Investigation of enzyme-sensitive lipid nanoparticles for delivery of siRNA to blood-brain barrier and Glioma cells

International Journal of Nanomedicine

Volumn 10, Issue , 2015, Pages 5995-6008

  Bruun, Jonas ^a   Larsen, Trine B ^a   Jølck, Rasmus I ^a   Eliasen, Rasmus ^a   Holm, René ^b   Gjetting, Torben ^a   Andresen, Thomas L ^a  

^a TECHNICAL UNIVERSITY OF DENMARK   (Denmark)

^b H LUNDBECK A S   (Denmark)

Author keywords

Angiopep; BBB; Cleavable PEG lipid; Gene therapy; Matrix metalloproteinase; Nanocarrier

Indexed keywords

1,2 DIOLEOYL 3 DIMETHYLAMMONIUM PROPANE; 1,2 DIOLEOYL SN GLYCERO 3 PHOSPHOETHANOLAMINE N (LISSAMINE RHODAMINE B SULFONYL); 1,2 DISTEAROYL SN GLYCERO 3 PHOSPHOETHANOLAMINE (POLYETHYLENE GLYCOL)2000; 2 OLEOYL 1 PALMITOYLPHOSPHATIDYLCHOLINE; GLUTAMIC ACID; LIPID NANOPARTICLE; LIPOPEPTIDE; LOW DENSITY LIPOPROTEIN RECEPTOR RELATED PROTEIN; MACROGOL; MATRIX METALLOPROTEINASE; NANOPARTICLE; SMALL INTERFERING RNA; UNCLASSIFIED DRUG;

ARTICLE; BLOOD BRAIN BARRIER; BRAIN TUMOR; CYTOTOXICITY ASSAY; DRUG COATING; DRUG DELIVERY SYSTEM; DRUG TRANSPORT; ENDOTHELIUM CELL; FLOW CYTOMETRY; GENE SILENCING; GLIOMA CELL; HIGH PERFORMANCE LIQUID CHROMATOGRAPHY; HUMAN; HYDRODYNAMICS; MATRIX ASSISTED LASER DESORPTION IONIZATION TIME OF FLIGHT MASS SPECTROMETRY; NANOENCAPSULATION; NONHUMAN; PARTICLE SIZE; PROTEIN CLEAVAGE; PROTEIN EXPRESSION; PROTEIN SYNTHESIS; RNA INTERFERENCE; TUMOR MICROENVIRONMENT; ZETA POTENTIAL;

EID: 84942764986     PISSN: 11769114     EISSN: 11782013     Source Type: Journal    
DOI: 10.2l47/IJN.S87334     Document Type: Article

References (52)

1. Abbott NJ, Patabendige AA, Dolman DE, Yusof SR, Begley DJ. Structure and function of the blood-brain barrier. Neurobiol Dis. 2010;37(1): 13-25.
2. Tobias A, Ahmed A, Moon KS, Lesniak MS. The art of gene therapy for glioma: a review of the challenging road to the bedside. J Neurol Neurosurg Psychiatry. 2013;84(2):213-222.
3. Abbott NJ. Blood-brain barrier structure and function and the challenges for CNS drug delivery. J Inherit Metab Dis. 2013;36(3):437-449.
4. Pérez-Martínez FC, Guerra J, Posadas I, Ceña V. Barriers to non-viral vector-mediated gene delivery in the nervous system. Pharm Res. 2011;28(8): 1843-1858.
5. Huang R, Ma H, Guo Y, et al. Angiopep-conjugated nanoparticles for targeted long-term gene therapy of Parkinson's disease. Pharm Res. 2013; 30(10):2549-2559.
6. Demeule M, Currie JC, Bertrand Y, et al. Involvement of the low-density lipoprotein receptor-related protein in the transcytosis of the brain delivery vector angiopep-2. J Neurochem. 2008;106(4):1534-1544.
7. Demeule M, Régina A, Ché C, et al. Identification and design of peptides as a new drug delivery system for the brain. J Pharmacol Exp Ther. 2008;324(3):1064-1072.
8. Huang S, Li J, Han L, et al. Dual targeting effect of angiopep-2-modified, DNA-loaded nanoparticles for glioma. Biomaterials. 2011;32(28): 6832-6838.
9. 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;33(11):3324-3333.
10. Xin H, Sha X, Jiang X, Zhang W, Chen L, Fang X. Anti-glioblastoma efficacy and safety of paclitaxel-loading angiopep-conjugated dual targeting PEG-PCL nanoparticles. Biomaterials. 2012;33(32):8167-8176.
11. Wang J, Lu Z, Wientjes MG, Au JL. Delivery of siRNA therapeutics: barriers and carriers. AAPS J. 2010;12(4):492-503.
12. Gomes-da-Silva LC, Fonseca NA, Moura V, Pedroso de Lima MC, Simões S, Moreira JN. Lipid-based nanoparticles for siRNA delivery in cancer therapy: paradigms and challenges. Acc Chem Res. 2012;45(7): 1163-1171.
13. S0rensen DR, Leirdal M, Sioud M. Gene silencing by systemic delivery of synthetic siRNAs in adult mice. J Mol Biol. 2003;327(4):761-766.
14. Li W, Szoka FC. Lipid-based nanoparticles for nucleic acid delivery. Pharm Res. 2007;24(3):438-449.
15. Senior J, Delgado C, Fisher D, Tilcock C, Gregoriadis G. Influence of surface hydrophilicity of liposomes on their interaction with plasma protein and clearance from the circulation: studies with poly(ethylene glycol)-coated vesicles. Biochim Biophys Acta. 1991;1062(1):77-82.
16. Torchilin VP, Omelyanenko VG, Papisov MI, et al. Poly(ethylene glycol) on the liposome surface: on the mechanism of polymer-coated liposome longevity. Biochim Biophys Acta. 1994;1195:11-20.
17. Hatakeyama H, Akita H, Harashima H. The polyethyleneglycol dilemma: advantage and disadvantage of PEGylation of liposomes for systemic genes and nucleic acids delivery to tumors. Biol Pharm Bull. 2013;36(6):892-899.
18. Ishida T, Kirchmeier MJ, Moase EH, Zalipsky S, Allen TM. Targeted delivery and triggered release of liposomal doxorubicin enhances cyto-toxicity against human B lymphoma cells. Biochim Biophys Acta. 2001; 1515(2):144-158.
19. Kale AA, Torchilin VP. Enhanced transfection of tumor cells in vivo using "Smart" pH-sensitive TAT-modified pegylated liposomes. J Drug Target. 2007;15(7 8):538-545.
20. Xu H, Deng Y, Chen D, Hong W, Lu Y, Dong X. Esterase-catalyzed dePEGylation of pH-sensitive vesicles modified with cleavable PEG-lipid derivatives. J Control Release. 2008;130(3):238-245.
21. Zhu L, Kate P, Torchilin VP. Matrix metalloprotease 2-responsive multifunctional liposomal nanocarrier for enhanced tumor targeting. ACS Nano. 2012;6(4):3491-3498.
22. Andresen TL, Thompson DH, Kaasgaard T. Enzyme-triggered nano-medicine: drug release strategies in cancer therapy. Mol Membr Biol. 2010;27(7):353-363.
23. Egeblad M, Werb Z. New functions for the matrix metalloproteinases in cancer progression. Nat Rev Cancer. 2002;2(3):161-174.
24. Fujiwara S, Nakagawa K, Harada H, Nagato S, Iwata S, Ohnishi T. Silencing hypoxia-inducible factor-1a inhibits cell migration and invasion under hypoxic environment in malignant gliomas. Int J Oncol. 2007;30:793-802.
25. Gu G, Xia H, Hu Q, et al. PEG-co-PCL nanoparticles modified with MMP-2/9 activatable low molecular weight protamine for enhanced targeted glioblastoma therapy. Biomaterials. 2013;34(1):196-208.
26. Hatakeyama H, Akita H, Kogure K, et al. Development of a novel systemic gene delivery system for cancer therapy with a tumor-specific cleavable PEG-lipid. Gene Ther. 2007;14(1):68-77.
27. Terada T, Iwai M, Kawakami S, Yamashita F, Hashida M. Novel PEG-matrix metalloproteinase-2 cleavable peptide-lipid containing galactosylated liposomes for hepatocellular carcinoma-selective targeting. J Control Release. 2006;111(3):333-342.
28. Remaut K, Lucas B, Braeckmans K, Demeester J, De Smedt SC. Pegyla-tion of liposomes favours the endosomal degradation of the delivered phos-phodiester oligonucleotides. J Control Release. 2007;117(2):256-266.
29. Gjetting T, J0lck R, Andresen T. Effective nanoparticle based gene delivery by a protease triggered charge switch. Adv Healthc Mater. 2014; 3(7):1107-1118.
30. Miller CR, Bondurant B, McLean SD, McGovern KA, O'Brien DF. Liposome-cell interactions in vitro: effect of liposome surface charge on the binding and endocytosis of conventional and sterically stabilized liposomes. Biochemistry. 1998;37(37):12875-12883.
31. Jeffs LB, Palmer LR, Ambegia EG, Giesbrecht C, Ewanick S, MacLachlan I. A scalable, extrusion-free method for efficient liposomal encapsulation of plasmid DNA. Pharm Res. 2005;22(3):362-372.
32. Gjetting T, Arildsen NS, Christensen CL, et al. In vitro and in vivo effects of polyethylene glycol (PEG)-modified lipid in DOTAP/cholesterol-mediated gene transfection. Int JNanomedicine. 2010;5:371-383.
33. Sambrook J, Russel DW. Molecular Cloning: A Laboratory Manual. New York, NY: Cold Spring Harbor Laboratory Press; 2001.
34. Ke W, Shao K, Huang R, et al. Gene delivery targeted to the brain using an angiopep-conjugated polyethyleneglycol-modified polyamidoamine dendrimer. Biomaterials. 2009;30(36):6976-6985.
35. Turk BE, Huang LL, Piro ET, Cantley LC. Determination of protease cleavage site motifs using mixture-based oriented peptide libraries. Nat Biotechnol. 2001;19(7):661-667.
36. Okada Y, Morodomi T, Enghild JJ, et al. Matrix metalloproteinase 2 from human rheumatoid synovial fibroblasts. Purification and activation of the precursor and enzymic properties. Eur J Biochem. 1990;194(3): 721-730.
37. Liu J, Jin X, Liu KJ, Liu W. Matrix metalloproteinase-2-mediated occludin degradation and caveolin-1-mediated claudin-5 redistribution contribute to blood-brain barrier damage in early ischemic stroke stage. JNeurosci. 2012;32(9):3044-3057.
38. Puli S, Lai JC, Bhushan A. Inhibition of matrix degrading enzymes and invasion in human glioblastoma (U87MG) cells by isoflavones. JNeurooncol. 2006;79(2):135-142.
39. Shao K, Huang R, Li J, et al. Angiopep-2 modified PE-PEG based polymeric micelles for amphotericin B delivery targeted to the brain. J Control Release. 2010;147(1):118-126.
40. Gao H, Zhang S, Cao S, Yang Z, Pang Z, Jiang X. Angiopep-2 and activat-able cell-penetrating peptide dual-functionalized nanoparticles for systemic glioma-targeting delivery. Mol Pharm. 2014;11(8):2755-2763.
41. Pulford B, Reim N, Bell A, et al. Liposome-siRNA-peptide complexes cross the blood-brain barrier and significantly decrease PrP on neuronal cells and PrP in infected cell cultures. PLoS One. 2010;5(6):e11085.
42. Resnier P, David S, Lautram N, et al. EGFR siRNA lipid nanocapsules efficiently transfect glioma cells in vitro. Int J Pharm. 2013;454(2): 748-755.
43. Malmo J, Sandvig A, Varum KM, Strand SP. Nanoparticle mediated P-glycoprotein silencing for improved drug delivery across the blood-brain barrier: a siRNA-chitosan approach. PLoS One. 2013;8(1): e54182.
44. Engin K, Leeper DB, Cater JR, Thistlethwaite AJ, Tupchong L, McFarlane JD. Extracellular pH distribution in human tumours. Int J Hyperthermia. 1995;11(2):211-216.
45. Lee ES, Na K, Bae YH. Polymeric micelle for tumor pH and folate-mediated targeting. J Control Release. 2003;91(1 2):103-113.
46. Jin J, Bae KH, Yang H, et al. In vivo specific delivery of c-Met siRNA to glioblastoma using cationic solid lipid nanoparticles. Bioconjug Chem. 2011;22(12):2568-2572.
47. Cartellieri M, Hendruschk S, Wiedemuth R, et al. RNA interference targeting survivin exerts antitumoral effects in vitro and in established glioma xenografts in vivo. Neuro Oncol. 2011;13(10):1074-1089.
48. Rosenberg GA. Matrix metalloproteinases and their multiple roles in neurodegenerative diseases. Lancet Neurol. 2009;8(2):205-216.
49. Jin R, Yang G, Li G. Molecular insights and therapeutic targets for blood-brain barrier disruption in ischemic stroke: critical role of matrix metalloproteinases and tissue-type plasminogen activator. Neurobiol Dis. 2010;38(3):376-385.
50. Mahajan SD, Aalinkeel R, Reynolds JL, et al. Suppression of MMP-9 expression in brain microvascular endothelial cells (BMVEC) using a gold nanorod (GNR)-siRNA nanoplex. Immunol Invest. 2012; 41(4):337-355.
51. Zhang G, Fahmy RG, DiGirolamo N, Khachigian LM. JUN siRNA regulates matrix metalloproteinase-2 expression, microvascular endothelial growth and retinal neovascularisation. J Cell Sci. 2006; 119(15):3219-3226.
52. Bonoiu A, Mahajan SD, Ye L, et al. MMP-9 gene silencing by a quantum dot-siRNA nanoplex delivery to maintain the integrity of the blood brain barrier. Brain Res. 2009;1282:142-155.