al., Covalent nano delivery systems for selective imaging and treatment of brain tumors. Adv. Drug Deliv. Rev. 113, 177–200 (2017). https://doi.org/10.1016/j.addr.2017.06.002
  25. B. Oller-Salvia, M. Sanchez-Navarro, E. Giralt, M. Teixido, Blood-brain barrier shuttle peptides: an emerging paradigm for brain delivery. Chem. Soc. Rev. 45(17), 4690–4707 (2016). https://doi.org/10.1039/c6cs00076b
  26. Y. Luo, H. Yang, Y.F. Zhou, B. Hu, Dual and multi-targeted nanops for site-specific brain drug delivery. J. Control. Release 317, 195–215 (2020). https://doi.org/10.1016/j.jconrel.2019.11.037
  27. Y. Cheng, R.A. Morshed, B. Auffinger, A.L. Tobias, M.S. Lesniak, Multifunctional nanops for brain tumor imaging and therapy. Adv. Drug Deliv. Rev. 66, 42–57 (2014). https://doi.org/10.1016/j.addr.2013.09.006
  28. R. Pandit, L. Chen, J. Gotz, The blood-brain barrier: physiology and strategies for drug delivery. Adv. Drug Deliv. Rev. 165–166, 1–14 (2019). https://doi.org/10.1016/j.addr.2019.11.009
  29. W. Fu, W. Zhou, P.K. Chu, X.F. Yu, Inherent chemotherapeutic anti-cancer effects of low-dimensional nanomaterials. Chemistry 25(47), 10995–11006 (2019). https://doi.org/10.1002/chem.201901841
  30. C. Cheng, S. Li, A. Thomas, N.A. Kotov, R. Haag, Functional graphene nanomaterials based architectures: biointeractions, fabrications, and emerging biological applications. Chem. Rev. 117(3), 1826–1914 (2017). https://doi.org/10.1021/acs.chemrev.6b00520
  31. W. Chen, J. Ouyang, X. Yi, Y. Xu, C. Niu et al., Black phosphorus nanosheets as a neuroprotective nanomedicine for neurodegenerative disorder therapy. Adv. Mater. 30(3), 1703458 (2018). https://doi.org/10.1002/adma.201703458
  32. L.L. Dugan, L. Tian, K.L. Quick, J.I. Hardt, M. Karimi et al., Carboxyfullerene neuroprotection postinjury in Parkinsonian nonhuman primates. Ann. Neurol. 76(3), 393–402 (2014). https://doi.org/10.1002/ana.24220
  33. C. Hao, A. Qu, L. Xu, M. Sun, H. Zhang et al., Chiral molecule-mediated porous CuxO nanop clusters with antioxidation activity for ameliorating Parkinson’s disease. J. Am. Chem. Soc. 141(2), 1091–1099 (2019). https://doi.org/10.1021/jacs.8b11856
  34. C.D. Arvanitis, G.B. Ferraro, R.K. Jain, The blood-brain barrier and blood-tumour barrier in brain tumours and metastases. Nat. Rev. Cancer 20, 26–41 (2020). https://doi.org/10.1038/s41568-019-0205-x
  35. A. Oddo, B. Peng, Z. Tong, Y. Wei, W.Y. Tong et al., Advances in microfluidic blood-brain barrier (BBB) models. Trends Biotechnol. 37(12), 1295–1314 (2019). https://doi.org/10.1016/j.tibtech.2019.04.006
  36. L. Xu, A. Nirwane, Y. Yao, Basement membrane and blood-brain barrier. Stroke Vasc. Neurol. 4(2), 78–82 (2019). https://doi.org/10.1136/svn-2018-000198
  37. Z. Zhao, A.R. Nelson, C. Betsholtz, B.V. Zlokovic, Establishment and dysfunction of the blood-brain barrier. Cell 163(5), 1064–1078 (2015). https://doi.org/10.1016/j.cell.2015.10.067
  38. S. Liebner, R.M. Dijkhuizen, Y. Reiss, K.H. Plate, D. Agalliu et al., Functional morphology of the blood-brain barrier in health and disease. Acta Neuropathol. 135, 311–336 (2018). https://doi.org/10.1007/s00401-018-1815-1
  39. N. Bengoa-Vergniory, R.F. Roberts, W. Rade-Martins, J. Alegre-Abarrategui, Alpha-synuclein oligomers: a new hope. Acta Neuropathol. 134, 819–838 (2017). https://doi.org/10.1007/s00401-017-1755-1
  40. L.H. Morais, H.L. Schreiber, S.K. Mazmanian, The gut microbiota-brain axis in behaviour and brain disorders. Nat. Rev. Microbiol. 19, 241–255 (2021). https://doi.org/10.1038/s41579-020-00460-0
  41. R.A. Travagli, K.N. Browning, M. Camilleri, Parkinson disease and the gut: new insights into pathogenesis and clinical relevance. Nat. Rev. Gastroenterol. Hepatol. 17, 673–685 (2020). https://doi.org/10.1038/s41575-020-0339-z
  42. I. Javed, X. Cui, X. Wang, M. Mortimer, N. Andrikopoulos et al., Implications of the human gut-brain and gut-cancer axes for future nanomedicine. ACS Nano 14(11), 14391–14416 (2020). https://doi.org/10.1021/acsnano.0c07258
  43. S. Kim, S.H. Kwon, T.I. Kam, N. Panicker, S.S. Karuppagounder et al., Transneuronal propagation of pathologic α-synuclein from the gut to the brain models Parkinson’s disease. Neuron 103(4), 627–641 (2019). https://doi.org/10.1016/j.neuron.2019.05.035
  44. T.R. Sampson, J.W. Debelius, T. Thron, S. Janssen, G.G. Shastri et al., Gut microbiota regulate motor deficits and neuroinflammation in a model of Parkinson’s disease. Cell 167(6), 1469–1480 (2016). https://doi.org/10.1016/j.cell.2016.11.018
  45. J. Samal, A.L. Rebelo, A. Pandit, A window into the brain: tools to assess pre-clinical efficacy of biomaterials-based therapies on central nervous system disorders. Adv. Drug Deliv. Rev. 148, 68–145 (2019). https://doi.org/10.1016/j.addr.2019.01.012
  46. Y.H. Tsou, X.Q. Zhang, H. Zhu, S. Syed, X. Xu, Drug delivery to the brain across the blood-brain barrier using nanomaterials. Small 13(43), 170192 (2018). https://doi.org/10.1002/smll.201701921
  47. S. Shen, Y. Wu, Y. Liu, D. Wu, High drug-loading nanomedicines: progress, current status, and prospects. Int. J. Nanomed. 12, 4085–4109 (2017). https://doi.org/10.2147/IJN.S132780
  48. Y. Liu, Y.G. Ang, S. Jin, L. Xu, C.X. Zhao, Development of high-drug-loading nanops. ChemPlusChem 85(9), 2143–2157 (2020). https://doi.org/10.1002/cplu.202000496
  49. W. Chen, J. Ouyang, H. Liu, M. Chen, K. Zeng et al., Black phosphorus nanosheet-based drug delivery system for synergistic photodynamic/photothermal/chemotherapy of cancer. Adv. Mater. 29(5), 1603864 (2017). https://doi.org/10.1002/adma.201603864
  50. J. Mosquera, I. Garcia, L.M. Liz-Marzan, Cellular uptake of nanops versus small molecules: a matter of size. Acc. Chem. Res. 51(9), 2305–2313 (2018). https://doi.org/10.1021/acs.accounts.8b00292
  51. O. Betzer, M. Shilo, R. Opochinsky, E. Barnoy, M. Motiei et al., The effect of nanop size on the ability to cross the blood-brain barrier: an in vivo study. Nanomedicine 12(13), 1533–1546 (2017). https://doi.org/10.2217/nnm-2017-0022
  52. G. Wen, X. Li, Y. Zhang, X. Han, X. Xu et al., Effective phototheranostics of brain tumor assisted by near-infrared-II light-responsive semiconducting polymer nanops. ACS Appl. Mater. Interfaces 12(30), 33492–33499 (2020). https://doi.org/10.1021/acsami.0c08562
  53. Y.H. Tsou, X.Q. Zhang, H. Zhu, S. Syed, X. Xu, Drug delivery to the brain across the blood-brain barrier using nanomaterials. Small 14(25), 1801588 (2018). https://doi.org/10.1002/smll.201801588
  54. W. Xie, Z. Guo, F. Gao, Q. Gao, D. Wang et al., Shape-, size- and structure-controlled synthesis and biocompatibility of iron oxide nanops for magnetic theranostics. Theranostics 8(12), 3284–3307 (2018). https://doi.org/10.7150/thno.25220
  55. Z. Shen, H. Ye, X. Yi, Y. Li, Membrane wrapping efficiency of elastic nanops during endocytosis: size and shape matter. ACS Nano 13(1), 215–228 (2018). https://doi.org/10.1021/acsnano.8b05340
  56. P. Kolhar, A.C. Anselmo, V. Gupta, K. Pant, B. Prabhakarpandian et al., Using shape effects to target antibody-coated nanops to lung and brain endothelium. PNAS 110(26), 10753–10758 (2013). https://doi.org/10.1073/pnas.1308345110
  57. H.J. Byeon, Q. Thao, S. Lee, S.Y. Min, E.S. Lee et al., Doxorubicin-loaded nanops consisted of cationic- and mannose-modified-albumins for dual-targeting in brain tumors. J. Control. Release 225, 301–313 (2016). https://doi.org/10.1016/j.jconrel.2016.01.046
  58. J.S. Suk, Q. Xu, N. Kim, J. Hanes, L.M. Ensign, PEGylation as a strategy for improving nanop-based drug and gene delivery. Adv. Drug Deliv. Rev. 99, 28–51 (2016). https://doi.org/10.1016/j.addr.2015.09.012
  59. G.T. Kozma, T. Shimizu, T. Ishida, J. Szebeni, Anti-PEG antibodies: properties, formation, testing and role in adverse immune reactions to PEGylated nano-biopharmaceuticals. Adv. Drug Deliv. Rev. 154–155, 163–175 (2020). https://doi.org/10.1016/j.addr.2020.07.024
  60. K.Y. Choi, H.S. Han, E.S. Lee, J.M. Shin, B.D. Almquist et al., Hyaluronic acid-based activatable nanomaterials for stimuli-responsive imaging and therapeutics: beyond CD44-mediated drug delivery. Adv. Mater. 31(34), 1803549 (2019). https://doi.org/10.1002/adma.201803549
  61. L. Ye, Y. Zhang, B. Yang, X. Zhou, J. Li et al., Zwitterionic-modified starch-based stealth micelles for prolonging circulation time and reducing macrophage response. ACS Appl. Mater. Interfaces 8(7), 4385–4398 (2016). https://doi.org/10.1021/acsami.5b10811
  62. A.R. Khan, X. Yang, M. Fu, G. Zhai, Recent progress of drug nanoformulations targeting to brain. J. Control. Release 291, 37–64 (2018). https://doi.org/10.1016/j.jconrel.2018.10.004
  63. D. Furtado, M. Bjornmalm, S. Ayton, A.I. Bush, K. Kempe et al., Overcoming the blood-brain barrier: the role of nanomaterials in treating neurological diseases. Adv. Mater. 30, 1801362 (2018). https://doi.org/10.1002/adma.201801362
  64. V. Agrahari, P.A. Burnouf, T. Burnouf, V. Agrahari, Nanoformulation properties, characterization, and behavior in complex biological matrices: challenges and opportunities for brain-targeted drug delivery applications and enhanced translational potential. Adv. Drug Deliv. Rev. 148, 146–180 (2019). https://doi.org/10.1016/j.addr.2019.02.008
  65. M.J. Fowler, J.D. Cotter, B.E. Knight, E.M. Sevick-Muraca, D.I. Sandberg et al., Intrathecal drug delivery in the era of nanomedicine. Adv. Drug Deliv. Rev. 165–166, 77–95 (2020). https://doi.org/10.1016/j.addr.2020.02.006
  66. N. Tambasco, M. Romoli, P. Calabresi, Levodopa in Parkinson’s disease: current status and future developments. Curr. Neuropharmacol. 16(8), 1239–1252 (2018). https://doi.org/10.2174/1570159X15666170510143821
  67. X. Li, Q. Liu, D. Zhu, Y. Che, X. Feng, Preparation of levodopa-loaded crystalsomes through thermally induced crystallization reverses functional deficits in Parkinsonian mice. Biomater. Sci. 7(4), 1623–1631 (2019). https://doi.org/10.1039/c8bm01098f
  68. V. Sánchez-Giraldo, Y. Monsalve, J. Palacio, M. Mendivil-Perez, L. Sierra et al., Role of a novel (−)-epigallocatechin-3-gallate delivery system on the prevention against oxidative stress damage in vitro and in vivo model of Parkinson’s disease. J. Drug Deliv. Sci. Technol. 55, 101466 (2020). https://doi.org/10.1016/j.jddst.2019.101466
  69. S. Xiong, W. Liu, Y. Zhou, Y. Mo, Y. Liu et al., Enhancement of oral bioavailability and anti-Parkinsonian efficacy of resveratrol through a nanocrystal formulation. Asian J. Pharm. Sci. 15(4), 518–528 (2019). https://doi.org/10.1016/j.ajps.2019.04.003
  70. Y. Liu, W. Liu, S. Xiong, J. Luo, Y. Li et al., Highly stabilized nanocrystals delivering Ginkgolide B in protecting against the Parkinson’s disease. Int. J. Pharm. 577, 119053 (2020). https://doi.org/10.1016/j.ijpharm.2020.119053
  71. T. Chen, C. Li, Y. Li, X. Yi, S.M. Lee et al., Oral delivery of a nanocrystal formulation of Schisantherin A with improved bioavailability and brain delivery for the treatment of Parkinson’s disease. Mol. Pharm. 13(11), 3864–3875 (2016). https://doi.org/10.1021/acs.molpharmaceut.6b00644
  72. S. Xiong, W. Liu, D. Li, X. Chen, F. Liu et al., Oral delivery of puerarin nanocrystals to improve brain accumulation and anti-Parkinsonian efficacy. Mol. Pharm. 16(4), 1444–1455 (2019). https://doi.org/10.1021/acs.molpharmaceut.8b01012
  73. T. Chen, Y. Li, C. Li, X. Yi, R. Wang et al., Pluronic P85/F68 micelles of baicalein could interfere with mitochondria to overcome MRP2-mediated efflux and offer improved anti-Parkinsonian activity. Mol. Pharm. 14(10), 3331–3342 (2017). https://doi.org/10.1021/acs.molpharmaceut.7b00374
  74. N. Dudhipala, T. Gorre, Neuroprotective effect of ropinirole lipid nanops enriched hydrogel for Parkinson’s disease: in vitro, ex vivo, pharmacokinetic and pharmacodynamic evaluation. Pharmaceutics 12(5), 448 (2020). https://doi.org/10.3390/pharmaceutics12050448
  75. P. Kundu, M. Das, K. Tripathy, S.K. Sahoo, Delivery of dual drug loaded lipid based nanops across the blood-brain barrier impart enhanced neuroprotection in a rotenone induced mouse model of Parkinson’s disease. ACS Chem. Neurosci. 7(12), 1658–1670 (2016). https://doi.org/10.1021/acschemneuro.6b00207
  76. T. Chen, W. Liu, S. Xiong, D. Li, S. Fang et al., Nanops mediating the sustained puerarin release facilitate improved brain delivery to treat Parkinson’s disease. ACS Appl. Mater. Interfaces 11(48), 45276–45289 (2019). https://doi.org/10.1021/acsami.9b16047
  77. E. Barcia, L. Boeva, L. Garcia-Garcia, K. Slowing, A. Fernandez-Carballido et al., Nanotechnology-based drug delivery of ropinirole for Parkinson’s disease. Drug Deliv. 24(1), 1112–1123 (2017). https://doi.org/10.1080/10717544.2017.1359862
  78. K. Hu, X. Chen, W. Chen, L. Zhang, J. Li et al., Neuroprotective effect of gold nanops composites in Parkinson’s disease model. Nanomed. Nanotechnol. Bio. Med. 14(4), 1123–1136 (2018). https://doi.org/10.1016/j.nano.2018.01.020
  79. A.K. Srivastava, S.R. Choudhury, S. Karmakar, Melatonin/polydopamine nanostructures for collective neuroprotection-based Parkinson’s disease therapy. Biomater. Sci. 8(5), 1345–1363 (2020). https://doi.org/10.1039/c9bm01602c
  80. M.N. Sardoiwala, A.K. Srivastava, B. Kaundal, S. Karmakar, S.R. Choudhury, Recuperative effect of metformin loaded polydopamine nanoformulation promoting EZH2 mediated proteasomal degradation of phospho-alpha-synuclein in Parkinson’s disease model. Nanomedicine 24, 102088 (2020). https://doi.org/10.1016/j.nano.2019.102088
  81. N.R. Bali, P.S. Salve, Selegiline nanop embedded transdermal film: an alternative approach for brain targeting in Parkinson’s disease. J. Drug Deliv. Sci. Technol. 54, 101299 (2019). https://doi.org/10.1016/j.jddst.2019.101299
  82. T. Chen, C. Li, Y. Li, X. Yi, R. Wang et al., Small-sized mPEG–PLGA nanops of Schisantherin A with sustained release for enhanced brain uptake and anti-Parkinsonian activity. ACS Appl. Mater. Interfaces 9(11), 9516–9527 (2017). https://doi.org/10.1021/acsami.7b01171
  83. L.B. Vong, Y. Sato, P. Chonpathompikunlert, S. Tanasawet, P. Hutamekalin et al., Self-assembled polydopamine nanops improve treatment in Parkinson’s disease model mice and suppress dopamine-induced dyskinesia. Acta Biomater. 109, 220–228 (2020). https://doi.org/10.1016/j.actbio.2020.03.021
  84. X.Y. Meng, A.Q. Huang, A. Khan, L. Zhang, X.Q. Sun et al., Vascular endothelial growth factor-loaded poly-lactic-co-glycolic acid nanops with controlled release protect the dopaminergic neurons in Parkinson’s rats. Chem. Biol. Drug Des. 95(6), 631–639 (2020). https://doi.org/10.1111/cbdd.13681
  85. S. Sharma, S.A. Rabbani, J.K. Narang, F.H. Pottoo, J. Ali et al., Role of rutin nanoemulsion in ameliorating oxidative stress: pharmacokinetic and pharmacodynamics studies. Chem. Phys. Lipids 228, 104890 (2020). https://doi.org/10.1016/j.chemphyslip.2020.104890
  86. B.K. Gupta, S. Kumar, H. Kaur, J. Ali, S. Baboota, Attenuation of oxidative damage by coenzyme Q10 loaded nanoemulsion through oral route for the management of Parkinson’s disease. Rejuv. Res. 21(3), 232–248 (2018). https://doi.org/10.1089/rej.2017.1959
  87. S. Setya, T. Madaan, M. Tariq, B.K. Razdan, S. Talegaonkar, Appraisal of transdermal water-in-oil nanoemulgel of selegiline HCl for the effective management of Parkinson’s disease: pharmacodynamic, pharmacokinetic, and biochemical investigations. AAPS PharmSciTech 19, 573–589 (2018). https://doi.org/10.1208/s12249-017-0868-0
  88. L. Liu, M. Li, M. Xu, Z. Wang, Z. Zeng et al., Actively targeted gold nanop composites improve behavior and cognitive impairment in Parkinson’s disease mice. Mater. Sci. Eng. C 114, 111028 (2020). https://doi.org/10.1016/j.msec.2020.111028
  89. S. Niu, L.K. Zhang, L. Zhang, S. Zhuang, X. Zhan et al., Inhibition by multifunctional magnetic nanops loaded with alpha-synuclein RNAi plasmid in a Parkinson’s disease model. Theranostics 7(2), 344–356 (2017). https://doi.org/10.7150/thno.16562
  90. L. Gan, Z. Li, Q. Lv, W. Huang, Rabies virus glycoprotein (RVG29)-linked microRNA-124-loaded polymeric nanops inhibit neuroinflammation in a Parkinson’s disease model. Int. J. Pharm. 567, 118449 (2019). https://doi.org/10.1016/j.ijpharm.2019.118449
  91. L. You, J. Wang, T. Liu, Y. Zhang, X. Han et al., Targeted brain delivery of rabies virus glycoprotein 29-modified deferoxamine-loaded nanops reverses functional deficits in Parkinsonian mice. ACS Nano 12(5), 4123–4139 (2018). https://doi.org/10.1021/acsnano.7b08172
  92. M. Qu, Q. Lin, S. He, L. Wang, Y. Fu et al., A brain targeting functionalized liposomes of the dopamine derivative N-3,4-bis(pivaloyloxy)-dopamine for treatment of Parkinson’s disease. J. Control. Release 277, 173–182 (2018). https://doi.org/10.1016/j.jconrel.2018.03.019
  93. M. Kahana, A. Weizman, M. Gabay, Y. Loboda, H. Segal-Gavish et al., Liposome-based targeting of dopamine to the brain: a novel approach for the treatment of Parkinson’s disease. Mol. Psychiatry. 26, 2626–2632 (2020). https://doi.org/10.1038/s41380-020-0742-4
  94. W. Zhang, H. Chen, L. Ding, J. Gong, M. Zhang et al., Trojan horse delivery of 4,4’-dimethoxychalcone for Parkinsonian neuroprotection. Adv. Sci. 8, 2004555 (2021). https://doi.org/10.1002/advs.202004555
  95. Y. Li, Z. Chen, Z. Lu, Q. Yang, L. Liu et al., “Cell-addictive” dual-target traceable nanodrug for Parkinson’s disease treatment via flotillins pathway. Theranostics 8(9), 5469–5481 (2018). https://doi.org/10.7150/thno.28295
  96. H. Javed, S.A. Menon, K.M. Al-Mansoori, A. Al-Wandi, N.K. Majbour et al., Development of nonviral vectors targeting the brain as a therapeutic approach for Parkinson’s disease and other brain disorders. Mol. Ther. 24(4), 746–758 (2016). https://doi.org/10.1038/mt.2015.232
  97. Q. Guo, H. You, X. Yang, B. Lin, Z. Zhu et al., Functional single-walled carbon nanotubes ‘CAR’ for targeting dopamine delivery into the brain of parkinsonian mice. Nanoscale 9(30), 10832–10845 (2017). https://doi.org/10.1039/c7nr02682j
  98. V. Sridhar, R. Gaud, A. Bajaj, S. Wairkar, Pharmacokinetics and pharmacodynamics of intranasally administered selegiline nanops with improved brain delivery in Parkinson’s disease. Nanomedicine 14(8), 2609–2618 (2018). https://doi.org/10.1016/j.nano.2018.08.004
  99. C. Bi, A. Wang, Y. Chu, S. Liu, H. Mu et al., Intranasal delivery of rotigotine to the brain with lactoferrin-modified PEG-PLGA nanops for Parkinson’s disease treatment. Int. J. Nanomed. 11, 6547–6559 (2016). https://doi.org/10.2147/IJN.S120939
  100. C. Wu, B. Li, Y. Zhang, T. Chen, C. Chen et al., Intranasal delivery of paeoniflorin nanocrystals for brain targeting. Asian J. Pharm. Sci. 15(3), 326–335 (2020). https://doi.org/10.1016/j.ajps.2019.11.002
  101. S.K. Bhattamisra, A.T. Shak, L.W. Xi, N.H. Safian, H. Choudhury et al., Nose to brain delivery of rotigotine loaded chitosan nanops in human SH-SY5Y neuroblastoma cells and animal model of Parkinson’s disease. Int. J. Pharm. 579, 119148 (2020). https://doi.org/10.1016/j.ijpharm.2020.119148
  102. S. Kumar, S. Dang, K. Nigam, J. Ali, S. Baboota, Selegiline nanoformulation in attenuation of oxidative stress and upregulation of dopamine in the brain for the treatment of Parkinson’s disease. Rejuv. Res. 21(5), 464–476 (2018). https://doi.org/10.1089/rej.2017.2035
  103. B. Gaba, T. Khan, M.F. Haider, T. Alam, S. Baboota et al., Vitamin E loaded naringenin nanoemulsion via intranasal delivery for the management of oxidative stress in a 6-OHDA Parkinson’s disease model. Biomed. Res. Int. 2019, 2382563 (2019). https://doi.org/10.1155/2019/2382563
  104. S. Arisoy, O. Sayiner, T. Comoglu, D. Onal, O. Atalay et al., In vitro and in vivo evaluation of levodopa-loaded nanops for nose to brain delivery. Pharm. Dev. Technol. 25(6), 735–747 (2020). https://doi.org/10.1080/10837450.2020.1740257
  105. S. Hernando, E. Herran, J. Figueiro-Silva, J.L. Pedraz, M. Igartua et al., Intranasal administration of TAT-conjugated lipid nanocarriers loading GDNF for Parkinson’s disease. Mol. Neurobiol. 55, 145–155 (2018). https://doi.org/10.1007/s12035-017-0728-7
  106. E.R.O. Junior, E. Truzzi, L. Ferraro, M. Fogagnolo, B. Pavan et al., Nasal administration of nanoencapsulated geraniol/ursodeoxycholic acid conjugate: towards a new approach for the management of Parkinson’s disease. J. Control. Release 321, 540–552 (2020). https://doi.org/10.1016/j.jconrel.2020.02.033
  107. F. Rinaldi, L. Seguella, S. Gigli, P.N. Hanieh, E.D. Favero et al., inPentasomes: an innovative nose-to-brain pentamidine delivery blunts MPTP Parkinsonism in mice. J. Control. Release 294, 17–26 (2019). https://doi.org/10.1016/j.jconrel.2018.12.007
  108. O. Gartziandia, E. Herran, J.A. Ruiz-Ortega, C. Miguelez, M. Igartua et al., Intranasal administration of chitosan-coated nanostructured lipid carriers loaded with GDNF improves behavioral and histological recovery in a partial lesion model of Parkinson’s disease. J. Biomed. Nanotechnol. 12(12), 2220–2230 (2016). https://doi.org/10.1166/jbn.2016.2313
  109. J. Liu, C. Liu, J. Zhang, Y. Zhang, K. Liu et al., A self-assembled alpha-synuclein nanoscavenger for Parkinson’s disease. ACS Nano 14(2), 1533–1549 (2020). https://doi.org/10.1021/acsnano.9b06453
  110. S. Tang, A. Wang, X. Yan, L. Chu, X. Yang et al., Brain-targeted intranasal delivery of dopamine with borneol and lactoferrin co-modified nanops for treating Parkinson’s disease. Drug Deliv. 26(1), 700–707 (2019). https://doi.org/10.1080/10717544.2019.1636420
  111. M. Rao, D.K. Agrawal, C. Shirsath, Thermoreversible mucoadhesive in situ nasal gel for treatment of Parkinson’s disease. Drug Dev. Ind. Pharm. 43(1), 142–150 (2017). https://doi.org/10.1080/03639045.2016.1225754
  112. Y. Tan, Y. Liu, Y. Liu, R. Ma, J. Luo et al., Rational design of thermosensitive hydrogel to deliver nanocrystals with intranasal administration for brain targeting in Parkinson’s disease. Research (2021). https://doi.org/10.34133/2021/9812523
  113. J. Garcia-Pardo, F. Novio, F. Nador, I. Cavaliere, S. Suarez-Garcia et al., Bioinspired theranostic coordination polymer nanops for intranasal dopamine replacement in Parkinson’s disease. ACS Nano 15(5), 8592–8609 (2021). https://doi.org/10.1021/acsnano.1c00453
  114. H. Peng, Y. Li, W. Ji, R. Zhao, Z. Lu et al., Intranasal administration of self-oriented nanocarriers based on therapeutic exosomes for synergistic treatment of Parkinson’s disease. ACS Nano 16(1), 869–884 (2022). https://doi.org/10.1021/acsnano.1c08473
  115. X. Ren, Y. Zhao, F. Xue, Y. Zheng, H. Huang et al., Exosomal DNA aptamer targeting alpha-synuclein aggregates reduced neuropathological deficits in a mouse Parkinson’s disease model. Mol. Ther. Nucleic Acids 17, 726–740 (2019). https://doi.org/10.1016/j.omtn.2019.07.008
  116. M. Qu, Q. Lin, L. Huang, Y. Fu, L. Wang et al., Dopamine-loaded blood exosomes targeted to brain for better treatment of Parkinson’s disease. J. Control. Release 287, 156–166 (2018). https://doi.org/10.1016/j.jconrel.2018.08.035
  117. C.Y. Lin, Y.C. Lin, C.Y. Huang, S.R. Wu, C.M. Chen et al., Ultrasound-responsive neurotrophic factor-loaded microbubble- liposome complex: preclinical investigation for Parkinson’s disease treatment. J. Control. Release 321, 519–528 (2020). https://doi.org/10.1016/j.jconrel.2020.02.044
  118. B. Ji, M. Wang, D. Gao, S. Xing, L. Li et al., Combining nanoscale magnetic nimodipine liposomes with magnetic resonance image for Parkinson’s disease targeting therapy. Nanomedicine 12(3), 237–253 (2017). https://doi.org/10.2217/nnm-2016-0267
  119. M. Wang, L. Li, X. Zhang, Y. Liu, R. Zhu et al., Magnetic resveratrol liposomes as a new theranostic platform for magnetic resonance imaging guided Parkinson’s disease targeting therapy. ACS Sustain. Chem. Eng. 6(12), 17124–17133 (2018). https://doi.org/10.1021/acssuschemeng.8b04507
  120. S. Xiong, Z. Li, Y. Liu, Q. Wang, J. Luo et al., Brain-targeted delivery shuttled by black phosphorus nanostructure to treat Parkinson’s disease. Biomaterials 260, 120339 (2020). https://doi.org/10.1016/j.biomaterials.2020.120339
  121. Y. Liu, D. Zhu, J. Luo, X. Chen, L. Gao et al., NIR-II-activated yolk–shell nanostructures as an intelligent platform for Parkinsonian therapy. ACS Appl. Bio Mater. 3(10), 6876–6887 (2020). https://doi.org/10.1021/acsabm.0c00794
  122. Y. Liu, H. Hong, J. Xue, J. Luo, Q. Liu et al., Near-infrared radiation-assisted drug delivery nanoplatform to realize blood-brain barrier crossing and protection for Parkinsonian therapy. ACS Appl. Mater. Interfaces 13(31), 37746–37760 (2021). https://doi.org/10.1021/acsami.1c12675
  123. J. Niu, J. Xie, K. Guo, X. Zhang, F. Xia et al., Efficient treatment of Parkinson’s disease using ultrasonography-guided rhFGF20 proteoliposomes. Drug Deliv. 25(1), 1560–1569 (2018). https://doi.org/10.1080/10717544.2018.1482972
  124. B.P. Mead, N. Kim, G.W. Miller, D. Hodges, P. Mastorakos et al., Novel focused ultrasound gene therapy approach noninvasively restores dopaminergic neuron function in a rat Parkinson’s disease model. Nano Lett. 17(6), 3533–3542 (2017). https://doi.org/10.1021/acs.nanolett.7b00616
  125. N. Zhang, F. Yan, X. Liang, M. Wu, Y. Shen et al., Localized delivery of curcumin into brain with polysorbate 80-modified cerasomes by ultrasound-targeted microbubble destruction for improved Parkinson’s disease therapy. Theranostics 8(8), 2264–2277 (2018). https://doi.org/10.7150/thno.23734
  126. C.Y. Lin, H.Y. Hsieh, C.M. Chen, S.R. Wu, C.H. Tsai et al., Non-invasive, neuron-specific gene therapy by focused ultrasound-induced blood-brain barrier opening in Parkinson’s disease mouse model. J. Control. Release 235, 72–81 (2016). https://doi.org/10.1016/j.jconrel.2016.05.052
  127. L. Long, X. Cai, R. Guo, P. Wang, L. Wu et al., Treatment of Parkinson’s disease in rats by Nrf2 transfection using MRI-guided focused ultrasound delivery of nanomicrobubbles. Biochem. Biophys. Res. Commun. 482(1), 75–80 (2017). https://doi.org/10.1016/j.bbrc.2016.10.141
  128. H. Liu, Y. Han, T. Wang, H. Zhang, Q. Xu et al., Targeting microglia for therapy of Parkinson’s disease by using biomimetic ultrasmall nanops. J. Am. Chem. Soc. 142(52), 21730–21742 (2020). https://doi.org/10.1021/jacs.0c09390
  129. S.G. Antimisiaris, A. Marazioti, M. Kannavou, E. Natsaridis, F. Gkartziou et al., Overcoming barriers by local drug delivery with liposomes. Adv. Drug Deliv. Rev. 174, 53–86 (2021). https://doi.org/10.1016/j.addr.2021.01.019
  130. A. Singh, W. Kim, Y. Kim, K. Jeong, C.S. Kang et al., Multifunctional photonics nanops for crossing the blood-brain barrier and effecting optically trackable brain theranostics. Adv. Funct. Mater. 26(39), 7057–7066 (2016). https://doi.org/10.1002/adfm.201602808
  131. R. Pandit, L. Chen, J. Götz, The blood-brain barrier: physiology and strategies for drug delivery. Adv. Drug Deliv. Rev. 165–166, 1–14 (2020). https://doi.org/10.1016/j.addr.2019.11.009
  132. D. Wu, M. Qin, D. Xu, L. Wang, C. Liu et al., A bioinspired platform for effective delivery of protein therapeutics to the central nervous system. Adv. Mater. 31(18), 1807557 (2019). https://doi.org/10.1002/adma.201807557
  133. L.N. Nguyen, D. Ma, G. Shui, P. Wong, A. Cazenave-Gassiot et al., Mfsd2a is a transporter for the essential omega-3 fatty acid docosahexaenoic acid. Nature 509, 503–506 (2014). https://doi.org/10.1038/nature13241
  134. G.C. Terstappen, A.H. Meyer, R.D. Bell, W. Zhang, Strategies for delivering therapeutics across the blood-brain barrier. Nat. Rev. Drug Discov. 20, 362–383 (2021). https://doi.org/10.1038/s41573-021-00139-y
  135. E.D. Hood, C.F. Greineder, C. Dodia, J. Han, C. Mesaros et al., Antioxidant protection by PECAM-targeted delivery of a novel NADPH-oxidase inhibitor to the endothelium in vitro and in vivo. J. Control. Release 163(2), 161–169 (2012). https://doi.org/10.1016/j.jconrel.2012.08.031
  136. V.V. Shuvaev, S. Muro, E. Arguiri, M. Khoshnejad, S. Tliba et al., Size and targeting to PECAM vs ICAM control endothelial delivery, internalization and protective effect of multimolecular SOD conjugates. J. Control. Release 234, 115–123 (2016). https://doi.org/10.1016/j.jconrel.2016.05.040
  137. O.A. Marcos-Contreras, J.S. Brenner, R.Y. Kiseleva, V. Zuluaga-Ramirez, C.F. Greineder et al., Combining vascular targeting and the local first pass provides 100-fold higher uptake of ICAM-1-targeted vs untargeted nanocarriers in the inflamed brain. J. Control. Release 301, 54–61 (2019). https://doi.org/10.1016/j.jconrel.2019.03.008
  138. O.A. Marcos-Contreras, C.F. Greineder, R.Y. Kiseleva, H. Parhiz, L.R. Walsh et al., Selective targeting of nanomedicine to inflamed cerebral vasculature to enhance the blood-brain barrier. PNAS 117(7), 3405–3414 (2020). https://doi.org/10.1073/pnas.1912012117
  139. C.C. Yu, H.L. Chen, M.H. Chen, C.H. Lu, N.W. Tsai et al., Vascular inflammation is a risk factor associated with brain atrophy and disease severity in Parkinson’s disease: a case-control study. Oxid. Med. Cell. Longev. 2020, 2591248 (2020). https://doi.org/10.1155/2020/2591248
  140. T.P. Crowe, M.H.W. Greenlee, A.G. Kanthasamy, W.H. Hsu, Mechanism of intranasal drug delivery directly to the brain. Life Sci. 195, 44–52 (2018). https://doi.org/10.1016/j.lfs.2017.12.025
  141. M. Agrawal, S. Saraf, S. Saraf, S.G. Antimisiaris, M.B. Chougule et al., Nose-to-brain drug delivery: an update on clinical challenges and progress towards approval of anti-Alzheimer drugs. J. Control. Release 281, 139–177 (2018). https://doi.org/10.1016/j.jconrel.2018.05.011
  142. U.K. Sukumar, R.J.C. Bose, M. Malhotra, H.A. Babikir, R. Afjei et al., Intranasal delivery of targeted polyfunctional gold-iron oxide nanops loaded with therapeutic microRNAs for combined theranostic multimodality imaging and presensitization of glioblastoma to temozolomide. Biomaterials 218, 119342 (2019). https://doi.org/10.1016/j.biomaterials.2019.119342
  143. E. Samaridou, H. Walgrave, E. Salta, D.M. Alvarez, V. Castro-Lopez et al., Nose-to-brain delivery of enveloped RNA - cell permeating peptide nanocomplexes for the treatment of neurodegenerative diseases. Biomaterials 230, 119657 (2020). https://doi.org/10.1016/j.biomaterials.2019.119657
  144. P. Balakrishnan, E.K. Park, C.K. Song, H.J. Ko, T.W. Hahn et al., Carbopol-incorporated thermoreversible gel for intranasal drug delivery. Molecules 20, 4124–4135 (2015). https://doi.org/10.3390/molecules20034124
  145. C.M.J. Hu, L. Zhang, S. Aryal, C. Cheung, R.H. Fang et al., Erythrocyte membrane-camouflaged polymeric nanops as a biomimetic delivery platform. PNAS 108(27), 10980–10985 (2011). https://doi.org/10.1073/pnas.1106634108
  146. X. Dong, J. Gao, C.Y. Zhang, C. Hayworth, M. Frank et al., Neutrophil membrane-derived nanovesicles alleviate inflammation to protect mouse brain injury from ischemic stroke. ACS Nano 13(2), 1272–1283 (2019). https://doi.org/10.1021/acsnano.8b06572
  147. J. Ma, S. Zhang, J. Liu, F. Liu, F. Du et al., Targeted drug delivery to stroke via chemotactic recruitment of nanops coated with membrane of engineered neural stem cells. Small 15(35), e1902011 (2019). https://doi.org/10.1002/smll.201902011
  148. H. Ye, K. Wang, M. Wang, R. Liu, H. Song et al., Bioinspired nanoplatelets for chemo-photothermal therapy of breast cancer metastasis inhibition. Biomaterials 206, 1–12 (2019). https://doi.org/10.1016/j.biomaterials.2019.03.024
  149. Y. Zou, Y. Liu, Z. Yang, D. Zhang, Y. Lu et al., Effective and targeted human orthotopic glioblastoma xenograft therapy via a multifunctional biomimetic nanomedicine. Adv. Mater. 30(51), 1803717 (2018). https://doi.org/10.1002/adma.201803717
  150. S. Fu, M. Liang, Y. Wang, L. Cui, C. Gao et al., Dual-modified novel biomimetic nanocarriers improve targeting and therapeutic efficacy in glioma. ACS Appl. Mater. Interfaces 11(2), 1841–1854 (2019). https://doi.org/10.1021/acsami.8b18664
  151. N. Perets, O. Betzer, R. Shapira, S. Brenstein, A. Angel et al., Golden exosomes selectively target brain pathologies in neurodegenerative and neurodevelopmental disorders. Nano Lett. 19(6), 3422–3431 (2019). https://doi.org/10.1021/acs.nanolett.8b04148
  152. E.V. Batrakova, S. Li, A.D. Reynolds, R.L. Mosley, T.K. Bronich et al., A macrophage-nanozyme delivery system for Parkinson’s disease. Bioconjugate Chem. 18(5), 1498–1506 (2007). https://doi.org/10.1021/bc700184b
  153. A.M. Brynskikh, Y. Zhao, R.L. Mosley, S. Li, M.D. Boska et al., Macrophage delivery of therapeutic nanozymes in a murine model of Parkinson’s disease. Nanomedicine 5(3), 379–396 (2010). https://doi.org/10.2217/nnm.10.7
  154. K. Biju, Q. Zhou, G. Li, S.Z. Imam, J.L. Roberts, W.W. Morgan et al., Macrophage-mediated GDNF delivery protects against dopaminergic neurodegeneration: a therapeutic strategy for Parkinson’s disease. Mol. Ther. 18(8), 1536–1544 (2010). https://doi.org/10.1038/mt.2010.107
  155. Y. Zhao, M.J. Haney, V. Mahajan, B.C. Reiner, A. Dunaevsky et al., Active targeted macrophage-mediated delivery of catalase to affected brain regions in models of Parkinson’s disease. J. Nanomed. Nanotechnol. S4, 003 (2011). https://doi.org/10.4172/2157-7439.S4-003
  156. Y. Zhao, M.J. Haney, Y.S. Jin, O. Uvarov, N. Vinod et al., GDNF-expressing macrophages restore motor functions at a severe late-stage, and produce long-term neuroprotective effects at an early-stage of Parkinson’s disease in transgenic Parkin Q311X(A) mice. J. Control. Release 315, 139–149 (2019). https://doi.org/10.1016/j.jconrel.2019.10.027
  157. K.C. Biju, R.A. Santacruz, C. Chen, Q. Zhou, J. Yao et al., Bone marrow-derived microglia-based neurturin delivery protects against dopaminergic neurodegeneration in a mouse model of Parkinson’s disease. Neurosci. Lett. 535, 24–29 (2013). https://doi.org/10.1016/j.neulet.2012.12.034
  158. J. Xue, Z. Zhao, L. Zhang, L. Xue, S. Shen et al., Neutrophil-mediated anticancer drug delivery for suppression of postoperative malignant glioma recurrence. Nat. Nanotechnol. 12, 692–700 (2017). https://doi.org/10.1038/nnano.2017.54
  159. D. Dehaini, X. Wei, R.H. Fang, S. Masson, P. Angsantikul et al., Erythrocyte-platelet hybrid membrane coating for enhanced nanop functionalization. Adv. Mater. 29(16), 1606209 (2017). https://doi.org/10.1002/adma.201606209
  160. L.L. Israel, A. Galstyan, E. Holler, J.Y. Ljubimova, Magnetic iron oxide nanops for imaging, targeting and treatment of primary and metastatic tumors of the brain. J. Control. Release 320, 45–62 (2020). https://doi.org/10.1016/j.jconrel.2020.01.009
  161. G. Liu, J. Gao, H. Ai, X. Chen, Applications and potential toxicity of magnetic iron oxide nanops. Small 9(9–10), 1533–1545 (2013). https://doi.org/10.1002/smll.201201531
  162. Y. Huang, B. Zhang, S. Xie, B. Yang, Q. Xu et al., Superparamagnetic iron oxide nanops modified with tween 80 pass through the intact blood-brain barrier in rats under magnetic field. ACS Appl. Mater. Interfaces 8(18), 11336–11341 (2016). https://doi.org/10.1021/acsami.6b02838
  163. H.Y. Kim, T.J. Kim, L. Kang, Y.J. Kim, M.K. Kang et al., Mesenchymal stem cell-derived magnetic extracellular nanovesicles for targeting and treatment of ischemic stroke. Biomaterials 243, 119942 (2020). https://doi.org/10.1016/j.biomaterials.2020.119942
  164. Y. Liu, P. Bhattarai, Z. Dai, X. Chen, Photothermal therapy and photoacoustic imaging via nanotheranostics in fighting cancer. Chem. Soc. Rev. 48(7), 2053–2108 (2019). https://doi.org/10.1039/c8cs00618k
  165. S. Liu, X. Pan, H. Liu, Two-dimensional nanomaterials for photothermal therapy. Angew. Chem. Int. Ed. 59(15), 5890–5900 (2020). https://doi.org/10.1002/anie.201911477
  166. X. Li, J.F. Lovell, J. Yoon, X. Chen, Clinical development and potential of photothermal and photodynamic therapies for cancer. Nat. Rev. Clin Oncol. 17, 657–674 (2020). https://doi.org/10.1038/s41571-020-0410-2
  167. H. Zhou, Y. Gong, Y. Liu, A. Huang, X. Zhu et al., Intelligently thermoresponsive flower-like hollow nano-ruthenium system for sustained release of nerve growth factor to inhibit hyperphosphorylation of tau and neuronal damage for the treatment of Alzheimer’s disease. Biomaterials 237, 119822 (2020). https://doi.org/10.1016/j.biomaterials.2020.119822
  168. M. Aryal, C.D. Arvanitis, P.M. Alexander, N. McDannold, Ultrasound-mediated blood–brain barrier disruption for targeted drug delivery in the central nervous system. Adv. Drug Deliv. Rev. 72, 94–109 (2014). https://doi.org/10.1016/j.addr.2014.01.008
  169. K. Hynynen, N. McDannold, N. Vykhodtseva, F.A. Jolesz, Noninvasive MR imaging-guided focal opening of the blood-brain barrier in rabbits. Radiology 220(30), 640–646 (2001). https://doi.org/10.1148/radiol.2202001804
  170. H. Zhang, T. Wang, W. Qiu, Y. Han, Q. Sun et al., Monitoring the opening and recovery of the blood–brain barrier with noninvasive molecular imaging by biodegradable ultrasmall Cu2–xSe nanops. Nano Lett. 18(8), 4985–4992 (2018). https://doi.org/10.1021/acs.nanolett.8b01818
  171. J.O. Szablowski, A. Lee-Gosselin, B. Lue, D. Malounda, M.G. Shapiro, Acoustically targeted chemogenetics for the non-invasive control of neural circuits. Nat. Biomed. Eng. 2, 475–484 (2018). https://doi.org/10.1038/s41551-018-0258-2
  172. Y. Jiang, J.M. Fay, C.D. Poon, N. Vinod, Y. Zhao et al., Nanoformulation of brain-derived neurotrophic factor with target receptor-triggered-release in the central nervous system. Adv. Funct. Mater. 28(6), 1703982 (2018). https://doi.org/10.1002/adfm.201703982
  173. K. Xhima, K. Markham-Coultes, H. Nedev, S. Heinen, H.U. Saragovi et al., Focused ultrasound delivery of a selective TrkA agonist rescues cholinergic function in a mouse model of Alzheimer's disease. Sci. Adv. 6(4), eaax6646 (2020). https://doi.org/10.1126/sciadv.aax6646
  174. N. Lipsman, Y. Meng, A.J. Bethune, Y. Huang, B. Lam et al., Blood-brain barrier opening in Alzheimer’s disease using MR-guided focused ultrasound. Nat. Commun. 9, 2336 (2018). https://doi.org/10.1038/s41467-018-04529-6
  175. C. Gasca-Salas, B. Fernandez-Rodriguez, J.A. Pineda-Pardo, R. Rodriguez-Rojas, I. Obeso et al., Blood-brain barrier opening with focused ultrasound in Parkinson’s disease dementia. Nat. Commun. 12, 779 (2021). https://doi.org/10.1038/s41467-021-21022-9
  176. G. Foffani, I. Trigo-Damas, J.A. Pineda-Pardo, J. Blesa, R. Rodríguez-Rojas et al., Focused ultrasound in Parkinson’s disease: a twofold path toward disease modification. Mov. Disord. 34(9), 1262–1273 (2019). https://doi.org/10.1002/mds.27805
  177. G. Leinenga, C. Langton, R. Nisbet, J. Gotz, Ultrasound treatment of neurological diseases–current and emerging applications. Nat. Rev. Neurol. 12, 161–174 (2016). https://doi.org/10.1038/nrneurol.2016.13
  178. A. Joseph, C. Contini, D. Cecchin, S. Nyberg, L. Ruiz-Perez et al., Chemotactic synthetic vesicles: design and applications in blood-brain barrier crossing. Sci. Adv. 3(8), e1700362 (2017). https://doi.org/10.1126/sciadv.1700362
  179. C.P. Foley, D.G. Rubin, A. Santillan, D. Sondhi, J.P. Dyke et al., Intra-arterial delivery of AAV vectors to the mouse brain after mannitol mediated blood brain barrier disruption. J. Control. Release 196, 71–78 (2014). https://doi.org/10.1016/j.jconrel.2014.09.018
  180. S.I. Rapoport, Advances in osmotic opening of the blood-brain barrier to enhance CNS chemotherapy. Expert Opin. Investig. Drugs. 10(10), 1809–1818 (2001). https://doi.org/10.1517/13543784.10.10.1809
  181. R. Shaltiel-Karyo, M. Frenkel-Pinter, E. Rockenstein, C. Patrick, M. Levy-Sakin et al., A blood-brain barrier (BBB) disrupter is also a potent alpha-synuclein (alpha-syn) aggregation inhibitor: a novel dual mechanism of mannitol for the treatment of Parkinson disease (PD). J. Biol. Chem. 288(24), 17579–17588 (2013). https://doi.org/10.1074/jbc.M112.434787
  182. X. Zhang, G. Chen, L. Wen, F. Yang, A.L. Shao et al., Novel multiple agents loaded PLGA nanops for brain delivery via inner ear administration: in vitro and in vivo evaluation. Eur. J. Pharm. Sci. 48, 595–603 (2013). https://doi.org/10.1016/j.ejps.2013.01.007
  183. N. Singh, M.A. Savanur, S. Srivastava, P. D’Silva, G. Mugesh, A redox modulatory Mn3O4 nanozyme with multi-enzyme activity provides efficient cytoprotection to human cells in a Parkinson’s disease model. Angew. Chem. Int. Ed. 56(45), 14267–14271 (2017). https://doi.org/10.1002/anie.201708573
  184. H.J. Kwon, D. Kim, K. Seo, Y.G. Kim, S.I. Han et al., Ceria nanop systems for selective scavenging of mitochondrial, intracellular, and extracellular reactive oxygen species in Parkinson’s disease. Angew. Chem. Int. Ed. 57(30), 9408–9412 (2018). https://doi.org/10.1002/anie.201805052
  185. C. Ren, X. Hu, Q. Zhou, Graphene oxide quantum dots reduce oxidative stress and inhibit neurotoxicity in vitro and in vivo through catalase-like activity and metabolic regulation. Adv. Sci. 5(5), 1700595 (2018). https://doi.org/10.1002/advs.201700595
  186. M.A. Hegazy, H.M. Maklad, D.M. Samy, D.A. Abdelmonsif, B.M.E. Sabaa et al., Cerium oxide nanops could ameliorate behavioral and neurochemical impairments in 6-hydroxydopamine induced Parkinson’s disease in rats. Neurochem. Int. 108, 361–371 (2017). https://doi.org/10.1016/j.neuint.2017.05.011
  187. Y.Q. Liu, Y. Mao, E. Xu, H. Jia, S. Zhang et al., Nanozyme scavenging ROS for prevention of pathologic α-synuclein transmission in Parkinson’s disease. Nano Today 36, 101027 (2021). https://doi.org/10.1016/j.nantod.2020.101027
  188. Y. Li, Y. Li, H. Wang, R. Liu, Yb3+, Er3+ codoped cerium oxide upconversion nanops enhanced the enzymelike catalytic activity and antioxidative activity for Parkinson’s disease treatment. ACS Appl. Mater. Interfaces 13(12), 13968–13977 (2021). https://doi.org/10.1021/acsami.1c00157
  189. W. Feng, X. Han, H. Hu, M. Chang, L. Ding et al., 2D vanadium carbide MXenzyme to alleviate ROS-mediated inflammatory and neurodegenerative diseases. Nat. Commun. 12, 2203 (2021). https://doi.org/10.1038/s41467-021-22278-x
  190. D. Kim, J.M. Yoo, H. Wang, J. Lee, S.H. Lee et al., Graphene quantum dots prevent α-synucleinopathy in Parkinson’s disease. Nat. Nanotechnol. 13, 812–818 (2018). https://doi.org/10.1038/s41565-018-0179-y
  191. G. Gao, R. Chen, M. He, J. Li, J. Li et al., Gold nanoclusters for Parkinson’s disease treatment. Biomaterials 194, 36–46 (2019). https://doi.org/10.1016/j.biomaterials.2018.12.013
  192. L. Wang, X. Li, Y. Han, T. Wang, Y. Zhao et al., Quantum dots protect against MPP+-induced neurotoxicity in a cell model of Parkinson’s disease through autophagy induction. Sci. China Chem. 59, 1486–1491 (2016). https://doi.org/10.1007/s11426-016-0103-7
  193. H. Mohammad-Beigi, A. Hosseini, M. Adeli, M.R. Ejtehadi, G. Christiansen et al., Mechanistic understanding of the interactions between nano-objects with different surface properties and alpha-synuclein. ACS Nano 13(3), 3243–3256 (2019). https://doi.org/10.1021/acsnano.8b08983
  194. N. Joshi, S. Basak, S. Kundu, G. De, A. Mukhopadhyay et al., Attenuation of the early events of alpha-synuclein aggregation: a fluorescence correlation spectroscopy and laser scanning microscopy study in the presence of surface-coated Fe3O4 nanops. Langmuir 31(4), 1469–1478 (2015). https://doi.org/10.1021/la503749e
  195. J. Yoo, E. Lee, H.Y. Kim, D.H. Youn, J. Jung et al., Electromagnetized gold nanops mediate direct lineage reprogramming into induced dopamine neurons in vivo for Parkinson’s disease therapy. Nat. Nanotechnol. 12, 1006–1014 (2017). https://doi.org/10.1038/nnano.2017.133
  196. S. Zhang, P. Sun, K. Lin, F.H.L. Chan, Q. Gao et al., Extracellular nanomatrix-induced self-organization of neural stem cells into miniature substantia nigra-like structures with therapeutic effects on Parkinsonian rats. Adv. Sci. 6(24), 1901822 (2019). https://doi.org/10.1002/advs.201901822
  197. T.H. Chung, S.C. Hsu, S.H. Wu, J.K. Hsiao, C.P. Lin et al., Dextran-coated iron oxide nanop-improved therapeutic effects of human mesenchymal stem cells in a mouse model of Parkinson’s disease. Nanoscale 10(6), 2998–3007 (2018). https://doi.org/10.1039/c7nr06976f
  198. B. Yang, Y. Chen, J. Shi, Reactive oxygen species (ROS)-based nanomedicine. Chem. Rev. 119(8), 4881–4985 (2019). https://doi.org/10.1021/acs.chemrev.8b00626
  199. S. Manoharan, G.J. Guillemin, R.S. Abiramasundari, M.M. Essa, M. Akbar et al., The role of reactive oxygen species in the pathogenesis of Alzheimer’s disease, Parkinson’s disease, and Huntington’s disease: a mini review. Oxid. Med. Cell. Longev. 2016, 8590578 (2016). https://doi.org/10.1155/2016/8590578
  200. M.D. Howard, E.D. Hood, C.F. Greineder, I.S. Alferiev, M. Chorny et al., Targeting to endothelial cells augments the protective effect of novel dual bioactive antioxidant/anti-inflammatory nanops. Mol. Pharm. 11(7), 2262–2270 (2014). https://doi.org/10.1021/mp400677y
  201. V.V. Shuvaev, J. Han, K.J. Yu, S. Huang, B.J. Hawkins et al., PECAM-targeted delivery of SOD inhibits endothelial inflammatory response. FASEB J. 25(1), 348–357 (2011). https://doi.org/10.1096/fj.10-169789
  202. N. Feliu, D. Docter, M. Heine, P.D. Pino, S. Ashraf et al., In vivo degeneration and the fate of inorganic nanops. Chem. Soc. Rev. 45, 2440–2457 (2016). https://doi.org/10.1039/c5cs00699f
  203. A. Bencsik, P. Lestaevel, I.G. Canu, Nano- and neurotoxicology: an emerging discipline. Prog. Neurobiol. 160, 45–63 (2018). https://doi.org/10.1016/j.pneurobio.2017.10.003
  204. L. Maroteaux, J.T. Campanelli, R.H. Scheller, Synuclein: a neuron-specific protein localized to the nucleus and presynaptic nerve terminal. J. Neurosci. 8(8), 2804–2815 (1988). https://doi.org/10.1523/JNEUROSCI.08-08-02804.1988
  205. A.D. Stephens, M. Zacharopoulou, G.S.K. Schierle, The cellular environment affects monomeric α-synuclein structure. Trends Biochem. Sci. 44(5), 453–466 (2019). https://doi.org/10.1016/j.tibs.2018.11.005
  206. S. Ghio, F. Kamp, R. Cauchi, A. Giese, N. Vassallo, Interaction of alpha-synuclein with biomembranes in Parkinson’s disease–role of cardiolipin. Prog. Lipid Res. 61, 73–82 (2016). https://doi.org/10.1016/j.plipres.2015.10.005
  207. Z.A. Sorrentino, B.I. Giasson, P. Chakrabarty, α-Synuclein and astrocytes: tracing the pathways from homeostasis to neurodegeneration in Lewy body disease. Acta Neuropathol. 138, 1–21 (2019). https://doi.org/10.1007/s00401-019-01977-2
  208. M.J. Hajipour, M.R. Santoso, F. Rezaee, H. Aghaverdi, M. Mahmoudi et al., Advances in Alzheimer’s diagnosis and therapy: the implications of nanotechnology. Trends Biotechnol. 35(10), 937–953 (2017). https://doi.org/10.1016/j.tibtech.2017.06.002
  209. A. Villar-Piqué, T.L. Fonseca, T.F. Outeiro, Structure, function and toxicity of alpha-synuclein: the Bermuda triangle in synucleinopathies. J. Neurochem. 139(S1), 240–255 (2016). https://doi.org/10.1111/jnc.13249
  210. R.A. Barker, M. Götz, M. Parmar, New approaches for brain repair—from rescue to reprogramming. Nature 557, 329–334 (2018). https://doi.org/10.1038/s41586-018-0087-1
  211. C. Vissers, G.L. Ming, H. Song, Nanop technology and stem cell therapy team up against neurodegenerative disorders. Adv. Drug Deliv. Rev. 148, 239–251 (2019). https://doi.org/10.1016/j.addr.2019.02.007
  212. N. Daviaud, R.H. Friedel, H. Zou, Vascularization and engraftment of transplanted human cerebral organoids in mouse cortex. eNeuro 5(6), 219–18 (2018). https://doi.org/10.1523/ENEURO.0219-18.2018
  213. H. Qian, X. Kang, J. Hu, D. Zhang, Z. Liang et al., Reversing a model of Parkinson’s disease with in situ converted nigral neurons. Nature 582, 550–556 (2020). https://doi.org/10.1038/s41586-020-2388-4
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