Reversal of P-glycoprotein-mediated multidrug resistance by CD44 antibody-targeted nanocomplexes for short hairpin RNA-encoding plasmid DNA delivery

Biomaterials

Volumn 45, Issue , 2015, Pages 99-114

  Gu, Jijin ^a,b   Fang, Xiaoling ^a   Hao, Junguo ^a   Sha, Xianyi ^a  

^a FUDAN UNIVERSITY   (China)

^b UNIVERSITY OF MANITOBA   (Canada)

Author keywords

Anti CD44 antibody; Gene delivery; Multidrug resistance; Nanocomplexes; P glycoprotein

Indexed keywords

ADENOSINETRIPHOSPHATE; CELL CULTURE; CHEMOTHERAPY; CONTROLLED DRUG DELIVERY; DISEASES; ENCODING (SYMBOLS); GENE TRANSFER; GENES; GLYCOPROTEINS; LIPOSOMES; MAMMALS; MONOCLONAL ANTIBODIES; PHARMACODYNAMICS; RNA; SIGNAL ENCODING; TUMORS;

ADENOSINE TRIPHOSPHATE BINDING CASSETTE; CHEMOTHERAPEUTIC AGENTS; GENE DELIVERY; MULTIDRUG RESISTANCE; NANOCOMPLEXES; P-GLYCOPROTEIN; SHORT HAIRPIN RNA (SHRNA); TRANSFECTION EFFICIENCY;

TARGETED DRUG DELIVERY;

DENDRIMER; DOXORUBICIN; HERMES ANTIGEN; LIPOFECTAMINE; MONOCLONAL ANTIBODY; MULTIDRUG RESISTANCE PROTEIN; NANOCOMPOSITE; PLASMID DNA; PLURONIC P123 CONJUGATED POLYPROPYLENIMINE DENDRIMER; POLOXAMER; SHORT HAIRPIN RNA; UNCLASSIFIED DRUG; ANTIBODY; DNA; MESSENGER RNA; NANOPARTICLE; PLURONIC BLOCK COPOLYMER P123; POLY(PROPYLENEIMINE); POLYPROPYLENE; SMALL INTERFERING RNA;

ANIMAL EXPERIMENT; ANIMAL MODEL; ARTICLE; BREAST CANCER CELL LINE; CANCER INHIBITION; CONTROLLED STUDY; CYTOTOXICITY; DOWN REGULATION; DRUG EFFICACY; EXPRESSION VECTOR; FEMALE; GENE TARGETING; HUMAN; HUMAN CELL; IN VITRO STUDY; INTERNALIZATION; MOUSE; NONHUMAN; PRIORITY JOURNAL; PROMOTER REGION; RNA INTERFERENCE; TUMOR RESISTANCE; ANIMAL; CELL DEATH; CHEMISTRY; DRUG EFFECTS; DRUG RESISTANCE; ENDOCYTOSIS; ENDOSOME; GENE SILENCING; GENE TRANSFER; GENETIC TRANSFECTION; GENETICS; IMMUNOLOGY; INTRACELLULAR SPACE; MCF 7 CELL LINE; METABOLISM; MULTIDRUG RESISTANCE; PLASMID; REPORTER GENE; SYNTHESIS; TISSUE DISTRIBUTION; UMBILICAL VEIN ENDOTHELIAL CELL;

MUS MUSCULUS;

ANIMALS; ANTIBODIES; ANTIGENS, CD44; CELL DEATH; DNA; DOXORUBICIN; DRUG RESISTANCE, MULTIPLE; DRUG RESISTANCE, NEOPLASM; ENDOCYTOSIS; ENDOSOMES; FEMALE; GENE SILENCING; GENE TRANSFER TECHNIQUES; GENES, REPORTER; HUMAN UMBILICAL VEIN ENDOTHELIAL CELLS; HUMANS; INTRACELLULAR SPACE; MCF-7 CELLS; NANOPARTICLES; P-GLYCOPROTEIN; PLASMIDS; POLOXALENE; POLYPROPYLENES; RNA, MESSENGER; RNA, SMALL INTERFERING; TISSUE DISTRIBUTION; TRANSFECTION;

EID: 84922041585     PISSN: 01429612     EISSN: 18785905     Source Type: Journal    
DOI: 10.1016/j.biomaterials.2014.12.030     Document Type: Article

References (64)

1. Harris A.L., Hochhauser D. Mechanisms of multidrug resistance in cancer treatment. Acta Oncol 1992, 31:205-213.
2. Gradilone A., Raimondi C., Naso G., Silvestri I., Repetto L., Palazzo A., et al. How circulating tumor cells escape from multidrug resistance: translating molecular mechanisms in metastatic breast cancer treatment. Am J Clin Oncol 2011, 34:625-627.
3. Tredan O., Galmarini C.M., Patel K., Tannock I.F. Drug resistance and the solid tumor microenvironment. JNatl Cancer Inst 2007, 99:1441-1454.
4. Leighton J.C., Goldstein L.J. P-glycoprotein in adult solid tumors. Expression and prognostic significance. Hematol/Oncol Clin N. Am 1995, 9:251-273.
5. Stege A., Kruhn A., Lage H. Overcoming multidrug resistance by RNA interference. Methods Mol Biol 2010, 596:447-465.
6. Mei L., Zhang Y., Zheng Y., Tian G., Song C., Yang D., et al. Anovel docetaxel-loaded poly (epsilon-caprolactone)/Pluronic F68 nanoparticle overcoming multidrug resistance for breast cancer treatment. Nanoscale Res Lett 2009, 4:1530-1539.
7. Ganguly A., Banerjee K., Chakraborty P., Das S., Sarkar A., Hazra A., et al. Overcoming multidrug resistance (MDR) in cancer invitro and invivo by a quinoline derivative. Biomed Pharmacother= Biomed Pharmacother 2011, 65:387-394.
8. Pan L., Liu J., He Q., Wang L., Shi J. Overcoming multidrug resistance of cancer cells by direct intranuclear drug delivery using TAT-conjugated mesoporous silica nanoparticles. Biomaterials 2013, 34:2719-2730.
9. Milane L., Ganesh S., Shah S., Duan Z.F., Amiji M. Multi-modal strategies for overcoming tumor drug resistance: hypoxia, the Warburg effect, stem cells, and multifunctional nanotechnology. JControl Release: Off J Control Release Soc 2011, 155:237-247.
10. Yadav S., van Vlerken L.E., Little S.R., Amiji M.M. Evaluations of combination MDR-1 gene silencing and paclitaxel administration in biodegradable polymeric nanoparticle formulations to overcome multidrug resistance in cancer cells. Cancer Chemother Pharmacol 2009, 63:711-722.
11. Li J.M., Wang Y.Y., Zhao M.X., Tan C.P., Li Y.Q., Le X.Y., et al. Multifunctional QD-based co-delivery of siRNA and doxorubicin to HeLa cells for reversal of multidrug resistance and real-time tracking. Biomaterials 2012, 33:2780-2790.
12. Stege A., Priebsch A., Nieth C., Lage H. Stable and complete overcoming of MDR1/P-glycoprotein-mediated multidrug resistance in human gastric carcinoma cells by RNA interference. Cancer Gene Ther 2004, 11:699-706.
13. Kaszubiak A., Holm P.S., Lage H. Overcoming the classical multidrug resistance phenotype by adenoviral delivery of anti-MDR1 short hairpin RNAs and ribozymes. Int J Oncol 2007, 31:419-430.
14. Han M., Lv Q., Tang X.J., Hu Y.L., Xu D.H., Li F.Z., et al. Overcoming drug resistance of MCF-7/ADR cells by altering intracellular distribution of doxorubicin via MVP knockdown with a novel siRNA polyamidoamine-hyaluronic acid complex. JControl Release: Off J Control Release Soc 2012, 163:136-144.
15. Zhang L., Zhang T., Wang L., Shao S., Chen Z., Zhang Z. Invivo targeted delivery of CD40 shRNA to mouse intestinal dendritic cells by oral administration of recombinant Sacchromyces cerevisiae. Gene Ther 2014.
16. Stein U., Walther W., Stege A., Kaszubiak A., Fichtner I., Lage H. Complete invivo reversal of the multidrug resistance phenotype by jet-injection of anti-MDR1 short hairpin RNA-encoding plasmid DNA. Mol Ther J Am Soc Gene Ther 2008, 16:178-186.
17. Jensen L.B., Pavan G.M., Kasimova M.R., Rutherford S., Danani A., Nielsen H.M., et al. Elucidating the molecular mechanism of PAMAM-siRNA dendriplex self-assembly: effect of dendrimer charge density. Int J Pharm 2011, 416:410-418.
18. Chen J.H. Application of cationic polymer vector for gene delivery systems. Yao xue xue bao= Acta Pharm Sinica 2003, 38:316-320.
19. Chen C.K., Law W.C., Aalinkeel R., Yu Y., Nair B., Wu J., et al. Biodegradable cationic polymeric nanocapsules for overcoming multidrug resistance and enabling drug-gene co-delivery to cancer cells. Nanoscale 2014, 6:1567-1572.
20. De Smedt S.C., Demeester J., Hennink W.E. Cationic polymer based gene delivery systems. Pharm Res 2000, 17:113-126.
21. Sun X., Zhang N. Cationic polymer optimization for efficient gene delivery. Mini Rev Med Chem 2010, 10:108-125.
22. Sanchez-Nieves J., Fransen P., Pulido D., Lorente R., Munoz-Fernandez M.A., Albericio F., et al. Amphiphilic cationic carbosilane-PEG dendrimers: synthesis and applications in gene therapy. Eur J Med Chem 2014, 76:43-52.
23. Chaplot S.P., Rupenthal I.D. Dendrimers for gene delivery-a potential approach for ocular therapy?. JPharm Pharmacol 2014, 66:542-556.
24. Luo K., Li C., Wang G., Nie Y., He B., Wu Y., et al. Peptide dendrimers as efficient and biocompatible gene delivery vectors: synthesis and invitro characterization. JControl Release: Off J Control Release Soc 2011, 155:77-87.
25. Wu H.M., Pan S.R., Chen M.W., Wu Y., Wang C., Wen Y.T., et al. Aserum-resistant polyamidoamine-based polypeptide dendrimer for gene transfection. Biomaterials 2011, 32:1619-1634.
26. Tang M.X., Szoka F.C. The influence of polymer structure on the interactions of cationic polymers with DNA and morphology of the resulting complexes. Gene Ther 1997, 4:823-832.
27. Schatzlein A.G., Zinselmeyer B.H., Elouzi A., Dufes C., Chim Y.T., Roberts C.J., et al. Preferential liver gene expression with polypropylenimine dendrimers. JControl Release: Off J Control Release Soc 2005, 101:247-258.
28. Dai F., Liu W. Enhanced gene transfection and serum stability of polyplexes by PDMAEMA-polysulfobetaine diblock copolymers. Biomaterials 2011, 32:628-638.
29. Kumar A., Yellepeddi V.K., Davies G.E., Strychar K.B., Palakurthi S. Enhanced gene transfection efficiency by polyamidoamine (PAMAM) dendrimers modified with ornithine residues. Int J Pharm 2010, 392:294-303.
30. Kumar A., Yellepeddi V.K., Vangara K.K., Strychar K.B., Palakurthi S. Mechanism of gene transfection by polyamidoamine (PAMAM) dendrimers modified with ornithine residues. JDrug Target 2011, 19:770-780.
31. Taratula O., Garbuzenko O.B., Kirkpatrick P., Pandya I., Savla R., Pozharov V.P., et al. Surface-engineered targeted PPI dendrimer for efficient intracellular and intratumoral siRNA delivery. JControl Release: Off J Control Release Soc 2009, 140:284-293.
32. Kim T.I., Baek J.U., Zhe Bai C., Park J.S. Arginine-conjugated polypropylenimine dendrimer as a non-toxic and efficient gene delivery carrier. Biomaterials 2007, 28:2061-2067.
33. Zinselmeyer B.H., Mackay S.P., Schatzlein A.G., Uchegbu I.F. The lower-generation polypropylenimine dendrimers are effective gene-transfer agents. Pharm Res 2002, 19:960-967.
34. Xiong X.B., Uludag H., Lavasanifar A. Biodegradable amphiphilic poly(ethylene oxide)-block-polyesters with grafted polyamines as supramolecular nanocarriers for efficient siRNA delivery. Biomaterials 2009, 30:242-253.
35. Itaka K., Yamauchi K., Harada A., Nakamura K., Kawaguchi H., Kataoka K. Polyion complex micelles from plasmid DNA and poly(ethylene glycol)-poly(L-lysine) block copolymer as serum-tolerable polyplex system: physicochemical properties of micelles relevant to gene transfection efficiency. Biomaterials 2003, 24:4495-4506.
36. Velluto D., Thomas S.N., Simeoni E., Swartz M.A., Hubbell J.A. PEG-b-PPS-b-PEI micelles and PEG-b-PPS/PEG-b-PPS-b-PEI mixed micelles as non-viral vectors for plasmid DNA: tumor immunotoxicity in B16F10 melanoma. Biomaterials 2011, 32:9839-9847.
37. Liu C., Yu W., Chen Z., Zhang J., Zhang N. Enhanced gene transfection efficiency in CD13-positive vascular endothelial cells with targeted poly(lactic acid)-poly(ethylene glycol) nanoparticles through caveolae-mediated endocytosis. JControl Release: Off J Control Release Soc 2011, 151:162-175.
38. Tanaka K., Kanazawa T., Shibata Y., Suda Y., Fukuda T., Takashima Y., et al. Development of cell-penetrating peptide-modified MPEG-PCL diblock copolymeric nanoparticles for systemic gene delivery. Int J Pharm 2010, 396:229-238.
39. Lai T.C., Kataoka K., Kwon G.S. Pluronic-based cationic block copolymer for forming pDNA polyplexes with enhanced cellular uptake and improved transfection efficiency. Biomaterials 2011, 32:4594-4603.
40. Nguyen H.K., Lemieux P., Vinogradov S.V., Gebhart C.L., Guerin N., Paradis G., et al. Evaluation of polyether-polyethyleneimine graft copolymers as gene transfer agents. Gene Ther 2000, 7:126-138.
41. Batrakova E.V., Kabanov A.V. Pluronic block copolymers: evolution of drug delivery concept from inert nanocarriers to biological response modifiers. JControl Release: Off J Control Release Soc 2008, 130:98-106.
42. Liu Y., Sun J., Lian H., Cao W., Wang Y., He Z. Folate and CD44 receptors dual-targeting hydrophobized hyaluronic acid paclitaxel-loaded polymeric micelles for overcoming multidrug resistance and improving tumor distribution. JPharm Sci 2014, 103:1538-1547.
43. Ganesh S., Iyer A.K., Morrissey D.V., Amiji M.M. Hyaluronic acid based self-assembling nanosystems for CD44 target mediated siRNA delivery to solid tumors. Biomaterials 2013, 34:3489-3502.
44. Choi K.Y., Chung H., Min K.H., Yoon H.Y., Kim K., Park J.H., et al. Self-assembled hyaluronic acid nanoparticles for active tumor targeting. Biomaterials 2010, 31:106-114.
45. Miletti-Gonzalez K.E., Chen S., Muthukumaran N., Saglimbeni G.N., Wu X., Yang J., et al. The CD44 receptor interacts with P-glycoprotein to promote cell migration and invasion in cancer. Cancer Res 2005, 65:6660-6667.
46. Yang X., Sarvestani S.K., Moeinzadeh S., He X., Jabbari E. Effect of CD44 binding peptide conjugated to an engineered inert matrix on maintenance of breastcancer stem cells and tumorsphere formation. PloS One 2013, 8:e59147.
47. Lee T., Lim E.K., Lee J., Kang B., Choi J., Park H.S., et al. Efficient CD44-targeted magnetic resonance imaging (MRI) of breast cancer cells using hyaluronicacid (HA)-modified MnFe2O4 nanocrystals. Nanoscale Res Lett 2013, 8:149.
48. Surace C., Arpicco S., Dufay-Wojcicki A., Marsaud V., Bouclier C., Clay D., et al. Lipoplexes targeting the CD44 hyaluronic acid receptor for efficient transfection of breast cancer cells. Mol Pharm 2009, 6:1062-1073.
49. Wu H., Hait W.N., Yang J.M. Small interfering RNA-induced suppression of MDR1 (P-glycoprotein) restores sensitivity to multidrug-resistant cancer cells. Cancer Res 2003, 63:1515-1519.
50. Hao J., Sha X., Tang Y., Jiang Y., Zhang Z., Zhang W., et al. Enhanced transfection of polyplexes based on pluronic-polypropylenimine dendrimer for gene transfer. Arch Pharmacal Res 2009, 32:1045-1054.
51. Shahbazi-Gahrouei D., Abdolahi M., Zarkesh-Esfahani S.H., Laurent S., Sermeus C., Gruettner C. Functionalized magnetic nanoparticles for the detection and quantitative analysis of cell surface antigen. BioMed Res Int 2013, 2013:349408.
52. Pan J., Yang Q. Antibody-functionalized magnetic nanoparticles for the detection of carcinoembryonic antigen using a flow-injection electrochemical device. Anal Bioanal Chem 2007, 388:279-286.
53. Owen S.C., Patel N., Logie J., Pan G., Persson H., Moffat J., et al. Targeting HER2+ breast cancer cells: lysosomal accumulation of anti-HER2 antibodies is influenced by antibody binding site and conjugation to polymeric nanoparticles. JControl Release: Off J Control Release Soc 2013, 172:395-404.
54. Mahmoudian J., Jeddi-Tehrani M., Rabbani H., Mahmoudi A.R., Akhondi M.M., Zarnani A.H., et al. Conjugation of R-phycoerythrin to a polyclonal antibody and F (ab')2 fragment of a polyclonal antibody by two different methods. Avicenna J Med Biotechnol 2010, 2:87-91.
55. Vinogradov S.V., Batrakova E.V., Li S., Kabanov A.V. Mixed polymer micelles of amphiphilic and cationic copolymers for delivery of antisense oligonucleotides. JDrug Target 2004, 12:517-526.
56. Putnam D., Zelikin A.N., Izumrudov V.A., Langer R. Polyhistidine-PEG: DNA nanocomposites for gene delivery. Biomaterials 2003, 24:4425-4433.
57. Shen J., Yin Q., Chen L., Zhang Z., Li Y. Co-delivery of paclitaxel and survivin shRNA by pluronic P85-PEI/TPGS complex nanoparticles to overcome drug resistance in lung cancer. Biomaterials 2012, 33:8613-8624.
58. Ahmed M., Narain R. Cell line dependent uptake and transfection efficiencies of PEI-anionic glycopolymer systems. Biomaterials 2013, 34:4368-4376.
59. Douglas K.L., Piccirillo C.A., Tabrizian M. Cell line-dependent internalization pathways and intracellular trafficking determine transfection efficiency of nanoparticle vectors. Eur J Pharm Biopharm Off J Arbeitsgemeinschaft fur Pharmazeutische Verfahrenstechnik eV 2008, 68:676-687.
60. Astafieva I., Maksimova I., Lukanidin E., Alakhov V., Kabanov A. Enhancement of the polycation-mediated DNA uptake and cell transfection with Pluronic P85 block copolymer. FEBS Lett 1996, 389:278-280.
61. Kabanov A.V., Astafieva I.V., Maksimova I.V., Lukanidin E.M., Georgiev G.P., Kabanov V.A. Efficient transformation of mammalian cells using DNA interpolyelectrolyte complexes with carbon chain polycations. Bioconjugate Chem 1993, 4:448-454.
62. Batrakova E.V., Li S., Brynskikh A.M., Sharma A.K., Li Y., Boska M., et al. Effects of pluronic and doxorubicin on drug uptake, cellular metabolism, apoptosis and tumor inhibition in animal models of MDR cancers. JControl Release: Off J Control Release Soc 2010, 143:290-301.
63. Savani R.C., Cao G., Pooler P.M., Zaman A., Zhou Z., DeLisser H.M. Differential involvement of the hyaluronan (HA) receptors CD44 and receptor for HA-mediated motility in endothelial cell function and angiogenesis. JBiol Chem 2001, 276:36770-36778.
64. Khalil I.A., Kogure K., Akita H., Harashima H. Uptake pathways and subsequent intracellular trafficking in nonviral gene delivery. Pharmacol Rev 2006, 58:32-45.