Nanomedicine therapeutic approaches to overcome cancer drug resistance

Markman, Janet L.; Rekechenetskiy, Arthur; Holler, Eggehard; Ljubimova, Julia Y.

doi:10.1016/j.addr.2013.09.019

Cited by 733Nanoparticle-Based Drug DeliveryDrug Transport and Resistance MechanismsRNA Interference and Gene Delivery

Nanomedicine therapeutic approaches to overcome cancer drug resistance

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Markman, Janet L., Rekechenetskiy, Arthur, Holler, Eggehard, Ljubimova, Julia Y.·2013·Advanced Drug Delivery Reviews

DOI 10.1016/j.addr.2013.09.019PMC PMC5812459

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Abstract

Nanomedicine is an emerging form of therapy that focuses on alternative drug delivery and improvement of the treatment efficacy while reducing detrimental side effects to normal tissues. Cancer drug resistance is a complicated process that involves multiple mechanisms. Here we discuss the major forms of drug resistance and the new possibilities that nanomedicines offer to overcome these treatment obstacles. Novel nanomedicines that have a high ability for flexible, fast drug design and production based on tumor genetic profiles can be created making drug selection for personal patient treatment much more intensive and effective. This review aims to demonstrate the advantage of the young medical science field, nanomedicine, for overcoming cancer drug resistance. With the advanced design and alternative mechanisms of drug delivery known for different nanodrugs including liposomes, polymer conjugates, micelles, dendrimers, carbon-based, and metallic nanoparticles, overcoming various forms of multi-drug resistance looks promising and opens new horizons for cancer treatment.

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Primary rationale of using a suitable drug delivery system is its ability to ensure higher and longer duration of drug bioavailability and thereby enhanced therapeutic efficacy.
“The primary rationale of using a suitable drug delivery system is its ability to ensure a higher and longer duration of drug bioavailability and thereby enhanced therapeutic efficacy.14,15”
From Targeted therapy in chronic diseases using nanomaterial-based drug delivery vehicles (2019) · cites this paper as [15]

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“stem cells [135,145]”
NF-κB transcription factor induces drug resistance through MDR1 expression in cancer cells
Bentires‐Alj, M., Barbu, V., Fillet, M., Chariot, A., Relić, B., Jacobs, N., GIELEN, J. E., Merville, M., & Bours, V. (2003) · Oncogene · doi:10.1038/sj.onc.1206056 · Cited by 429 · cited 1× · see citing works
“Further, the anti-apoptotic, pro-survival regulator Bcl-2 [31] and nuclear factor kappa B (NF-κB), a transcription factor that controls genes that suppress apoptotic responses [32], are frequently overexpressed in cancer cells and lead to increased survival.”
Background
Peptides as Targeting Elements and Tissue Penetration Devices for Nanoparticles
Ruoslahti, E. I. (2012) · Advanced Materials · doi:10.1002/adma.201200454 · Cited by 418 · cited 2× · see citing works
“Further, these peptides may not only play a role in homing but in tumor-penetration, as is the case with iRGD, because they allow for the exit from blood vessels and can activate a tissue-specific transport pathway [105], which is a big advantage in treating resistant tumors.”
BackgroundMethod
Molecular aspects of cancer cell resistance to chemotherapy
Rebucci, M., & Michiels, C. (2013) · Biochemical Pharmacology · doi:10.1016/j.bcp.2013.02.017 · Cited by 409 · cited 1× · see citing works
“Cell cycle arrest does not occur when mutations, chromosomal rearrangements, and epigenetic changes are present, even when induced by anticancer therapies that induce DNA damage to cause cytotoxicity [30].”
Background
Super pH-sensitive multifunctional polymeric micelle for tumor pHe specific TAT exposure and multidrug resistance
Lee, E. S., Gao, Z., Kim, D., Park, K., Kwon, I. C., & Bae, Y. H. (2008) · Journal of Controlled Release · doi:10.1016/j.jconrel.2008.04.024 · Cited by 400 · cited 1× · see citing works
“Regression of tumors was apparent in xenograft models of human ovarian tumor drug-resistant A2780/AD, human breast tumor MCF-7, human lung tumor A549, and human epidermoid tumor KB using this drug as a non-specific targeting agent [109].”
Method
Inorganic Nanoparticles in Cancer Therapy
Bhattacharyya, S., Kudgus, R. A., Bhattacharya, R., & Mukherjee, P. (2010) · Pharmaceutical Research · doi:10.1007/s11095-010-0318-0 · Cited by 395 · cited 1× · see citing works
“presently understood due to the acute in vivo toxicity [15].”
Background
Mouse myeloma tumor stem cells: a primary cell culture assay.
Park, C. H., Bergsagel, D. E., & McCulloch, E. A. (1971) · PubMed · Cited by 388 · see citing works
5′-triphosphate-siRNA: turning gene silencing and Rig-I activation against melanoma
Poeck, H., Besch, R., Maihoefer, C., Renn, M., Tormo, D., Morskaya, S. S., Kirschnek, S., Gaffal, E., Landsberg, J., Hellmuth, J., et al. (2008) · Nature Medicine · doi:10.1038/nm.1887 · Cited by 387 · see citing works
In vivo delivery of siRNA to immune cells by conjugation to a TLR9 agonist enhances antitumor immune responses
Kortylewski, M., Swiderski, P. M., Herrmann, A., Wang, L., Kowolik, C. M., Kujawski, M., Lee, H., Scuto, A., Liu, Y., Yang, C., et al. (2009) · Nature Biotechnology · doi:10.1038/nbt.1564 · Cited by 378 · see citing works
Co-Delivery of siRNA and An Anticancer Drug for Treatment of Multidrug-Resistant Cancer
Saad, M., Garbuzenko, O. B., & Minko, T. (2008) · Nanomedicine · doi:10.2217/17435889.3.6.761 · Cited by 368 · cited 1× · see citing works
“Further, liposomal anti-MRP-1 and anti-Bcl2 siRNA in combination with Doxorubicin were used to suppress pump and non-pump mediated cellular resistance and to cause death in MDR lung cancer cells [116].”
Method
Tumor acidity, ion trapping and chemotherapeutics
Mahoney, B. P., Raghunand, N., Baggett, B. K., & Gillies, R. J. (2003) · Biochemical Pharmacology · doi:10.1016/s0006-2952(03)00467-2 · Cited by 366 · cited 1× · see citing works
“Weakly acidic drugs, such as cyclophosphamide, tend to concentrate in neutral extracellular space [66].”
Background
Nanomedicinal Strategies to Treat Multidrug-Resistant Tumors: Current Progress
Dong, X., & Mumper, R. J. (2010) · Nanomedicine · doi:10.2217/nnm.10.35 · Cited by 314 · cited 1× · see citing works
“With repeated treatment, tumors often become resistant not only to the specific chemotherapeutic agent being employed, but cross-resistant to both similar and structurally unrelated classes of cytotoxic drugs [16-18].”
Background
v Integrins in Angiogenesis and CancerPreprint
Weis, S. M., & Cheresh, D. A. (2011) · Cold Spring Harbor Perspectives in Medicine · doi:10.1101/cshperspect.a006478 · Cited by 311 · cited 1× · see citing works
“a binding motif for integrins, such as αvβ3, which is specifically expressed on tumor endothelia [104], and those that have a form of aminopeptidase N (CD13) that binds peptides with the NGR motif.”
Background
Targeting carbon nanotubes against cancer
Fabbro, C., Ali‐Boucetta, H., Ros, T. D., Kostarelos, K., Bianco, A., & Prato, M. (2012) · Chemical Communications · doi:10.1039/c2cc17995d · Cited by 281 · cited 1× · see citing works
“Current approaches to nanotubes include the incorporation of drugs such as Doxorubicin and Paclitaxel, nucleic acids including antisense oligonucleotides and short interfering RNAs (siRNAs), [12] and the use of nanotubes as contrast agents for imaging.”
Highly penetrative, drug-loaded nanocarriers improve treatment of glioblastoma
Zhou, J., Patel, T., Sirianni, R. W., Strohbehn, G. W., Zheng, M., Duong, N. T., Schafbauer, T., Huttner, A. J., Huang, Y. H., Carson, R. E., et al. (2013) · Proceedings of the National Academy of Sciences · doi:10.1073/pnas.1304504110 · Cited by 272 · see citing works
Use of rituximab, the new FDA-approved antibody
Leget, G. A., & Czuczman, M. S. (1998) · Current Opinion in Oncology · doi:10.1097/00001622-199811000-00012 · Cited by 252 · cited 1× · see citing works
“1 Antibodies and their fragments specifically target cancer cells—A number of mAbs have been approved for the treatment of various cancers including rituximab (Rituxan) for non-Hodgkin's lymphoma [95], the anti-HER2 trastuzumab (Herceptin) [96], the anti-VEGF bevacizumab (Avastin) to inhibit angiogenesis [97], and the…”
Background
Increased penetration of paclitaxel into the brain by inhibition of P-Glycoprotein.
Kemper, E. M., van Zandbergen, A. E., Cleypool, C. G. J., Mos, H. A., Boogerd, W. J., Beijnen, J. H., & van Tellingen, O. (2003) · PubMed · Cited by 243 · see citing works
Recent Trends in Multifunctional Liposomal Nanocarriers for Enhanced Tumor Targeting
Perche, F., & Torchilin, V. P. (2013) · Journal of Drug Delivery · doi:10.1155/2013/705265 · Cited by 232 · cited 3× · see citing works
“The delivery of these liposomes to cancer cells often relies on passive targeting and is based on the enhanced permeability and retention (EPR) effect, for which a leaky tumor vasculature is necessary [1].”
BackgroundMethod
The resistance of breast cancer stem cells to conventional hyperthermia and their sensitivity to nanoparticle-mediated photothermal therapy
Burke, A. R., Singh, R. N., Carroll, D., Wood, J. C. S., D’Agostino, R. B., Ajayan, P. M., Torti, F. M., & Torti, S. V. (2012) · Biomaterials · doi:10.1016/j.biomaterials.2011.12.052 · Cited by 227 · cited 4× · see citing works
“diacrylate-β-tetraethylenepentamine]-polycaprolactone copolymer [131] for the inhibition of efflux-dependent mechanisms or carbon nanotubes for membrane permeabilization and sensitization to photo thermal therapy [132].”
BackgroundInfluential
Beta4 integrin-dependent formation of polarized three-dimensional architecture confers resistance to apoptosis in normal and malignant mammary epithelium
Weaver, V. M., Lelièvre, S. A., Lakins, J. N., Chrenek, M. A., Jones, J., Giancotti, F. G., Werb, Z., & Bissell, M. J. (2002) · University of North Texas Digital Library (University of North Texas) · doi:10.1016/s1535-6108%2802%2900125-3 · Cited by 208 · see citing works
CD133-targeted paclitaxel delivery inhibits local tumor recurrence in a mouse model of breast cancer
Swaminathan, S. K., Roger, E., Toti, U. S., Niu, L., Ohlfest, J. R., & Panyam, J. (2013) · Journal of Controlled Release · doi:10.1016/j.jconrel.2013.07.014 · Cited by 196 · cited 4× · see citing works
“Active cargo, such as siRNA, and antibodies specifically inhibit synthesis or function of proteins, which are key players in resistance mechanisms [134,135,137].”
BackgroundInfluential
The eradication of breast cancer and cancer stem cells using octreotide modified paclitaxel active targeting micelles and salinomycin passive targeting micelles
Zhang, Y., Zhang, H., Wang, X., et al. (2011) · Biomaterials · doi:10.1016/j.biomaterials.2011.09.072 · Cited by 194 · cited 5× · see citing works
“Tang QL, Zhao ZQ, Li JC, Liang Y, Yin JQ, Zou CY, Xie XB, Zeng YX, Shen JN, Kang T, Wang J. Salinomycin inhibits osteosarcoma by targeting its tumor stem cells.”
BackgroundInfluential
Overcoming drug efflux-based multidrug resistance in cancer with nanotechnology
Xue, X., & Liang, X. (2012) · 癌症：英文版 · doi:10.5732/cjc.011.10326 · Cited by 189 · cited 3× · see citing works
“Thirteen of the 48 known ABC transporters contribute to MDR [16].”
Background
Tumor acidity, ion trapping and chemotherapeutics
Raghunand, N., Mahoney, B. P., & Gillies, R. J. (2003) · Biochemical Pharmacology · doi:10.1016/s0006-2952(03)00468-4 · Cited by 182 · cited 1× · see citing works
“Thus, weakly basic drugs, such as Doxorubicin, are protonated and have reduced cellular uptake [65].”
Background
Chemical vectors for gene delivery: uptake and intracellular trafficking
Pichon, C., Billiet, L., & Midoux, P. (2010) · Current Opinion in Biotechnology · doi:10.1016/j.copbio.2010.07.003 · Cited by 182 · cited 1× · see citing works
“However, once inside the cell, these nanoparticles may either fuse with lysosomes or be recycled back to the cell surface, making endosome escape a key limitation [107].”
Background
Nanodelivery Strategies in Cancer Chemotherapy: Biological Rationale and Pharmaceutical Perspectives
Mattheolabakis, G., Rigas, B., & Constantinides, P. P. (2012) · Nanomedicine · doi:10.2217/nnm.12.128 · Cited by 177 · cited 5× · see citing works
“Further, covalent attachment of hydrophobic drugs such as Doxorubicin and Paclitaxel is frequently employed [6,7,10].”
BackgroundInfluential
Endogenous interleukin 6 is a resistance factor for cis-diamminedichloroplatinum and etoposide-mediated cytotoxicity of human prostate carcinoma cell lines.
Borsellino, N., Belldegrun, A. S., & Bonavida, B. (1995) · PubMed · Cited by 172 · see citing works
Reversal of multidrug resistance by transferrin-conjugated liposomes co-encapsulating doxorubicin and verapamil.
Wu, J. H., Lu, Y., Lee, A., Pan, X., Yang, X., Zhao, X. B., & Lee, R. J. (2007) · PubMed · Cited by 172 · see citing works
Aptamer-Functionalized Nanoparticles for Medical Applications: Challenges and Opportunities
Xiao, Z., & Farokhzad, O. C. (2012) · ACS Nano · doi:10.1021/nn301869z · Cited by 171 · cited 1× · see citing works
“Currently, all nanoparticles using aptamers as target agents are still in the preclinical phase [103].”
Background
Enhanced endosomal escape of siRNA-incorporating hybrid nanoparticles from calcium phosphate and PEG-block charge-conversional polymer for efficient gene knockdown with negligible cytotoxicity
Pittella, F., Zhang, M., Lee, Y., Kim, H. J., Tockary, T. A., Osada, K., Ishii, T., Miyata, K., Nishiyama, N., & Kataoka, K. (2011) · Biomaterials · doi:10.1016/j.biomaterials.2010.12.057 · Cited by 169 · cited 1× · see citing works
“Rapid endosomal escape was confirmed using confocal laser scanning microscopy, and ~80% VEGF mRNA knockdown in pancreatic cancer cells was achieved [108].”
Inhibition of brain tumor growth by intravenous poly(β- l -malic acid) nanobioconjugate with pH-dependent drug release
Ding, H., Inoue, S., Ljubimov, A. V., Patil, R., Portilla‐Arias, J., Hu, J., Konda, B. M., Wawrowsky, K., Fujita, M., Karabalin, N., et al. (2010) · Proceedings of the National Academy of Sciences · doi:10.1073/pnas.1003919107 · Cited by 167 · cited 2× · see citing works
“5 (the range of acidification in late endosomes and lysosomes), activity was upregulated and membrane disruption allowed for endosomal escape of the nanoconjugate [76].”
BackgroundSelf-citation
Triazine dendrimers as drug delivery systems: From synthesis to therapy
Lim, J., & Simanek, E. E. (2012) · Advanced Drug Delivery Reviews · doi:10.1016/j.addr.2012.03.008 · Cited by 164 · cited 1× · see citing works
“Further, covalent attachment of hydrophobic drugs such as Doxorubicin and Paclitaxel is frequently employed [6,7,10].”
Background
Mechanisms Associated with cell Adhesion Mediated Drug Resistance (CAM-DR) in Hematopoietic Malignancies
Hazlehurst, L., & Dalton, W. S. (2001) · Cancer and Metastasis Reviews · doi:10.1023/a:1013156407224 · Cited by 162 · cited 1× · see citing works
“The adhesion leads to a G1 arrest associated with increased p27kip1 expression and inhibition of cyclin A and E kinase activity; disruption of this interaction returns the tumor cells to a drug-sensitive state [62].”
Background
Salinomycin inhibits osteosarcoma by targeting its tumor stem cells
Tang, Q.-L., Zhao, Z.-Q., Li, J.-C., et al. (2011) · Cancer Letters · doi:10.1016/j.canlet.2011.07.016 · Cited by 159 · cited 1× · see citing works
“A study of osteosarcoma cell lines showed that an anti-cancer drug Salinomycin could suppress tumor cells in vitro and in vivo by targeting CSC, potentially through the Wnt/β-catenin signaling pathway [119].”
Background
In-vivo efficacy of novel paclitaxel nanoparticles in paclitaxel-resistant human colorectal tumors
Koziara, J. M., Whisman, T. R., Tseng, M. T., & Mumper, R. J. (2006) · Journal of Controlled Release · doi:10.1016/j.jconrel.2006.03.001 · Cited by 155 · cited 9× · see citing works
“Other proteins including multidrug resistance proteins (MRPs/ABCC) and breast cancer resistance protein (BCRP/ABCG2) are also upregulated in cancer cells and effectively remove cytotoxic agents including Doxorubicin [20-23] and Paclitaxel [24-27] greatly decreasing their concentration within tumor cells, as shown in F…”
BackgroundInfluential
Pegylated Liposomal Doxorubicin: Optimizing the Dosing Schedule in Ovarian Cancer
Rose, P. G. (2005) · The Oncologist · doi:10.1634/theoncologist.10-3-205 · Cited by 155 · cited 1× · see citing works
“The first PEGylated nanoparticle approved in the United States and Europe is liposomal Doxorubicin (Doxil®/Caelyx® [PLD]) for the treatment of Kaposi's sarcoma [85], recurrent ovarian cancer [86] and multiple myeloma [87], with additional clinical trials ongoing for metastatic breast [88], and hormone refractory prost…”
Background
Multifunctional Nanomedicine Platform for Cancer Specific Delivery of siRNA by Superparamagnetic Iron Oxide Nanoparticles-Dendrimer Complexes
Taratula, O., Garbuzenko, O. B., Savla, R., et al. (2010) · Current Drug Delivery · doi:10.2174/156720111793663642 · Cited by 151 · cited 1× · see citing works
“The conjugation of PEG to liposomes [1,90], polymer-based nanoparticles and micelles [7,91], dendrimers [92], gold nanoparticles [11,13], and superparamagnetic iron oxide [93] is now a common practice to improve circulation time and avoid clearance.”
Background
Use of liposomal anthracyclines in Kaposi’s sarcoma
Krown, S. E., Northfelt, D., Osoba, D., & Stewart, J. S. W. (2004) · Seminars in Oncology · doi:10.1053/j.seminoncol.2004.08.003 · Cited by 150 · cited 1× · see citing works
“The first PEGylated nanoparticle approved in the United States and Europe is liposomal Doxorubicin (Doxil®/Caelyx® [PLD]) for the treatment of Kaposi's sarcoma [85], recurrent ovarian cancer [86] and multiple myeloma [87], with additional clinical trials ongoing for metastatic breast [88], and hormone refractory prost…”
Background
Increased accumulation of doxorubicin and doxorubicinol in cardiac tissue of mice lacking mdr1a P-glycoprotein
van Asperen, J., van Tellingen, O., Tijssen, F., Schinkel, A. H., & Beijnen, J. H. (1998) · British Journal of Cancer · doi:10.1038/sj.bjc.6690019 · Cited by 147 · cited 16× · see citing works
“The micelle core then disintegrates in the early endosomal pH of the cells to release Doxorubicin.”
BackgroundInfluential
Injectable nanomaterials for drug delivery: Carriers, targeting moieties, and therapeutics
Webster, D. M., Sundaram, P., & Byrne, M. E. (2013) · European Journal of Pharmaceutics and Biopharmaceutics · doi:10.1016/j.ejpb.2012.12.009 · Cited by 145 · cited 3× · see citing works
“Multiple clinical trials are ongoing using amphiphilic diblock copolymer forming micelles to deliver Paclitaxel to treat breast, non-small cell lung cancer, and advanced pancreatic cancer [11].”
Background
Curcumin-loaded nanoparticles induce apoptotic cell death through regulation of the function of MDR1 and reactive oxygen species in cisplatin-resistant CAR human oral cancer cells
Chang, P., Peng, S., Lee, C., Lu, C., Tsai, S.-C., Shieh, T., Wu, T.-S., Tu, M., Chen, M. Y., & Yang, J. (2013) · International Journal of Oncology · doi:10.3892/ijo.2013.2050 · Cited by 137 · cited 3× · see citing works
“diacrylate-β-tetraethylenepentamine]-polycaprolactone copolymer [131] for the inhibition of efflux-dependent mechanisms or carbon nanotubes for membrane permeabilization and sensitization to photo thermal therapy [132].”
Background
Targeting the lymphatics using dendritic polymers (dendrimers)
Kaminskas, L. M., & Porter, C. J. H. (2011) · Advanced Drug Delivery Reviews · doi:10.1016/j.addr.2011.05.016 · Cited by 131 · cited 1× · see citing works
“The conjugation of PEG to liposomes [1,90], polymer-based nanoparticles and micelles [7,91], dendrimers [92], gold nanoparticles [11,13], and superparamagnetic iron oxide [93] is now a common practice to improve circulation time and avoid clearance.”
Background
Transferrin-Modified c[RGDfK]-Paclitaxel Loaded Hybrid Micelle for Sequential Blood-Brain Barrier Penetration and Glioma Targeting Therapy
Zhang, P., Hu, L., Yin, Q., Feng, L., & Li, Y. (2012) · Molecular Pharmaceutics · doi:10.1021/mp200600t · Cited by 129 · cited 1× · see citing works
“These therapeutic antibodies, as well as targeting antibodies such as 2C5 [2] and anti-transferrin receptor mAbs [99-101], can be conjugated to various nanoparticles to improve efficacy and increase binding affinity to the cancer cells.”
Background
Multi-modal strategies for overcoming tumor drug resistance: Hypoxia, the Warburg effect, stem cells, and multifunctional nanotechnology
Milane, L. S., Ganesh, S., Shah, S., Duan, Z., & Amiji, M. M. (2011) · Journal of Controlled Release · doi:10.1016/j.jconrel.2011.03.032 · Cited by 128 · cited 1× · see citing works
“These hypoxic cells often revert to aerobic metabolism for the production of ATP (the Warburg effect) [73,74] to maintain enough energy to continue to thrive.”
Background
Kinetics of P-Glycoprotein-Mediated Efflux of Paclitaxel
Jang, S. H., Wientjes, M. G., & Au, J. L. ‐. (2001) · Journal of Pharmacology and Experimental Therapeutics · doi:10.1016/s0022-3565(24)29498-2 · Cited by 125 · cited 9× · see citing works
“Other proteins including multidrug resistance proteins (MRPs/ABCC) and breast cancer resistance protein (BCRP/ABCG2) are also upregulated in cancer cells and effectively remove cytotoxic agents including Doxorubicin [20-23] and Paclitaxel [24-27] greatly decreasing their concentration within tumor cells, as shown in F…”
BackgroundInfluential
Comparison of IgG diffusion and extracellular matrix composition in rhabdomyosarcomas grown in mice versus in vitro as spheroids reveals the role of host stromal cells
Davies, C. D. L., Berk, D. A., Pluen, A., & Jain, R. K. (2002) · British Journal of Cancer · doi:10.1038/sj.bjc.6600270 · Cited by 121 · cited 1× · see citing works
“Drug distribution is also affected by the composition and organization of the extracellular matrix [67].”
Background
Precise Quantification of Nanoparticle Internalization
Gottstein, C., Wu, G., Wong, B. J., et al. (2013) · ACS Nano · doi:10.1021/nn400243d · Cited by 120 · cited 1× · see citing works
“used a mathematical model combined with high throughput flow cytometry and quantitative confocal microscopy to confirm a general trend of reduced internalization by RES cells [84].”
Method
Antitumor Effect of Paclitaxel-Loaded PEGylated Immunoliposomes Against Human Breast Cancer Cells
Yang, T., Choi, M.-K., Fu-de, C., et al. (2007) · Pharmaceutical Research · doi:10.1007/s11095-007-9425-y · Cited by 119 · cited 1× · see citing works
“A number of liposomes with the addition of targeting ligands, such as the mAb 2C5 with Doxorubicin (Doxil®) [2] and an anti-HER2 mAb with Paclitaxel [3], are in the preclinical phase, whereas others are already undergoing clinical trials.”
Background
Application of poly(ethylene glycol)– distearoylphosphatidylethanolamine (PEG-DSPE) block copolymers and their derivatives as nanomaterials in drug delivery
Xiao, R., Wang, R., Zeng, Z., et al. (2012) · International Journal of Nanomedicine · doi:10.2147/ijn.s34489 · Cited by 112 · cited 1× · see citing works
“The conjugation of PEG to liposomes [1,90], polymer-based nanoparticles and micelles [7,91], dendrimers [92], gold nanoparticles [11,13], and superparamagnetic iron oxide [93] is now a common practice to improve circulation time and avoid clearance.”
Background
Inhibition of P-Glycoprotein-Mediated Paclitaxel Resistance by Reversibly Linked Quinine Homodimers
Pires, M. M., Emmert, D., Hrycyna, C. A., et al. (2008) · Molecular Pharmacology · doi:10.1124/mol.108.050492 · Cited by 111 · cited 9× · see citing works
“Other proteins including multidrug resistance proteins (MRPs/ABCC) and breast cancer resistance protein (BCRP/ABCG2) are also upregulated in cancer cells and effectively remove cytotoxic agents including Doxorubicin [20-23] and Paclitaxel [24-27] greatly decreasing their concentration within tumor cells, as shown in F…”
BackgroundInfluential
Therapeutic Significance of Elevated Tissue Transglutaminase Expression in Pancreatic Cancer
Verma, A. K., Guha, S., Diagaradjane, P., Kunnumakkara, A. B., Sanguino, A. M., Lopez‐Berestein, G., Sood, A. K., Aggarwal, B. B., Krishnan, S., Gelovani, J. G., et al. (2008) · Clinical Cancer Research · doi:10.1158/1078-0432.ccr-07-4529 · Cited by 101 · cited 1× · see citing works
“The knockdown of other CSC related pathways including tissue transglutaminase (TG2) by gene silencing using liposomal anti-TG2 siRNA combined with gemcitabine to treat Panc-28 pancreatic cancer cells was efficacious in reducing tumor growth and preventing metastasis [120].”
Background
Temozolomide Delivery to Tumor Cells by a Multifunctional Nano Vehicle Based on Poly(β-L-malic acid)
Patil, R., Portilla‐Arias, J., Ding, H., et al. (2010) · Pharmaceutical Research · doi:10.1007/s11095-010-0091-0 · Cited by 89 · cited 1× · see citing works
“The greater drug accumulation was due to the avoidance of the drug efflux pump mechanism via receptor-mediated endocytosis [111].”
BackgroundSelf-citation
pH-Sensitive Docetaxel-Loaded d -α-Tocopheryl Polyethylene Glycol Succinate–Poly(β-amino ester) Copolymer Nanoparticles for Overcoming Multidrug Resistance
Zhao, S., Tan, S., Guo, Y., Huang, J., Chu, M., Liu, H., & Zhang, Z. (2013) · Biomacromolecules · doi:10.1021/bm4005113 · Cited by 85 · see citing works
Cellular Delivery of Doxorubicin via pH-Controlled Hydrazone Linkage Using Multifunctional Nano Vehicle Based on Poly(β-L-Malic Acid)
Patil, R., Portilla‐Arias, J., Ding, H., Konda, B. M., Rekechenetskiy, A., Inoue, S., Black, K. L., Holler, E., & Ljubimova, J. Y. (2012) · International Journal of Molecular Sciences · doi:10.3390/ijms130911681 · Cited by 83 · cited 1× · see citing works
“Another version of PMLA containing PEG, with Doxorubicin conjugated via pH-sensitive hydrazone linkage, was able to effectively inhibit growth of U251 more than Doxorubicin alone due to the modified drug uptake mechanism that evaded drug efflux pumps [112].”
BackgroundSelf-citation
Cationic core–shell nanoparticles with carmustine contained within O6-benzylguanine shell for glioma therapy
Qian, L., Zheng, J., Wang, K., et al. (2013) · Biomaterials · doi:10.1016/j.biomaterials.2013.07.097 · Cited by 83 · see citing works
Resistance to EGF-R (erbB-1) and VEGF-R modulating agents
Dempke, W. C. M., & Heinemann, V. (2009) · European Journal of Cancer · doi:10.1016/j.ejca.2008.11.038 · Cited by 80 · cited 1× · see citing works
“An initial response to anti-VEGF therapy often results in a hypoxia-triggered upregulation of non-VEGF angiogenic factors, such as those in the fibroblast growth factor (FGF) family, and a recurrence of angiogenesis [50].”
Background
Cetuximab: an IgG1 monoclonal antibody for the treatment of epidermal growth factor receptor-expressing tumours
Humblet, Y. (2004) · Expert Opinion on Pharmacotherapy · doi:10.1517/14656566.5.7.1621 · Cited by 75 · cited 1× · see citing works
“1 Antibodies and their fragments specifically target cancer cells—A number of mAbs have been approved for the treatment of various cancers including rituximab (Rituxan) for non-Hodgkin's lymphoma [95], the anti-HER2 trastuzumab (Herceptin) [96], the anti-VEGF bevacizumab (Avastin) to inhibit angiogenesis [97], and the…”
Background
Antiandrogen Gold Nanoparticles Dual-Target and Overcome Treatment Resistance in Hormone-Insensitive Prostate Cancer Cells
Dreaden, E. C., Gryder, B. E., Austin, L. A., Defo, B. A. T., Hayden, S. C., Pi, M., Quarles, L. D., Oyelere, A. K., & El‐Sayed, M. A. (2012) · Bioconjugate Chemistry · doi:10.1021/bc300158k · Cited by 74 · cited 3× · see citing works
“Drug efflux systems [129–131,133–136], resistance due to presence of CSC [132,137–139], DNA damage/repair [136,140–142], apoptosis signaling pathways [139,141,143], resistance against radiation therapy [136,139,141,142], and resistance against thermal treatment [142] are being studied in vitro and in vivo as targets f…”
Background
Expression of Multidrug Resistance-associated Protein (MRP) in Human Gliomas
Mohri, M., Nitta, H., & Yamashita, J. (2000) · Journal of Neuro-Oncology · doi:10.1023/a:1026528926482 · Cited by 73 · cited 4× · see citing works
“In vivo model Gold nanoparticles Multiple α-Bic- and β-Bic antiandrogens Multivalent binding to androgen receptor and to Gprotein coupled receptor (GPRC6A); The antiandrogens inhibit binding of androgen [143,146] Human breast MDA-MB-231 and MDA-MB-468 cell lines, and brain cancer cell lines U87MG and T98G In vitro mod…”
Influential
Reversal of Lung Cancer Multidrug Resistance by pH-Responsive Micelleplexes Mediating Co-Delivery of siRNA and Paclitaxel
Yu, H., Xu, Z., Chen, X., Xu, L., Yin, Q., Zhang, Z., & Li, Y. (2013) · Macromolecular Bioscience · doi:10.1002/mabi.201300282 · Cited by 70 · cited 4× · see citing works
“Drug efflux systems [129–131,133–136], resistance due to presence of CSC [132,137–139], DNA damage/repair [136,140–142], apoptosis signaling pathways [139,141,143], resistance against radiation therapy [136,139,141,142], and resistance against thermal treatment [142] are being studied in vitro and in vivo as targets f…”
BackgroundInfluential
TRAIL conjugated to nanoparticles exhibits increased anti-tumor activities in glioma cells and glioma stem cells in vitro and in vivo
Perlstein, B., Finniss, S., Miller, C. G., et al. (2012) · Neuro-Oncology · doi:10.1093/neuonc/nos248 · Cited by 69 · cited 4× · see citing works
“oxide nanoparticle [139]”
BackgroundInfluential
Combined pegylated liposomal doxorubicin and bortezomib is highly effective in patients with recurrent or refractory multiple myeloma who received prior thalidomide/lenalidomide therapy
Sonneveld, P., Hájek, R., Nagler, A., et al. (2008) · Cancer · doi:10.1002/cncr.23326 · Cited by 69 · see citing works
Cancer stem cell theory: therapeutic implications for nanomedicine
Huang, J., Wang, X., Wu, et al. (2013) · International Journal of Nanomedicine · doi:10.2147/ijn.s38641 · Cited by 65 · cited 1× · see citing works
“CSC resistance is achieved through increased Wnt/β-catenin and Notch signaling, high levels of ATP cassette reporters, altered DNA repair mechanisms, and slow proliferation rate [118].”
Background
Soluble polymer conjugates for drug delivery
Minko, T. (2005) · Drug Discovery Today Technologies · doi:10.1016/j.ddtec.2005.05.005 · Cited by 60 · cited 1× · see citing works
“For water-soluble polymers, drugs can be covalently bound to increase circulation time and limit toxicity to normal tissues [6-9].”
Background
Strategies to Overcome or Circumvent P-Glycoprotein Mediated Multidrug Resistance
Li, X., Yuan, H., Wu, J., Li, J., Qu, X., Xu, W., & Tang, W. (2008) · Current Medicinal Chemistry · doi:10.2174/092986708783503258 · Cited by 57 · cited 1× · see citing works
“Numerous modifications of these inhibitors have appeared as promising candidates, but clinical trials continue to fail [113].”
Background
A novel approach to deliver anticancer drugs to key cell types in tumors using a PDGF receptor-binding cyclic peptide containing carrier
Prakash, J., de Jong, E., Post, E., Gouw, A. S. H., Beljaars, L., & Poelstra, K. (2010) · Journal of Controlled Release · doi:10.1016/j.jconrel.2010.03.018 · Cited by 55 · see citing works
Co-delivery of Doxorubicin and PSC 833 (Valspodar) by Stealth Nanoliposomes for Efficient Overcoming of Multidrug Resistance
Bajelan, E., Haeri, A., Vali, A. M., et al. (2012) · Journal of Pharmacy & Pharmaceutical Sciences · doi:10.18433/j3sc7j · Cited by 54 · cited 1× · see citing works
“Finally, stealth liposomes containing PSC 833 (Valspodar, a cyclosporin A analogue that is more effective) and Doxorubicin were able to reverse MDR in the Doxorubicin-resistant human breast cancer cell line T47D/TAMR-6 [117].”
Background
Copolymers of poly(lactic acid) and d -α-tocopheryl polyethylene glycol 1000 succinate-based nanomedicines: versatile multifunctional platforms for cancer diagnosis and therapy
Vijayakumar, M. R., Muthu, M. S., & Singh, S. K. (2013) · Expert Opinion on Drug Delivery · doi:10.1517/17425247.2013.758632 · Cited by 54 · cited 1× · see citing works
“The conjugation of PEG to liposomes [1,90], polymer-based nanoparticles and micelles [7,91], dendrimers [92], gold nanoparticles [11,13], and superparamagnetic iron oxide [93] is now a common practice to improve circulation time and avoid clearance.”
Background
Defining the optimal biological dose of NGR-hTNF, a selective vascular targeting agent, in advanced solid tumours
Gregorc, V., Citterio, G., Vitali, G., et al. (2009) · European Journal of Cancer · doi:10.1016/j.ejca.2009.10.005 · Cited by 54 · cited 1× · see citing works
“Delivery of TNFα using both RGD and NGR peptides has shown to decrease the effective dose by up to 1,000-fold [105] and an NGR-hTNF peptide is currently in phase III clinical trials [106].”
Method
Anti-ABCG2 Monoclonal Antibody in Combination with Paclitaxel Nanoparticles Against Cancer Stem-Like Cell Activity in Multiple Myeloma
Yang, C., Xiong, F., Wang, J., et al. (2013) · Nanomedicine · doi:10.2217/nnm.12.216 · Cited by 54 · cited 2× · see citing works
“Drug efflux systems [129–131,133–136], resistance due to presence of CSC [132,137–139], DNA damage/repair [136,140–142], apoptosis signaling pathways [139,141,143], resistance against radiation therapy [136,139,141,142], and resistance against thermal treatment [142] are being studied in vitro and in vivo as targets f…”
Background
Toxicity and efficacy evaluation of multiple targeted polymalic acid conjugates for triple-negative breast cancer treatment
Ljubimova, J. Y., Portilla‐Arias, J., Patil, R., et al. (2013) · Journal of drug targeting · doi:10.3109/1061186x.2013.837470 · Cited by 53 · cited 1× · see citing works
“Antisense oligonucleotides attached to polymalic acid biopolymer that block wild-type EGFR and mutated EGFRvIII receptor synthesis have been successfully used to treat triple negative breast cancer [60] employing a strategy based on acquired mutations by the MDA-MB-468 breast cancer cell line.”
MethodSelf-citation
Transferrin-PEG-PE modified dexamethasone conjugated cationic lipid carrier mediated gene delivery system for tumor-targeted transfection
Kong, F., Wang, Zhou, Ge, G., & Liu (2012) · International Journal of Nanomedicine · doi:10.2147/ijn.s31915 · Cited by 49 · cited 1× · see citing works
“These therapeutic antibodies, as well as targeting antibodies such as 2C5 [2] and anti-transferrin receptor mAbs [99-101], can be conjugated to various nanoparticles to improve efficacy and increase binding affinity to the cancer cells.”
Background
siRNA‐induced immunostimulation through TLR7 promotes antitumoral activity against HPV‐driven tumors in vivo
Khairuddin, N., Gantier, M. P., Blake, S. J., Wu, S. Y., Behlke, M. A., Williams, B. R. G., & McMillan, N. A. J. (2011) · Immunology and Cell Biology · doi:10.1038/icb.2011.19 · Cited by 48 · see citing works
Development and characterization of liposomal formulations for rapamycin delivery and investigation of their antiproliferative effect on MCF7 cells
Rouf, M. A., Vural, İ., Renoir, J. M., et al. (2009) · Journal of Liposome Research · doi:10.3109/08982100902963043 · Cited by 48 · cited 1× · see citing works
“Despite the fact that the EPR-based targeting is only passive and may be unpredictable, nanodrugs consistently have a better accumulation within a tumor than free drugs including Paclitaxel [80], rapamycin [81], thiostrepton [8], Doxorubicin [82], and Salinomycin [83], among countless others.”
Background
Polymalic acid nanobioconjugate for simultaneous immunostimulation and inhibition of tumor growth in HER2/neu-positive breast cancer
Ding, H., Helguera, G. F., Rodríguez, J. A., Markman, J. L., Lurı́a-Pérez, R., Gangalum, P. R., Portilla‐Arias, J., Inoue, S., Daniels‐Wells, T. R., Black, K. L., et al. (2013) · Journal of Controlled Release · doi:10.1016/j.jconrel.2013.06.001 · Cited by 47 · see citing works
Self-citation
In vitro and in vivo study of a nanoliposomal cisplatin as a radiosensitizer
Zhang, X., Yang, Gu, Chen, Rui, R., & Jiang, G. L. (2011) · International Journal of Nanomedicine · doi:10.2147/ijn.s15997 · Cited by 44 · see citing works
Mutations in the epidermal growth factor receptor gene and effects of EGFR-tyrosine kinase inhibitors on lung cancers
Fukui, T., & Mitsudomi, T. (2008) · General Thoracic and Cardiovascular Surgery · doi:10.1007/s11748-007-0193-8 · Cited by 38 · cited 1× · see citing works
“Nearly 70% of patients with a mutation (found in 10-25% of all NSCLC patients) respond to therapy compared to only a 10% response rate when no mutations are present [55,56].”
Background
Biotechnology Update
Brenner, T. L., & Adams, V. R. (1999) · Journal of the American Pharmaceutical Association (1996) · doi:10.1016/s1086-5802(16)30498-3 · Cited by 36 · see citing works
Reversal of P‐Glycoprotein‐mediated Paclitaxel Resistance by New Synthetic Isoprenoids in Human Bladder Cancer Cell Line
Enokida, H., Gotanda, T., Oku, S., et al. (2002) · Japanese Journal of Cancer Research · doi:10.1111/j.1349-7006.2002.tb02481.x · Cited by 35 · cited 9× · see citing works
“Other proteins including multidrug resistance proteins (MRPs/ABCC) and breast cancer resistance protein (BCRP/ABCG2) are also upregulated in cancer cells and effectively remove cytotoxic agents including Doxorubicin [20-23] and Paclitaxel [24-27] greatly decreasing their concentration within tumor cells, as shown in F…”
BackgroundInfluential
Grand Challenges in Modulating The Immune Response with RNAi Nanomedicines
Goldsmith, M., Mizrahy, S., & Peer, D. (2011) · Nanomedicine · doi:10.2217/nnm.11.162 · Cited by 35 · cited 1× · see citing works
“Therefore, it is not only the inhibitory effect of the siRNA, but also the immunostimulatory effect of the treatment that leads to a reduction in tumor size [124].”
Background
Multifunctional Nanoparticles Improve Therapeutic Effect for Breast Cancer by Simultaneously Antagonizing Multiple Mechanisms of Multidrug Resistance
Yin, Q., Shen, J., Zhang, Z., Yu, H., Chen, L., Gu, W., & Li, Y. (2013) · Biomacromolecules · doi:10.1021/bm400378x · Cited by 29 · cited 4× · see citing works
“Active cargo, such as siRNA, and antibodies specifically inhibit synthesis or function of proteins, which are key players in resistance mechanisms [134,135,137].”
BackgroundInfluential
Multifunctional Nanoparticles Based on a Single-Molecule Modification for the Treatment of Drug-Resistant Cancer
Wang, D., Tang, J., Wang, Y., et al. (2013) · Molecular Pharmaceutics · doi:10.1021/mp400022h · Cited by 26 · cited 3× · see citing works
“Drug efflux systems [129–131,133–136], resistance due to presence of CSC [132,137–139], DNA damage/repair [136,140–142], apoptosis signaling pathways [139,141,143], resistance against radiation therapy [136,139,141,142], and resistance against thermal treatment [142] are being studied in vitro and in vivo as targets f…”
Background
Chemotoxicity of doxorubicin and surface expression of P-glycoprotein (MDR1) is regulated by thePseudomonas aeruginosatoxin Cif
Ye, S., MacEachran, D. P., Hamilton, J. W., et al. (2008) · American Journal of Physiology-Cell Physiology · doi:10.1152/ajpcell.00234.2008 · Cited by 26 · cited 16× · see citing works
“The micelle core then disintegrates in the early endosomal pH of the cells to release Doxorubicin.”
BackgroundInfluential
Paclitaxel-Fe3O4 nanoparticles inhibit growth of CD138– CD34– tumor stem-like cells in multiple myeloma-bearing mice
Dou, J., Yang, C., Wang, J., et al. (2013) · International Journal of Nanomedicine · doi:10.2147/ijn.s38447 · Cited by 25 · cited 1× · see citing works
“resistance; PTX inhibition of cell division [138,144]”
Survivin-miRNA-loaded nanoparticles as auxiliary tools for radiation therapy: preparation, characterisation, drug release, cytotoxicity and therapeutic effect on colorectal cancer cells
Gaca, S., Reichert, S., Rödel, C. M., et al. (2012) · Journal of Microencapsulation · doi:10.3109/02652048.2012.680511 · Cited by 24 · see citing works
Down-regulation of P-glycoprotein is associated with resistance to cisplatin and VP-16 in human lung cancer cell lines.
Wang, J., Wang, H., Zhao, L., et al. (2010) · PubMed · Cited by 23 · see citing works
Phase II trial of non-pegylated liposomal doxorubicin and low-dose prednisone in second-line chemotherapy for hormone-refractory prostate cancer
Montanari, M., Fabbri, F., Rondini, E., et al. (2012) · Tumori Journal · doi:10.1177/030089161209800604 · Cited by 22 · cited 1× · see citing works
“The first PEGylated nanoparticle approved in the United States and Europe is liposomal Doxorubicin (Doxil®/Caelyx® [PLD]) for the treatment of Kaposi's sarcoma [85], recurrent ovarian cancer [86] and multiple myeloma [87], with additional clinical trials ongoing for metastatic breast [88], and hormone refractory prost…”
Background
Antinuclear Antibodies With nucleosome-restricted Specificity for Targeted Delivery of Chemotherapeutic Agents
Torchilin, V. P. (2010) · Therapeutic Delivery · doi:10.4155/tde.10.30 · Cited by 15 · cited 2× · see citing works
“These therapeutic antibodies, as well as targeting antibodies such as 2C5 [2] and anti-transferrin receptor mAbs [99-101], can be conjugated to various nanoparticles to improve efficacy and increase binding affinity to the cancer cells.”
Background
Increase in Doxorubicin Cytotoxicity by Inhibition of P-glycoprotein Activity with Lomerizine.
Shiraki, N., Hamada, A., Ohmura, T., et al. (2001) · Biological and Pharmaceutical Bulletin · doi:10.1248/bpb.24.555 · Cited by 14 · cited 16× · see citing works
“The micelle core then disintegrates in the early endosomal pH of the cells to release Doxorubicin.”
BackgroundInfluential
Persistence—luck—Avastin
Goodman, L. (2004) · Journal of Clinical Investigation · doi:10.1172/jci21507 · Cited by 14 · cited 1× · see citing works
“Antibodies and their fragments specifically target cancer cells A number of mAbs have been approved for the treatment of various cancers including rituximab (Rituxan) for non-Hodgkin's lymphoma [95], the anti-HER2 trastuzumab (Herceptin) [96], the anti-VEGF bevacizumab (Avastin) to inhibit angiogenesis [97], and the a…”
Background
Pegylated liposomal doxorubicin plus carboplatin in patients with metastatic breast cancer: a phase II study
Collea, R., Kruter, F., Cantrell, J. E., et al. (2012) · Annals of Oncology · doi:10.1093/annonc/mds052 · Cited by 9 · cited 1× · see citing works
“The first PEGylated nanoparticle approved in the United States and Europe is liposomal Doxorubicin (Doxil®/Caelyx® [PLD]) for the treatment of Kaposi's sarcoma [85], recurrent ovarian cancer [86] and multiple myeloma [87], with additional clinical trials ongoing for metastatic breast [88], and hormone refractory prost…”
Background
Enhanced Radiosensitization by Liposome-Encapsulated Pimonidazole for Anticancer Effects on Human Melanoma Cells
Kato, S., Kimura, M., Kageyama, K., Tanaka, H., & Miwa, N. (2012) · Journal of Nanoscience and Nanotechnology · doi:10.1166/jnn.2012.6180 · Cited by 6 · cited 4× · see citing works
“Drug efflux systems [129–131,133–136], resistance due to presence of CSC [132,137–139], DNA damage/repair [136,140–142], apoptosis signaling pathways [139,141,143], resistance against radiation therapy [136,139,141,142], and resistance against thermal treatment [142] are being studied in vitro and in vivo as targets f…”
BackgroundInfluential
Untitled work
Cowan (2001) · doi:10.1002/1097-0215(20010101)91:1

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Development of exosome-encapsulated paclitaxel to overcome MDR in cancer cells
Kim, M. S., Haney, M. J., Zhao, Y., Mahajan, V., Le‐Deygen, I. M., Klyachko, N. L., Inskoe, E., Piroyan, A., Sokolsky‐Papkov, M., Okolie, O., et al. (2015) · Nanomedicine Nanotechnology Biology and Medicine · doi:10.1016/j.nano.2015.10.012 · Cited by 1,498 · see citing works
“To date, there has been limited success in overcoming drug resistance in cancers through the use of novel small molecule chemotherapeutics (5, 6), or nanoformulations of existing chemotherapeutics (7-9).”
Nanomaterials for cancer therapy: current progress and perspectives
Cheng, Z., Li, M., Dey, R., & Chen, Y. (2021) · Journal of Hematology & Oncology · doi:10.1186/s13045-021-01096-0 · Cited by 1,193 · see citing works
Mechanisms and biomaterials in pH-responsive tumour targeted drug delivery: A review
Kanamala, M., Wilson, W. R., Yang, M., Palmer, B. D., & Wu, Z. (2016) · Biomaterials · doi:10.1016/j.biomaterials.2016.01.061 · Cited by 1,004 · see citing works
Targeted therapy in chronic diseases using nanomaterial-based drug delivery vehicles
Singh, A. P., Biswas, A., Shukla, A., & Maiti, P. (2019) · Signal Transduction and Targeted Therapy · doi:10.1038/s41392-019-0068-3 · Cited by 645 · see citing works
“The primary rationale of using a suitable drug delivery system is its ability to ensure a higher and longer duration of drug bioavailability and thereby enhanced therapeutic efficacy.(14,15) Various materials with different structural forms are conjugated with drugs to prepare nano drug delivery systems.”
Background
Multidrug Resistance in Cancer: Understanding Molecular Mechanisms, Immunoprevention and Therapeutic Approaches
Emran, T. B., Shahriar, A., Mahmud, A. R., Rahman, T., Abir, M. H., Siddiquee, M. F. R., Ahmed, H., Rahman, N., Nainu, F., Wahyudin, E., et al. (2022) · Frontiers in Oncology · doi:10.3389/fonc.2022.891652 · Cited by 606 · see citing works
Emerging roles of lncRNA in cancer and therapeutic opportunities.
Jiang, M., Ni, J., Cui, W., Wang, B., & Zhuo, W. (2019) · PubMed Central · Cited by 476 · see citing works
Recent progress in nanomedicine for enhanced cancer chemotherapy
Wei, G., Wang, Y., Yang, G. Y., Wang, Y., & Ju, R. (2021) · Theranostics · doi:10.7150/thno.57828 · Cited by 468 · see citing works
“Therefore, overcoming the P-gp-mediated MDR mechanism is one of most widely employed strategies to improve the effect of chemotherapeutics on MDR tumors [85].”
Advances in redox-responsive drug delivery systems of tumor microenvironment
Guo, X., Cheng, Y., Zhao, X., Luo, Y., Chen, J., & Yuan, W.-E. (2018) · Journal of Nanobiotechnology · doi:10.1186/s12951-018-0398-2 · Cited by 459 · see citing works
“ATNDDS can improve the solubility and stability of drugs, enhance the targeting ability, reduce potential toxicity, achieve the co-delivery of drugs and genes, and realize the collaborative treatment [3].”
Background
Synthetic polypeptides: from polymer design to supramolecular assembly and biomedical application
Song, Z., Han, Z., Lv, S., Chen, C., Chen, L., Yin, L., & Cheng, J. (2017) · Chemical Society Reviews · doi:10.1039/c7cs00460e · Cited by 407 · see citing works
Understanding and targeting resistance mechanisms in cancer
Lei, Z., Qin, T., Teng, Q., Wurpel, J. N. D., Zeng, L., Pan, Y., & Chen, Z. (2023) · MedComm · doi:10.1002/mco2.265 · Cited by 378 · see citing works
Natural products as multidrug resistance modulators in cancer
Kumar, A., & Jaitak, V. (2019) · European Journal of Medicinal Chemistry · doi:10.1016/j.ejmech.2019.05.027 · Cited by 340 · see citing works
Nanotechnology-based antiviral therapeutics
Chakravarty, M., & Vora, A. (2020) · Drug Delivery and Translational Research · doi:10.1007/s13346-020-00818-0 · Cited by 342 · see citing works
Advanced drug delivery applications of layered double hydroxide
Shirin, V. K. A., Sankar, R., Johnson, A. P., Gangadharappa, H. V., & Pramod, K. (2020) · Journal of Controlled Release · doi:10.1016/j.jconrel.2020.12.041 · Cited by 308 · see citing works
Bottom-Up Synthesis of Metal-Ion-Doped WS2 Nanoflakes for Cancer Theranostics
Cheng, L., Yuan, C., Shen, S., Yi, X., Gong, H., Yang, K., & Liu, Z. (2015) · ACS Nano · doi:10.1021/acsnano.5b04606 · Cited by 302 · see citing works
“treatment, the tumor tissues in group (1), (3), (5), and (6) were dissected to make paraffin section for”
Method
The role of tumor microenvironment in therapeutic resistance
Son, B., Lee, S., Youn, H., Kim, E., Kim, W., & Youn, B. (2016) · Oncotarget · doi:10.18632/oncotarget.13907 · Cited by 302 · see citing works
“Tumor microenvironment has been considered to be of great importance in various therapeutic attempts including one investigating the use of nanomedicine [124, 125].”
Background
Pulmonary delivery of nanoparticle chemotherapy for the treatment of lung cancers: challenges and opportunities
Mangal, S., Gao, W., Li, T., & Zhou, Q. T. (2017) · Acta Pharmacologica Sinica · doi:10.1038/aps.2017.34 · Cited by 290 · see citing works
The Promise of Nanotechnology in Personalized Medicine
Alghamdi, M. A., Fallica, A. N., Virzì, N. F., Kesharwani, P., Pittalà, V., & Greish, K. F. (2022) · Journal of Personalized Medicine · doi:10.3390/jpm12050673 · Cited by 291 · see citing works
“Furthermore, cells who acquire resistance to chemotherapeutic agents usually become resistant also to drugs belonging to different chemical classes or to drugs acting with a different mechanism of action, globally worsening the MDR phenomena [28].”
Reversibly crosslinked hyaluronic acid nanoparticles for active targeting and intelligent delivery of doxorubicin to drug resistant CD44+ human breast tumor xenografts
Zhong, Y., Zhang, J., Cheng, R., Deng, C., Meng, F., Xie, F., & Zhong, Z. (2015) · Journal of Controlled Release · doi:10.1016/j.jconrel.2015.01.012 · Cited by 285 · see citing works
The PDGF/PDGFR pathway as a drug target
Papadopoulos, N., & Lennartsson, J. (2017) · Molecular Aspects of Medicine · doi:10.1016/j.mam.2017.11.007 · Cited by 283 · see citing works
Self-Assembled Core–Shell Nanoparticles for Combined Chemotherapy and Photodynamic Therapy of Resistant Head and Neck Cancers
He, C., Liu, D., & Lin, W. (2015) · ACS Nano · doi:10.1021/nn506963h · Cited by 274 · see citing works
“Combination therapy, such as the combination of chemotherapy and PDT, can promote synergism between different treatment modalities, overcome drug resistance through distinct mechanisms of actions, and enhance the anticancer efficacy.(56,57) To further enhance the potency of the NCP platform, we incorporated the effici…”
Method
Review of Natural Compounds for Potential Skin Cancer Treatment
Chinembiri, T. N., Plessis, D., Gerber, M., Hamman, J. H., & du Plessis, J. (2014) · Molecules · doi:10.3390/molecules190811679 · Cited by 273 · see citing works
“Various strategies have been attempted to overcome drug resistance, such as the use of nanoparticles, liposomes and micellar drug delivery vehicles, with some reported successes [11].”
Background
Magnetic Nanoparticles for Precision Oncology: Theranostic Magnetic Iron Oxide Nanoparticles for Image-Guided and Targeted Cancer Therapy
Zhu, L., Zhou, Z., Mao, H. Z., & Yang, L. P. H. (2016) · Nanomedicine · doi:10.2217/nnm-2016-0316 · Cited by 267 · see citing works
Synergistic nanomedicine by combined gene and photothermal therapy
Kim, J., Kim, J., Jeong, C., & Kim, W. J. (2015) · Advanced Drug Delivery Reviews · doi:10.1016/j.addr.2015.12.018 · Cited by 262 · see citing works
Mesoporous silica nanoparticles with organo-bridged silsesquioxane framework as innovative platforms for bioimaging and therapeutic agent delivery
Du, X. C., Li, X., Xiong, L., Zhang, X., Kleitz, F., & Qiao, S. (2016) · Biomaterials · doi:10.1016/j.biomaterials.2016.03.019 · Cited by 262 · see citing works
Chitosan nanopolymers: An overview of drug delivery against cancer
Shanmuganathan, R., Edison, T. N. J. I., LewisOscar, F., Kumar, P., Shanmugam, S., & Pugazhendhi, A. (2019) · International Journal of Biological Macromolecules · doi:10.1016/j.ijbiomac.2019.02.060 · Cited by 248 · see citing works
Current developments and applications of microfluidic technology toward clinical translation of nanomedicines
Liu, D., Zhang, H., Fontana, F., Hirvonen, J. J., & Santos, H. A. (2017) · Advanced Drug Delivery Reviews · doi:10.1016/j.addr.2017.08.003 · Cited by 238 · see citing works
“, gold, porous silica, porous silicon, carbon nanotubes, and fullerenes) [11].”
Advances of medical nanorobots for future cancer treatments
Kong, X., Gao, P., Wang, J., Fang, Y., & Hwang, K. C. (2023) · Journal of Hematology & Oncology · doi:10.1186/s13045-023-01463-z · Cited by 253 · see citing works
“The MDR phenomenon refers to the development of resistance of cancer cells, after repeated treatment, not only to the specific chemotherapeutic agent used, but also to other cytotoxic agents with different chemical structures or mechanisms of action, resulting in cross-resistance [270, 271].”
Background
The landscape of nanoparticle-based siRNA delivery and therapeutic development
Moazzam, M., Zhang, M., Hussain, A., Yu, X., Huang, J., & Huang, Y. (2024) · Molecular Therapy · doi:10.1016/j.ymthe.2024.01.005 · Cited by 230 · see citing works
Overcoming ABC transporter-mediated multidrug resistance: The dual role of tyrosine kinase inhibitors as multitargeting agents
Beretta, G. L., Cassinelli, G., Pennati, M., Zuco, V., & Gatti, L. (2017) · European Journal of Medicinal Chemistry · doi:10.1016/j.ejmech.2017.07.062 · Cited by 234 · see citing works
“Generally, cancer drug resistance is divided in three major types on the base of different aspects [8]: i) kinetic, involving tumors possessing slow growth rate.”
Background
Stimuli-Responsive Nanomedicines for Overcoming Cancer Multidrug Resistance
Zhou, L., Wang, H., & Li, Y. (2018) · Theranostics · doi:10.7150/thno.22679 · Cited by 232 · see citing works
“Multiple mechanisms of tumor resistance have been explored [5, 7, 8], which can be grouped into: a) overexpression of ATP-binding cassette pumps (e.”
Background
Multicellular Tumor Spheroids (MCTS) as a 3D In Vitro Evaluation Tool of Nanoparticles
Lu, H., & Stenzel, M. H. (2018) · Small · doi:10.1002/smll.201702858 · Cited by 229 · see citing works
Application of polydopamine in tumor targeted drug delivery system and its drug release behavior
Wang, Z., Duan, Y., & Duan, Y. (2018) · Journal of Controlled Release · doi:10.1016/j.jconrel.2018.10.009 · Cited by 231 · see citing works
Redox regulation in tumor cell epithelial–mesenchymal transition: molecular basis and therapeutic strategy
Jiang, J., Wang, K., Chen, Y., Chen, H., Nice, E. C., & Huang, C. (2017) · Signal Transduction and Targeted Therapy · doi:10.1038/sigtrans.2017.36 · Cited by 229 · see citing works
Mesoporous Silica Nanoparticle-Supported Lipid Bilayers (Protocells) for Active Targeting and Delivery to Individual Leukemia Cells
Durfee, P. N., Lin, Y., Dunphy, D. R., Muñiz, A. J., Butler, K. S., Humphrey, K. R., Lokke, A. J., Agola, J. O., Chou, S. S., Chen, I., et al. (2016) · ACS Nano · doi:10.1021/acsnano.6b02819 · Cited by 219 · see citing works
Nanostructured materials functionalized with metal complexes: In search of alternatives for administering anticancer metallodrugs
Wani, W. A., Prashar, S., Shreaz, S., & Gómez‐Ruiz, S. (2016) · Coordination Chemistry Reviews · doi:10.1016/j.ccr.2016.01.001 · Cited by 217 · see citing works
Intracellular Self‐Assembly of Taxol Nanoparticles for Overcoming Multidrug Resistance
Yuan, Y., Wang, L., Du, W., et al. (2015) · Angewandte Chemie International Edition · doi:10.1002/anie.201504329 · Cited by 209 · see citing works
Near-infrared-light responsive nanoscale drug delivery systems for cancer treatment
Yang, G., Liu, J., Wu, Y., Feng, L., & Liu, Z. (2016) · Coordination Chemistry Reviews · doi:10.1016/j.ccr.2016.04.004 · Cited by 207 · see citing works
Dynamically PEGylated and Borate‐Coordination‐Polymer‐Coated Polydopamine Nanoparticles for Synergetic Tumor‐Targeted, Chemo‐Photothermal Combination Therapy
Liu, S., Pan, J., Liu, J., Ma, Y., Qiu, F., Mei, L., Zeng, X., & Pan, G. (2018) · Small · doi:10.1002/smll.201703968 · Cited by 200 · see citing works
Melanin‐Like Nanomaterials for Advanced Biomedical Applications: A Versatile Platform with Extraordinary Promise
Liu, H., Yang, Y., Liu, Y., Pan, J., Wang, J., Man, F., Zhang, W., & Liu, G. (2020) · Advanced Science · doi:10.1002/advs.201903129 · Cited by 197 · see citing works
Actively targeted nanomedicines for precision cancer therapy: Concept, construction, challenges and clinical translation
Gu, W., Meng, F., Haag, R., & Zhong, Z. (2020) · Journal of Controlled Release · doi:10.1016/j.jconrel.2020.10.003 · Cited by 195 · see citing works
Combination of nitric oxide and drug delivery systems: tools for overcoming drug resistance in chemotherapy
Kim, J., Yung, B. C., Kim, W. J., & Chen, X. S. (2016) · Journal of Controlled Release · doi:10.1016/j.jconrel.2016.12.026 · Cited by 190 · see citing works
Targeted nanomedicines remodeling immunosuppressive tumor microenvironment for enhanced cancer immunotherapy
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Authors: Markman, J. L., Rekechenetskiy, A., Holler, E., & Ljubimova, J. Y.
Affiliations: Cedars-Sinai Medical Center (US)
Corresponding author: Ljubimova, Julia Y.
ORCID: Markman, Janet L.
Holler, Eggehard
Ljubimova, Julia Y.
Venue: Advanced Drug Delivery Reviews
Publisher: Elsevier BV
Published: 2013-11
Volume: 65
Issue: 13-14
Pages: 1866-1879
ISSN: 0169-409X (ISSN-L)
DOI: 10.1016/j.addr.2013.09.019
PMC: PMC5812459
OpenAlex: W2086374939
Semantic Scholar: 45ee9c859bb1f5d84491499a8da3d69d2e4c8976
Cited by: 733
References: 156
Citations by year: 2026: 23 · 2025: 44 · 2024: 56 · 2023: 50 · 2022: 66 · 2021: 63 · 2020: 68 · 2019: 73 · 2018: 66 · 2017: 67 · 2016: 75 · 2015: 59 · 2014: 22
FWCI: 3.54
Type: journal article
Language: en
Open access: hybrid
doi.org
Licence: cc-by-nc-nd
www.elsevier.com/tdm/userlicense/1.0/ (tdm)
creativecommons.org/licenses/by-nc-nd/3.0/ (vor, 147 d)
Locations: Advanced Drug Delivery Reviews (publishedVersion, cc-by-nc-nd)
PubMed (publishedVersion)
PubMed Central (acceptedVersion)
Funders: National Cancer Institute (R01CA188743, R01CA123495, R01CA136841, U01CA151815)
Topics: Physical Sciences › Materials Science › Biomaterials › Nanoparticle-Based Drug Delivery
Health Sciences › Medicine › Oncology › Drug Transport and Resistance Mechanisms
Life Sciences › Biochemistry, Genetics and Molecular Biology › Molecular Biology › RNA Interference and Gene Delivery
Keywords: nanomedicine, chemoresistance, drug delivery, multidrug resistance, liposomes, polymer conjugates, micelles, dendrimers, carbon nanoparticles, metal nanoparticles, precision oncology, tumor genomic profiling
MeSH terms: Animals, Antineoplastic Agents, Clinical Trials as Topic, Drug Carriers, Humans, Neoplasms, Neoplastic Stem Cells, Drug Design, Drug Resistance, Multiple, Drug Resistance, Neoplasm, Cell Line, Tumor, Nanomedicine, Nanoparticles, Tumor Microenvironment

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