The DOI matches its Crossref record; 148 of the 151 references it cites were found in a registry or an index.
Endosomal escape pathways for delivery of biologicals
Open accessAbstract
Despite continuous improvements in delivery systems, the development of methods for efficient and specific delivery of targeted therapeutic agents still remains an issue in biological treatments such as protein and gene therapy. The endocytic pathway is the major uptake mechanism of cells and any biological agents, such as DNA, siRNA and proteins. These agents become entrapped in endosomes and are degraded by specific enzymes in the lysosome. Thus, a limiting step in achieving an effective biological based therapy is to facilitate the endosomal escape and ensure cytosolic delivery of the therapeutics. Bacteria and viruses are pathogens which use different mechanisms to penetrate the membranes of their target cells and escape the endosomal pathway. Different mechanisms such as pore formation in the endosomal membrane, pH-buffering effect of protonable groups and fusion into the lipid bilayer of endosomes have been proposed to facilitate the endosomal escape. Several viral and bacterial proteins have been identified that are involved in this process. In addition, chemical agents and photochemical methods to rupture the endosomal membrane have been described. New synthetic biomimetic peptides and polymers with high efficacy in facilitating the endosomal escape, low pathogenicity and toxicity have been developed. Each strategy has different characteristics and challenges for designing the best agents and techniques to facilitate the endosomal escape are ongoing. In this review, several mechanisms and agents which are involved in endosomal escape are introduced.
Overview
Integrity signals
Registry
Cites
Statistics
Verification
Claims the paper makes
Self-check
Percentages, sums and reported differences re-computed from the paper’s own numbers.
The text we found for this paper looks like another document, so the self-check wasn’t run.
Citations
Cites
Boussif, O., Lezoualc’h, F., Zanta, M. A., Djavaheri‐Mergny, M., Scherman, D., DEMENEIX, B. A., & Behr, J. (1995) · Proceedings of the National Academy of Sciences · doi:10.1073/pnas.92.16.7297 · Cited by 6,256
Jenssen, H., Hamill, P., & Hancock, R. E. W. (2006) · Clinical Microbiology Reviews · doi:10.1128/cmr.00056-05 · Cited by 2,605
ACIDIFICATION OF THE ENDOCYTIC AND EXOCYTIC PATHWAYS
Mellman, I., Fuchs, R., & Helenius, A. (1986) · Annual Review of Biochemistry · doi:10.1146/annurev.bi.55.070186.003311 · Cited by 2,045
Lewin, M., Carlesso, N., Tung, C., Tang, X. S., Cory, D. G., Scadden, D. T., & Weissleder, R. (2000) · Nature Biotechnology · doi:10.1038/74464 · Cited by 1,716
Viral vectors for gene therapy: the art of turning infectious agents into vehicles of therapeutics
Kay, M., Glorioso, J., & Naldini, L. (2001) · Nature Medicine · doi:10.1038/83324 · Cited by 1,444
THE STRUCTURE AND FUNCTION OF THE HEMAGGLUTININ MEMBRANE GLYCOPROTEIN OF INFLUENZA VIRUS
Wiley, D. C., & Skehel, J. J. (1987) · Annual Review of Biochemistry · doi:10.1146/annurev.bi.56.070187.002053 · Cited by 1,413
Cell Internalization of the Third Helix of the Antennapedia Homeodomain Is Receptor-independent
Derossi, D., Calvet, S., Trembleau, A., Brunissen, A., Chassaing, G., & Prochiantz, A. (1996) · Journal of Biological Chemistry · doi:10.1074/jbc.271.30.18188 · Cited by 1,073
The actions of melittin on membranes
Dempsey, C. E. (1990) · Biochimica et Biophysica Acta (BBA) - Reviews on Biomembranes · doi:10.1016/0304-4157(90)90006-x · Cited by 852
Stepwise dismantling of adenovirus 2 during entry into cells
Greber, U. F., Willetts, M., Webster, P. C., & Helenius, A. (1993) · Cell · doi:10.1016/0092-8674(93)90382-z · Cited by 811
Nonviral Gene Delivery: Principle, Limitations, and Recent Progress
Al-Dosari, M. S., & Gao, X. (2009) · The AAPS Journal · doi:10.1208/s12248-009-9143-y · Cited by 706
Plank, C., Oberhauser, B., Mechtler, K., Koch, C., & Wagner, E. (1994) · Journal of Biological Chemistry · doi:10.1016/s0021-9258(18)99963-1 · Cited by 666
Wagner, E., Plank, C., Zatloukal, K., Cotten, M. L., & Birnstiel, M. L. (1992) · Proceedings of the National Academy of Sciences · doi:10.1073/pnas.89.17.7934 · Cited by 657
A triploblast origin for Myxozoa?
Anderson, C. L., Canning, E. U., & Okamura, B. (1998) · Nature · doi:10.1038/32801 · Cited by 654
Yang, Y., Ertl, H. C. J., & Wilson, J. M. (1994) · Immunity · doi:10.1016/1074-7613(94)90074-4 · Cited by 612
Marsh, M., & Helenius, A. (1989) · Advances in virus research · doi:10.1016/s0065-3527(08)60583-7 · Cited by 602
Nonviral Vectors in the New Millennium: Delivery Barriers in Gene Transfer
Nishikawa, M., & Huang, L. (2001) · Human Gene Therapy · doi:10.1089/104303401750195836 · Cited by 574
Efficient Gene Transfer by Histidylated Polylysine/pDNA Complexes
Midoux, P., & Monsigny, M. L. P. (1999) · Bioconjugate Chemistry · doi:10.1021/bc9801070 · Cited by 513
Simeoni, F. (2003) · Nucleic Acids Research · doi:10.1093/nar/gkg385 · Cited by 481
Cholesterol-Dependent Cytolysins, a Family of Versatile Pore-Forming Toxins
Tweten, R. K. (2005) · Infection and Immunity · doi:10.1128/iai.73.10.6199-6209.2005 · Cited by 464
Wyman, T. B., Nicol, F., Zelphati, O., Scaria, P. V., Plank, C., & Szoka, F. C. (1997) · Biochemistry · doi:10.1021/bi9618474 · Cited by 454
Photochemical internalization: a novel technology for delivery of macromolecules into cytosol.
Berg, K., Selbo, P. K., Prasmickaite, L., Tjelle, T. E., Sandvig, K., Moan, J. E., Gaudernack, G., Fodstad, Ø., Kjølsrud, S., Anholt, H., et al. (1999) · PubMed · Cited by 423
Meier, O. C., & Greber, U. F. (2004) · The Journal of Gene Medicine · doi:10.1002/jgm.553 · Cited by 421
Cell transfection in vitro and in vivo with nontoxic TAT peptide-liposome–DNA complexes
Torchilin, V. P., Levchenko, T. S., Rammohan, R., Volodina, N., Papahadjopoulos‐Sternberg, B., & D’Souza, G. G. M. (2003) · Proceedings of the National Academy of Sciences · doi:10.1073/pnas.0435906100 · Cited by 419
Ribosome-inactivating proteins
Stirpe, F. (2004) · Toxicon · doi:10.1016/j.toxicon.2004.05.004 · Cited by 389
Mechanisms of pathogen entry through the endosomal compartments
Grüenberg, J., & van der Goot, F. G. (2006) · Nature Reviews Molecular Cell Biology · doi:10.1038/nrm1959 · Cited by 375
Poliovirus Cell Entry: Common Structural Themes in Viral Cell Entry Pathways
Hogle, J. M. (2002) · Annual Review of Microbiology · doi:10.1146/annurev.micro.56.012302.160757 · Cited by 352
Gene Therapy: Promises and Problems
Pfeifer, A., & Verma, I. M. (2001) · Annual Review of Genomics and Human Genetics · doi:10.1146/annurev.genom.2.1.177 · Cited by 345
Molecular Mechanism of Peptide-Induced Pores in Membranes
Huang, H. W., Chen, F.-Y., & Lee, M.-T. (2004) · Physical Review Letters · doi:10.1103/physrevlett.92.198304 · Cited by 335
Delivery of short interfering RNA using endosomolytic cell‐penetrating peptides
Lundberg, P., Andaloussi, S. E., Sütlü, T., Johansson, H. J., & Langel, Ü. (2007) · The FASEB Journal · doi:10.1096/fj.06-6502com · Cited by 331
Novel Bioreducible Poly(amido amine)s for Highly Efficient Gene Delivery
Lin, C., Zhong, Z., Lok, M. C., Jiang, X., Hennink, W. E., Feijén, J., & Engbersen, J. F. J. (2006) · Bioconjugate Chemistry · doi:10.1021/bc060200l · Cited by 311
Chernomordik, L., Melikyan, G. B., & Chizmadzhev, Y. A. (1987) · Biochimica et Biophysica Acta (BBA) - Reviews on Biomembranes · doi:10.1016/0304-4157(87)90016-5 · Cited by 308
Mechanism of leakage of phospholipid vesicle contents induced by the peptide GALA
Parente, R. A., Nir, S., & Szoka, F. C. (1990) · Biochemistry · doi:10.1021/bi00489a031 · Cited by 301
Lo, S. L., & Wang, S. (2008) · Biomaterials · doi:10.1016/j.biomaterials.2008.01.031 · Cited by 290
Eguchi, A., Akuta, T., Okuyama, H., Senda, T., Yokoi, H., Inokuchi, H., Fujita, S., Hayakawa, T., Takeda, K., Hasegawa, M., et al. (2001) · Journal of Biological Chemistry · doi:10.1074/jbc.m010625200 · Cited by 289
Douar, A.-M., Poulard, K., Stockholm, D., & Danos, O. (2001) · Journal of Virology · doi:10.1128/jvi.75.4.1824-1833.2001 · Cited by 282
Glomski, I. J., Gedde, M. M., Tsang, A. W., Swanson, J. A., & Portnoy, D. A. (2002) · The Journal of Cell Biology · doi:10.1083/jcb.200201081 · Cited by 281
Rudolph, C., Plank, C., Lausier, J., Schillinger, U., Müller, R. H., & Rosenecker, J. (2003) · Journal of Biological Chemistry · doi:10.1074/jbc.m211891200 · Cited by 275
Funhoff, A. M., van Nostrum, C. F., Koning, G. A., Schuurmans-Nieuwenbroek, N. M. E., Crommelin, D. J. A., & Hennink, W. E. (2003) · Biomacromolecules · doi:10.1021/bm034041+ · Cited by 272
Kakudo, T., Chaki, S., Futaki, S., Nakase, I., Akaji, K., Kawakami, T., Maruyama, K., Kamiya, H., & Harashima, H. (2004) · Biochemistry · doi:10.1021/bi035802w · Cited by 269
Meyer, M., Philipp, A. B., Oskuee, R. K., Schmidt, C., & Wagner, E. (2008) · Journal of the American Chemical Society · doi:10.1021/ja710344v · Cited by 263
Lear, J. D., & DeGrado, W. F. (1987) · Journal of Biological Chemistry · doi:10.1016/s0021-9258(18)48270-1 · Cited by 258
A novel DNA-peptide complex for efficient gene transfer and expression in mammalian cells.
Gottschalk, S. M., Sparrow, J. T., Hauer, J., Mims, M. P., Leland, F. E., Woo, S. L. C., & Smith, L. C. (1996) · PubMed · Cited by 252
A PEST-Like Sequence in Listeriolysin O Essential for Listeria monocytogenes Pathogenicity
Decatur, A. L., & Portnoy, D. A. (2000) · Science · doi:10.1126/science.290.5493.992 · Cited by 239
Wickham, T. (2000) · Gene Therapy · doi:10.1038/sj.gt.3301115 · Cited by 236
Leopold, P. L., Ferris, B., Grinberg, I., Worgall, S., Hackett, N. R., & Crystal, R. G. (1998) · Human Gene Therapy · doi:10.1089/hum.1998.9.3-367 · Cited by 231
Kichler, A., Leborgne, C., März, J., Danos, O., & Bechinger, B. (2003) · Proceedings of the National Academy of Sciences · doi:10.1073/pnas.0337677100 · Cited by 229
Ogris, M., Carlisle, R. C., Bettinger, T., & Seymour, L. W. (2001) · Journal of Biological Chemistry · doi:10.1074/jbc.m108331200 · Cited by 226
Bettinger, T. (2001) · Nucleic Acids Research · doi:10.1093/nar/29.18.3882 · Cited by 224
Vorburger, S. A., & Hunt, K. K. (2002) · The Oncologist · doi:10.1634/theoncologist.7-1-46 · Cited by 220
Browne, K. A., Blink, E. J., Sutton, V. R., Froelich, C. J., Jans, D. A., & Trapani, J. A. (1999) · Molecular and Cellular Biology · doi:10.1128/mcb.19.12.8604 · Cited by 208
Degradable-Brushed pHEMA–pDMAEMA Synthesized via ATRP and Click Chemistry for Gene Delivery
Jiang, X., Lok, M. C., & Hennink, W. E. (2007) · Bioconjugate Chemistry · doi:10.1021/bc0701186 · Cited by 194
Kämper, N., Day, P. M., Nowak, T., Selinka, H., Florin, L., Bolscher, J. G. M., Hilbig, L., Schiller, J. T., & Sapp, M. J. (2005) · Journal of Virology · doi:10.1128/jvi.80.2.759-768.2006 · Cited by 194
Cell penetrating peptide conjugates of steric block oligonucleotides
Lebleu, B., Moulton, H. M., Abes, R., Ivanova, G. D., Abes, S., Stein, D. A., Iversen, P. L., Arzumanov, A. A., & Gait, M. J. (2007) · Advanced Drug Delivery Reviews · doi:10.1016/j.addr.2007.09.002 · Cited by 183
A novel potent strategy for gene delivery using a single peptide vector as a carrier
Morris, M. C., Chaloin, L., Méry, J., Heitz, F., & Divita, G. (1999) · Nucleic Acids Research · doi:10.1093/nar/27.17.3510 · Cited by 182
Single cell optical transfection
Stevenson, D. J., Gunn‐Moore, F. J., Campbell, P. A., & Dholakia, K. (2010) · Journal of The Royal Society Interface · doi:10.1098/rsif.2009.0463 · Cited by 177
Parente, R. A., Nir, S., & Szoka, F. C. (1988) · Journal of Biological Chemistry · doi:10.1016/s0021-9258(18)68843-x · Cited by 175
Cell killing by lysosomotropic detergents.
Miller, D. K., Griffiths, E., Lenard, J., & Firestone, R. A. (1983) · The Journal of Cell Biology · doi:10.1083/jcb.97.6.1841 · Cited by 174
Cytotoxic ribosome-inactivating lectins from plants
Hartley, M. R., & Lord, J. M. (2004) · Biochimica et Biophysica Acta (BBA) - Proteins and Proteomics · doi:10.1016/j.bbapap.2004.06.004 · Cited by 173
Mastrobattista, E., Koning, G. A., van Bloois, L., Filipe, A. C. S., Jiskoot, W., & Storm, G. (2002) · Journal of Biological Chemistry · doi:10.1074/jbc.m200429200 · Cited by 173
Self-citationFernández‐Carneado, J., Kogan, M. J., Castel, S., & Giralt, E. (2004) · Angewandte Chemie International Edition · doi:10.1002/anie.200352540 · Cited by 170
A pH-Sensitive Polymer That Enhances Cationic Lipid-Mediated Gene Transfer
Cheung, C., Murthy, N., Stayton, P. S., & Hoffman, A. S. (2001) · Bioconjugate Chemistry · doi:10.1021/bc0100408 · Cited by 164
Simões, S., Slepushkin, V., Pires, P., Gaspar, R. S., de Lima, M. C. P., & Düzgüneş, N. (1999) · Gene Therapy · doi:10.1038/sj.gt.3301015 · Cited by 161
Moreira, C., Oliveira, H., Pires, L. R., Simões, S., Barbosa, M. A., & Pêgo, A. P. (2009) · Acta Biomaterialia · doi:10.1016/j.actbio.2009.04.021 · Cited by 160
Meier, O. C., & Greber, U. F. (2003) · The Journal of Gene Medicine · doi:10.1002/jgm.409 · Cited by 160
Arginine-rich cell penetrating peptides: from endosomal uptake to nuclear delivery
Melikov, K., & Chernomordik, L. (2005) · Cellular and Molecular Life Sciences · doi:10.1007/s00018-005-5293-y · Cited by 159
Efficient splicing correction by PNA conjugation to an R6-Penetratin delivery peptide
Abes, S., Turner, J. J., Ivanova, G. D., Owen, D., Williams, D., Arzumanov, A. A., Clair, P., Gait, M. J., & Lebleu, B. (2007) · Nucleic Acids Research · doi:10.1093/nar/gkm418 · Cited by 157
Fusogenic peptides enhance endosomal escape improving siRNA-induced silencing of oncogenes
Oliveira, S., VANROOY, I., Kranenburg, O., Storm, G., & Schiffelers, R. M. (2006) · International Journal of Pharmaceutics · doi:10.1016/j.ijpharm.2006.11.050 · Cited by 155
Self-citationTransfer of monoclonal antibodies into mammalian cells by electroporation
Chakrabarti, R., Wylie, D. E., & Schuster, S. M. (1989) · Journal of Biological Chemistry · doi:10.1016/s0021-9258(19)84857-3 · Cited by 148
Hansen, J. J., Qing, K., Kwon, H., Mah, C. S., & Srivastava, A. (2000) · Journal of Virology · doi:10.1128/jvi.74.2.992-996.2000 · Cited by 147
Induction of splice correction by cell‐penetrating peptide nucleic acids
Andaloussi, S. E., Johansson, H. J., Lundberg, P., & Langel, Ü. (2006) · The Journal of Gene Medicine · doi:10.1002/jgm.950 · Cited by 141
Prchla, E., Plank, C., Wagner, E., Blaas, D., & Fuchs, R. (1995) · The Journal of Cell Biology · doi:10.1083/jcb.131.1.111 · Cited by 140
siRNA applications in nanomedicine
Tokatlian, T., & Segura, T. (2010) · Wiley Interdisciplinary Reviews Nanomedicine and Nanobiotechnology · doi:10.1002/wnan.81 · Cited by 138
Foerg, C., Ziegler, U., Fernández‐Carneado, J., Giralt, E., Rennert, R. C., Beck‐Sickinger, A. G., & Merkle, H. P. (2004) · Biochemistry · doi:10.1021/bi048330+ · Cited by 133
Boeckle, S., Fahrmeir, J., Röedl, W., Ogris, M., & Wagner, E. (2006) · Journal of Controlled Release · doi:10.1016/j.jconrel.2006.02.002 · Cited by 132
Effect of chemical functionalities in poly(amido amine)s for non-viral gene transfection
Lin, C., & Engbersen, J. F. J. (2008) · Journal of Controlled Release · doi:10.1016/j.jconrel.2008.06.022 · Cited by 132
Ilan, Y., Prakash, R., Davidson, A., Jona, Droguett, G., Horwitz, M. S., Chowdhury, N. R., & Chowdhury, J. R. (1997) · Journal of Clinical Investigation · doi:10.1172/jci119238 · Cited by 132
Pathways followed by protein toxins into cells
Sandvig, K., Spilsberg, B., Lauvrak, S. U., Torgersen, M. L., Iversen, T., & van Deurs, B. O. (2004) · International Journal of Medical Microbiology · doi:10.1078/1438-4221-00294 · Cited by 130
Fielden, M. L., Perrin, C., Kremer, A., Bergsma, M., Stuart, M. C. A., Camilleri, P., & Engberts, J. B. F. N. (2001) · European Journal of Biochemistry · doi:10.1046/j.1432-1327.2001.01995.x · Cited by 128
Target Cell-specific DNA Transfer Mediated by a Chimeric Multidomain Protein
Fominaya, J. M., & Wels, W. S. (1996) · Journal of Biological Chemistry · doi:10.1074/jbc.271.18.10560 · Cited by 126
Theoretical and functional analysis of the SIV fusion peptide.
Horth, M., Lambrecht, B., Khim, M. C. L., Bex, F., Thiriart, C., Ruysschaert, J., Burny, A., & Brasseur, R. (1991) · The EMBO Journal · doi:10.1002/j.1460-2075.1991.tb07823.x · Cited by 125
Lee, H., Jeong, J. H., & Park, T. G. (2001) · Journal of Controlled Release · doi:10.1016/s0168-3659(01)00426-6 · Cited by 125
Poly(3-guanidinopropyl methacrylate): A Novel Cationic Polymer for Gene Delivery
Funhoff, A. M., van Nostrum, C. F., Lok, M. C., Fretz, M. M., Crommelin, D. J. A., & Hennink, W. E. (2004) · Bioconjugate Chemistry · doi:10.1021/bc049864q · Cited by 118
Sasaki, K., Kogure, K., Chaki, S., Nakamura, Y., Moriguchi, R., Hamada, H., Danev, R., Nagayama, K., Futaki, S., & Harashima, H. (2008) · Analytical and Bioanalytical Chemistry · doi:10.1007/s00216-008-2012-1 · Cited by 115
Wang, X.-L., Ramusovic, S., Nguyen, T. D., & Lu, Z. (2007) · Bioconjugate Chemistry · doi:10.1021/bc700285q · Cited by 115
Galanis, E., Vile, R. G., & Russell, S. J. (2001) · Critical Reviews in Oncology/Hematology · doi:10.1016/s1040-8428(01)00103-2 · Cited by 111
Magzoub, M. M., Pramanik, A., & Gräslund, A. (2005) · Biochemistry · doi:10.1021/bi051356w · Cited by 110
Defective lysosomal targeting of activated fibroblast growth factor receptor 3 in achondroplasia
Cho, J. Y., Guo, C., Torello, M., Lunstrum, G. P., Iwata, T., Deng, C., & Horton, W. A. (2003) · Proceedings of the National Academy of Sciences · doi:10.1073/pnas.2237184100 · Cited by 110
del Pozo‐Rodríguez, A., Pujals, S., Delgado, D., Solinís, M. Á., Rodríguez‐Gascón, A., Giralt, E., & Pedraz, J. L. (2008) · Journal of Controlled Release · doi:10.1016/j.jconrel.2008.09.004 · Cited by 106
N-terminal peptides from unprocessed prion proteins enter cells by macropinocytosis
Magzoub, M. M., Sandgren, S., Lundberg, P., Oglęcka, K., Lilja, J., Wittrup, A., Eriksson, L. E. G., Langel, Ü., Belting, M., & Gräslund, A. (2006) · Biochemical and Biophysical Research Communications · doi:10.1016/j.bbrc.2006.07.065 · Cited by 105
Oliveira, S., Fretz, M. M., Høgset, A., Storm, G., & Schiffelers, R. M. (2007) · Biochimica et Biophysica Acta (BBA) - Biomembranes · doi:10.1016/j.bbamem.2007.01.013 · Cited by 104
Self-citationKwon, E. J., Bergen, J. M., & Pun, S. H. (2008) · Bioconjugate Chemistry · doi:10.1021/bc700448h · Cited by 101
Reversal of doxorubicin resistance in breast cancer cells by photochemical internalization
Lou, P., Lai, P., Shieh, M., MacRobert, A. J., Berg, K., & Bown, S. G. (2006) · International Journal of Cancer · doi:10.1002/ijc.22098 · Cited by 100
Legendre, J., & Szoka, F. C. (1993) · Proceedings of the National Academy of Sciences · doi:10.1073/pnas.90.3.893 · Cited by 98
Dynamic optimization of hybridoma growth in a fed-batch bioreactor
Dhir, S., Morrow, K. J., Rhinehart, R. R., & Wiesner, T. F. (2000) · Biotechnology and Bioengineering · doi:10.1002/(sici)1097-0290(20000120)67:2 · Cited by 96
Cell membrane translocation of the N-terminal (1-28) part of the prion protein.
Lundberg, P., Magzoub, M., Lindberg, M., Hällbrink, M., Jarvet, J., Eriksson, L., Langel, Ü., & Gräslund, A. (2002) · Biochemical and Biophysical Research Communications - BBRC · doi:10.1016/s0006-291x(02)02595-0 · Cited by 94
A molecular code dictates sequence‐specific DNA recognition by homeodomains.
Damante, G., Pellizzari, L., Esposito, G., Fogolari, F., Viglino, P., Fabbro, D., Tell, G., Formisano, S., & Lauro, R. D. (1996) · The EMBO Journal · doi:10.1002/j.1460-2075.1996.tb00879.x · Cited by 93
Vago, R., Marsden, C. J., Lord, J. M., Ippoliti, R., Flavell, D. J., Flavell, S. U., Ceriotti, A., & Fabbrini, M. S. (2005) · FEBS Journal · doi:10.1111/j.1742-4658.2005.04908.x · Cited by 91
Arnheiter, H., & Haller, O. (1988) · The EMBO Journal · doi:10.1002/j.1460-2075.1988.tb02946.x · Cited by 91
Evaluation of Different Photosensitizers for Use in Photochemical Gene Transfection¶
Prasmickaite, L., Høgset, A., & Berg, K. (2001) · Photochemistry and Photobiology · doi:10.1562/0031-8655(2001)0730388eodpfu2.0.co2 · Cited by 87
Polymer Side-Chain Degradation as a Tool to Control the Destabilization of Polyplexes
Funhoff, A. M., van Nostrum, C. F., Janssen, A. P. C. A., Fens, M. H. A. M., Crommelin, D. J. A., & Hennink, W. E. (2004) · Pharmaceutical Research · doi:10.1023/b:pham.0000012165.68765.e6 · Cited by 86
Mandal, M., & Lee, K. (2002) · Biochimica et Biophysica Acta (BBA) - Biomembranes · doi:10.1016/s0005-2736(02)00368-1 · Cited by 82
Teter, K., & Holmes, R. K. (2002) · Infection and Immunity · doi:10.1128/iai.70.11.6172-6179.2002 · Cited by 82
Endoh, T., Sisido, M., & Ohtsuki, T. (2008) · Bioconjugate Chemistry · doi:10.1021/bc800020n · Cited by 81
Design of “Smart” polymers that can direct intracellular drug delivery
Hoffman, A. S., Stayton, P. S., Press, O. W., Murthy, N., Lackey, C. A., Cheung, C., Black, F. E., Campbell, J. S., Fausto, N., Kyriakides, T. R., et al. (2002) · Polymers for Advanced Technologies · doi:10.1002/pat.232 · Cited by 80
Cabral, H., Nakanishi, M., Kumagai, M., Jang, W., Nishiyama, N., & Kataoka, K. (2008) · Pharmaceutical Research · doi:10.1007/s11095-008-9712-2 · Cited by 79
Saito, G., Amidon, G. L., & Lee, K.-D. (2003) · Gene Therapy · doi:10.1038/sj.gt.3301859 · Cited by 77
Day, P. J., Pinheiro, T. J. T., Roberts, L. M., & Lord, J. M. (2002) · Biochemistry · doi:10.1021/bi012012i · Cited by 76
Conditional gene targeting for cancer gene therapy
Haviv, Y. S., & Curiel, D. T. (2001) · Advanced Drug Delivery Reviews · doi:10.1016/s0169-409x(01)00225-3 · Cited by 75
On the Gene Delivery Efficacies of pH-Sensitive Cationic Lipids via Endosomal Protonation
Singh, R. S., Gonçalves, C., Sandrin, P., Pichon, C., Midoux, P., & Chaudhuri, A. (2004) · Chemistry & Biology · doi:10.1016/j.chembiol.2004.03.026 · Cited by 74
Futaki, S., Masui, Y., Nakase, I., Sugiura, Y., Nakamura, T., Kogure, K., & Harashima, H. (2005) · The Journal of Gene Medicine · doi:10.1002/jgm.796 · Cited by 72
Jia, L., Zhang, L.-H., Yu, C.-J., Zhao, J., Xu, Y., Gui, J.-H., Jin, M., Ji, Z., Wen, W.-H., Wang, C.-J., et al. (2003) · PubMed · Cited by 69
Maiolo, J. R., Ottinger, E. A., & Ferrer, M. (2004) · Journal of the American Chemical Society · doi:10.1021/ja044867z · Cited by 67
A composite gene delivery system consisting of polyethylenimine and an amphipathic peptide KALA
Min, S., Lee, D. C., Lim, M. J., Park, H. S., Kim, D., Cho, C., Yoon, D. Y., & Yeom, Y. I. (2006) · The Journal of Gene Medicine · doi:10.1002/jgm.973 · Cited by 63
Kimura, T., & Ohyama, A. (1988) · Journal of General Virology · doi:10.1099/0022-1317-69-6-1247 · Cited by 62
Characterization of the gene transfer process mediated by histidine-rich peptides
Kichler, A., Leborgne, C., Danos, O., & Bechinger, B. (2006) · Journal of Molecular Medicine · doi:10.1007/s00109-006-0119-4 · Cited by 62
Kakimoto, S., Hamada, T., Komatsu, Y., Takagi, M., Tanabe, T., Azuma, H., Shinkai, S., & Nagasaki, T. (2008) · Biomaterials · doi:10.1016/j.biomaterials.2008.09.042 · Cited by 60
Abes, R., Arzumanov, A. A., Moulton, H. M., Abes, S., Ivanova, G. D., Gait, M. J., Iversen, P. L., & Lebleu, B. (2008) · Journal of Peptide Science · doi:10.1002/psc.979 · Cited by 59
Poly(amidoamine)-mediated intracytoplasmic delivery of ricin A-chain and gelonin
Pattrick, N. G., Richardson, S. C. W., Casolaro, M., Ferruti, P., & Duncan, R. (2001) · Journal of Controlled Release · doi:10.1016/s0168-3659(01)00476-x · Cited by 58
Roy, K., Ghosn, B., & Kasturi, S. P. (2008) · Current Topics in Medicinal Chemistry · doi:10.2174/156802608783790947 · Cited by 58
Protein Transduction Domains and their Utility in Gene Therapy
Beerens, A.-S., Hadithy, A. A., Rots, M. G., & Haisma, H. J. (2003) · Current Gene Therapy · doi:10.2174/1566523034578258 · Cited by 57
Self-citationFoerg, C., Ziegler, U., Fernández‐Carneado, J., Giralt, E., & Merkle, H. P. (2007) · Pharmaceutical Research · doi:10.1007/s11095-006-9212-1 · Cited by 55
How bacterial protein toxins enter cells: the role of partial unfolding in membrane translocation
London, E. (1992) · Molecular Microbiology · doi:10.1111/j.1365-2958.1992.tb02195.x · Cited by 54
Bruell, D., Stöcker, M., Hühn, M., Redding, N., Kupper, M. B., Schumacher, P., Paetz, A., Bruns, C. J., Haisma, H. J., Fischer, R., et al. (2003) · International Journal of Oncology · doi:10.3892/ijo.23.4.1179 · Cited by 53
Self-citationHatefi, A., Megeed, Z., & Ghandehari, H. (2006) · The Journal of Gene Medicine · doi:10.1002/jgm.872 · Cited by 52
Tu, Y., & Kim, J. (2008) · The Journal of Gene Medicine · doi:10.1002/jgm.1184 · Cited by 52
Nonviral gene delivery to human breast cancer cells by targeted Ad5 penton proteins
Medina‐Kauwe, L. K., Maguire, M., Kasahara, N., & Kedes, L. (2001) · Gene Therapy · doi:10.1038/sj.gt.3301583 · Cited by 52
Translocation mediated by domain II of Pseudomonas exotoxin A: transport of barnase into the cytosol
Prior, T. I., FitzGerald, D. J., & Pastan, I. H. (1992) · Biochemistry · doi:10.1021/bi00129a001 · Cited by 47
Nishiyama, N., Arnida, Jang, W., Date, K., Miyata, K., & Kataoka, K. (2006) · Journal of drug targeting · doi:10.1080/10611860600834508 · Cited by 46
Heparin-Induced Cancer Cell Death
Linhardt, R. J. (2004) · Chemistry & Biology · doi:10.1016/j.chembiol.2004.04.001 · Cited by 43
Cytosolic Delivery of Liposomally Targeted Proteins Induced by Photochemical Internalization
Fretz, M. M., Høgset, A., Koning, G. A., Jiskoot, W., & Storm, G. (2007) · Pharmaceutical Research · doi:10.1007/s11095-007-9338-9 · Cited by 43
Self-citationIn vitro gene delivery by a novel human calcitonin (hCT)-derived carrier peptide
Krauss, U., Müller, M. J., Stahl, M., & Beck‐Sickinger, A. G. (2003) · Bioorganic & Medicinal Chemistry Letters · doi:10.1016/j.bmcl.2003.10.014 · Cited by 40
Specific gene transfer mediated by galactosylated poly-l-lysine into hepatoma cells
Han, J., & Yeom, Y. I. (2000) · International Journal of Pharmaceutics · doi:10.1016/s0378-5173(00)00441-5 · Cited by 40
Mateos‐Timoneda, M. A., Lok, M. C., Hennink, W. E., Feijén, J., & Engbersen, J. F. J. (2007) · ChemMedChem · doi:10.1002/cmdc.200700279 · Cited by 39
Listeriolysin O enhances cytoplasmic delivery by Her-2 targeting liposomes
Kullberg, M., Owens, J. L., & Mann, K. (2010) · Journal of drug targeting · doi:10.3109/10611861003663549 · Cited by 37
Time-dependent effects of chloroquine on pH of hepatocyte lysosomes
Tietz, P. S., Yamazaki, K., & LaRusso, N. F. (1990) · Biochemical Pharmacology · doi:10.1016/0006-2952(90)90414-g · Cited by 36
Calcitonin-derived peptide carriers: Mechanisms and application
Rennert, R. C., Neundorf, I., & Beck‐Sickinger, A. G. (2007) · Advanced Drug Delivery Reviews · doi:10.1016/j.addr.2007.09.008 · Cited by 34
Membrane translocation of diphtheria toxin A-fragment: role of carboxy-terminal region
Ariansen, S. L., Afanasiev, B. N., Moskaug, J. Ø., Stenmark, H., Madshus, I. H., & Olsnes, S. (1993) · Biochemistry · doi:10.1021/bi00052a012 · Cited by 33
Lipoplex and peptide-based strategies for the delivery of steric-block oligonucleotides
Resina, S., Abes, S., Turner, J. J., Prévôt, P., Travo, A., Clair, P., Gait, M. J., Thierry, A. R., & Lebleu, B. (2007) · International Journal of Pharmaceutics · doi:10.1016/j.ijpharm.2007.04.039 · Cited by 32
Subramanian, A., Ma, H., Dahl, K. N., Zhu, J., & Diamond, S. L. (2001) · The Journal of Gene Medicine · doi:10.1002/jgm.235 · Cited by 31
Enhanced plasmid DNA delivery using anionic LPDII by listeriolysin O incorporation
Lorenzi, G. L., & Lee, K. (2005) · The Journal of Gene Medicine · doi:10.1002/jgm.750 · Cited by 29
Barati, S., Chegini, F., Hurtado, P. R., & Rush, R. A. (2002) · Experimental Neurology · doi:10.1006/exnr.2002.7999 · Cited by 24
Membrane destabilization by ricin
Sun, J., Pohl, E. E., Krylova, O. O., Krause, E., Agapov, I. I., Tonevitsky, A., & Pohl, P. (2004) · European Biophysics Journal · doi:10.1007/s00249-004-0400-9 · Cited by 19
Photochemical Enhancement of DNA Delivery by EGF Receptor Targeted Polyplexes
Bonsted, A., Wagner, E., Prasmickaite, L., Høgset, A., & Berg, K. (2008) · Humana Press eBooks · doi:10.1007/978-1-60327-248-3_11 · Cited by 19
Walton, C. M. (1999) · World Journal of Gastroenterology · doi:10.3748/wjg.v5.i6.465 · Cited by 18
Rasper, D., & Merrill, A. R. (1994) · Biochemistry · doi:10.1021/bi00248a006 · Cited by 17
Aminated poly(L-histidine) as new pH-sensitive DNA carrier
Asayama, S. (2004) · Nucleic Acids Symposium Series · doi:10.1093/nass/48.1.229 · Cited by 13
Efficient splicing correction by PNA conjugation to an R6-Penetratin delivery peptide
Abes, S., Turner, J. J., Ivanova, G. D., Owen, D., Williams, D. K., Arzumanov, A. A., Clair, P., Gait, M. J., & Lebleu, B. (2007) · Nucleic Acids Research · doi:10.1093/nar/gkm1115 · Cited by 8
On the Gene Delivery Efficacies of pH-Sensitive Cationic Lipids via Endosomal Protonation
Singh, R. S., Gonçalves, C., Sandrin, P., Pichon, C., Midoux, P., & Chaudhuri, A. (2004) · Chemistry & Biology · doi:10.1016/j.chembiol.2004.05.006 · Cited by 1
Flagged first, then by citations
3 of the 151 references couldn’t be matched to a known paper.
Cited by
Sorted by citations
Targeted polymeric therapeutic nanoparticles: design, development and clinical translation
Kamaly, N., Xiao, Z., Valencia, P. M., Radovic‐Moreno, A. F., & Farokhzad, O. C. (2012) · Chemical Society Reviews · doi:10.1039/c2cs15344k · Cited by 1,774
Noncoding RNA therapeutics—Challenges and potential solutions
Winkle, M., El-Daly, S. M., Fabbri, M., & Calin, G. A. (2021) · Nature Reviews Drug Discovery · doi:10.1038/s41573-021-00219-z · Cited by 1,551
Cell-Penetrating Peptides: From Basic Research to Clinics
Guidotti, G., Brambilla, L., & Rossi, D. (2017) · Trends in Pharmacological Sciences · doi:10.1016/j.tips.2017.01.003 · Cited by 1,192
DNA Nanotechnology-Enabled Drug Delivery Systems
Hu, Q., Li, H., Wang, L., Gu, H., & Fan, C. (2018) · Chemical Reviews · doi:10.1021/acs.chemrev.7b00663 · Cited by 1,140
Multifunctional Mesoporous Silica Nanoparticles as a Universal Platform for Drug Delivery
Argyo, C., Weiß, V., Bräuchle, C., & Bein, T. (2013) · Chemistry of Materials · doi:10.1021/cm402592t · Cited by 922
Metadata
- Authors
- Varkouhi, A. K., Scholte, M., Storm, G., & Haisma, H. J.
- Affiliations
- Utrecht University (NL)
- University of Groningen (NL)
- Corresponding author
- Haisma, Hidde J.
- Venue
- Journal of Controlled Release
- Publisher
- Elsevier BV
- Published
- 2011-05
- Volume
- 151
- Issue
- 3
- Pages
- 220-228
- ISSN
- 0168-3659 (ISSN-L)
- OpenAlex
- W2008028087
- Cited by
- 1,561
- References
- 151
- Citations by year
- 2026: 82 · 2025: 82 · 2024: 90 · 2023: 94 · 2022: 122 · 2021: 100 · 2020: 123 · 2019: 120 · 2018: 137 · 2017: 111 · 2016: 127 · 2015: 116 · 2014: 98 · 2013: 90 · 2012: 51
- FWCI
- 4.32
- Type
- journal article
- Language
- en
- Open access
- green
- research.wur.nl
- Locations
- Journal of Controlled Release (publishedVersion)
- PubMed (publishedVersion)
- University of Groningen research database (University of Groningen / Centre for Information Technology) (publishedVersion)
- Socio-Environmental Systems Modeling (acceptedVersion)
- University of Groningen research database (University of Groningen / Centre for Information Technology) (submittedVersion)
- Data Archiving and Networked Services (DANS) (submittedVersion)
- Funders
- European Commission
- Topics
- Life Sciences › Biochemistry, Genetics and Molecular Biology › Molecular Biology › RNA Interference and Gene Delivery
- Physical Sciences › Materials Science › Biomaterials › Nanoparticle-Based Drug Delivery
- Life Sciences › Biochemistry, Genetics and Molecular Biology › Cell Biology › Cellular transport and secretion
- Keywords
- endosomal escape, endocytosis, lysosomal degradation, protein delivery, gene delivery, siRNA delivery, viral fusion, pH buffering, biomimetic peptides, polymers, biologic therapy
- MeSH terms
- Animals, Cytosol, DNA, Drug Carriers, Endocytosis, Humans, Intracellular Membranes, Membrane Fusion, Models, Biological, Proteins, Endosomes, RNA, Small Interfering
About these checks
Registry, retraction, Cites and statistics results are computed, not judged, with one exception: a printed reference that no index lists is read once by a model before it counts as a citation error. Claims are extracted by a model and kept only when their quote appears verbatim in the text; each cited source is then checked, with a model’s help, for whether it says what the claim relies on. Those verdicts can be wrong — read the claim’s quote and the cited source before relying on one.
Statistics and arithmetic are recomputed, not judged.
Confidence bands are shown only for fields calibrated on our annotated test set. None is calibrated yet, so no band is shown.
What counts as a claim ›How we measure confidence ›How we check this ›
Are you an author, or do you see a problem with this page? Request a review