The DOI matches its Crossref record; 61 of the 61 references it cites were found in a registry or an index.
Passive versus Active Tumor Targeting Using RGD- and NGR-Modified Polymeric Nanomedicines
Open accessAbstract
Enhanced permeability and retention (EPR) and the (over-) expression of angiogenesis-related surface receptors are key features of tumor blood vessels. As a consequence, EPR-mediated passive and Arg-Gly-Asp (RGD) and Asn-Gly-Arg (NGR) based active tumor targeting have received considerable attention in the last couple of years. Using several different in vivo and ex vivo optical imaging techniques, we here visualized and quantified the benefit of RGD- and NGR-based vascular vs EPR-mediated passive tumor targeting. This was done using ∼ 10 nm sized polymeric nanocarriers, which were either labeled with DY-676 (peptide-modified polymers) or with DY-750 (peptide-free polymers). Upon coinjection into mice bearing both highly leaky CT26 and poorly leaky BxPC3 tumors, it was found that vascular targeting did work, resulting in rapid and efficient early binding to tumor blood vessels, but that over time, passive targeting was significantly more efficient, leading to higher overall levels and to more efficient retention within tumors. Although this situation might be different for larger carrier materials, these insights indicate that caution should be taken not to overestimate the potential of active over passive tumor targeting.
Overview
The claims and statistics of this paper haven’t been checked yet.
Run the check — free, no account needed. It reads the open-access text and checks the sources it cites.
Integrity signals
Registry
Cites
Statistics
Verification
Claims the paper makes
The claims and statistics of this paper haven’t been checked yet.
Run the check — free, no account needed. It reads the open-access text and checks the sources it cites.
Self-check
Percentages, sums and reported differences re-computed from the paper’s own numbers.
The self-check needs the paper’s full text.
Citations
Cites
Nanocarriers as an emerging platform for cancer therapy
Peer, D., Karp, J. M., Hong, S., Farokhzad, O. C., Margalit, R., & Langer, R. (2007) · Nature Nanotechnology · doi:10.1038/nnano.2007.387 · Cited by 8,710
Matsumura, Y., & Maeda, H. (1986) · PubMed · Cited by 6,781
Doxil® — The first FDA-approved nano-drug: Lessons learned
Barenholz, Y. (. (2012) · Journal of Controlled Release · doi:10.1016/j.jconrel.2012.03.020 · Cited by 4,792
Drug Delivery Systems: Entering the Mainstream
Allen, T. M., & Cullis, P. R. (2004) · Science · doi:10.1126/science.1095833 · Cited by 4,552
Nanoparticle therapeutics: an emerging treatment modality for cancer
Davis, M. E., Chen, Z., & Shin, D. M. (2008) · Nature Reviews Drug Discovery · doi:10.1038/nrd2614 · Cited by 4,233
Impact of Nanotechnology on Drug Delivery
Farokhzad, O. C., & Langer, R. (2009) · ACS Nano · doi:10.1021/nn900002m · Cited by 3,348
Delivering nanomedicine to solid tumors
Jain, R. K., & Stylianopoulos, T. (2010) · Nature Reviews Clinical Oncology · doi:10.1038/nrclinonc.2010.139 · Cited by 3,180
Accumulation of sub-100 nm polymeric micelles in poorly permeable tumours depends on size
Cabral, H., Matsumoto, Y., Mizuno, K., Chen, Q., Murakami, M., Kimura, M., Terada, Y., Kano, M. R., Miyazono, K., Uesaka, M., et al. (2011) · Nature Nanotechnology · doi:10.1038/nnano.2011.166 · Cited by 2,429
Salvati, A., Pitek, A. S., Monopoli, M. P., Prapainop, K., Bombelli, F. B., Hristov, D. R., Kelly, P. M., Åberg, C., Mahon, E., & Dawson, K. A. (2013) · Nature Nanotechnology · doi:10.1038/nnano.2012.237 · Cited by 1,912
O’Brien, M. E. R., Wigler, N., Inbar, M., Rosso, R., Grischke, E., Santoro, A., Catane, R., Kieback, D. G., Tomczak, P., Ackland, S. P., et al. (2004) · Annals of Oncology · doi:10.1093/annonc/mdh097 · Cited by 1,738
Prabhakar, U., Maeda, H., Jain, R. K., Sevick-Muraca, E. M., Zamboni, W., Farokhzad, O. C., Barry, S. T., Gabizon, A., Grodzinski, P., & Blakey, D. C. (2013) · Cancer Research · doi:10.1158/0008-5472.can-12-4561 · Cited by 1,485
Drug targeting to tumors: Principles, pitfalls and (pre-) clinical progress
Lammers, T., Kiessling, F., Hennink, W. E., & Storm, G. (2012) · Journal of Controlled Release · doi:10.1016/j.jconrel.2011.09.063 · Cited by 1,324
Self-citationHrkach, J., Von Hoff, D., Ali, M. M., Andrianova, E., Auer, J., Campbell, T., De Witt, D., Figa, M., Figueiredo, M., Horhota, A., et al. (2012) · Science Translational Medicine · doi:10.1126/scitranslmed.3003651 · Cited by 1,147
Tissue-Penetrating Delivery of Compounds and Nanoparticles into Tumors
Sugahara, K. N., Teesalu, T., Karmali, P. P., Kotamraju, V. R., Agemy, L., Girard, O. M., Hanahan, D., Mattrey, R. F., & Ruoslahti, E. (2009) · Cancer Cell · doi:10.1016/j.ccr.2009.10.013 · Cited by 1,136
Kirpotin, D. B., Drummond, D. C., Shao, Y., Shalaby, M. R., Hong, K., Nielsen, U. B., Marks, J. D., Benz, C. C., & Park, J. W. (2006) · Cancer Research · doi:10.1158/0008-5472.can-05-4199 · Cited by 1,125
Multistage nanoparticle delivery system for deep penetration into tumor tissue
Wong, C., Stylianopoulos, T., Cui, J., Martin, J., Chauhan, V. P., Jiang, W., Popović, Z., Jain, R. K., Bawendi, M. G., & Fukumura, D. (2011) · Proceedings of the National Academy of Sciences · doi:10.1073/pnas.1018382108 · Cited by 1,062
Microbubbles in ultrasound-triggered drug and gene delivery
Hernot, S., & Klibanov, A. L. (2008) · Advanced Drug Delivery Reviews · doi:10.1016/j.addr.2008.03.005 · Cited by 990
Davis, M. E. (2009) · Molecular Pharmaceutics · doi:10.1021/mp900015y · Cited by 977
Enhanced Permeability and Retention (EPR) Effect for Anticancer Nanomedicine Drug Targeting
Greish, K. (2010) · Methods in Molecular Biology · doi:10.1007/978-1-60761-609-2_3 · Cited by 841
Macromolecular therapeutics in cancer treatment: The EPR effect and beyond
Maeda, H. (2012) · Journal of Controlled Release · doi:10.1016/j.jconrel.2012.04.038 · Cited by 814
αv Integrins as receptors for tumor targeting by circulating ligands
Pasqualini, R., Koivunen, E., & Ruoslahti, E. (1997) · Nature Biotechnology · doi:10.1038/nbt0697-542 · Cited by 744
Mechanism of active targeting in solid tumors with transferrin-containing gold nanoparticles
Choi, C. H. J., Alabi, C. A., Webster, P., & Davis, M. E. (2010) · Proceedings of the National Academy of Sciences · doi:10.1073/pnas.0914140107 · Cited by 699
In vivo imaging of siRNA delivery and silencing in tumors
Medarova, Z., Pham, W., Farrar, C., Petkova, V., & Moore, A. (2007) · Nature Medicine · doi:10.1038/nm1486 · Cited by 697
Northfelt, D. W., Dezube, B. J., Thommes, J. A., Miller, B. J., Fischl, M. A., Friedman-Kien, A., Kaplan, L. D., Du Mond, C., Mamelok, R. D., & Henry, D. H. (1998) · Journal of Clinical Oncology · doi:10.1200/jco.1998.16.7.2445 · Cited by 649
HPMA copolymers: Origins, early developments, present, and future☆
Kopeček, J., & Kopečková, P. (2010) · Advanced Drug Delivery Reviews · doi:10.1016/j.addr.2009.10.004 · Cited by 576
Harrington, K. J., Mohammadtaghi, S., Uster, P. S., Glass, D. M., Peters, A. M., Vile, R. G., & Stewart, J. S. W. (2001) · PubMed · Cited by 575
Tumour-targeted nanomedicines: principles and practice
Lammers, T., Hennink, W. E., & Storm, G. (2008) · British Journal of Cancer · doi:10.1038/sj.bjc.6604483 · Cited by 542
Self-citationTemming, K., Schiffelers, R. M., Molema, G., & Kok, R. J. (2005) · Drug Resistance Updates · doi:10.1016/j.drup.2005.10.002 · Cited by 467
Huang, X., Peng, X., Wang, Y., Wang, Y., Shin, D. M., El-Sayed, M. A., & Nie, S. (2010) · ACS Nano · doi:10.1021/nn102055s · Cited by 427
RGD-Modified Apoferritin Nanoparticles for Efficient Drug Delivery to Tumors
Zhen, Z., Tang, W., Chen, H., Lin, X., Todd, T., Wang, G., Cowger, T., Chen, X., & Xie, J. (2013) · ACS Nano · doi:10.1021/nn305791q · Cited by 368
Zhang, C., Jugold, M., Woenne, E. C., Lammers, T., Morgenstern, B., Mueller, M. M., Zentgraf, H., Bock, M., Eisenhut, M., Semmler, W., et al. (2007) · Cancer Research · doi:10.1158/0008-5472.can-06-1668 · Cited by 336
Self-citationA Nanoparticle Size Series for In Vivo Fluorescence Imaging
Popović, Z., Liu, W., Chauhan, V. P., Lee, J., Wong, C., Greytak, A. B., Insin, N., Nocera, D. G., Fukumura, D., Jain, R. K., et al. (2010) · Angewandte Chemie International Edition · doi:10.1002/anie.201003142 · Cited by 332
Anticancer nanomedicine and tumor vascular permeability; Where is the missing link?
Taurin, S., Nehoff, H., & Greish, K. (2012) · Journal of Controlled Release · doi:10.1016/j.jconrel.2012.07.013 · Cited by 309
Ultrasound Microbubbles for Molecular Diagnosis, Therapy, and Theranostics
Kiessling, F., Fokong, S., Koczera, P., Lederle, W., & Lammers, T. (2012) · Journal of Nuclear Medicine · doi:10.2967/jnumed.111.099754 · Cited by 305
Self-citationDNAzyme Targeting c- jun Suppresses Skin Cancer Growth
Cai, H., Santiago, F. S., Prado-Lourenco, L., Wang, B., Patrikakis, M., Davenport, M. P., Maghzal, G. J., Stocker, R., Parish, C. R., Chong, B. H., et al. (2012) · Science Translational Medicine · doi:10.1126/scitranslmed.3003960 · Cited by 282
Ale, A., Ermolayev, V., Herzog, E., Cohrs, C., de Angelis, M. H., & Ntziachristos, V. (2012) · Nature Methods · doi:10.1038/nmeth.2014 · Cited by 276
Mamot, C., Ritschard, R., Wicki, A., Stehle, G., Dieterle, T., Bubendorf, L., Hilker, C., Deuster, S., Herrmann, R., & Rochlitz, C. (2012) · The Lancet Oncology · doi:10.1016/s1470-2045(12)70476-x · Cited by 244
Lammers, T., Subr, V., Ulbrich, K., Peschke, P., Huber, P. E., Hennink, W. E., & Storm, G. (2009) · Biomaterials · doi:10.1016/j.biomaterials.2009.02.040 · Cited by 240
Self-citationDuncan, R., & Vicent, M. J. (2010) · Advanced Drug Delivery Reviews · doi:10.1016/j.addr.2009.12.005 · Cited by 230
Nanomedicine based approaches for the delivery of siRNA in cancer
Ozpolat, B., Sood, A. K., & Lopez‐Berestein, G. (2010) · Journal of Internal Medicine · doi:10.1111/j.1365-2796.2009.02191.x · Cited by 218
Smith, B. R., Kempen, P., Bouley, D., Xu, A., Liu, Z., Melosh, N., Dai, H., Sinclair, R., & Gambhir, S. S. (2012) · Nano Letters · doi:10.1021/nl204175t · Cited by 212
Multifunctional Nanoemulsion Platform for Imaging Guided Therapy Evaluated in Experimental Cancer
Gianella, A., Jarzyna, P. A., Mani, V., Ramachandran, S., Calcagno, C., Tang, J., Kann, B., Dijk, W. J. R., Thijssen, V. L., Griffioen, A. W., et al. (2011) · ACS Nano · doi:10.1021/nn103336a · Cited by 212
Self-citationRecent advances in molecular, multimodal and theranostic ultrasound imaging
Kiessling, F., Fokong, S., Bzyl, J., Lederle, W., Palmowski, M., & Lammers, T. (2014) · Advanced Drug Delivery Reviews · doi:10.1016/j.addr.2013.11.013 · Cited by 201
Self-citationLammers, T., Rizzo, L. Y., Storm, G., & Kiessling, F. (2012) · Clinical Cancer Research · doi:10.1158/1078-0432.ccr-12-1414 · Cited by 195
Self-citationImage-guided, targeted and triggered drug delivery to tumors using polymer-based microbubbles
Fokong, S., Theek, B., Wu, Z., Koczera, P., Appold, L. C., Jorge, S., Resch‐Genger, U., van Zandvoort, M. A. M. J., Storm, G., Kiessling, F. M., et al. (2012) · Journal of Controlled Release · doi:10.1016/j.jconrel.2012.05.007 · Cited by 161
Self-citationHybrid System for Simultaneous Fluorescence and X-Ray Computed Tomography
Schulz, R. B., Ale, A. B. F., Sarantopoulos, A., Freyer, M., Soehngen, E., Zientkowska, M., & Ntziachristos, V. (2009) · IEEE Transactions on Medical Imaging · doi:10.1109/tmi.2009.2035310 · Cited by 157
Etrych, T., Šubr, V., Strohalm, J., Šírová, M., Řı́hová, B., & Ulbrich, K. (2012) · Journal of Controlled Release · doi:10.1016/j.jconrel.2012.06.029 · Cited by 136
Self-citationIntrinsically active nanobody-modified polymeric micelles for tumor-targeted combination therapy
Talelli, M., Oliveira, S., Rijcken, C. J. F., Pieters, E. H. E., Etrych, T., Ulbrich, K., van Nostrum, R., Storm, G., Hennink, W. E., & Lammers, T. (2012) · Biomaterials · doi:10.1016/j.biomaterials.2012.09.064 · Cited by 132
Self-citationLammers, T., Kühnlein, R., Kissel, M., Šubr, V., Etrych, T., Pola, R., Pechar, M., Ulbrich, K., Storm, G., Huber, P. E., et al. (2005) · Journal of Controlled Release · doi:10.1016/j.jconrel.2005.09.010 · Cited by 131
Self-citationGao, J., Chen, K., Luong, R. H., Bouley, D. M., Mao, H., Qiao, T., Gambhir, S. S., & Cheng, Z. (2011) · Nano Letters · doi:10.1021/nl203526f · Cited by 127
Chattopadhyay, N., Fonge, H., Cai, Z., Scollard, D. A., Lechtman, E., Done, S. J., Pignol, J., & Reilly, R. M. (2012) · Molecular Pharmaceutics · doi:10.1021/mp300016p · Cited by 115
Chen, W., Jarzyna, P. A., van Tilborg, G. A. F., Nguyen, A. V., Cormode, D. P., Klink, A., Griffioen, A. W., Randolph, G. J., Fisher, E. A. A., Mulder, W. J. M., et al. (2010) · The FASEB Journal · doi:10.1096/fj.09-139865 · Cited by 112
Noninvasive Optical Imaging of Nanomedicine Biodistribution
Kunjachan, S., Gremse, F., Theek, B., Koczera, P., Pola, R., Pechar, M., Etrych, T., Ulbrich, K., Storm, G., Kiessling, F. M., et al. (2012) · ACS Nano · doi:10.1021/nn303955n · Cited by 109
Self-citationTargeting tumor angiogenesis: comparison of peptide and polymer-peptide conjugates.
Line, B. R., Mitra, A., Nan, A., & Ghandehari, H. (2005) · PubMed · Cited by 108
Evans blue dye-enhanced capillary-resolution photoacoustic microscopy in vivo
Yao, J., Maslov, K., Hu, S., & Wang, L. V. (2009) · Journal of Biomedical Optics · doi:10.1117/1.3251044 · Cited by 81
HPMA copolymers: 30years of advances☆
Lammers, T., & Ulbrich, K. (2009) · Advanced Drug Delivery Reviews · doi:10.1016/j.addr.2009.12.004 · Cited by 70
Self-citationTumor Vasculature Targeting Through NGR Peptide-Based Drug Delivery Systems
Corti, A., & Curnis, F. (2011) · Current Pharmaceutical Biotechnology · doi:10.2174/138920111796117373 · Cited by 70
Duncan, R., Sat-Klopsch, Y.-N., Burger, A. M., Bibby, M. C., Fiebig, H., & Sausville, E. A. (2013) · Cancer Chemotherapy and Pharmacology · doi:10.1007/s00280-013-2209-7 · Cited by 61
Chytil, P., Hoffmann, S. R. K., Schindler, L., Kostka, L., Ulbrich, K., Caysa, H., Mueller, T., Mäder, K., & Etrych, T. (2013) · Journal of Controlled Release · doi:10.1016/j.jconrel.2013.05.008 · Cited by 51
Self-citationTumour vasculature targeting agents in hybrid/conjugate drugs
Prokopiou, E., Ryder, S. A., & Walsh, J. J. (2013) · Angiogenesis · doi:10.1007/s10456-013-9347-8 · Cited by 35
HPMA-copolymer conjugates targeted to tumor endothelium using synthetic oligopeptides
Pola, R., Studenovský, M., Pechar, M., Ulbrich, K., Hovorka, O., Větvička, D., & Řı́hová, B. (2009) · Journal of drug targeting · doi:10.3109/10611860903115282 · Cited by 22
Self-citation
Cited by
Analysis of nanoparticle delivery to tumours
Wilhelm, S., Tavares, A. J., Dai, Q., Ohta, S., Audet, J., Dvorak, H. F., & Chan, W. C. W. (2016) · Nature Reviews Materials · doi:10.1038/natrevmats.2016.14 · Cited by 5,218
Tumor targeting via EPR: Strategies to enhance patient responses
Golombek, S. K., May, J.-N., Theek, B., Appold, L., Drude, N., Kiessling, F., & Lammers, T. (2018) · Advanced Drug Delivery Reviews · doi:10.1016/j.addr.2018.07.007 · Cited by 1,262
van der Meel, R., Sulheim, E., Shi, Y., Kiessling, F., Mulder, W. J. M., & Lammers, T. (2019) · Nature Nanotechnology · doi:10.1038/s41565-019-0567-y · Cited by 1,234
Self-citationPolymeric Nanoparticles for Drug Delivery
Beach, M. A., Nayanathara, U., Gao, Y., Zhang, C., Xiong, Y., Wang, Y., & Such, G. K. (2024) · Chemical Reviews · doi:10.1021/acs.chemrev.3c00705 · Cited by 1,155
Attia, M. F., Anton, N., Wallyn, J., Omran, Z., & Vandamme, T. F. (2019) · Journal of Pharmacy and Pharmacology · doi:10.1111/jphp.13098 · Cited by 1,085
Metadata
- Authors
- Kunjachan, S., Pola, R., Gremse, F., Theek, B., Ehling, J., Moeckel, D., Hermanns-Sachweh, B., Pechar, M., Ulbrich, K., Hennink, W. E., Storm, G., Lederle, W., Kiessling, F., & Lammers, T.
- Venue
- Nano Letters
- Publisher
- American Chemical Society (ACS)
- Published
- 2014-01-17
- Volume
- 14
- Issue
- 2
- Pages
- 972-981
- ISSN
- 1530-6984 (ISSN-L)
- 1530-6992
- OpenAlex
- W1996275708
- Cited by
- 317
- References
- 61
- FWCI
- 16.32
- Type
- journal article
- Language
- en
- Open access
- green
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
Data sources
Bibliographic data: Semantic Scholar, OpenAlex, Crossref.
Contains information from the Semantic Scholar Academic Graph Datasets, made available under the ODC Attribution License (ODC-BY 1.0).
Semantic Scholar’s data is described in: Kinney, R., et al. (2023). The Semantic Scholar Open Data Platform. arXiv:2301.10140.