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Erschienen in: Wiener Medizinische Wochenschrift 7-8/2016

01.05.2016 | main topic

Endocytosis in gene therapy with non-viral vectors

verfasst von: Aritz Perez Ruiz de Garibay

Erschienen in: Wiener Medizinische Wochenschrift | Ausgabe 7-8/2016

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Summary

Gene therapy or the delivery of genetic material can be carried out not only with viral vectors, but with non-viral vectors too. Although the use of non-viral carriers is safer, this approach has generally been poorer in terms of transfection efficiency. In order to improve the transfection rates, it is important to exactly know the path that the nanoparticles go through. In this way, we can understand the reason why some of these vectors fail or are successful in their duties. This review aims to summarize the different stages and barriers that nanocarriers have to overcome during endocytosis so as to reach the cytoplasm, in the case of RNA, or the nucleus, in the case of DNA. In addition, different strategies that could be employed to improve the success of the carriers in each stage are suggested.
Literatur
1.
Zurück zum Zitat Griesenbach U, Alton EWFW. Moving forward: cystic fibrosis gene therapy. Hum Mol Genet. 2013;22:R52–8.CrossRefPubMed Griesenbach U, Alton EWFW. Moving forward: cystic fibrosis gene therapy. Hum Mol Genet. 2013;22:R52–8.CrossRefPubMed
2.
Zurück zum Zitat Solinis MA, Del Pozo-Rodriguez A, Apaolaza PS, Rodriguez-Gascon A. Treatment of ocular disorders by gene therapy. Eur J Pharm Biopharm. 2015;95:331–342.CrossRefPubMed Solinis MA, Del Pozo-Rodriguez A, Apaolaza PS, Rodriguez-Gascon A. Treatment of ocular disorders by gene therapy. Eur J Pharm Biopharm. 2015;95:331–342.CrossRefPubMed
3.
Zurück zum Zitat Walther W, Schlag PM. Current status of gene therapy for cancer. Curr Opin Oncol. 2013;25:659–664.CrossRefPubMed Walther W, Schlag PM. Current status of gene therapy for cancer. Curr Opin Oncol. 2013;25:659–664.CrossRefPubMed
4.
Zurück zum Zitat Yin H, Kanasty RL, Eltoukhy AA, Vegas AJ, Dorkin JR, Anderson DG. Non-viral vectors for gene-based therapy. Nat Rev Genet. 2014;15:541–555.CrossRefPubMed Yin H, Kanasty RL, Eltoukhy AA, Vegas AJ, Dorkin JR, Anderson DG. Non-viral vectors for gene-based therapy. Nat Rev Genet. 2014;15:541–555.CrossRefPubMed
5.
Zurück zum Zitat Hacein-Bey-Abina S, Hauer J, Lim A, Picard C, Wang GP, Berry CC, et al. Efficacy of gene therapy for X‑linked severe combined immunodeficiency. N Engl J Med. 2010;363:355–364.CrossRefPubMedPubMedCentral Hacein-Bey-Abina S, Hauer J, Lim A, Picard C, Wang GP, Berry CC, et al. Efficacy of gene therapy for X‑linked severe combined immunodeficiency. N Engl J Med. 2010;363:355–364.CrossRefPubMedPubMedCentral
6.
Zurück zum Zitat Gaspar HB, Parsley KL, Howe S, King D, Gilmour KC, Sinclair J, et al. Gene therapy of X‑linked severe combined immunodeficiency by use of a pseudotyped gammaretroviral vector. Lancet. 2004;364:2181–2187.CrossRefPubMed Gaspar HB, Parsley KL, Howe S, King D, Gilmour KC, Sinclair J, et al. Gene therapy of X‑linked severe combined immunodeficiency by use of a pseudotyped gammaretroviral vector. Lancet. 2004;364:2181–2187.CrossRefPubMed
7.
Zurück zum Zitat Cavazzana-Calvo M, Hacein-Bey S, de Saint BG, Gross F, Yvon E, Nusbaum P, et al. Gene therapy of human severe combined immunodeficiency (SCID)-X1 disease. Science. 2000;288:669–672.CrossRefPubMed Cavazzana-Calvo M, Hacein-Bey S, de Saint BG, Gross F, Yvon E, Nusbaum P, et al. Gene therapy of human severe combined immunodeficiency (SCID)-X1 disease. Science. 2000;288:669–672.CrossRefPubMed
8.
Zurück zum Zitat Sakuma T, Barry MA, Ikeda Y. Lentiviral vectors: basic to translational. Biochem J. 2012;443:603–618.CrossRefPubMed Sakuma T, Barry MA, Ikeda Y. Lentiviral vectors: basic to translational. Biochem J. 2012;443:603–618.CrossRefPubMed
10.
Zurück zum Zitat Balakrishnan B, Jayandharan GR. Basic biology of adeno-associated virus (AAV) vectors used in gene therapy. Curr Gene Ther. 2014;14:86–100.CrossRefPubMed Balakrishnan B, Jayandharan GR. Basic biology of adeno-associated virus (AAV) vectors used in gene therapy. Curr Gene Ther. 2014;14:86–100.CrossRefPubMed
11.
Zurück zum Zitat Grieger JC, Samulski RJ. Adeno-associated virus vectorology, manufacturing, and clinical applications. Methods Enzym. 2012;507:229–254.CrossRef Grieger JC, Samulski RJ. Adeno-associated virus vectorology, manufacturing, and clinical applications. Methods Enzym. 2012;507:229–254.CrossRef
12.
Zurück zum Zitat Yla-Herttuala S. Endgame: glybera finally recommended for approval as the first gene therapy drug in the European union. Mol Ther. 2012;p:1831–1832.CrossRef Yla-Herttuala S. Endgame: glybera finally recommended for approval as the first gene therapy drug in the European union. Mol Ther. 2012;p:1831–1832.CrossRef
13.
Zurück zum Zitat Junquera E, Aicart E. Cationic lipids as transfecting agents of DNA in gene therapy. Curr Top Med Chem. 2014;14:649–663.CrossRefPubMed Junquera E, Aicart E. Cationic lipids as transfecting agents of DNA in gene therapy. Curr Top Med Chem. 2014;14:649–663.CrossRefPubMed
14.
15.
Zurück zum Zitat Bates K, Kostarelos K. Carbon nanotubes as vectors for gene therapy: past achievements, present challenges and future goals. Adv Drug Deliv Rev. 2013;65:2023–2033.CrossRefPubMed Bates K, Kostarelos K. Carbon nanotubes as vectors for gene therapy: past achievements, present challenges and future goals. Adv Drug Deliv Rev. 2013;65:2023–2033.CrossRefPubMed
16.
Zurück zum Zitat Shcharbin D, Pedziwiatr E, Blasiak J, Bryszewska M. How to study dendriplexes II: Transfection and cytotoxicity. J Control Release. 2010;141:110–127.CrossRefPubMed Shcharbin D, Pedziwiatr E, Blasiak J, Bryszewska M. How to study dendriplexes II: Transfection and cytotoxicity. J Control Release. 2010;141:110–127.CrossRefPubMed
17.
18.
Zurück zum Zitat Pack DW, Hoffman AS, Pun S, Stayton PS. Design and development of polymers for gene delivery. Nat Rev Drug Discov. 2005;4:581–593.CrossRefPubMed Pack DW, Hoffman AS, Pun S, Stayton PS. Design and development of polymers for gene delivery. Nat Rev Drug Discov. 2005;4:581–593.CrossRefPubMed
19.
Zurück zum Zitat von Gersdorff K, Sanders NN, Vandenbroucke R, De Smedt SC, Wagner E, Ogris M. The internalization route resulting in successful gene expression depends on both cell line and polyethylenimine polyplex type. Mol Ther. 2006;14:745–753.CrossRef von Gersdorff K, Sanders NN, Vandenbroucke R, De Smedt SC, Wagner E, Ogris M. The internalization route resulting in successful gene expression depends on both cell line and polyethylenimine polyplex type. Mol Ther. 2006;14:745–753.CrossRef
20.
Zurück zum Zitat Duncan R, Richardson SCW. Endocytosis and intracellular trafficking as gateways for nanomedicine delivery: opportunities and challenges. Mol Pharm. 2012;9:2380–2402.CrossRefPubMed Duncan R, Richardson SCW. Endocytosis and intracellular trafficking as gateways for nanomedicine delivery: opportunities and challenges. Mol Pharm. 2012;9:2380–2402.CrossRefPubMed
21.
Zurück zum Zitat Zaki NM, Tirelli N. Gateways for the intracellular access of nanocarriers: a review of receptor-mediated endocytosis mechanisms and of strategies in receptor targeting. Expert Opin Drug Deliv. 2010;7:895–913.CrossRefPubMed Zaki NM, Tirelli N. Gateways for the intracellular access of nanocarriers: a review of receptor-mediated endocytosis mechanisms and of strategies in receptor targeting. Expert Opin Drug Deliv. 2010;7:895–913.CrossRefPubMed
22.
Zurück zum Zitat de Ruiz GAP, Solinis AMA, Rodriguez GA, Ganjian H, Fuchs R. Role of endocytic uptake in transfection efficiency of solid lipid nanoparticles-based nonviral vectors. J Gene Med. 2013;15:427–440.CrossRef de Ruiz GAP, Solinis AMA, Rodriguez GA, Ganjian H, Fuchs R. Role of endocytic uptake in transfection efficiency of solid lipid nanoparticles-based nonviral vectors. J Gene Med. 2013;15:427–440.CrossRef
23.
Zurück zum Zitat Wilhelm C, Billotey C, Roger J, Pons JN, Bacri J‑C, Gazeau F. Intracellular uptake of anionic superparamagnetic nanoparticles as a function of their surface coating. Biomaterials. 2003;24:1001–1011.CrossRefPubMed Wilhelm C, Billotey C, Roger J, Pons JN, Bacri J‑C, Gazeau F. Intracellular uptake of anionic superparamagnetic nanoparticles as a function of their surface coating. Biomaterials. 2003;24:1001–1011.CrossRefPubMed
24.
Zurück zum Zitat del Pozo-Rodriguez A, Delgado D, Solinis MA, Gascon AR, Pedraz JL. Solid lipid nanoparticles: formulation factors affecting cell transfection capacity. Int J Pharm. 2007;339:261–268.CrossRefPubMed del Pozo-Rodriguez A, Delgado D, Solinis MA, Gascon AR, Pedraz JL. Solid lipid nanoparticles: formulation factors affecting cell transfection capacity. Int J Pharm. 2007;339:261–268.CrossRefPubMed
25.
26.
Zurück zum Zitat Vercauteren D, Rejman J, Martens TF, Demeester J, De Smedt SC, Braeckmans K. On the cellular processing of non-viral nanomedicines for nucleic acid delivery: mechanisms and methods. J Control Release. 2012;161:566–581.CrossRefPubMed Vercauteren D, Rejman J, Martens TF, Demeester J, De Smedt SC, Braeckmans K. On the cellular processing of non-viral nanomedicines for nucleic acid delivery: mechanisms and methods. J Control Release. 2012;161:566–581.CrossRefPubMed
27.
Zurück zum Zitat Favretto ME, Wallbrecher R, Schmidt S, van de Putte R, Brock R. Glycosaminoglycans in the cellular uptake of drug delivery vectors – bystanders or active players? J Control Release. 2014;180:81–90.CrossRefPubMed Favretto ME, Wallbrecher R, Schmidt S, van de Putte R, Brock R. Glycosaminoglycans in the cellular uptake of drug delivery vectors – bystanders or active players? J Control Release. 2014;180:81–90.CrossRefPubMed
28.
Zurück zum Zitat Aggarwal P, Hall JB, McLeland CB, Dobrovolskaia MA, McNeil SE. Nanoparticle interaction with plasma proteins as it relates to particle biodistribution, biocompatibility and therapeutic efficacy. Adv Drug Deliv Rev. 2009;61:428–437.CrossRefPubMedPubMedCentral Aggarwal P, Hall JB, McLeland CB, Dobrovolskaia MA, McNeil SE. Nanoparticle interaction with plasma proteins as it relates to particle biodistribution, biocompatibility and therapeutic efficacy. Adv Drug Deliv Rev. 2009;61:428–437.CrossRefPubMedPubMedCentral
29.
Zurück zum Zitat Bahrami B, Mohammadnia-Afrouzi M, Bakhshaei P, Yazdani Y, Ghalamfarsa G, Yousefi M, et al. Folate-conjugated nanoparticles as a potent therapeutic approach in targeted cancer therapy. Tumour Biol. 2015;36:5727–5742.CrossRefPubMed Bahrami B, Mohammadnia-Afrouzi M, Bakhshaei P, Yazdani Y, Ghalamfarsa G, Yousefi M, et al. Folate-conjugated nanoparticles as a potent therapeutic approach in targeted cancer therapy. Tumour Biol. 2015;36:5727–5742.CrossRefPubMed
30.
Zurück zum Zitat de Tros IC, Duzgunes N. Delivery of therapeutic nucleic acids via transferrin and transferrin receptors: lipoplexes and other carriers. Expert Opin Drug Deliv. 2013;10:1583–1591.CrossRef de Tros IC, Duzgunes N. Delivery of therapeutic nucleic acids via transferrin and transferrin receptors: lipoplexes and other carriers. Expert Opin Drug Deliv. 2013;10:1583–1591.CrossRef
31.
Zurück zum Zitat Ashraf SQ, Nicholls AM, Wilding JL, Ntouroupi TG, Mortensen NJ, Bodmer WF. Direct and immune mediated antibody targeting of ERBB receptors in a colorectal cancer cell-line panel. Proc Natl Acad Sci USA. 2012;109:21046–21051.CrossRefPubMedPubMedCentral Ashraf SQ, Nicholls AM, Wilding JL, Ntouroupi TG, Mortensen NJ, Bodmer WF. Direct and immune mediated antibody targeting of ERBB receptors in a colorectal cancer cell-line panel. Proc Natl Acad Sci USA. 2012;109:21046–21051.CrossRefPubMedPubMedCentral
32.
Zurück zum Zitat Yang T, Li B, Qi S, Liu Y, Gai Y, Ye P, et al. Co-delivery of doxorubicin and Bmi1 siRNA by folate receptor targeted liposomes exhibits enhanced anti-tumor effects in vitro and in vivo. Theranostics. 2014;4:1096–1111.CrossRefPubMedPubMedCentral Yang T, Li B, Qi S, Liu Y, Gai Y, Ye P, et al. Co-delivery of doxorubicin and Bmi1 siRNA by folate receptor targeted liposomes exhibits enhanced anti-tumor effects in vitro and in vivo. Theranostics. 2014;4:1096–1111.CrossRefPubMedPubMedCentral
33.
Zurück zum Zitat Ogris M, Walker G, Blessing T, Kircheis R, Wolschek M, Wagner E. Tumor-targeted gene therapy: strategies for the preparation of ligand-polyethylene glycol-polyethylenimine/DNA complexes. J Control Release. 2003;91:173–181.CrossRefPubMed Ogris M, Walker G, Blessing T, Kircheis R, Wolschek M, Wagner E. Tumor-targeted gene therapy: strategies for the preparation of ligand-polyethylene glycol-polyethylenimine/DNA complexes. J Control Release. 2003;91:173–181.CrossRefPubMed
34.
Zurück zum Zitat Ding Y, Wang W, Feng M, Wang Y, Zhou J, Ding X, et al. A biomimetic nanovector-mediated targeted cholesterol-conjugated siRNA delivery for tumor gene therapy. Biomaterials. 2012;33:8893–8905.CrossRefPubMed Ding Y, Wang W, Feng M, Wang Y, Zhou J, Ding X, et al. A biomimetic nanovector-mediated targeted cholesterol-conjugated siRNA delivery for tumor gene therapy. Biomaterials. 2012;33:8893–8905.CrossRefPubMed
35.
Zurück zum Zitat Cai L‑L, Liu P, Li X, Huang X, Ye Y‑Q, Chen F‑Y, et al. RGD peptide-mediated chitosan-based polymeric micelles targeting delivery for integrin-overexpressing tumor cells. Int J Nanomedicine. 2011;6:3499–3508.PubMedPubMedCentral Cai L‑L, Liu P, Li X, Huang X, Ye Y‑Q, Chen F‑Y, et al. RGD peptide-mediated chitosan-based polymeric micelles targeting delivery for integrin-overexpressing tumor cells. Int J Nanomedicine. 2011;6:3499–3508.PubMedPubMedCentral
36.
Zurück zum Zitat Varshosaz J, Farzan M. Nanoparticles for targeted delivery of therapeutics and small interfering RNAs in hepatocellular carcinoma. World J Gastroenterol. 2015;21:12022–12041.CrossRefPubMedPubMedCentral Varshosaz J, Farzan M. Nanoparticles for targeted delivery of therapeutics and small interfering RNAs in hepatocellular carcinoma. World J Gastroenterol. 2015;21:12022–12041.CrossRefPubMedPubMedCentral
37.
Zurück zum Zitat Siu KS, Chen D, Zheng X, Zhang X, Johnston N, Liu Y, et al. Non-covalently functionalized single-walled carbon nanotube for topical siRNA delivery into melanoma. Biomaterials. 2014;35:3435–3442.CrossRefPubMed Siu KS, Chen D, Zheng X, Zhang X, Johnston N, Liu Y, et al. Non-covalently functionalized single-walled carbon nanotube for topical siRNA delivery into melanoma. Biomaterials. 2014;35:3435–3442.CrossRefPubMed
38.
Zurück zum Zitat Guo C, Al-Jamal WT, Toma FM, Bianco A, Prato M, Al-Jamal KT, et al. Design of Cationic Multiwalled carbon Nanotubes as efficient siRNA vectors for lung cancer xenograft eradication. Bioconjug Chem. 2015;26:1370–1379.CrossRefPubMed Guo C, Al-Jamal WT, Toma FM, Bianco A, Prato M, Al-Jamal KT, et al. Design of Cationic Multiwalled carbon Nanotubes as efficient siRNA vectors for lung cancer xenograft eradication. Bioconjug Chem. 2015;26:1370–1379.CrossRefPubMed
39.
Zurück zum Zitat Spinato C, de Ruiz PGA, Kierkowicz M, Pach E, Martincic M, Klippstein R, et al. Design of antibody-functionalized carbon nanotubes filled with radioactivable metals towards a targeted anticancer therapy. Nanoscale. 2015; doi:10.1039/C5NR07923C. Spinato C, de Ruiz PGA, Kierkowicz M, Pach E, Martincic M, Klippstein R, et al. Design of antibody-functionalized carbon nanotubes filled with radioactivable metals towards a targeted anticancer therapy. Nanoscale. 2015; doi:10.1039/C5NR07923C.
40.
Zurück zum Zitat Lacerda L, Russier J, Pastorin G, Herrero MA, Venturelli E, Dumortier H, et al. Translocation mechanisms of chemically functionalised carbon nanotubes across plasma membranes. Biomaterials. 2012;33:3334–3343.CrossRefPubMed Lacerda L, Russier J, Pastorin G, Herrero MA, Venturelli E, Dumortier H, et al. Translocation mechanisms of chemically functionalised carbon nanotubes across plasma membranes. Biomaterials. 2012;33:3334–3343.CrossRefPubMed
41.
Zurück zum Zitat Mercer J, Schelhaas M, Helenius A. Virus entry by endocytosis. Annu Rev Biochem. 2010;79:803–833.CrossRefPubMed Mercer J, Schelhaas M, Helenius A. Virus entry by endocytosis. Annu Rev Biochem. 2010;79:803–833.CrossRefPubMed
42.
Zurück zum Zitat El-Sayed A, Harashima H. Endocytosis of gene delivery vectors: from clathrin-dependent to lipid raft-mediated endocytosis. Mol Ther. 2013;21:1118–1130.CrossRefPubMedPubMedCentral El-Sayed A, Harashima H. Endocytosis of gene delivery vectors: from clathrin-dependent to lipid raft-mediated endocytosis. Mol Ther. 2013;21:1118–1130.CrossRefPubMedPubMedCentral
44.
Zurück zum Zitat Jafari M, Soltani M, Naahidi S, Karunaratne DN, Chen P. Nonviral approach for targeted nucleic acid delivery. Curr Med Chem. 2012;19:197–208.CrossRefPubMed Jafari M, Soltani M, Naahidi S, Karunaratne DN, Chen P. Nonviral approach for targeted nucleic acid delivery. Curr Med Chem. 2012;19:197–208.CrossRefPubMed
45.
Zurück zum Zitat Kumari S, Mg S, Mayor S. Endocytosis unplugged: multiple ways to enter the cell. Cell Res. 2010;20:256–275.CrossRefPubMed Kumari S, Mg S, Mayor S. Endocytosis unplugged: multiple ways to enter the cell. Cell Res. 2010;20:256–275.CrossRefPubMed
47.
Zurück zum Zitat Norbury CC, Chambers BJ, Prescott AR, Ljunggren HG, Watts C. Constitutive macropinocytosis allows TAP-dependent major histocompatibility complex class I presentation of exogenous soluble antigen by bone marrow-derived dendritic cells. Eur J Immunol. 1997;27:280–288.CrossRefPubMed Norbury CC, Chambers BJ, Prescott AR, Ljunggren HG, Watts C. Constitutive macropinocytosis allows TAP-dependent major histocompatibility complex class I presentation of exogenous soluble antigen by bone marrow-derived dendritic cells. Eur J Immunol. 1997;27:280–288.CrossRefPubMed
48.
Zurück zum Zitat Mercer J, Helenius A. Gulping rather than sipping: macropinocytosis as a way of virus entry. Curr Opin Microbiol. 2012;15:490–499.CrossRefPubMed Mercer J, Helenius A. Gulping rather than sipping: macropinocytosis as a way of virus entry. Curr Opin Microbiol. 2012;15:490–499.CrossRefPubMed
49.
Zurück zum Zitat Delgado D, del Pozo-Rodriguez A, Solinis MA, Rodriguez-Gascon A. Understanding the mechanism of protamine in solid lipid nanoparticle-based lipofection: the importance of the entry pathway. Eur J Pharm Biopharm. 2011;79:495–502.CrossRefPubMed Delgado D, del Pozo-Rodriguez A, Solinis MA, Rodriguez-Gascon A. Understanding the mechanism of protamine in solid lipid nanoparticle-based lipofection: the importance of the entry pathway. Eur J Pharm Biopharm. 2011;79:495–502.CrossRefPubMed
50.
Zurück zum Zitat Yao J‑J, Du Y‑Z, Yuan H, You J, Hu F‑Q. Efficient gene delivery system mediated by cis-aconitate-modified chitosan-g-stearic acid micelles. Int J Nanomedicine. 2014;9:2993–3003.PubMedPubMedCentral Yao J‑J, Du Y‑Z, Yuan H, You J, Hu F‑Q. Efficient gene delivery system mediated by cis-aconitate-modified chitosan-g-stearic acid micelles. Int J Nanomedicine. 2014;9:2993–3003.PubMedPubMedCentral
51.
Zurück zum Zitat Bae Y‑U, Kim B‑K, Park J‑W, Seu Y‑B, Doh K‑O. Endocytic pathway and resistance to cholesterol depletion of cholesterol derived cationic lipids for gene delivery. Mol Pharm. 2012;9:3579–3585.CrossRefPubMed Bae Y‑U, Kim B‑K, Park J‑W, Seu Y‑B, Doh K‑O. Endocytic pathway and resistance to cholesterol depletion of cholesterol derived cationic lipids for gene delivery. Mol Pharm. 2012;9:3579–3585.CrossRefPubMed
52.
Zurück zum Zitat Russier J, Grillaud M, Bianco A. Elucidation of the cellular uptake mechanisms of Polycationic HYDRAmers. Bioconjug Chem. 2015;26:1484–1493.CrossRefPubMed Russier J, Grillaud M, Bianco A. Elucidation of the cellular uptake mechanisms of Polycationic HYDRAmers. Bioconjug Chem. 2015;26:1484–1493.CrossRefPubMed
53.
Zurück zum Zitat Suresh D, Zambre A, Chanda N, Hoffman TJ, Smith CJ, Robertson JD, et al. Bombesin peptide conjugated gold nanocages internalize via clathrin mediated endocytosis. Bioconjug Chem. 2014;25:1565–1579.CrossRefPubMed Suresh D, Zambre A, Chanda N, Hoffman TJ, Smith CJ, Robertson JD, et al. Bombesin peptide conjugated gold nanocages internalize via clathrin mediated endocytosis. Bioconjug Chem. 2014;25:1565–1579.CrossRefPubMed
54.
Zurück zum Zitat Yu D, Zhang Y, Mao Z, Gao C. Study of the selective uptake progress of aptamer-modified PLGA particles by liver cells. Macromol Biosci. 2013;13:1413–1421.CrossRefPubMed Yu D, Zhang Y, Mao Z, Gao C. Study of the selective uptake progress of aptamer-modified PLGA particles by liver cells. Macromol Biosci. 2013;13:1413–1421.CrossRefPubMed
55.
Zurück zum Zitat Bathori G, Cervenak L, Karadi I. Caveolae – an alternative endocytotic pathway for targeted drug delivery. Crit Rev Ther Drug Carr Syst. 2004;21:67–95.CrossRef Bathori G, Cervenak L, Karadi I. Caveolae – an alternative endocytotic pathway for targeted drug delivery. Crit Rev Ther Drug Carr Syst. 2004;21:67–95.CrossRef
56.
Zurück zum Zitat Perumal OP, Inapagolla R, Kannan S, Kannan RM. The effect of surface functionality on cellular trafficking of dendrimers. Biomaterials. 2008;29:3469–3476.CrossRefPubMed Perumal OP, Inapagolla R, Kannan S, Kannan RM. The effect of surface functionality on cellular trafficking of dendrimers. Biomaterials. 2008;29:3469–3476.CrossRefPubMed
57.
Zurück zum Zitat Gabrielson NP, Pack DW. Efficient polyethylenimine-mediated gene delivery proceeds via a caveolar pathway in HeLa cells. J Control Release. 2009;136:54–61.CrossRefPubMed Gabrielson NP, Pack DW. Efficient polyethylenimine-mediated gene delivery proceeds via a caveolar pathway in HeLa cells. J Control Release. 2009;136:54–61.CrossRefPubMed
58.
Zurück zum Zitat Letoha T, Kolozsi C, Ekes C, Keller-pinter A, Kusz E, Szakonyi G, et al. Contribution of syndecans to lipoplex-mediated gene delivery. Eur J Pharm Sci. 2013;49:550–555.CrossRefPubMed Letoha T, Kolozsi C, Ekes C, Keller-pinter A, Kusz E, Szakonyi G, et al. Contribution of syndecans to lipoplex-mediated gene delivery. Eur J Pharm Sci. 2013;49:550–555.CrossRefPubMed
59.
Zurück zum Zitat Kobayashi S, Hattori Y, Osakada H, Toma K, Maitani Y, Hiraoka Y, et al. Early entry and deformation of macropinosomes correlates with high efficiency of decaarginine-polyethylene glycol-lipid-mediated gene delivery. J Gene Med. 2012;14:262–271.CrossRefPubMed Kobayashi S, Hattori Y, Osakada H, Toma K, Maitani Y, Hiraoka Y, et al. Early entry and deformation of macropinosomes correlates with high efficiency of decaarginine-polyethylene glycol-lipid-mediated gene delivery. J Gene Med. 2012;14:262–271.CrossRefPubMed
60.
Zurück zum Zitat Hsu CYM, Uludag H. Cellular uptake pathways of lipid-modified cationic polymers in gene delivery to primary cells. Biomater. 2012;33:7834–7848.CrossRef Hsu CYM, Uludag H. Cellular uptake pathways of lipid-modified cationic polymers in gene delivery to primary cells. Biomater. 2012;33:7834–7848.CrossRef
61.
Zurück zum Zitat Kasper J, Hermanns MI, Bantz C, Utech S, Koshkina O, Maskos M, et al. Flotillin-involved uptake of silica nanoparticles and responses of an alveolar-capillary barrier in vitro. Eur J Pharm Biopharm. 2013;84:275–287.CrossRefPubMed Kasper J, Hermanns MI, Bantz C, Utech S, Koshkina O, Maskos M, et al. Flotillin-involved uptake of silica nanoparticles and responses of an alveolar-capillary barrier in vitro. Eur J Pharm Biopharm. 2013;84:275–287.CrossRefPubMed
62.
Zurück zum Zitat Vercauteren D, Piest M, van der Aa LJ, Soraj AM, Jones AT, Engbersen JFJ, et al. Flotillin-dependent endocytosis and a phagocytosis-like mechanism for cellular internalization of disulfide-based poly(amido amine)/DNA polyplexes. Biomaterials. 2011;32:3072–3084.CrossRefPubMed Vercauteren D, Piest M, van der Aa LJ, Soraj AM, Jones AT, Engbersen JFJ, et al. Flotillin-dependent endocytosis and a phagocytosis-like mechanism for cellular internalization of disulfide-based poly(amido amine)/DNA polyplexes. Biomaterials. 2011;32:3072–3084.CrossRefPubMed
63.
Zurück zum Zitat Yang HN, Park JS, Jeon SY, Park W, Na K, Park K‑H. The effect of quantum dot size and poly(ethylenimine) coating on the efficiency of gene delivery into human mesenchymal stem cells. Biomaterials. 2014;35:8439–8449.CrossRefPubMed Yang HN, Park JS, Jeon SY, Park W, Na K, Park K‑H. The effect of quantum dot size and poly(ethylenimine) coating on the efficiency of gene delivery into human mesenchymal stem cells. Biomaterials. 2014;35:8439–8449.CrossRefPubMed
64.
Zurück zum Zitat Wang Z, Tiruppathi C, Minshall RD, Malik AB. Size and dynamics of caveolae studied using nanoparticles in living endothelial cells. Acs Nano. 2009;3:4110–4116.CrossRefPubMedPubMedCentral Wang Z, Tiruppathi C, Minshall RD, Malik AB. Size and dynamics of caveolae studied using nanoparticles in living endothelial cells. Acs Nano. 2009;3:4110–4116.CrossRefPubMedPubMedCentral
65.
Zurück zum Zitat Rejman J, Oberle V, Zuhorn IS, Hoekstra D. Size-dependent internalization of particles via the pathways of clathrin- and caveolae-mediated endocytosis. Biochem J. 2004;377:159–169.CrossRefPubMedPubMedCentral Rejman J, Oberle V, Zuhorn IS, Hoekstra D. Size-dependent internalization of particles via the pathways of clathrin- and caveolae-mediated endocytosis. Biochem J. 2004;377:159–169.CrossRefPubMedPubMedCentral
66.
Zurück zum Zitat Ravindran S, Snee PT, Ramachandran A, George A. Acidic domain in dentin phosphophoryn facilitates cellular uptake: implications in targeted protein delivery. J Biol Chem. 2013;288:16098–16109.CrossRefPubMedPubMedCentral Ravindran S, Snee PT, Ramachandran A, George A. Acidic domain in dentin phosphophoryn facilitates cellular uptake: implications in targeted protein delivery. J Biol Chem. 2013;288:16098–16109.CrossRefPubMedPubMedCentral
67.
Zurück zum Zitat Han H‑S, Martin JD, Lee J, Harris DK, Fukumura D, Jain RK, et al. Spatial charge configuration regulates nanoparticle transport and binding behavior in vivo. Angew Chem Int Ed Engl. 2013;52:1414–1419.CrossRefPubMedPubMedCentral Han H‑S, Martin JD, Lee J, Harris DK, Fukumura D, Jain RK, et al. Spatial charge configuration regulates nanoparticle transport and binding behavior in vivo. Angew Chem Int Ed Engl. 2013;52:1414–1419.CrossRefPubMedPubMedCentral
68.
Zurück zum Zitat Boeneman K, Delehanty JB, Blanco-Canosa JB, Susumu K, Stewart MH, Oh E, et al. Selecting improved peptidyl motifs for cytosolic delivery of disparate protein and nanoparticle materials. Acs Nano. 2013;7:3778–3796.CrossRefPubMed Boeneman K, Delehanty JB, Blanco-Canosa JB, Susumu K, Stewart MH, Oh E, et al. Selecting improved peptidyl motifs for cytosolic delivery of disparate protein and nanoparticle materials. Acs Nano. 2013;7:3778–3796.CrossRefPubMed
71.
Zurück zum Zitat Serrano D, Bhowmick T, Chadha R, Garnacho C, Muro S. Intercellular adhesion molecule 1 engagement modulates sphingomyelinase and ceramide, supporting uptake of drug carriers by the vascular endothelium. Arter Thromb Vasc Biol. 2012;32:1178–1185.CrossRef Serrano D, Bhowmick T, Chadha R, Garnacho C, Muro S. Intercellular adhesion molecule 1 engagement modulates sphingomyelinase and ceramide, supporting uptake of drug carriers by the vascular endothelium. Arter Thromb Vasc Biol. 2012;32:1178–1185.CrossRef
72.
73.
Zurück zum Zitat ur Rehman Z, Zuhorn IS, Hoekstra D. How cationic lipids transfer nucleic acids into cells and across cellular membranes: recent advances. J Control Release. 2013;166:46–56.CrossRefPubMed ur Rehman Z, Zuhorn IS, Hoekstra D. How cationic lipids transfer nucleic acids into cells and across cellular membranes: recent advances. J Control Release. 2013;166:46–56.CrossRefPubMed
74.
Zurück zum Zitat Sheppard D. Dominant negative mutants: tools for the study of protein function in vitro and in vivo. Am J Respir Cell Mol Biol. 1994;11:1–6.CrossRefPubMed Sheppard D. Dominant negative mutants: tools for the study of protein function in vitro and in vivo. Am J Respir Cell Mol Biol. 1994;11:1–6.CrossRefPubMed
75.
Zurück zum Zitat Damke H, Baba T, Warnock DE, Schmid SL. Induction of mutant dynamin specifically blocks endocytic coated vesicle formation. J Cell Biol. 1994;127:915–934.CrossRefPubMed Damke H, Baba T, Warnock DE, Schmid SL. Induction of mutant dynamin specifically blocks endocytic coated vesicle formation. J Cell Biol. 1994;127:915–934.CrossRefPubMed
76.
Zurück zum Zitat Galperin E, Sorkin A. Visualization of Rab5 activity in living cells by FRET microscopy and influence of plasma-membrane-targeted Rab5 on clathrin-dependent endocytosis. J Cell Sci. 2003;116:4799–4810.CrossRefPubMed Galperin E, Sorkin A. Visualization of Rab5 activity in living cells by FRET microscopy and influence of plasma-membrane-targeted Rab5 on clathrin-dependent endocytosis. J Cell Sci. 2003;116:4799–4810.CrossRefPubMed
77.
Zurück zum Zitat Meister M, Zuk A, Tikkanen R. Role of dynamin and clathrin in the cellular trafficking of flotillins. FEBS J. 2014;281:2956–2976.CrossRefPubMed Meister M, Zuk A, Tikkanen R. Role of dynamin and clathrin in the cellular trafficking of flotillins. FEBS J. 2014;281:2956–2976.CrossRefPubMed
78.
Zurück zum Zitat Shen W, van Dongen MA, Han Y, Yu M, Li Y, Liu G, et al. The role of caveolin-1 and syndecan-4 in the internalization of PEGylated PAMAM dendrimer polyplexes into myoblast and hepatic cells. Eur J Pharm Biopharm. 2014;88:658–663.CrossRefPubMedPubMedCentral Shen W, van Dongen MA, Han Y, Yu M, Li Y, Liu G, et al. The role of caveolin-1 and syndecan-4 in the internalization of PEGylated PAMAM dendrimer polyplexes into myoblast and hepatic cells. Eur J Pharm Biopharm. 2014;88:658–663.CrossRefPubMedPubMedCentral
79.
Zurück zum Zitat Predescu DN, Neamu R, Bardita C, Wang M, Predescu SA. Impaired caveolae function and upregulation of alternative endocytic pathways induced by experimental modulation of intersectin-1 s expression in mouse lung endothelium. Biochem Res Int. 2012;2012:672705.CrossRefPubMedPubMedCentral Predescu DN, Neamu R, Bardita C, Wang M, Predescu SA. Impaired caveolae function and upregulation of alternative endocytic pathways induced by experimental modulation of intersectin-1 s expression in mouse lung endothelium. Biochem Res Int. 2012;2012:672705.CrossRefPubMedPubMedCentral
80.
Zurück zum Zitat Ma Y, Jin J, Dong C, Cheng E‑C, Lin H, Huang Y, et al. High-efficiency siRNA-based gene knockdown in human embryonic stem cells. RNA. 2010;16:2564–2569.CrossRefPubMedPubMedCentral Ma Y, Jin J, Dong C, Cheng E‑C, Lin H, Huang Y, et al. High-efficiency siRNA-based gene knockdown in human embryonic stem cells. RNA. 2010;16:2564–2569.CrossRefPubMedPubMedCentral
81.
Zurück zum Zitat Rajendran L, Knolker H‑J, Simons K. Subcellular targeting strategies for drug design and delivery. Nat Rev Drug Discov. 2010;9:29–42.CrossRefPubMed Rajendran L, Knolker H‑J, Simons K. Subcellular targeting strategies for drug design and delivery. Nat Rev Drug Discov. 2010;9:29–42.CrossRefPubMed
82.
Zurück zum Zitat Prabha S, Zhou W‑Z, Panyam J, Labhasetwar V. Size-dependency of nanoparticle-mediated gene transfection: studies with fractionated nanoparticles. Int J Pharm. 2002;244:105–115.CrossRefPubMed Prabha S, Zhou W‑Z, Panyam J, Labhasetwar V. Size-dependency of nanoparticle-mediated gene transfection: studies with fractionated nanoparticles. Int J Pharm. 2002;244:105–115.CrossRefPubMed
83.
Zurück zum Zitat Lechardeur D, Verkman AS, Lukacs GL. Intracellular routing of plasmid DNA during non-viral gene transfer. Adv Drug Deliv Rev. 2005;57:755–767.CrossRefPubMed Lechardeur D, Verkman AS, Lukacs GL. Intracellular routing of plasmid DNA during non-viral gene transfer. Adv Drug Deliv Rev. 2005;57:755–767.CrossRefPubMed
84.
Zurück zum Zitat Shim MS, Kwon YJ. Stimuli-responsive polymers and nanomaterials for gene delivery and imaging applications. Adv Drug Deliv Rev. 2012;64:1046–1059.CrossRefPubMed Shim MS, Kwon YJ. Stimuli-responsive polymers and nanomaterials for gene delivery and imaging applications. Adv Drug Deliv Rev. 2012;64:1046–1059.CrossRefPubMed
86.
Zurück zum Zitat Boussif O, Lezoualc’h F, Zanta MA, Mergny MD, Scherman D, Demeneix B, et al. A versatile vector for gene and oligonucleotide transfer into cells in culture and in vivo: polyethylenimine. Proc Natl Acad Sci USA. 1995;92:7297–7301.CrossRefPubMedPubMedCentral Boussif O, Lezoualc’h F, Zanta MA, Mergny MD, Scherman D, Demeneix B, et al. A versatile vector for gene and oligonucleotide transfer into cells in culture and in vivo: polyethylenimine. Proc Natl Acad Sci USA. 1995;92:7297–7301.CrossRefPubMedPubMedCentral
87.
Zurück zum Zitat Midoux P, Monsigny M. Efficient gene transfer by histidylated polylysine/pDNA complexes. Bioconjug Chem. 1999;10:406–411.CrossRefPubMed Midoux P, Monsigny M. Efficient gene transfer by histidylated polylysine/pDNA complexes. Bioconjug Chem. 1999;10:406–411.CrossRefPubMed
88.
Zurück zum Zitat John JV, Johnson RP, Heo MS, Moon BK, Byeon SJ, Kim I. Polymer-Block-Polypeptides and Polymer-Conjugated Hybrid Materials as Stimuli-Responsive Nanocarriers for Biomedical Applications. J Biomed Nanotechnol. 2015;11:1–39.CrossRefPubMed John JV, Johnson RP, Heo MS, Moon BK, Byeon SJ, Kim I. Polymer-Block-Polypeptides and Polymer-Conjugated Hybrid Materials as Stimuli-Responsive Nanocarriers for Biomedical Applications. J Biomed Nanotechnol. 2015;11:1–39.CrossRefPubMed
89.
Zurück zum Zitat Li W, Nicol F, Szoka FCJ. GALA: a designed synthetic pH-responsive amphipathic peptide with applications in drug and gene delivery. Adv Drug Deliv Rev. 2004;56:967–985.CrossRefPubMed Li W, Nicol F, Szoka FCJ. GALA: a designed synthetic pH-responsive amphipathic peptide with applications in drug and gene delivery. Adv Drug Deliv Rev. 2004;56:967–985.CrossRefPubMed
90.
Zurück zum Zitat Carmona S, Jorgensen MR, Kolli S, Crowther C, Salazar FH, Marion PL, et al. Controlling HBV replication in vivo by intravenous administration of triggered PEGylated siRNA-nanoparticles. Mol Pharm. 2009;6:706–717.CrossRefPubMed Carmona S, Jorgensen MR, Kolli S, Crowther C, Salazar FH, Marion PL, et al. Controlling HBV replication in vivo by intravenous administration of triggered PEGylated siRNA-nanoparticles. Mol Pharm. 2009;6:706–717.CrossRefPubMed
92.
Zurück zum Zitat Xiang S, Tong H, Shi Q, Fernandes JC, Jin T, Dai K, et al. Uptake mechanisms of non-viral gene delivery. J Control Release. 2012;158:371–378.CrossRefPubMed Xiang S, Tong H, Shi Q, Fernandes JC, Jin T, Dai K, et al. Uptake mechanisms of non-viral gene delivery. J Control Release. 2012;158:371–378.CrossRefPubMed
93.
Zurück zum Zitat Li JJ, Hartono D, Ong C‑N, Bay B‑H, L‑YL Y. Autophagy and oxidative stress associated with gold nanoparticles. Biomaterials. 2010;31:5996–6003.CrossRefPubMed Li JJ, Hartono D, Ong C‑N, Bay B‑H, L‑YL Y. Autophagy and oxidative stress associated with gold nanoparticles. Biomaterials. 2010;31:5996–6003.CrossRefPubMed
94.
Zurück zum Zitat Sramkova M, Parente L, Wigand T, Aye M‑P, Shitara A, Weigert R. Polyethylenimine-mediated expression of transgenes in the acinar cells of rats salivary glands in vivo. Front Cell Dev Biol. 2014;2:74.PubMedPubMedCentral Sramkova M, Parente L, Wigand T, Aye M‑P, Shitara A, Weigert R. Polyethylenimine-mediated expression of transgenes in the acinar cells of rats salivary glands in vivo. Front Cell Dev Biol. 2014;2:74.PubMedPubMedCentral
95.
Zurück zum Zitat Wasungu L, Hoekstra D. Cationic lipids, lipoplexes and intracellular delivery of genes. J Control Release. 2006;116:255–264.CrossRefPubMed Wasungu L, Hoekstra D. Cationic lipids, lipoplexes and intracellular delivery of genes. J Control Release. 2006;116:255–264.CrossRefPubMed
96.
Zurück zum Zitat Ooya T, Choi HS, Yamashita A, Yui N, Sugaya Y, Kano A, et al. Biocleavable polyrotaxane-plasmid DNA polyplex for enhanced gene delivery. J Am Chem Soc. 2006;128:3852–3853.CrossRefPubMed Ooya T, Choi HS, Yamashita A, Yui N, Sugaya Y, Kano A, et al. Biocleavable polyrotaxane-plasmid DNA polyplex for enhanced gene delivery. J Am Chem Soc. 2006;128:3852–3853.CrossRefPubMed
97.
Zurück zum Zitat Fasbender A, Zabner J, Zeiher BG, Welsh MJ. A low rate of cell proliferation and reduced DNA uptake limit cationic lipid-mediated gene transfer to primary cultures of ciliated human airway epithelia. Gene Ther. 1997;4:1173–1180.CrossRefPubMed Fasbender A, Zabner J, Zeiher BG, Welsh MJ. A low rate of cell proliferation and reduced DNA uptake limit cationic lipid-mediated gene transfer to primary cultures of ciliated human airway epithelia. Gene Ther. 1997;4:1173–1180.CrossRefPubMed
98.
Zurück zum Zitat Brunner S, Sauer T, Carotta S, Cotten M, Saltik M, Wagner E. Cell cycle dependence of gene transfer by lipoplex, polyplex and recombinant adenovirus. Gene Ther. 2000;7:401–407.CrossRefPubMed Brunner S, Sauer T, Carotta S, Cotten M, Saltik M, Wagner E. Cell cycle dependence of gene transfer by lipoplex, polyplex and recombinant adenovirus. Gene Ther. 2000;7:401–407.CrossRefPubMed
99.
Zurück zum Zitat van der Aa MAEM, Mastrobattista E, Oosting RS, Hennink WE, Koning GA, Crommelin DJA. The nuclear pore complex: the gateway to successful nonviral gene delivery. Pharm Res. 2006;23:447–459.CrossRefPubMed van der Aa MAEM, Mastrobattista E, Oosting RS, Hennink WE, Koning GA, Crommelin DJA. The nuclear pore complex: the gateway to successful nonviral gene delivery. Pharm Res. 2006;23:447–459.CrossRefPubMed
100.
Zurück zum Zitat Cartier R, Reszka R. Utilization of synthetic peptides containing nuclear localization signals for nonviral gene transfer systems. Gene Ther. 2002;9:157–167.CrossRefPubMed Cartier R, Reszka R. Utilization of synthetic peptides containing nuclear localization signals for nonviral gene transfer systems. Gene Ther. 2002;9:157–167.CrossRefPubMed
Metadaten
Titel
Endocytosis in gene therapy with non-viral vectors
verfasst von
Aritz Perez Ruiz de Garibay
Publikationsdatum
01.05.2016
Verlag
Springer Vienna
Erschienen in
Wiener Medizinische Wochenschrift / Ausgabe 7-8/2016
Print ISSN: 0043-5341
Elektronische ISSN: 1563-258X
DOI
https://doi.org/10.1007/s10354-016-0450-5

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