Nose-to-Brain Delivery of Biomimetic Nanoparticles for Glioblastoma Targeted Therapy

Overview

Journal ACS Appl Mater Interfaces

Publisher American Chemical Society

Specialties Biomedical Engineering
Biotechnology

Date 2024 Dec 18

PMID 39692595

Authors

Natalia Noronha Ferreira

Celisnolia Morais Leite

Natalia Sanchez Moreno

Renata Rank Miranda

Paula Maria Pincela Lins

Camila Fernanda Rodero

Edilson de Oliveira Junior

Eliana Martins Lima

Rui M Reis

Valtencir Zucolotto

Affiliations

Soon will be listed here.

Abstract

Glioblastoma (GBM) is an extremely aggressive form of brain cancer that remains challenging to treat, especially owing to the lack of effective targeting and drug delivery concerns. Due to its anatomical advantages, the nose-to-brain strategy is an interesting route for drug delivery. Nanoengineering has provided technological tools and innovative strategies to overcome biotechnological limitations, which is promising for improving the effectiveness of conventional therapies. Herein, we designed a biomimetic multifunctional nanostructure produced by polymeric poly(d,l-lactic--glycolic) acid (PLGA) core loaded with Temozolomide (TMZ) coated with cell membrane isolated from glioma cancer cells. The developed nanostructures (NP-MB) were fully characterized, and their biological performance was investigated extensively. The results indicate that NP-MB could control TMZ release and promote TMZ permeation in the nasal porcine mucosa. The higher cytotoxicity of NP-MB in different glioma cell lines, particularly against U251 cells, reinforces their potential for homotypic targeting. The chicken chorioallantoic membrane assay revealed a tumor size reduction and antiangiogenic activity. biodistribution studies showed that NP-MB effectively reaches the brain following nasal administration. These findings suggest that NP-MB holds promise as a biomimetic nanoplatform for effective targeting and homotypic recognition in GBM therapy with high potential for clinical translation.

References

Victorelli F, Cardoso V, Ferreira N, Calixto G, Fontana C, Baltazar F . Chick embryo chorioallantoic membrane as a suitable in vivo model to evaluate drug delivery systems for cancer treatment: A review. Eur J Pharm Biopharm. 2020; 153:273-284. DOI: 10.1016/j.ejpb.2020.06.010. View

Xu Y, Shen M, Li Y, Sun Y, Teng Y, Wang Y . The synergic antitumor effects of paclitaxel and temozolomide co-loaded in mPEG-PLGA nanoparticles on glioblastoma cells. Oncotarget. 2016; 7(15):20890-901. PMC: 4991499. DOI: 10.18632/oncotarget.7896. View

Papadopoulou V, Kosmidis K, Vlachou M, Macheras P . On the use of the Weibull function for the discernment of drug release mechanisms. Int J Pharm. 2005; 309(1-2):44-50. DOI: 10.1016/j.ijpharm.2005.10.044. View

Zeraatpisheh Z, Mirzaei E, Nami M, Alipour H, Mahdavipour M, Sarkoohi P . Local delivery of fingolimod through PLGA nanoparticles and PuraMatrix-embedded neural precursor cells promote motor function recovery and tissue repair in spinal cord injury. Eur J Neurosci. 2021; 54(4):5620-5637. DOI: 10.1111/ejn.15391. View

Singh P, Lim B . Targeting Apoptosis in Cancer. Curr Oncol Rep. 2022; 24(3):273-284. DOI: 10.1007/s11912-022-01199-y. View

Ferreira N, de Oliveira Junior E, Granja S, Boni F, Ferreira L, Cury B . Nose-to-brain co-delivery of drugs for glioblastoma treatment using nanostructured system. Int J Pharm. 2021; 603:120714. DOI: 10.1016/j.ijpharm.2021.120714. View

Jiang C, Cheng H, Yuan A, Tang X, Wu J, Hu Y . Hydrophobic IR780 encapsulated in biodegradable human serum albumin nanoparticles for photothermal and photodynamic therapy. Acta Biomater. 2014; 14:61-9. DOI: 10.1016/j.actbio.2014.11.041. View

Ananta J, Paulmurugan R, Massoud T . Temozolomide-loaded PLGA nanoparticles to treat glioblastoma cells: a biophysical and cell culture evaluation. Neurol Res. 2016; 38(1):51-9. DOI: 10.1080/01616412.2015.1133025. View

Partikel K, Korte R, Mulac D, Humpf H, Langer K . Serum type and concentration both affect the protein-corona composition of PLGA nanoparticles. Beilstein J Nanotechnol. 2019; 10:1002-1015. PMC: 6541368. DOI: 10.3762/bjnano.10.101. View

10.

Adams E, De Maesschalck R, De Spiegeleer B, Vander Heyden Y, Smeyers-Verbeke J, Massart D . Evaluation of dissolution profiles using principal component analysis. Int J Pharm. 2001; 212(1):41-53. DOI: 10.1016/s0378-5173(00)00581-0. View

11.

Murugan K, Choonara Y, Kumar P, Bijukumar D, du Toit L, Pillay V . Parameters and characteristics governing cellular internalization and trans-barrier trafficking of nanostructures. Int J Nanomedicine. 2015; 10:2191-206. PMC: 4370919. DOI: 10.2147/IJN.S75615. View

12.

Ferreira N, Miranda R, Moreno N, Pincela Lins P, Leite C, Leite A . Using design of experiments (DoE) to optimize performance and stability of biomimetic cell membrane-coated nanostructures for cancer therapy. Front Bioeng Biotechnol. 2023; 11:1120179. PMC: 9932601. DOI: 10.3389/fbioe.2023.1120179. View

13.

Kumar M, Pandey R, Patra K, Jain S, Soni M, Dangi J . Evaluation of neuropeptide loaded trimethyl chitosan nanoparticles for nose to brain delivery. Int J Biol Macromol. 2013; 61:189-95. DOI: 10.1016/j.ijbiomac.2013.06.041. View

14.

Marangoni V, Cancino Bernardi J, Reis I, Favaro W, Zucolotto V . Photothermia and Activated Drug Release of Natural Cell Membrane Coated Plasmonic Gold Nanorods and β-Lapachone. ACS Appl Bio Mater. 2022; 2(2):728-736. DOI: 10.1021/acsabm.8b00603. View

14.

Cappello V, Marchetti L, Parlanti P, Landi S, Tonazzini I, Cecchini M . Ultrastructural Characterization of the Lower Motor System in a Mouse Model of Krabbe Disease. Sci Rep. 2017; 6(1):1. PMC: 5431369. DOI: 10.1038/s41598-016-0001-8. View

15.

Lee Y, Kim M, Ha J, Lee M . Brain-targeted exosome-mimetic cell membrane nanovesicles with therapeutic oligonucleotides elicit anti-tumor effects in glioblastoma animal models. Bioeng Transl Med. 2023; 8(2):e10426. PMC: 10013800. DOI: 10.1002/btm2.10426. View

16.

Sabuncu A, Grubbs J, Qian S, Abdel-Fattah T, Stacey M, Beskok A . Probing nanoparticle interactions in cell culture media. Colloids Surf B Biointerfaces. 2012; 95:96-102. DOI: 10.1016/j.colsurfb.2012.02.022. View

17.

Chu L, Wang A, Ni L, Yan X, Song Y, Zhao M . Nose-to-brain delivery of temozolomide-loaded PLGA nanoparticles functionalized with anti-EPHA3 for glioblastoma targeting. Drug Deliv. 2018; 25(1):1634-1641. PMC: 6127843. DOI: 10.1080/10717544.2018.1494226. View

18.

Watchorn J, Clasky A, Prakash G, Johnston I, Chen P, Gu F . Untangling Mucosal Drug Delivery: Engineering, Designing, and Testing Nanoparticles to Overcome the Mucus Barrier. ACS Biomater Sci Eng. 2022; 8(4):1396-1426. DOI: 10.1021/acsbiomaterials.2c00047. View

19.

Wu H, Hu K, Jiang X . From nose to brain: understanding transport capacity and transport rate of drugs. Expert Opin Drug Deliv. 2008; 5(10):1159-68. DOI: 10.1517/17425247.5.10.1159. View