Nanoparticle Mediated P-Glycoprotein Silencing for Improved Drug Delivery across the Blood-Brain Barrier: A siRNA-Chitosan Approach

PLoS ONE

Volumn 8, Issue 1, 2013, Pages

  Malmo, Jostein ^a   Sandvig, Axel ^a,b   Vårum, Kjell M ^a   Strand, Sabina P ^a  

^a NORWEGIAN UNIVERSITY OF SCIENCE AND TECHNOLOGY   (Norway)

^b UMEÅ UNIVERSITY HOSPITAL   (Sweden)

Author keywords

[No Author keywords available]

Indexed keywords

CHITOSAN; DOXORUBICIN; MULTIDRUG RESISTANCE PROTEIN; NANOPARTICLE; RHODAMINE 123; RNA; SMALL INTERFERING RNA; XENOBIOTIC AGENT;

ANIMAL EXPERIMENT; ANIMAL MODEL; ANIMAL TISSUE; ARTICLE; BLOOD BRAIN BARRIER; CENTRAL NERVOUS SYSTEM; DRUG BIOAVAILABILITY; DRUG DELIVERY SYSTEM; DRUG EFFICACY; EFFUSION; ENDOTHELIUM CELL; FLOW CYTOMETRY; HUMAN; NONHUMAN; RAT; REVERSE TRANSCRIPTION POLYMERASE CHAIN REACTION; RNA INTERFERENCE;

ANIMALS; ANTIBIOTICS, ANTINEOPLASTIC; BIOLOGICAL TRANSPORT; BLOOD-BRAIN BARRIER; CELL LINE, TRANSFORMED; CELL SURVIVAL; CHITOSAN; DOXORUBICIN; DRUG CARRIERS; ENDOTHELIAL CELLS; KINETICS; NANOPARTICLES; P-GLYCOPROTEINS; RATS; RNA, SMALL INTERFERING; TRANSFECTION;

RATTUS;

EID: 84872794963     PISSN: None     EISSN: 19326203     Source Type: Journal    
DOI: 10.1371/journal.pone.0054182     Document Type: Article

References (49)

1. Elbashir SM, Harborth J, Lendeckel W, Yalcin A, Weber K, et al. (2001) Duplexes of 21-nucleotide RNAs mediate RNA interference in cultured mammalian cells. Nature 411: 494-498.
2. Whitehead KA, Langer R, Anderson DG, (2009) Knocking down barriers: advances in siRNA delivery. Nat Rev Drug Discov 8: 129-138.
3. Khoury M, Louis-Plence P, Escriou V, Noel D, Largeau C, et al. (2006) Efficient new cationic liposome formulation for systemic delivery of small interfering RNA silencing tumor necrosis factor alpha in experimental arthritis. Arthritis Rheum 54: 1867-1877.
4. Malmo J, Sørgård H, Vårum KM, Strand SP, (2012) siRNA delivery with chitosan nanoparticles: Molecular properties favoring efficient gene silencing. J Control Release 158: 261-268.
5. Grayson AR, Doody A, Putnam D, (2006) Biophysical and Structural Characterization of Polyethylenimine-Mediated siRNA Delivery in Vitro. Pharmaceut Res 23: 1868-1876.
6. Hoon JJ, Christensen LV, Yockman JW, Zhong Z, Engbersen JFJ, et al. (2007) Reducible poly(amido ethylenimine) directed to enhance RNA interference. Biomaterials 28: 1912-1917.
7. Han HD, Mangala LS, Lee JW, Shahzad MMK, Kim HS, et al. (2010) Targeted Gene Silencing Using RGD-Labeled Chitosan Nanoparticles. Clin Cancer Res 16: 3910-3922.
8. Vårum K, Smidsrød O (2005) Structure-Property Relationship in Chitosans. In: Dumitriu S, editor. Polysaccharides: Structural diversity and functional versatility. New York: CRC Press. pp. 625-643.
9. Baldrick P, (2010) The safety of chitosan as a pharmaceutical excipient. Regul Toxicol Pharmacol 56: 290-299.
10. Nordtveit RJ, Vårum KM, Smidsrød O, (1996) Degradation of partially N-acetylated chitosans with hen egg white and human lysozyme. Carbohydr Polym 29: 163-167.
11. Vårum KM, Myhr MM, Hjerde RJN, Smidsrød O, (1997) In vitro degradation rates of partially N-acetylated chitosans in human serum. Carbohydr Res 299: 99-101.
12. Strand SP, Lelu S, Reitan NK, de Lange Davies C, Artursson P, et al. (2009) Molecular design of chitosan gene delivery systems with an optimized balance between polyplex stability and polyplex unpacking. Biomaterials 31: 975-987.
13. Malmo J, Vårum KM, Strand SP, (2011) Effect of Chitosan Chain Architecture on Gene Delivery: Comparison of Self-Branched and Linear Chitosans. Biomacromolecules 12: 721-729.
14. Liu X, Howard KA, Dong M, Andersen MØ, Rahbek UL, et al. (2007) The influence of polymeric properties on chitosan/siRNA nanoparticle formulation and gene silencing. Biomaterials 28: 1280-1288.
15. Abbott NJ, Patabendige AAK, Dolman DEM, Yusof SR, Begley DJ, (2009) Structure and function of the blood-brain barrier. Neurobiol Dis 37: 13-25.
16. de Klerk OL, Willemsen ATM, Bosker FJ, Bartels AL, Hendrikse NH, et al. (2010) Regional increase in P-glycoprotein function in the blood-brain barrier of patients with chronic schizophrenia: A PET study with [11C]verapamil as a probe for P-glycoprotein function. Psychiat Res-Neuroim 183: 151-156.
17. Weiss J, Dormann S-MG, Martin-Facklam M, Kerpen CJ, Ketabi-Kiyanvash N, et al. (2003) Inhibition of P-Glycoprotein by Newer Antidepressants. J Pharmacol Exp Ther 305: 197-204.
18. Kemper EM, van Zandbergen AE, Cleypool C, Mos HA, Boogerd W, et al. (2003) Increased Penetration of Paclitaxel into the Brain by Inhibition of P-Glycoprotein. Clin Cancer Res 9: 2849-2855.
19. Lee CGL, Gottesman MM, Cardarelli CO, Ramachandra M, Jeang K-T, et al. (1998) HIV-1 Protease Inhibitors Are Substrates for the MDR1 Multidrug Transporter. Biochemistry 37: 3594-3601.
20. Tishler DM, Weinberg KI, Hinton DR, Barbaro N, Annett GM, et al. (1995) MDR1 Gene Expression in Brain of Patients with Medically Intractable Epilepsy. Epilepsia 36: 1-6.
21. Scheffer GL, Pijnenborg ACLM, Smit EF, Müller M, Postma DS, et al. (2002) Multidrug resistance related molecules in human and murine lung. J Clin Path 55: 332-339.
22. Thiebaut F, Tsuruo T, Hamada H, Gottesman MM, Pastan I, et al. (1987) Cellular localization of the multidrug-resistance gene product P-glycoprotein in normal human tissues. Proc Natl Acad Sci U S A 84: 7735-7738.
23. Schinkel AH, Smit JJM, van Tellingen O, Beijnen JH, Wagenaar E, et al. (1994) Disruption of the mouse mdr1a P-glycoprotein gene leads to a deficiency in the blood-brain barrier and to increased sensitivity to drugs. Cell 77: 491-502.
24. Cordon-Cardo C, O'Brien JP, Casals D, Rittman-Grauer L, Biedler JL, et al. (1989) Multidrug-resistance gene (P-glycoprotein) is expressed by endothelial cells at blood-brain barrier sites. Proc Natl Acad Sci U S A 86: 695-698.
25. Demeule M, Labelle M, Régina A, Berthelet F, Béliveau R, (2001) Isolation of Endothelial Cells from Brain, Lung, and Kidney: Expression of the Multidrug Resistance P-Glycoprotein Isoforms. Biochem Biophys Res Commun 281: 827-834.
26. Chen C-j, Chin JE, Ueda K, Clark DP, Pastan I, et al. (1986) Internal duplication and homology with bacterial transport proteins in the mdr1 (P-glycoprotein) gene from multidrug-resistant human cells. Cell 47: 381-389.
27. Meng H, Liong M, Xia T, Li Z, Ji Z, et al. (2010) Engineered Design of Mesoporous Silica Nanoparticles to Deliver Doxorubicin and P-Glycoprotein siRNA to Overcome Drug Resistance in a Cancer Cell Line. ACS Nano 4: 4539-4550.
28. Susa M, Iyer AK, Ryu K, Choy E, Hornicek FJ, et al. (2010) Inhibition of ABCB1 (MDR1) Expression by an siRNA Nanoparticulate Delivery System to Overcome Drug Resistance in Osteosarcoma. PLoS ONE 5: e10764.
29. Wu H, Hait WN, Yang J-M, (2003) Small Interfering RNA-induced Suppression of MDR1 (P-Glycoprotein) Restores Sensitivity to Multidrug-resistant Cancer Cells. Cancer Res 63: 1515-1519.
30. Fellner S, Bauer B, Miller DS, Schaffrik M, Fankhänel M, et al. (2002) Transport of paclitaxel (Taxol) across the blood-brain barrier in vitro and in vivo. Clin Investig 110: 1309-1318.
31. Goralski KB, Hartmann G, Piquette-Miller M, Renton KW, (2003) Downregulation of mdr1a expression in the brain and liver during CNS inflammation alters the in vivo disposition of digoxin. Br J Pharmacol 139: 35-48.
32. Gupta Y, Jain A, Jain SK, (2007) Transferrin-conjugated solid lipid nanoparticles for enhanced delivery of quinine dihydrochloride to the brain. J Pharm Pharmacol 59: 935-940.
33. Fuest C, Bankstahl M, Winter P, Helm M, Pekcec A, et al. (2009) In vivo down-regulation of mouse brain capillary P-glycoprotein: A preliminary investigation. Neurosci Lett 464: 47-51.
34. Begley DJ, Lechardeur D, Chen Z-D, Rollinson C, Bardoul M, et al. (1996) Functional Expression of P-Glycoprotein in an Immortalised Cell Line of Rat Brain Endothelial Cells, RBE4. J Neurochem 67: 988-995.
35. Roux F, Durieu-Trautmann O, Chaverot N, Claire M, Mailly P, et al. (1994) Regulation of gamma-glutamyl transpeptidase and alkaline phosphatase activities in immortalized rat brain microvessel endothelial cells. J Cell Physiol 159: 101-113.
36. Tømmeraas K, Vårum KM, Christensen BE, Smidsrød O, (2001) Preparation and characterisation of oligosaccharides produced by nitrous acid depolymerisation of chitosans. Carbohydr Res 333: 137-144.
37. Sauna Z, Smith M, Müller M, Kerr K, Ambudkar S, (2001) The Mechanism of Action of Multidrug-Resistance-Linked P-Glycoprotein. J Bioenerg Biomembr 33: 481-491.
38. Matsui Y, Kobayashi N, Nishikawa M, Takakura Y, (2005) Sequence-Specific Suppression of mdr1a/1b Expression in Mice via RNA Interference. Pharm Res 22: 2091-2098.
39. Howard KA, Rahbek UL, Liu X, Damgaard CK, Glud SZ, et al. (2006) RNA Interference in Vitro and in Vivo Using a Chitosan/siRNA Nanoparticle System. Mol Ther 14: 476-484.
40. Rojanarata T, Opanasopit P, Techaarpornkul S, Ngawhirunpat T, Ruktanonchai U, (2008) Chitosan-Thiamine Pyrophosphate as a Novel Carrier for siRNA Delivery. Pharm Res 25: 2807-2814.
41. Techaarpornkul S, Wongkupasert S, Opanasopit P, Apirakaramwong A, Nunthanid J, et al. (2010) Chitosan-Mediated siRNA Delivery In Vitro: Effect of Polymer Molecular Weight, Concentration and Salt Forms. AAPS PharmSciTech 11: 64-72.
42. Lavertu M, Méthot S, Tran-Khanh N, Buschmann MD, (2006) High efficiency gene transfer using chitosan/DNA nanoparticles with specific combinations of molecular weight and degree of deacetylation. Biomaterials 27: 4815-4824.
43. Regina A, Koman A, Piciotti M, El Hafny B, Center MS, et al. (1998) Mrp1 Multidrug Resistance-Associated Protein and P-Glycoprotein Expression in Rat Brain Microvessel Endothelial Cells. J Neurochem 71: 705-715.
44. Saito T, Saetrom P, (2012) Target gene expression levels and competition between transfected and endogenous microRNAs are strong confounding factors in microRNA high-throughput experiments. Silence 3: 3.
45. Larsson E, Sander C, Marks D, (2010) mRNA turnover rate limits siRNA and microRNA efficacy. Mol Syst Biol 6: 433.
46. Muller C, Laurent G, Ling V, (1995) P-glycoprotein stability is affected by serum deprivation and high cell density in multidrug-resistant cells. J Cell Physiol 163: 538-544.
47. Babakhanian K, Bendayan M, Bendayan R, (2007) Localization of P-glycoprotein at the nuclear envelope of rat brain cells. Biochem Biophys Res Commun 361: 301-306.
48. Daoud R, Kast C, Gros P, Georges E, (2000) Rhodamine 123 Binds to Multiple Sites in the Multidrug Resistance Protein (MRP1). Biochemistry 39: 15344-15352.
49. Gros P, Dhir R, Croop J, Talbot F, (1991) A single amino acid substitution strongly modulates the activity and substrate specificity of the mouse mdr1 and mdr3 drug efflux pumps. Proc Natl Acad Sci U S A 88: 7289-7293.