Macrophage-derived exosome-mimetic hybrid vesicles for tumor targeted drug delivery
Abstract
Extracellular vesicles (EVs) are phospholipid and protein constructs which are continuously secreted by cells in the form of smaller (30-200 nm) and larger (micron size) particles. While all of these vesicles are called as EVs, the smaller size are normally called as exosomes. Small EVs (sEVs) have now been explored as a potential candidate in therapeutics delivery owing to their endogenous functionality, intrinsic targeting property, and ability to cooperate with a host defense mechanism. Considering these potentials, we hypothesize that immune cell-derived sEVs can mimic immune cell to target cancer. However, different sEVs isolation technique reported poor yield and loss of functional properties. To solve this problem, herein we hybridized sEVs with synthetic liposome to engineer vesicles with size less than 200 nm to mimic the size of exosome and named as hybrid exosome (HE). To achieve this goal, sEVs from mouse macrophage was hybridized with synthetic liposome to engineer HE. The fluorescence-based experiment confirmed the successful hybridization process yielding HE with the size of 177 ± 21 nm. Major protein analysis from Blot techniques reveal the presence of EV marker proteins CD81, CD63, and CD9. Differential cellular interaction of HE was observed when treated with normal and cancerous cells thereby supporting our hypothesis. Moreover, a water-soluble doxorubicin was loaded in HE. Drug-loaded HE showed enhanced toxicity against cancer cells and pH-sensitive drug release in acidic condition, benefiting drug delivery to acidic cancer environment. These results suggest that the engineered HE would be an exciting platform for tumor-targeted drug delivery. STATEMENT OF SIGNIFICANCE: Extracellular vesicles (EVs) are phospholipid and protein constructs which are continuously secreted by cells in the human body. These vesicles can efficiently deliver their parental biomolecules to the recipient cells and assist in intracellular communication without a direct cell-to-cell contact. Moreover, they have the ability to perform some of the molecular task similar to that of its parent cells. For example, exosome derived from immune cells can seek for diseased and/or inflammatory cells by reading the cell surface proteins. However, different EVs isolation techniques reported poor yield and loss of functional properties. Therefore, to overcome this limitation, we herein propose to re-engineer immuno-exosome with a synthetic liposome as a refined biomimetic nanostructure for the delivery of doxorubicin (clinical drug) for breast cancer treatment.
Integrity signals
Registry
Cites
Statistics
Claims the paper makes
Claims other papers make about this one
Each is checked against this paper’s own text: does it say what the citing paper says it does?
Engineered exosomes will be a promising platform for tumor-targeted drug delivery.
“It strongly suggests that the engineered exosomes will be a promising platform for tumor-targeted drug delivery [60].”
From The Therapeutic Potential and Clinical Significance of Exosomes as Carriers of Drug Delivery System (2022) · cites this paper as [60]
Water-soluble doxorubicin loaded in engineered exosomes under acidic conditions had significantly enhanced toxicity to cancer cells.
“For example, the researchers used mouse macrophage exosomes to hybridize with synthetic liposomes to obtain engineered exosomes, water-soluble doxorubicin loaded in the engineered exosomes under acidic conditions had a significantly enhanced toxicity to cancer cells.”
From The Therapeutic Potential and Clinical Significance of Exosomes as Carriers of Drug Delivery System (2022) · cites this paper as [60]
Cites
Théry, C., Witwer, K. W., Aikawa, E., Alcaraz, M. J., Anderson, J. D., Andriantsitohaina, R., Antoniou, A., Arab, T., Archer, F., Atkin‐Smith, G. K., et al. (2018) · Journal of Extracellular Vesicles · doi:10.1080/20013078.2018.1535750 · Cited by 11,099 · see citing works
Membrane vesicles as conveyors of immune responses
Théry, C., Ostrowski, M., & Segura, É. (2009) · Nature reviews. Immunology · doi:10.1038/nri2567 · Cited by 3,887 · see citing works
Kowal, J., Arras, G., Colombo, M., Jouve, M., Morath, J. P., Primdal-Bengtson, B., Dingli, F., Loew, D., Tkach, M., & Théry, C. (2016) · Proceedings of the National Academy of Sciences · doi:10.1073/pnas.1521230113 · Cited by 3,426 · see citing works
Reassessment of exosome composition
Jeppesen, D. K., Fenix, A. M., Franklin, J. L., Higginbotham, J. N., Zhang, Q., Zimmerman, L. J., Liebler, D. C., Ping, J., Liu, Q., Evans, R., et al. (2019) · Cell · doi:10.1016/j.cell.2019.02.029 · Cited by 2,975 · see citing works
Exosomes: Extracellular organelles important in intercellular communication
Mathivanan, S., Ji, H. L., & Simpson, R. J. (2010) · Journal of Proteomics · doi:10.1016/j.jprot.2010.06.006 · Cited by 2,539 · see citing works
Erythrocyte membrane-camouflaged polymeric nanoparticles as a biomimetic delivery platform
Hu, C. J., Zhang, L., Aryal, S., Cheung, C., Fang, R. H., & Zhang, L. (2011) · Proceedings of the National Academy of Sciences · doi:10.1073/pnas.1106634108 · Cited by 2,449 · see citing works
Self-citationDistinct role of macrophages in different tumor microenvironments
Lewis, C. E., & Pollard, J. W. (2006) · Cancer Research · doi:10.1158/0008-5472.can-05-4005 · Cited by 2,225 · see citing works
Exosomes as drug delivery vehicles for Parkinson’s disease therapy
Haney, M. J., Klyachko, N. L., Zhao, Y., Gupta, R., Plotnikova, E. G., He, Z., Patel, T., Piroyan, A., Sokolsky, M., Kabanov, A. V., et al. (2015) · Journal of Controlled Release · doi:10.1016/j.jconrel.2015.03.033 · Cited by 2,009 · see citing works
Progress in Exosome Isolation Techniques
Li, P., Kaslan, M., Lee, S. H., Yao, J. D., & Gao, Z. (2017) · Theranostics · doi:10.7150/thno.18133 · Cited by 1,970 · see citing works
Abels, E., & Breakefield, X. (2016) · Cellular and molecular neurobiology · doi:10.1007/s10571-016-0366-z · Cited by 1,526 · see citing works
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
Extracellular Vesicles: Unique Intercellular Delivery Vehicles
Maas, S. L. N., Breakefield, X. O., & Weaver, A. M. (2016) · Trends in Cell Biology · doi:10.1016/j.tcb.2016.11.003 · Cited by 1,419 · see citing works
Acidic extracellular microenvironment and cancer
Kato, Y., Ozawa, S., Miyamoto, C., Maehata, Y., Suzuki, A., Maeda, T., & Baba, Y. (2013) · Cancer Cell International · doi:10.1186/1475-2867-13-89 · Cited by 1,294 · see citing works
The Bradford Method for Protein Quantitation
Kruger, N. J. (2003) · Humana Press eBooks · doi:10.1385/0-89603-268-x:9 · Cited by 1,266 · see citing works
Exosome Theranostics: Biology and Translational Medicine
He, C., Zheng, S., Luo, Y., & Wang, B. (2017) · Theranostics · doi:10.7150/thno.21945 · Cited by 1,259 · see citing works
Using exosomes, naturally-equipped nanocarriers, for drug delivery
Batrakova, E. V., & Kim, M. S. (2015) · Journal of Controlled Release · doi:10.1016/j.jconrel.2015.07.030 · Cited by 1,122 · see citing works
Tumour acidosis: from the passenger to the driver's seat
Corbet, C., & Féron, O. (2017) · Nature reviews. Cancer · doi:10.1038/nrc.2017.77 · Cited by 998 · see citing works
Role of tumor-associated macrophages in tumor progression and invasion
Mantovani, A., Schioppa, T., Porta, C., Allavena, P., & Sica, A. (2006) · Cancer and Metastasis Reviews · doi:10.1007/s10555-006-9001-7 · Cited by 885 · see citing works
Engineering hybrid exosomes by membrane fusion with liposomes
Sato, Y. T., Umezaki, K., Sawada, S., Mukai, S.-A., Sasaki, Y., Harada, N., Shiku, H., & Akiyoshi, K. (2016) · Scientific Reports · doi:10.1038/srep21933 · Cited by 744 · see citing works
Interaction and uptake of exosomes by ovarian cancer cells
Escrevente, C., Keller, S., Altevogt, P., & Costa, J. (2011) · BMC Cancer · doi:10.1186/1471-2407-11-108 · Cited by 666 · see citing works
Kim, M. S., Haney, M. J., Zhao, Y., Yuan, D., Deygen, I., Klyachko, N. L., Kabanov, A. V., & Batrakova, E. V. (2018) · Nanomedicine Nanotechnology Biology and Medicine · doi:10.1016/j.nano.2017.09.011 · Cited by 663 · see citing works
Bhatnagar, S., Shinagawa, K., Castellino, F., & Schorey, J. S. (2007) · Blood · doi:10.1182/blood-2007-03-079152 · Cited by 634 · see citing works
Exosome–Liposome Hybrid Nanoparticles Deliver CRISPR/Cas9 System in MSCs
Lin, Y., Wu, J., Gu, W., Huang, Y., Tong, Z., Huang, L., & Tan, J. (2018) · Advanced Science · doi:10.1002/advs.201700611 · Cited by 625 · see citing works
Saari, H., Lázaro-Ibáñez, E., Viitala, T., Vuorimaa-Laukkanen, E., Siljander, P., & Yliperttula, M. (2015) · Journal of Controlled Release · doi:10.1016/j.jconrel.2015.09.031 · Cited by 613 · see citing works
Macrophage exosomes as natural nanocarriers for protein delivery to inflamed brain
Yuan, D., Zhao, Y., Banks, W. A., Bullock, K. M., Haney, M., Batrakova, E., & Kabanov, A. V. (2017) · Biomaterials · doi:10.1016/j.biomaterials.2017.07.011 · Cited by 607 · see citing works
Recent advancements in the use of exosomes as drug delivery systems
Bunggulawa, E. J., Wang, W., Yin, T., Wang, N., Durkan, C., Wang, Y., & Wang, G. (2018) · Journal of Nanobiotechnology · doi:10.1186/s12951-018-0403-9 · Cited by 590 · see citing works
Mesenchymal stem cell exosomes
Lai, R. C., Yeo, R. W. Y., & Lim, S. K. (2015) · Seminars in Cell and Developmental Biology · doi:10.1016/j.semcdb.2015.03.001 · Cited by 573 · see citing works
Zarovni, N., Corrado, A., Guazzi, P., Zocco, D., Lari, E., Radano, G., Muhhina, J., Fondelli, C., Gavrilova, J., & Chiesi, A. (2015) · Methods · doi:10.1016/j.ymeth.2015.05.028 · Cited by 535 · see citing works
Cell or Cell Membrane-Based Drug Delivery Systems
Tan, S., Wu, T., Zhang, D., & Zhang, Z. (2015) · Theranostics · doi:10.7150/thno.11852 · Cited by 466 · see citing works
Piffoux, M., Silva, A., Wilhelm, C., Gazeau, F., & Tareste, D. C. (2018) · ACS Nano · doi:10.1021/acsnano.8b02053 · Cited by 463 · see citing works
Induction of heat shock proteins in B-cell exosomes
Clayton, A., Turkes, A., Navabi, H., Mason, M. D., & Tabi, Z. (2005) · Journal of Cell Science · doi:10.1242/jcs.02494 · Cited by 454 · see citing works
Activated T cells recruit exosomes secreted by dendritic cells via LFA-1
Hoen, E. N. M. N., Buschow, S. I., Anderton, S. M., Stoorvogel, W., & Wauben, M. H. M. (2008) · Blood · doi:10.1182/blood-2008-08-174094 · Cited by 436 · see citing works
Microvesicles and exosomes: Opportunities for cell-derived membrane vesicles in drug delivery
van Dommelen, S. M., Vader, P., Lakhal‐Littleton, S., Kooijmans, S. A. A., van Solinge, W. W., Wood, M. J. A., & Schiffelers, R. M. (2011) · Journal of Controlled Release · doi:10.1016/j.jconrel.2011.11.021 · Cited by 396 · see citing works
Effect of freezing and thawing rates on denaturation of proteins in aqueous solutions
Cao, E., Chen, Y., Cui, Z., et al. (2003) · Biotechnology and Bioengineering · doi:10.1002/bit.10612 · Cited by 388 · see citing works
Tumor-derived exosomes regulate expression of immune function-related genes in human T cell subsets
Müller, L., Mitsuhashi, M., Simms, P. E., Gooding, W. E., & Whiteside, T. L. (2016) · Scientific Reports · doi:10.1038/srep20254 · Cited by 310 · see citing works
Segura, É., Amigorena, S., & Théry, C. (2005) · Blood Cells Molecules and Diseases · doi:10.1016/j.bcmd.2005.05.003 · Cited by 301 · see citing works
Benchtop isolation and characterization of functional exosomes by sequential filtration.
Heinemann, M. L., Ilmer, M., Silva, L. P., Hawke, D., Recio, A., Vorontsova, M., Alt, E., & Vykoukal, J. (2014) · Journal of Chromatography A · doi:10.1016/j.chroma.2014.10.026 · Cited by 266 · see citing works
Natural killer cell membrane infused biomimetic liposomes for targeted tumor therapy
Pitchaimani, A., Nguyen, T. D. T., & Aryal, S. (2018) · Biomaterials · doi:10.1016/j.biomaterials.2018.01.018 · Cited by 252 · see citing works
Self-citationExosomes as new diagnostic tools in CNS diseases
Kanninen, K. M., Korvenlaita, N., Koıstınaho, J., & Malm, T. (2015) · Biochimica et Biophysica Acta (BBA) - Molecular Basis of Disease · doi:10.1016/j.bbadis.2015.09.020 · Cited by 218 · see citing works
Proteomics characterization of exosome cargo
Schey, K. L., Luther, J. M., & Rose, K. L. (2015) · Methods · doi:10.1016/j.ymeth.2015.03.018 · Cited by 201 · see citing works
Stimuli-Responsive Liposome Fusion Mediated by Gold Nanoparticles
Pornpattananangkul, D., Olson, S., Aryal, S., Sartor, M., Huang, C., Vecchio, K. S., & Zhang, L. (2010) · ACS Nano · doi:10.1021/nn9018587 · Cited by 173 · see citing works
Self-citationFrom structures to functions: insights into exosomes as promising drug delivery vehicles
Ren, J., He, W., Zheng, L., & Duan, H. (2016) · Biomaterials Science · doi:10.1039/c5bm00583c · Cited by 161 · see citing works
Eirin, A., Zhu, X.-Y., Puranik, A. S., Woollard, J. R., Tang, H., Dasari, S., Lerman, A., van Wijnen, A. J., & Lerman, L. O. (2016) · Scientific Reports · doi:10.1038/srep36120 · Cited by 156 · see citing works
Guerreiro, E. M., Vestad, B., Steffensen, L. A., Aass, H. C. D., Saeed, M., Øvstebø, R., Costea, D. E., Galtung, H. K., & Søland, T. M. (2018) · PLoS ONE · doi:10.1371/journal.pone.0204276 · Cited by 154 · see citing works
Abello, J., Nguyen, T. D. T., Marasini, R., Aryal, S., & Weiss, M. L. (2019) · Theranostics · doi:10.7150/thno.30030 · Cited by 140 · see citing works
Self-citationHao, S., Bai, O., Yuan, J., Qureshi, M., & Xiang, J. (2006) · PubMed · Cited by 132 · see citing works
Li, Y., Lu, A., Long, M., Cui, L., Chen, Z., & Zhu, L. (2018) · Acta Biomaterialia · doi:10.1016/j.actbio.2018.10.029 · Cited by 118 · see citing works
Membrane Proteins: The Key Players of a Cancer Cell
Kampen, K. R. (2011) · The Journal of Membrane Biology · doi:10.1007/s00232-011-9381-7 · Cited by 106 · see citing works
The New Deal: A Potential Role for Secreted Vesicles in Innate Immunity and Tumor Progression
Benito‐Martín, A., Giannatale, A. D., Ceder, S., & Peinado, H. (2015) · Frontiers in Immunology · doi:10.3389/fimmu.2015.00066 · Cited by 101 · see citing works
Biomimetic Natural Killer Membrane Camouflaged Polymeric Nanoparticle for Targeted Bioimaging
Pitchaimani, A., Nguyen, T. D. T., Marasini, R., et al. (2018) · Advanced Functional Materials · doi:10.1002/adfm.201806817 · Cited by 99 · see citing works
Self-citationDevelopment and regulation of exosome‐based therapy products
Batrakova, E. V., & Kim, M. S. (2016) · Wiley Interdisciplinary Reviews Nanomedicine and Nanobiotechnology · doi:10.1002/wnan.1395 · Cited by 94 · see citing works
Novel MHC Class I Structures on Exosomes
Lynch, S. J., Santos, S. G., Campbell, E. C., Nimmo, A., Botting, C. H., Prescott, A. R., Antoniou, A. N., & Powis, S. J. (2009) · The Journal of Immunology · doi:10.4049/jimmunol.0900798 · Cited by 89 · see citing works
O’Neill, H. S., Herron, C., Hastings, C. L., Deckers, R., Noriega, A. L., Kelly, H. M., Hennink, W. E., McDonnell, C., O’Brien, F. J., Ruiz‐Hernández, E., et al. (2016) · Acta Biomaterialia · doi:10.1016/j.actbio.2016.10.001 · Cited by 83 · see citing works
Bae, S., Brumbaugh, J., & Bonavida, B. (2018) · Genes & Cancer · doi:10.18632/genesandcancer.172 · Cited by 81 · see citing works
Human thymic epithelial primary cells produce exosomes carrying tissue‐restricted antigens
Skogberg, G., Lundberg, V., Berglund, M., Gudmundsdottir, J. A., Telemo, E., Lindgren, S., & Ekwall, O. (2015) · Immunology and Cell Biology · doi:10.1038/icb.2015.33 · Cited by 80 · see citing works
Jadus, M., Irwin, M., Irwin, M., et al. (1996) · Blood · doi:10.1182/blood.v87.12.5232.bloodjournal87125232 · Cited by 74 · see citing works
Bisht, G., Rayamajhi, S., Biplab, K. C., Paudel, S. N., Karna, D., & Shrestha, B. G. (2016) · Nanoscale Research Letters · doi:10.1186/s11671-016-1734-9 · Cited by 74 · see citing works
Self-citationTugues, S., Honjo, S., König, C. M., Padhan, N., Kroon, J., Gualandi, L., Li, X., Barkefors, I., Thijssen, V. L., Griffioen, A. W., et al. (2013) · Journal of Biological Chemistry · doi:10.1074/jbc.m113.468199 · Cited by 69 · see citing works
Mathematical Modeling of the Function of Warburg Effect in Tumor Microenvironment
Shamsi, M., Saghafian, M., Dejam, M., & Sanati‐Nezhad, A. (2018) · Scientific Reports · doi:10.1038/s41598-018-27303-6 · Cited by 63 · see citing works
Petrotchenko, E. V., Serpa, J. J., Hardie, D. B., Berjanskii, M. V., Suriyamongkol, B. P., Wishart, D. S., & Borchers, C. H. (2012) · Molecular & Cellular Proteomics · doi:10.1074/mcp.m111.013524 · Cited by 56 · see citing works
Cardiac endothelial cell-derived exosomes induce specific regulatory B cells
Song, J., Chen, X., Wang, M., et al. (2014) · Scientific Reports · doi:10.1038/srep07583 · Cited by 54 · see citing works
Biplab, K. C., Paudel, S. N., Rayamajhi, S., et al. (2016) · Chemistry Central Journal · doi:10.1186/s13065-016-0162-3 · Cited by 53 · see citing works
Self-citationAnderson, J. L., Park, A., Akiyama, R., Tap, W. D., Denny, C. T., & Federman, N. C. (2015) · PLoS ONE · doi:10.1371/journal.pone.0133610 · Cited by 40 · see citing works
Engineered biomimetic nanoabsorbent for cellular detoxification of chemotherapeutics
Nguyen, T. D. T., Pitchaimani, A., Koirala, M. B., et al. (2016) · RSC Advances · doi:10.1039/c6ra02026g · Cited by 31 · see citing works
Self-citationDesign and characterization of gadolinium infused theranostic liposomes
Pitchaimani, A., Nguyen, T. D. T., Wang, H., et al. (2016) · RSC Advances · doi:10.1039/c6ra00552g · Cited by 31 · see citing works
Self-citationParamagnetic Gd3+ labeled red blood cells for magnetic resonance angiography
Aryal, S., Stigliano, C., Key, J., et al. (2016) · Biomaterials · doi:10.1016/j.biomaterials.2016.05.002 · Cited by 30 · see citing works
Self-citationMembrane Fusion-Mediated Gold Nanoplating of Red Blood Cell: A Bioengineered CT-Contrast Agent
Aryal, S., Nguyen, T. D. T., Pitchaimani, A., et al. (2016) · ACS Biomaterials Science & Engineering · doi:10.1021/acsbiomaterials.6b00573 · Cited by 30 · see citing works
Self-citationMarasini, R., Pitchaimani, A., Nguyen, T. D. T., Comer, J. R., & Aryal, S. (2018) · Nanoscale · doi:10.1039/c8nr03026j · Cited by 30 · see citing works
Self-citationExosomes are fingerprints of originating cells: potential biomarkers for ovarian cancer
Salomón, C., Kobayashi, M., Tapia, J., et al. (2015) · Research and Reports in Biochemistry · doi:10.2147/rrbc.s58281 · Cited by 22 · see citing works
Synthesis of Ptsome: a platinum-based liposome-like nanostructure
Aryal, S., Hu, C. J., & Zhang, L. (2012) · Chemical Communications · doi:10.1039/c2cc18176b · Cited by 21 · see citing works
Self-citationHaney, M. J., Klyachko, N. L., Zhao, Y., Kabanov, A. V., & Batrakova, E. V. (2018) · Free Radical Biology and Medicine · doi:10.1016/j.freeradbiomed.2018.10.396 · Cited by 14 · see citing works
Extracellular Release of CD11b by TLR9 Stimulation in Macrophages
Kim, D., Kim, T. H., Wu, G. J., Park, B. K., Ha, J.-H., Kim, Y., Lee, K., Lee, Y., & Kwon, H. (2016) · PLoS ONE · doi:10.1371/journal.pone.0150677 · Cited by 8 · see citing works
Flagged first, then by citations
Cited by
Sorted by citations
Engineering exosomes for targeted drug delivery
Liang, Y., Duan, L., Lu, J., & Xia, J. (2021) · Theranostics · doi:10.7150/thno.52570 · Cited by 1,547 · see citing works
Engineered Extracellular Vesicles for Cancer Therapy
Zhang, X., Zhang, H., Gu, J., Zhang, J., Shi, H., Qian, H., Wang, D., Xu, W., Pan, J., & Santos, H. A. (2021) · Advanced Materials · doi:10.1002/adma.202005709 · Cited by 428 · see citing works
Extracellular vesicles: A bright star of nanomedicine
Wu, P., Zhang, B., Ocansey, D. K. W., Xu, W., & Qian, H. (2021) · Biomaterials · doi:10.1016/j.biomaterials.2020.120467 · Cited by 368 · see citing works
Chondrocyte-specific genomic editing enabled by hybrid exosomes for osteoarthritis treatment
Liang, Y., Xu, X., Xu, L., Iqbal, Z., Ouyang, K., Zhang, H., Wen, C., Duan, L., & Xia, J. (2022) · Theranostics · doi:10.7150/thno.69368 · Cited by 217 · see citing works
Mehryab, F., Rabbani, S., Shahhosseini, S., Shekari, F., Fatahi, Y., Baharvand, H., & Haeri, A. (2020) · Acta Biomaterialia · doi:10.1016/j.actbio.2020.06.036 · Cited by 216 · see citing works
Recent Advances in Exosome-Based Drug Delivery for Cancer Therapy
Kim, H., Jang, H., Cho, H., Choi, J., Hwang, K. Y., Choi, Y., Kim, S. H., & Yang, Y. (2021) · Cancers · doi:10.3390/cancers13174435 · Cited by 152 · see citing works
The Therapeutic Potential and Clinical Significance of Exosomes as Carriers of Drug Delivery System
Li, T., Li, X., Han, G., Liang, M., Yang, Z., Zhang, C., Huang, S., Tai, S., & Yu, S. (2022) · Pharmaceutics · doi:10.3390/pharmaceutics15010021 · Cited by 110 · see citing works
Programming assembly of biomimetic exosomes: An emerging theranostic nanomedicine platform
Xu, X., Xu, L., Wen, C., Xia, J., Zhang, Y., & Liang, Y. (2023) · Materials Today Bio · doi:10.1016/j.mtbio.2023.100760 · Cited by 101 · see citing works
Recent Progress in Extracellular Vesicle-Based Carriers for Targeted Drug Delivery in Cancer Therapy
Tang, Y., Liu, X., Sun, M., Xiong, S., Xiao, N., Li, J., He, X., & Xie, J. (2023) · Pharmaceutics · doi:10.3390/pharmaceutics15071902 · Cited by 24 · see citing works
Thermoresponsive M1 macrophage-derived hybrid nanovesicles for improved in vivo tumor targeting
Barone, A., Zimbo, A. M., d’Avanzo, N., Tolomeo, A. M., Ruga, S., Cardamone, A., Celia, C., Scalise, M., Torella, D., La Deda, M., et al. (2023) · Drug Delivery and Translational Research · doi:10.1007/s13346-023-01378-9 · Cited by 22 · see citing works
Sugimoto, Y., Suga, T., Umino, M., Yamayoshi, A., Mukai, H., & Kawakami, S. (2023) · Drug Delivery · doi:10.1080/10717544.2023.2191891 · Cited by 19 · see citing works
Tanaka, M., Araujo, A. C., Valenti, V. E., Guiguer, E. L., Catharin, V. C. S., Gualhardi, C. M., de Souza Bastos Mazuqueli Pereira, E., de Alvares Goulart, R., de Argolo Haber, R. S., de Carvalho, A. C. A., et al. (2026) · International Journal of Molecular Sciences · doi:10.3390/ijms27052370 · Cited by 13 · see citing works
- Authors
- Rayamajhi, S., Nguyen, T. D. T., Marasini, R., & Aryal, S.
- Affiliations
- Kansas State University (US)
- Corresponding author
- Aryal, Santosh
- Venue
- Acta Biomaterialia
- Publisher
- Elsevier BV
- Published
- 2019-08
- Volume
- 94
- Pages
- 482-494
- ISSN
- 1742-7061 (ISSN-L)
- OpenAlex
- W2946585494
- Cited by
- 429
- References
- 72
- Citations by year
- 2026: 41 · 2025: 59 · 2024: 88 · 2023: 72 · 2022: 72 · 2021: 53 · 2020: 42 · 2019: 2
- FWCI
- 14.01
- Type
- journal article
- Language
- en
- Open access
- closed
- Locations
- Acta Biomaterialia (publishedVersion)
- PubMed (publishedVersion)
- Funders
- Johnson Cancer Research Center
- Nanotechnology Innovative Centre of Kansas State
- Topics
- Life Sciences › Biochemistry, Genetics and Molecular Biology › Molecular Biology › Extracellular vesicles in disease
- Physical Sciences › Materials Science › Biomaterials › Nanoparticle-Based Drug Delivery
- Physical Sciences › Engineering › Biomedical Engineering › Nanoplatforms for cancer theranostics
- Keywords
- extracellular vesicles, macrophage-derived vesicles, anticancer drug delivery, doxorubicin, pH-responsive drug release, breast cancer, biomimetic nanostructures, vesicle isolation
- MeSH terms
- Animals, Macrophages, Neoplasms, Drug Delivery Systems, Biomimetic Materials, NIH 3T3 Cells, Cell Line, Tumor, Mice, Exosomes
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
