Bimodal Tumor-Targeting from Microenvironment Responsive Hyaluronan Layer-by-Layer (LbL) Nanoparticles
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Active targeting of nanoscale drug carriers can improve tumor-specific delivery; however, cellular heterogeneity both within and among tumor sites is a fundamental barrier to their success. Here, we describe a tumor microenvironment-responsive layer-by-layer (LbL) polymer drug carrier that actively targets tumors based on two independent mechanisms: pH-dependent cellular uptake at hypoxic tumor pH and hyaluronan-directed targeting of cell-surface CD44 receptor, a well-characterized biomarker for breast and ovarian cancer stem cells. Hypoxic pH-induced structural reorganization of hyaluronan-LbL nanoparticles was a direct result of the nature of the LbL electrostatic complex, and led to targeted cellular delivery in vitro and in vivo, with effective tumor penetration and uptake. The nanoscale drug carriers selectively bound CD44 and diminished cancer cell migration in vitro, while co-localizing with the CD44 receptor in vivo. Multimodal targeting of LbL nanoparticles is a powerful strategy for tumor-specific cancer diagnostics and therapy that can be accomplished using a single bilayer of polyamine and hyaluronan that, when assembled, produce a dynamic and responsive cell–particle interface.
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Low oxygen and pH levels induce hyaluronic acid LbL nanoparticles to effectively target and penetrate hypoxic cells in vitro and in vivo.
“Low oxygen and pH levels induce hyaluronic acid LbL nanoparticles to effectively target and penetrate hypoxic cells in vitro and in vivo.”
From Hypoxia signaling in cancer: Implications for therapeutic interventions (2023) · cites this paper as [188]
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Prospective identification of tumorigenic breast cancer cells
Al‐Hajj, M., Wicha, M. S., Benito‐Hernández, A., Morrison, S. J., & Clarke, M. F. (2003) · Proceedings of the National Academy of Sciences · doi:10.1073/pnas.0530291100 · Cited by 10,388 · see citing works
Vogelstein, B., Papadopoulos, N., Velculescu, V. E., Zhou, S., Diaz, L. A., & Kinzler, K. W. (2013) · Science · doi:10.1126/science.1235122 · Cited by 7,863 · see citing works
Understanding biophysicochemical interactions at the nano–bio interface
Nel, A. E., Mädler, L., Velegol, D., Xia, T., Hoek, E. M. V., Somasundaran, P., Klaessig, F., Castranova, V., & Thompson, M. (2009) · Nature Materials · doi:10.1038/nmat2442 · Cited by 7,083 · see citing works
Matsumura, Y., & Maeda, H. (1986) · PubMed · Cited by 6,771 · see citing works
Nanoengineering of Inorganic and Hybrid Hollow Spheres by Colloidal Templating
Caruso, F. S., Caruso, R. A., & Möhwald, H. (1998) · Science · doi:10.1126/science.282.5391.1111 · Cited by 4,137 · see citing works
Delivering nanomedicine to solid tumors
Jain, R. K., & Stylianopoulos, T. (2010) · Nature Reviews Clinical Oncology · doi:10.1038/nrclinonc.2010.139 · Cited by 3,196 · see citing works
Targeting hypoxia in cancer therapy
Wilson, W. R., & Hay, M. P. (2011) · Nature Reviews Cancer · doi:10.1038/nrc3064 · Cited by 3,172 · see citing works
Greaves, M., & Maley, C. C. (2012) · Nature · doi:10.1038/nature10762 · Cited by 3,162 · see citing works
Intra-tumour heterogeneity: a looking glass for cancer?
Marusyk, A., Almendro, V., & Polyák, K. (2012) · Nature reviews. Cancer · doi:10.1038/nrc3261 · Cited by 2,003 · see citing works
Friends or foes — bipolar effects of the tumour stroma in cancer
Mueller, M. M., & Fusenig, N. E. (2004) · Nature reviews. Cancer · doi:10.1038/nrc1477 · Cited by 1,757 · see citing works
pH-Dependent Thickness Behavior of Sequentially Adsorbed Layers of Weak Polyelectrolytes
Shiratori, S. S., & Rubner, M. F. (2000) · Macromolecules · doi:10.1021/ma991645q · Cited by 1,591 · see citing works
Transport of molecules in the tumor interstitium: a review.
Jain, R. K. (1987) · PubMed · Cited by 1,357 · see citing works
Identification and Characterization of Ovarian Cancer-Initiating Cells from Primary Human Tumors
Zhang, S., Balch, C., Chan, M. W. Y., Lai, H., Matei, D. E., Schilder, J. M., Yan, P. S., Huang, T. H. ‐., & Nephew, K. P. (2008) · Cancer Research · doi:10.1158/0008-5472.can-08-0364 · Cited by 1,295 · see citing works
A combinatorial library of lipid-like materials for delivery of RNAi therapeutics
Akinc, A., Zumbuehl, A., Goldberg, M. S., Leshchiner, E. S., Busini, V., Hossain, N., Bacallado, S., Nguyen, D. N., Fuller, J. E., Alvarez, R., et al. (2008) · Nature Biotechnology · doi:10.1038/nbt1402 · Cited by 1,228 · see citing works
Tumour heterogeneity in the clinic
Bedard, P. L., Hansen, A. R., Ratain, M. J., & Siu, L. L. (2013) · Nature · doi:10.1038/nature12627 · Cited by 1,214 · see citing works
CD44: can a cancer-initiating cell profit from an abundantly expressed molecule?
Zöller, M. (2011) · Nature reviews. Cancer · doi:10.1038/nrc3023 · Cited by 1,121 · see citing works
Multistage nanoparticle delivery system for deep penetration into tumor tissue
Wong, C., Stylianopoulos, T., Cui, J., Martin, J. D., 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 1,067 · see citing works
Vinci, M., Gowan, S., Boxall, F., Patterson, L., Zimmermann, M., Court, W., Lomas, C., Mendiola, M., Hardisson, D., & Eccles, S. A. (2012) · BMC Biology · doi:10.1186/1741-7007-10-29 · Cited by 1,024 · see citing works
High-molecular-mass hyaluronan mediates the cancer resistance of the naked mole rat
Tian, X., Azpurua, J., Hine, C., Vaidya, A. M., Myakishev-Rempel, M., Ablaeva, J., Mao, Z., Nevo, E., Gorbunova, V. A., & Seluanov, A. (2013) · Nature · doi:10.1038/nature12234 · Cited by 786 · see citing works
Mechanism of active targeting in solid tumors with transferrin-containing gold nanoparticles
Choi, C. H. J., Alabi, C. A., Webster, P. C., & Davis, M. E. (2009) · Proceedings of the National Academy of Sciences · doi:10.1073/pnas.0914140107 · Cited by 699 · see citing works
Genetic clonal diversity predicts progression to esophageal adenocarcinoma
Maley, C. C., Galipeau, P. C., Finley, J. C., Wongsurawat, V. J., Li, X., Sanchez, C. A., Paulson, T. G., Blount, P. L., Risques, R., Rabinovitch, P. S., et al. (2006) · Nature Genetics · doi:10.1038/ng1768 · Cited by 687 · see citing works
Fabrication of Microporous Thin Films from Polyelectrolyte Multilayers
Mendelsohn, J. D., Barrett, C. J., Chan, V., Pal, A. J., Mayes, A. M., & Rubner, M. F. (2000) · Langmuir · doi:10.1021/la000075g · Cited by 673 · see citing works
Ricardo, S. A. V., Vieira, A. F., Gerhard, R., Leitão, D., Pinto, R., Cameselle‐Teijeiro, J., Milanezi, F., Schmitt, F. C., & Paredes, J. (2011) · Journal of Clinical Pathology · doi:10.1136/jcp.2011.090456 · Cited by 621 · see citing works
Magnetic Nanocomposite Particles and Hollow Spheres Constructed by a Sequential Layering Approach
Caruso, F., Spasova, M., Susha, A. S., Giersig, M., & Caruso, R. A. (2000) · Chemistry of Materials · doi:10.1021/cm001164h · Cited by 590 · see citing works
Homogeneous Oxidation of Alkanes by Electrophilic Late Transition Metals
Stahl, S. S., Labinger, J. A., & Bercaw, J. E. (1998) · Angewandte Chemie International Edition · doi:10.1002/(sici)1521-3773(19980904)37:16 · Cited by 566 · see citing works
Cho, N., Frank, C. W., Kasemo, B., & Höök, F. (2010) · Nature Protocols · doi:10.1038/nprot.2010.65 · Cited by 544 · see citing works
Self-citationDeng, Z. J., Morton, S. W., Ben‐Akiva, E., Dreaden, E. C., Shopsowitz, K. E., & Hammond, P. T. (2013) · ACS Nano · doi:10.1021/nn4047925 · Cited by 513 · see citing works
Self-citationSelf-assembled RNA interference microsponges for efficient siRNA delivery
Lee, J. B., Hong, J., Bonner, D. K., Poon, Z., & Hammond, P. T. (2012) · Nature Materials · doi:10.1038/nmat3253 · Cited by 496 · see citing works
Self-citationAlvero, A. B., Chen, R., Fu, H., Montagna, M. K., Schwartz, P. E., Rutherford, T., Silasi, D., Steffensen, K. D., Waldstrøm, M., Visintin, I., et al. (2009) · Cell Cycle · doi:10.4161/cc.8.1.7533 · Cited by 488 · see citing works
Layer-by-Layer-Coated Gelatin Nanoparticles as a Vehicle for Delivery of Natural Polyphenols
Shutava, T. G., Balkundi, S. S., Vangala, P., Steffan, J. J., Bigelow, R. L. H., Cardelli, J. A., O’Neal, D. P., & LVOV, Y. M. (2009) · ACS Nano · doi:10.1021/nn900451a · Cited by 433 · see citing works
Smart Nanocarrier Based on PEGylated Hyaluronic Acid for Cancer Therapy
Choi, K. Y., Yoon, H. Y., Kim, J., Bae, S. M., Park, R., Kang, Y. M., Kim, I.-S., Kwon, I. C., Choi, K., Jeong, S. Y., et al. (2011) · ACS Nano · doi:10.1021/nn202070n · Cited by 398 · see citing works
Supramolecular organization of extracellular matrix glycosaminoglycans, in vitro and in the tissues
Scott, J. E. (1992) · The FASEB Journal · doi:10.1096/fasebj.6.9.1612287 · Cited by 385 · see citing works
From Functional Core/Shell Nanoparticles Prepared via Layer-by-Layer Deposition to Empty Nanospheres
Schneider, G. F., & Decher, G. (2004) · Nano Letters · doi:10.1021/nl0490826 · Cited by 366 · see citing works
Responsive polymer films and capsules via layer-by-layer assembly
Sukhishvili, S. A. (2005) · Current Opinion in Colloid & Interface Science · doi:10.1016/j.cocis.2005.05.001 · Cited by 355 · see citing works
Layer-by-Layer Nanoparticles with a pH-Sheddable Layer for<i>in Vivo</i>Targeting of Tumor Hypoxia
Poon, Z., Chang, D., Zhao, X., & Hammond, P. T. (2011) · ACS Nano · doi:10.1021/nn200876f · Cited by 343 · see citing works
Self-citationPark, S. Y., Gönen, M., Kim, H. J., Franziska Michor, A., & Polyák, K. (2010) · Journal of Clinical Investigation · doi:10.1172/jci40724 · Cited by 324 · see citing works
Harris, J. J., & Bruening, M. L. (1999) · Langmuir · doi:10.1021/la990620h · Cited by 309 · see citing works
Antiangiogenic therapy, hypoxia, and metastasis: risky liaisons, or not?
De Bock, K., Mazzone, M., & Carmeliet, P. (2011) · Nature Reviews Clinical Oncology · doi:10.1038/nrclinonc.2011.83 · Cited by 293 · see citing works
pH-Responsive Properties of Multilayered Poly( l -lysine)/Hyaluronic Acid Surfaces
Burke, S. E., & Barrett, C. J. (2003) · Biomacromolecules · doi:10.1021/bm034184w · Cited by 256 · see citing works
Petrov, A. I., Antipov, A. A., & Sukhorukov, G. B. (2003) · Macromolecules · doi:10.1021/ma034516p · Cited by 240 · see citing works
Poon, Z., Lee, J. B., Morton, S. W., & Hammond, P. T. (2011) · Nano Letters · doi:10.1021/nl200636r · Cited by 206 · see citing works
Self-citationCell Surface Engineering with Polyelectrolyte Multilayer Thin Films
Wilson, J. T., Cui, W., Kozlovskaya, V., Kharlampieva, E., Pan, D., Qu, Z., Krishnamurthy, V. R., Mets, J. M., Kumar, V., Wen, J., et al. (2011) · Journal of the American Chemical Society · doi:10.1021/ja110926s · Cited by 201 · see citing works
CD44 Attenuates Metastatic Invasion during Breast Cancer Progression
Lopez, J. I., Camenisch, T. D., Stevens, M. V., Sands, B. J., McDonald, J. A., & Schroeder, J. A. (2005) · Cancer Research · doi:10.1158/0008-5472.can-05-0863 · Cited by 178 · see citing works
Agarwal, A., LVOV, Y. M., Sawant, R., & Torchilin, V. P. (2008) · Journal of Controlled Release · doi:10.1016/j.jconrel.2008.03.017 · Cited by 159 · see citing works
Eliasof, S. D., Lazarus, D. D., Peters, C. G., Case, R. I., Cole, R. O., Hwang, J., Schluep, T., Chao, J., Lin, J. L., Yen, Y., et al. (2013) · Proceedings of the National Academy of Sciences · doi:10.1073/pnas.1309566110 · Cited by 144 · see citing works
Ganesh, S., Iyer, A. K., Gattacceca, F., Morrissey, D. V., & Amiji, M. M. (2013) · Journal of Controlled Release · doi:10.1016/j.jconrel.2013.10.016 · Cited by 142 · see citing works
Encapsulation of Drug Nanoparticles in Self-Assembled Macromolecular Nanoshells
Zahr, A. S., de Villiers, M. M., & Pishko, M. V. (2004) · Langmuir · doi:10.1021/la0478595 · Cited by 129 · see citing works
Biomimetic Coatings to Control Cellular Function through Cell Surface Engineering
Drachuk, I. V., Gupta, M. K., & Tsukruk, V. V. (2013) · Advanced Functional Materials · doi:10.1002/adfm.201300038 · Cited by 122 · see citing works
The architecture and biological performance of drug-loaded LbL nanoparticles
Morton, S. W., Poon, Z., & Hammond, P. T. (2013) · Biomaterials · doi:10.1016/j.biomaterials.2013.03.059 · Cited by 110 · see citing works
Self-citationMorton, S. W., Herlihy, K. P., Shopsowitz, K. E., Deng, Z. J., Chu, K. S., Bowerman, C. J., DeSimone, J. M., & Hammond, P. T. (2013) · Advanced Materials · doi:10.1002/adma.201302025 · Cited by 108 · see citing works
Self-citationAdhesion of Marine Fouling Organisms on Hydrophilic and Amphiphilic Polysaccharides
Bauer, S., Sancet, M. P. A., Finlay, J. A., Callow, M. E., Callow, J. A., & Rosenhahn, A. (2013) · Langmuir · doi:10.1021/la3038022 · Cited by 107 · see citing works
Cohen, K., Emmanuel, R., Kisin‐Finfer, E., Shabat, D., & Peer, D. (2014) · ACS Nano · doi:10.1021/nn500205b · Cited by 85 · see citing works
Osteotropic Therapy via Targeted Layer‐by‐Layer Nanoparticles
Morton, S. W., Shah, N. J., Quadir, M., Deng, Z. J., Poon, Z., & Hammond, P. T. (2013) · Advanced Healthcare Materials · doi:10.1002/adhm.201300465 · Cited by 82 · see citing works
Self-citationSwelling Behavior of Hyaluronic Acid/Polyallylamine Hydrochloride Multilayer Films
Burke, S. E., & Barrett, C. J. (2005) · Biomacromolecules · doi:10.1021/bm0492834 · Cited by 79 · see citing works
Surface Functionalization of Nanoparticles to Control Cell Interactions and Drug Release
Luo, R., Neu, B., & Venkatraman, S. S. (2012) · Small · doi:10.1002/smll.201200398 · Cited by 65 · see citing works
Layer‐by‐Layer Nanoparticles as an Efficient siRNA Delivery Vehicle for SPARC Silencing
Tan, Y., Mundargi, R. C., Chen, M. H. A., Leßig, J., Neu, B., Venkatraman, S. S., & Wong, T. T. L. (2014) · Small · doi:10.1002/smll.201303201 · Cited by 62 · see citing works
Permeability and Micromechanical Properties of Silk Ionomer Microcapsules
Ye, C., Drachuk, I. V., Calabrese, R., Dai, H., Kaplan, D. L., & Tsukruk, V. V. (2012) · Langmuir · doi:10.1021/la302455y · Cited by 53 · see citing works
c-Met recruits ICAM-1 as a coreceptor to compensate for the loss of CD44 inCd44null mice
Olaku, V., Matzke, A., Mitchell, C., Hasenauer, S., Sakkaravarthi, A., Pace, G., Ponta, H., & Orian‐Rousseau, V. (2011) · Molecular Biology of the Cell · doi:10.1091/mbc.e11-02-0134 · Cited by 50 · see citing works
Hammond, P. T. (2012) · Nanomedicine · doi:10.2217/nnm.12.47 · Cited by 48 · see citing works
Self-citationHashimoto, D., Hirota, M., Yagi, Y., & Baba, H. (2012) · Surgery Today · doi:10.1007/s00595-012-0191-z · Cited by 27 · see citing works
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Kamaly, N., Yameen, B., Wu, J., & Farokhzad, O. C. (2016) · Chemical Reviews · doi:10.1021/acs.chemrev.5b00346 · Cited by 3,070 · see citing works
Cellular uptake of nanoparticles: Journey inside the cell
Behzadi, S., Serpooshan, V., Tao, W., Hamaly, M. A., Alkawareek, M. Y., Dreaden, E. C., Brown, D., Alkilany, A. M., Farokhzad, O. C., & Mahmoudi, M. (2017) · Chemical Society Reviews · doi:10.1039/c6cs00636a · Cited by 2,859 · see citing works
Self-citationInnovation in Layer-by-Layer Assembly
Richardson, J. J., Cui, J., Björnmalm, M., Braunger, J. A., Ejima, H., & Caruso, F. (2016) · Chemical Reviews · doi:10.1021/acs.chemrev.6b00627 · Cited by 924 · see citing works
Polyphenol‐Containing Nanoparticles: Synthesis, Properties, and Therapeutic Delivery
Guo, Y., Sun, Q., Wu, F., Dai, Y., & Chen, X. S. (2021) · Advanced Materials · doi:10.1002/adma.202007356 · Cited by 658 · see citing works
Kim, M., Jeong, M., Hur, S., Cho, Y., Park, J., Jung, H. R., Seo, Y., Woo, H., Nam, K. T., Lee, K., et al. (2021) · Science Advances · doi:10.1126/sciadv.abf4398 · Cited by 390 · see citing works
Current Multistage Drug Delivery Systems Based on the Tumor Microenvironment
Chen, B., Dai, W., He, B., Zhang, H., Wang, X., Wang, Y., & Zhang, Q. (2017) · Theranostics · doi:10.7150/thno.16684 · Cited by 347 · see citing works
Choi, K. Y., Han, H. S., Lee, E. S., Shin, J. M., Almquist, B. D., Lee, D. S., & Park, J. H. (2019) · Advanced Materials · doi:10.1002/adma.201803549 · Cited by 320 · see citing works
Tumor microenvironment targeted nanotherapeutics for cancer therapy and diagnosis: A review
Thakkar, S., Sharma, D., Kalia, K., & Tekade, R. K. (2019) · Acta Biomaterialia · doi:10.1016/j.actbio.2019.09.009 · Cited by 316 · see citing works
Modified hyaluronic acid based materials for biomedical applications
Tiwari, S., & Bahadur, P. (2018) · International Journal of Biological Macromolecules · doi:10.1016/j.ijbiomac.2018.10.049 · Cited by 270 · see citing works
Xiao, B., Zhang, Z., Viennois, É., Kang, Y., Zhang, M., Han, M. K., Chen, J., & Merlin, D. (2016) · Theranostics · doi:10.7150/thno.15710 · Cited by 241 · see citing works
Schubert, J., & Chanana, M. (2018) · Current Medicinal Chemistry · doi:10.2174/0929867325666180601101859 · Cited by 236 · see citing works
Layer-by-Layer Biomaterials for Drug Delivery
Alkekhia, D., Hammond, P. T., & Shukla, A. (2020) · Annual Review of Biomedical Engineering · doi:10.1146/annurev-bioeng-060418-052350 · Cited by 218 · see citing works
Self-citationMassively parallel pooled screening reveals genomic determinants of nanoparticle delivery
Boehnke, N., Straehla, J. P., Safford, H. C., Kocak, M., Rees, M. G., Ronan, M. M., Rosenberg, D., Adelmann, C. H., Chivukula, R. R., Nabar, N., et al. (2022) · Science · doi:10.1126/science.abm5551 · Cited by 204 · see citing works
Self-citationExtracellular Matrix Mimics Using Hyaluronan-Based Biomaterials
Amorim, S., Reis, C. A., Reis, R. L., & Pires, R. A. (2020) · Trends in biotechnology · doi:10.1016/j.tibtech.2020.06.003 · Cited by 190 · see citing works
Dang, X., Gu, L., Qi, J., Correa, S., Zhang, G., Belcher, A. M., & Hammond, P. T. (2016) · Proceedings of the National Academy of Sciences · doi:10.1073/pnas.1521175113 · Cited by 190 · see citing works
Self-citationXiao, B., Xu, Z., Viennois, É., Zhang, Y., Zhang, Z., Zhang, M., Han, M. K., Kang, Y., & Merlin, D. (2017) · Molecular Therapy · doi:10.1016/j.ymthe.2016.11.020 · Cited by 184 · see citing works
Xu, G., Wang, S., Zhao, H.-L., Wu, S., Xu, J., Lu, L., & Li, X. (2015) · Journal of Membrane Science · doi:10.1016/j.memsci.2015.06.038 · Cited by 184 · see citing works
Sun, Y., & Davis, E. W. (2021) · Nanomaterials · doi:10.3390/nano11030746 · Cited by 180 · see citing works
Tumor Microenvironment Targeted Nanotherapy
Fernandes, C., Suares, D., & Yergeri, M. C. (2018) · Frontiers in Pharmacology · doi:10.3389/fphar.2018.01230 · Cited by 162 · see citing works
Li, F., Mei, H., Gao, Y., Xie, X., Nie, H., Li, T., Zhang, H., & Jia, L. (2017) · Biomaterials · doi:10.1016/j.biomaterials.2017.08.030 · Cited by 152 · see citing works
Chemical Modification of Hyaluronan and Their Biomedical Applications
Hintze, V., Schnabelrauch, M., & Rother, S. (2022) · Frontiers in Chemistry · doi:10.3389/fchem.2022.830671 · Cited by 143 · see citing works
Engineering nanolayered particles for modular drug delivery
Correa, S., Dreaden, E. C., Gu, L., & Hammond, P. T. (2016) · Journal of Controlled Release · doi:10.1016/j.jconrel.2016.01.040 · Cited by 137 · see citing works
Self-citationÁlvarez, M. M., Aizenberg, J., Analoui, M., Andrews, A. M., Bisker, G., Boyden, E. S., Kamm, R. D., Karp, J. M., Mooney, D. J., Öklü, R., et al. (2017) · ACS Nano · doi:10.1021/acsnano.7b01493 · Cited by 137 · see citing works
Aires, A., Ocampo, S. M., Simões, B. M., Rodríguez, M. J., Cadenas, J. F., Couleaud, P., Spence, K., Latorre, A., Miranda, R., Somoza, Á., et al. (2016) · Nanotechnology · doi:10.1088/0957-4484/27/6/065103 · Cited by 130 · see citing works
Park, S., Han, U., Choi, D., & Hong, J. (2018) · Biomaterials Research · doi:10.1186/s40824-018-0139-5 · Cited by 131 · see citing works
Advancing engineering design strategies for targeted cancer nanomedicine
Gomerdinger, V. F., Nabar, N., & Hammond, P. T. (2025) · Nature reviews. Cancer · doi:10.1038/s41568-025-00847-2 · Cited by 154 · see citing works
Self-citationSite-specific targeted drug delivery systems for the treatment of inflammatory bowel disease
Li, X., Lü, C., Yang, Y., Yu, C., & Rao, Y. (2020) · Biomedicine & Pharmacotherapy · doi:10.1016/j.biopha.2020.110486 · Cited by 127 · see citing works
Hung, C.-C., Huang, W., Lin, Y.-W., Yu, T.-W., Chen, H., Lin, S., Chiang, W., & Chiu, H. (2015) · Theranostics · doi:10.7150/thno.13686 · Cited by 121 · see citing works
Binary Targeting of siRNA to Hematologic Cancer Cells In Vivo Using Layer‐by‐Layer Nanoparticles
Choi, K. Y., Correa, S., Min, J., Li, J., Roy, S., Laccetti, K. H., Dreaden, E. C., Kong, S. M., Heo, R., Roh, Y. H., et al. (2019) · Advanced Functional Materials · doi:10.1002/adfm.201900018 · Cited by 119 · see citing works
Self-citationHypoxia signaling in cancer: Implications for therapeutic interventions
Zhuang, Y., Liu, K., He, Q., Gu, X., Jiang, C., & Wu, J. (2023) · MedComm · doi:10.1002/mco2.203 · Cited by 119 · see citing works
Nanoparticle Manufacturing – Heterogeneity through Processes to Products
Stavis, S. M., Fagan, J. A., Stopa, M. P., & Liddle, J. A. (2018) · ACS Applied Nano Materials · doi:10.1021/acsanm.8b01239 · Cited by 120 · see citing works
Correa, S., Boehnke, N., Barberio, A. E., Deiss‐Yehiely, E., Shi, A. C., Oberlton, B., Smith, S. G., Zervantonakis, I. K., Dreaden, E. C., & Hammond, P. T. (2020) · ACS Nano · doi:10.1021/acsnano.9b09213 · Cited by 117 · see citing works
Self-citationEngineered Metal-Phenolic Capsules Show Tunable Targeted Delivery to Cancer Cells
Ju, Y., Cui, J., Sun, H., Müllner, M., Dai, Y., Guo, J., Bertleff‐Zieschang, N., Suma, T., Richardson, J. J., & Caruso, F. (2016) · Biomacromolecules · doi:10.1021/acs.biomac.6b00537 · Cited by 112 · see citing works
Xiao, S.-L., Xu, P., Peng, Q., Chen, J., Huang, J., Wang, F., & Noor, N. (2017) · Polymers · doi:10.3390/polym9120735 · Cited by 111 · see citing works
Engineered materials for cancer immunotherapy
Cheung, A. S., & Mooney, D. J. (2015) · Nano Today · doi:10.1016/j.nantod.2015.06.007 · Cited by 107 · see citing works
Hyaluronic Acid-Based Nanosystems for CD44 Mediated Anti-Inflammatory and Antinociceptive Activity
Salathia, S., Gigliobianco, M. R., Casadidio, C., Martino, P. D., & Censi, R. (2023) · International Journal of Molecular Sciences · doi:10.3390/ijms24087286 · Cited by 105 · see citing works
Novel drug delivery systems for inflammatory bowel disease
Yasmin, F., Najeeb, H., Shaikh, S., Hasanain, M., Naeem, U., Moeed, A., Koritala, T., Hasan, S., & Surani, S. (2022) · World Journal of Gastroenterology · doi:10.3748/wjg.v28.i18.1922 · Cited by 102 · see citing works
Biosensor-Integrated Drug Delivery Systems as New Materials for Biomedical Applications
Cicha, I., Priefer, R., Severino, P. B., Souto, E. B., & Jain, S. A. (2022) · Biomolecules · doi:10.3390/biom12091198 · Cited by 102 · see citing works
Kong, S. M., Costa, D. F. G., Jagielska, A., Vliet, K. J. V., & Hammond, P. T. (2021) · Proceedings of the National Academy of Sciences · doi:10.1073/pnas.2104826118 · Cited by 100 · see citing works
Self-citationImproving Targeting of Metal–Phenolic Capsules by the Presence of Protein Coronas
Ju, Y., Dai, Q., Cui, J., Dai, Y., Suma, T., Richardson, J. J., & Caruso, F. (2016) · ACS Applied Materials & Interfaces · doi:10.1021/acsami.6b07613 · Cited by 99 · see citing works
Highly Scalable, Closed‐Loop Synthesis of Drug‐Loaded, Layer‐by‐Layer Nanoparticles
Correa, S., Choi, K. Y., Dreaden, E. C., Renggli, K., Shi, A. C., Gu, L., Shopsowitz, K. E., Quadir, M., Ben‐Akiva, E., & Hammond, P. T. (2016) · Advanced Functional Materials · doi:10.1002/adfm.201504385 · Cited by 98 · see citing works
Self-citationGu, L., Deng, Z. J., Roy, S., & Hammond, P. T. (2017) · Clinical Cancer Research · doi:10.1158/1078-0432.ccr-16-2186 · Cited by 98 · see citing works
Self-citationCai, Y., Zhang, L., Zhang, Y., & Lu, R. (2022) · Pharmaceutics · doi:10.3390/pharmaceutics14040822 · Cited by 98 · see citing works
Cancer Cell Coating Nanoparticles for Optimal Tumor-Specific Cytokine Delivery
Barberio, A. E., Smith, S. G., Correa, S., Nguyen, C., Nhan, B. T., Melo, M. B., Tokatlian, T., Suh, H., Irvine, D. J., & Hammond, P. T. (2020) · ACS Nano · doi:10.1021/acsnano.0c03109 · Cited by 97 · see citing works
Self-citationIndocyanine Green-Encapsulated Hybrid Polymeric Nanomicelles for Photothermal Cancer Therapy
Jian, W.-H., Yu, T.-W., Chen, C.-J., Huang, W., Chiu, H., & Chiang, W. (2015) · Langmuir · doi:10.1021/acs.langmuir.5b00963 · Cited by 93 · see citing works
Layer‐by‐Layer Assemblies for Cancer Treatment and Diagnosis
Liu, X. Q., & Picart, C. (2015) · Advanced Materials · doi:10.1002/adma.201502660 · Cited by 92 · see citing works
Smart nanosystems: Bio-inspired technologies that interact with the host environment
Kwon, E. J., Lo, J. H.-J., & Bhatia, S. N. (2015) · Proceedings of the National Academy of Sciences · doi:10.1073/pnas.1508522112 · Cited by 92 · see citing works
Correa, S., Boehnke, N., Deiss‐Yehiely, E., & Hammond, P. T. (2019) · ACS Nano · doi:10.1021/acsnano.9b00792 · Cited by 89 · see citing works
Self-citationЛенгерт, Е. В., Koltsov, S. I., Li, J., Ermakov, A. V., Parakhonskiy, B. V., Скорб, Е. В., & Skirtach, A. G. (2020) · Coatings · doi:10.3390/coatings10111131 · Cited by 88 · see citing works
Hyaluronan-Inorganic Nanohybrid Materials for Biomedical Applications
Cai, Z., Zhang, H., Wei, Y. Z., & Cong, F. (2017) · Biomacromolecules · doi:10.1021/acs.biomac.7b00424 · Cited by 87 · see citing works
Layer-by-Layer assembled nano-drug delivery systems for cancer treatment
Zhang, X., Liang, T., & Ma, Q. (2021) · Drug Delivery · doi:10.1080/10717544.2021.1905748 · Cited by 87 · see citing works
Abdel-Rahman, R. M., Abdel-Mohsen, A. M., Hrdina, R., Burgert, L., Fohlerová, Z., Pavliňák, D., Sayed, O. N., & Jancar, J. (2016) · International Journal of Biological Macromolecules · doi:10.1016/j.ijbiomac.2016.04.087 · Cited by 82 · see citing works
Crosslinked Hyaluronan Electrospun Nanofibers for Ferulic Acid Ocular Delivery
Grimaudo, M. A., Concheiro, Á., & Alvarez‐Lorenzo, C. (2020) · Pharmaceutics · doi:10.3390/pharmaceutics12030274 · Cited by 77 · see citing works
Ray, P., Confeld, M. I., Borowicz, P. P. P., Wang, T., Mallik, S., & Quadir, M. (2018) · Colloids and Surfaces B Biointerfaces · doi:10.1016/j.colsurfb.2018.10.069 · Cited by 75 · see citing works
Application of nanomaterials in cancer immunotherapy
Qian, H., Liu, B., & Jiang, X. (2018) · Materials Today Chemistry · doi:10.1016/j.mtchem.2018.01.001 · Cited by 75 · see citing works
Miller‐Kleinhenz, J. M., Bozeman, E. N., & Yang, L. P. H. (2015) · Wiley Interdisciplinary Reviews Nanomedicine and Nanobiotechnology · doi:10.1002/wnan.1343 · Cited by 73 · see citing works
Yu, M., Lei, B., Gao, C., Yan, J., & Ma, P. X. (2016) · Nano Research · doi:10.1007/s12274-016-1265-9 · Cited by 74 · see citing works
Huang, W.-C., Chen, S., Chiang, W., Huang, C.-W., Lo, C.-L., Chern, C., & Chiu, H. (2016) · Biomacromolecules · doi:10.1021/acs.biomac.6b00956 · Cited by 73 · see citing works
Li, Z., Wang, F., Li, Y., Wang, X., Qiao, L., Wang, D., Qi, C., Li, C., Li, Z., Lian, B., et al. (2021) · Biomaterials · doi:10.1016/j.biomaterials.2021.121003 · Cited by 64 · see citing works
Zou, H., Wang, Z., & Feng, M. (2015) · Journal of Controlled Release · doi:10.1016/j.jconrel.2015.07.014 · Cited by 64 · see citing works
Fan, B., Fan, Q., Cui, M., Wu, T., Wang, J., Ma, H., & Wei, Q. L. (2019) · ACS Applied Materials & Interfaces · doi:10.1021/acsami.9b06937 · Cited by 63 · see citing works
Li, D., Hu, X., & Zhang, S. (2019) · Biomaterials · doi:10.1016/j.biomaterials.2019.02.020 · Cited by 62 · see citing works
Li, M., Guo, R., Wei, J., Deng, M., Li, J., Tao, Y., Li, M., & He, Q. (2021) · Acta Biomaterialia · doi:10.1016/j.actbio.2021.09.014 · Cited by 61 · see citing works
Tumor-Targeted Synergistic Blockade of MAPK and PI3K from a Layer-by-Layer Nanoparticle
Dreaden, E. C., Kong, Y. W., Morton, S. W., Correa, S., Choi, K. Y., Shopsowitz, K. E., Renggli, K., Drapkin, R., Yaffe, M. B., & Hammond, P. T. (2015) · Clinical Cancer Research · doi:10.1158/1078-0432.ccr-15-0013 · Cited by 59 · see citing works
Self-citationResponsive Polymers as Smart Nanomaterials Enable Diverse Applications
Zhao, J., Lee, V. E., Liu, R., & Priestley, R. D. (2019) · Annual Review of Chemical and Biomolecular Engineering · doi:10.1146/annurev-chembioeng-060718-030155 · Cited by 61 · see citing works
Ray, P., Dutta, D., Haque, I., Nair, G., Mohammed, J., Parmer, M., Kale, N. R., Orr, M., Jain, P., Banerjee, S., et al. (2020) · Molecular Pharmaceutics · doi:10.1021/acs.molpharmaceut.0c00499 · Cited by 60 · see citing works
Intracameral Delivery of Layer‐by‐Layer Coated siRNA Nanoparticles for Glaucoma Therapy
Dillinger, A. E., Guter, M., Froemel, F., Weber, G. R., Perkumas, K. M., Stamer, W. D., Ohlmann, A., Fuchshofer, R., & Breunig, M. (2018) · Small · doi:10.1002/smll.201803239 · Cited by 66 · see citing works
Ray, P., Ferraro, M., Haag, R., & Quadir, M. (2019) · Macromolecular Bioscience · doi:10.1002/mabi.201900073 · Cited by 59 · see citing works
Targeting nucleic acid-based therapeutics to tumors: Challenges and strategies for polyplexes
Vetter, V. C., & Wagner, E. (2022) · Journal of Controlled Release · doi:10.1016/j.jconrel.2022.04.013 · Cited by 59 · see citing works
Abdel-Mohsen, A. M., Pavliňák, D., Čileková, M., Lepcio, P., Abdel-Rahman, R. M., & Jančář, J. (2019) · International Journal of Biological Macromolecules · doi:10.1016/j.ijbiomac.2019.07.205 · Cited by 59 · see citing works
Recent progress on functional polymeric membranes for CO2 separation from flue gases: A review
Jana, A., & Modi, A. (2024) · Carbon Capture Science & Technology · doi:10.1016/j.ccst.2024.100204 · Cited by 58 · see citing works
A cooperative polymeric platform for tumor-targeted drug delivery
Song, W., Tang, Z., Zhang, D., Li, M., Gu, J., & Chen, X. (2015) · Chemical Science · doi:10.1039/c5sc01698c · Cited by 57 · see citing works
Zheng, G., Zhang, B., Yu, H., Song, Z., Xu, X., Zheng, Z., Zhao, K., Zhao, J. H., & Zhao, Y. (2025) · Advanced Composites and Hybrid Materials · doi:10.1007/s42114-025-01292-3 · Cited by 56 · see citing works
Polyphenol-Based Nanoparticles: A Promising Frontier for Enhanced Colorectal Cancer Treatment
Wahnou, H., Liagre, B., Sol, V., Attar, H. E., Attar, R., Oudghiri, M., Duval, R. E., & Limami, Y. (2023) · Cancers · doi:10.3390/cancers15153826 · Cited by 55 · see citing works
Chen, W., Luo, G., Qiu, W., Lei, Q., Hong, S., Wang, S., Zheng, D., Zhu, C., Zeng, X., Feng, J. X., et al. (2015) · Small · doi:10.1002/smll.201503280 · Cited by 55 · see citing works
Hlaing, S. P., Cao, J., Lee, J., Kim, J., Saparbayeva, A., Kwak, D., Kim, H., Hwang, S., Yun, H., Moon, H. R., et al. (2022) · Pharmaceutics · doi:10.3390/pharmaceutics14102118 · Cited by 54 · see citing works
Chen, F., Liu, Q., Xiong, Y., & Xu, L. (2021) · International Journal of Nanomedicine · doi:10.2147/ijn.s310952 · Cited by 51 · see citing works
Ariga, K., Ji, Q., Nakanishi, W., & Hill, J. P. (2015) · Journal of Inorganic and Organometallic Polymers and Materials · doi:10.1007/s10904-015-0179-4 · Cited by 50 · see citing works
‘Smart’ nanoparticles as drug delivery systems for applications in tumor therapy
Fang, Z., Wan, L., Chu, L., Zhang, Y., & Wu, J. (2015) · Expert Opinion on Drug Delivery · doi:10.1517/17425247.2015.1071352 · Cited by 50 · see citing works
Nabar, N., Dacoba, T. G., Covarrubias, G., Romero-Cruz, D., & Hammond, P. T. (2024) · Proceedings of the National Academy of Sciences · doi:10.1073/pnas.2307809121 · Cited by 48 · see citing works
Self-citationGiarra, S., Serri, C., Russo, L., Zeppetelli, S., Rosa, G. D., Borzacchiello, A., Biondi, M., Ambrosio, L., & Mayol, L. (2015) · Carbohydrate Polymers · doi:10.1016/j.carbpol.2015.12.031 · Cited by 47 · see citing works
Luo, J., Schmaus, J., Cui, M., Hörterer, E., Wilk, U., Höhn, M., Däther, M., Berger, S., Benli‐Hoppe, T., Peng, L., et al. (2020) · Journal of Controlled Release · doi:10.1016/j.jconrel.2020.10.022 · Cited by 47 · see citing works
Smart and bioinspired systems for overcoming biological barriers and enhancing disease theranostics
Li, X., Gao, Y., Li, H., Majoral, J., Shi, X., & Pich, A. (2023) · Progress in Materials Science · doi:10.1016/j.pmatsci.2023.101170 · Cited by 46 · see citing works
Technological solutions for encapsulation
Trojanowska, A., Nogalska, A., Garcia‐Valls, R., Giamberini, M., & Tylkowski, B. (2017) · Physical Sciences Reviews · doi:10.1515/psr-2017-0020 · Cited by 45 · see citing works
Electrostatic Conjugation of Nanoparticle Surfaces with Functional Peptide Motifs
Boehnke, N., Dolph, K. J., Juarez, V. M., Lanoha, J., & Hammond, P. T. (2020) · Bioconjugate Chemistry · doi:10.1021/acs.bioconjchem.0c00384 · Cited by 43 · see citing works
Self-citationFacile fabrication of polydopamine nanotubes for combined chemo-photothermal therapy
Sun, Y., & Davis, E. W. (2019) · Journal of Materials Chemistry B · doi:10.1039/c9tb01338e · Cited by 44 · see citing works
Liu, J., Zhang, D., Lian, S., Zheng, J., Li, B., Li, T., & Jia, L. (2018) · International Journal of Nanomedicine · doi:10.2147/ijn.s173889 · Cited by 44 · see citing works
Hyaluronan/Poly-L-lysine/Berberine Nanogels for Impaired Wound Healing
Amato, G., Grimaudo, M. A., Alvarez‐Lorenzo, C., Concheiro, Á., Carbone, C., Bonaccorso, A., Puglisi, G., & Musumeci, T. (2020) · Pharmaceutics · doi:10.3390/pharmaceutics13010034 · Cited by 44 · see citing works
Lei, P., Yu, H., Ma, J., Du, J., Fang, Y., Yang, Q., Zhang, K., Luo, L., Jin, L., Wu, W., et al. (2023) · International Journal of Biological Macromolecules · doi:10.1016/j.ijbiomac.2023.126000 · Cited by 43 · see citing works
Kv, R., Liu, T., Lu, I.-L., Liu, C., Chen, H., Lu, T.-Y., Chiang, W., & Chiu, H. (2020) · Journal of Controlled Release · doi:10.1016/j.jconrel.2020.08.038 · Cited by 39 · see citing works
Layer‐by‐layer interleukin‐12 nanoparticles drive a safe and effective response in ovarian tumors
Barberio, A. E., Smith, S. G., Pires, I. S., Iyer, S., Reinhardt, F., Melo, M. B., Suh, H., Weinberg, R. A., Irvine, D. J., & Hammond, P. T. (2022) · Bioengineering & Translational Medicine · doi:10.1002/btm2.10453 · Cited by 38 · see citing works
Self-citationNanomechanical Behavior of High Gas Barrier Multilayer Thin Films
Humood, M., Chowdhury, S., Song, Y., Tzeng, P., Grunlan, J. C., & Polycarpou, A. A. (2016) · ACS Applied Materials & Interfaces · doi:10.1021/acsami.5b11478 · Cited by 36 · see citing works
Layer-by-layer technique for enhancing physicochemical properties of actives
Shende, P. K., Patil, A., & Prabhakar, B. R. (2020) · Journal of Drug Delivery Science and Technology · doi:10.1016/j.jddst.2020.101519 · Cited by 36 · see citing works
Hyaluronan/Hyaladherins - a Promising Axis for Targeted Drug Delivery in Cancer
Nikitovic, D., Kouvidi, K., Kavasi, R., Berdiaki, A., & Tzanakakis, G. N. (2015) · Current Drug Delivery · doi:10.2174/1567201813666151109103013 · Cited by 36 · see citing works
Gao, M., Deng, H. X., Zhang, Y., Wang, H., Liu, R., Hou, W., & Zhang, W. (2023) · Carbohydrate Polymers · doi:10.1016/j.carbpol.2023.121415 · Cited by 35 · see citing works
Kim, H., Park, Y., Stevens, M. M., Kwon, W., & Hahn, S. K. (2019) · Journal of Controlled Release · doi:10.1016/j.jconrel.2019.04.003 · Cited by 34 · see citing works
Wang, L., Yu, M., & Yang, H. (2021) · Journal of Inflammation Research · doi:10.2147/jir.s304101 · Cited by 33 · see citing works
Liu, R., Dai, J., Ma, L., Chen, J., Shi, X., Du, Y., Li, Z., & Deng, H. (2019) · Journal of Colloid and Interface Science · doi:10.1016/j.jcis.2019.01.054 · Cited by 31 · see citing works
Poudel, B. K., Hwang, J., Ku, S., Kim, J. O., & Byeon, J. H. (2018) · NPG Asia Materials · doi:10.1038/s41427-018-0068-8 · Cited by 30 · see citing works
Bi-Functionalized Clay Nanotubes for Anti-Cancer Therapy
Grimes, W., Luo, Y., McFarland, A., & Mills, D. K. (2018) · Applied Sciences · doi:10.3390/app8020281 · Cited by 29 · see citing works
- Authors
- Dreaden, E. C., Morton, S. W., Shopsowitz, K. E., Choi, J.-H., Deng, Z. J., Cho, N.-J., & Hammond, P. T.
- Affiliations
- Nanyang Technological University (SG)
- Corresponding author
- Hammond, Paula T.
- Venue
- ACS Nano
- Publisher
- American Chemical Society (ACS)
- Published
- 2014-08-06
- Volume
- 8
- Issue
- 8
- Pages
- 8374-8382
- ISSN
- 1936-0851 (ISSN-L)
- 1936-086X
- PMC
- PMC4148172
- OpenAlex
- W2047101821
- Cited by
- 179
- References
- 60
- Citations by year
- 2026: 5 · 2025: 13 · 2024: 6 · 2023: 12 · 2022: 18 · 2021: 14 · 2020: 26 · 2019: 16 · 2018: 15 · 2017: 11 · 2016: 21 · 2015: 22
- FWCI
- 6.83
- Type
- journal article
- Language
- en
- Open access
- hybrid
- doi.org
- Locations
- ACS Nano (publishedVersion, other-oa)
- PubMed Central (publishedVersion)
- PubMed (publishedVersion)
- DSpace@MIT (Massachusetts Institute of Technology) (submittedVersion, cc-by-nc)
- Funders
- National Science Foundation (NA)
- National Institutes of Health (1F32EB017614-02)
- National Cancer Institute (P30-CA14051)
- Division of Materials Research (DMR-0819762)
- Janssen Research and Development (NA)
- Natural Sciences and Engineering Research Council of Canada (NA)
- National Health and Medical Research Council (NA)
- National Research Foundation-Prime Minister's office, Republic of Singapore (NRF-NRFF2011-01)
- Topics
- Physical Sciences › Materials Science › Biomaterials › Nanoparticle-Based Drug Delivery
- Life Sciences › Biochemistry, Genetics and Molecular Biology › Molecular Medicine › Hydrogels: synthesis, properties, applications
- Physical Sciences › Engineering › Biomedical Engineering › Nanoplatforms for cancer theranostics
- Keywords
- layer-by-layer nanoparticles, hyaluronic acid, CD44 receptor, tumor microenvironment, pH-responsive drug delivery, tumor hypoxia, active tumor targeting, cancer stem cells, breast cancer, ovarian cancer, polyamines, tumor cell migration, tumor penetration
- MeSH terms
- Animals, Biological Transport, Cell Transformation, Neoplastic, Drug Carriers, Hyaluronic Acid, Hydrogen-Ion Concentration, Polylysine, Cell Hypoxia, Hyaluronan Receptors, Cell Line, Tumor, Mice, Nanoparticles, Tumor Microenvironment
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