Cancer Nanomedicines in an Evolving Oncology Landscape

2019, Global, regional, and national cancer incidence, mortality, years of life lost, years lived with disability, and disability-adjusted life-years for 29 cancer groups, 1990 to 2017: a systematic analysis for the Global Burden of Disease Study, JAMA Oncol., 5, 1749, 10.1001/jamaoncol.2019.2996 Shi, 2017, Cancer nanomedicine: progress, challenges and opportunities, Nat. Rev. Cancer, 17, 20, 10.1038/nrc.2016.108 Mitchell, 2017, Engineering and physical sciences in oncology: challenges and opportunities, Nat. Rev. Cancer, 17, 659, 10.1038/nrc.2017.83 Chen, 2017, Rethinking cancer nanotheranostics, Nat. Rev. Mater., 2, 10.1038/natrevmats.2017.24 Tran and Tran, 2019, Nanoconjugation and encapsulation strategies for improving drug delivery and therapeutic efficacy of poorly water-soluble drugs, Pharmaceutics, 11, 325, 10.3390/pharmaceutics11070325 Wang, 2017, External triggering and triggered targeting strategies for drug delivery, Nat. Rev. Mater., 2, 10.1038/natrevmats.2017.20 He, 2019, Survey of clinical translation of cancer nanomedicines – lessons learned from successes and failures, Acc. Chem. Res., 52, 2445, 10.1021/acs.accounts.9b00228 Wolfram, 2019, Clinical cancer nanomedicine, Nano Today, 25, 85, 10.1016/j.nantod.2019.02.005 Wan, 2020, Genome editing of mutant KRAS through supramolecular polymer-mediated delivery of Cas9 ribonucleoprotein for colorectal cancer therapy, J. Control. Release, 322, 236, 10.1016/j.jconrel.2020.03.015 Chiang, 2018, Combination of fucoidan-based magnetic nanoparticles and immunomodulators enhances tumour-localized immunotherapy, Nat. Nanotechnol., 13, 746, 10.1038/s41565-018-0146-7 Morad, 2019, Tumor-derived extracellular vesicles breach the intact blood–brain barrier via transcytosis, ACS Nano, 13, 13853, 10.1021/acsnano.9b04397 Kingston, 2019, Assessing micrometastases as a target for nanoparticles using 3D microscopy and machine learning, Proc. Natl. Acad. Sci. U. S. A., 116, 14937, 10.1073/pnas.1907646116 Zhou, 2017, Nonviral cancer gene therapy: delivery cascade and vector nanoproperty integration, Adv. Drug Deliv. Rev., 115, 115, 10.1016/j.addr.2017.07.021 Anguela, 2019, Entering the modern era of gene therapy, Annu. Rev. Med., 70, 273, 10.1146/annurev-med-012017-043332 Rui, 2019, Non-viral delivery to enable genome editing, Trends Biotechnol., 37, 281, 10.1016/j.tibtech.2018.08.010 Ginn, 2018, Gene therapy clinical trials worldwide to 2017: an update, J. Gene Med., 20, 10.1002/jgm.3015 Carboni, 2019, Synthetic vehicles for encapsulation and delivery of CRISPR/Cas9 gene editing machinery, Adv. Ther., 2 Kong, 2019, Synthetic mRNA nanoparticle-mediated restoration of p53 tumor suppressor sensitizes p53-deficient cancers to mTOR inhibition, Sci. Transl. Med., 11, 10.1126/scitranslmed.aaw1565 Islam, 2018, Restoration of tumour-growth suppression in vivo via systemic nanoparticle-mediated delivery of PTEN mRNA, Nat. Biomed. Eng., 2, 850, 10.1038/s41551-018-0284-0 Wang, 2018, Shape-controlled magnetic mesoporous silica nanoparticles for magnetically-mediated suicide gene therapy of hepatocellular carcinoma, Biomaterials, 154, 147, 10.1016/j.biomaterials.2017.10.047 Mullen, 1994, Tumors expressing the cytosine deaminase suicide gene can be eliminated in vivo with 5-fluorocytosine and induce protective immunity to wild type tumor, Cancer Res., 54, 1503 Rossignoli, 2019, Inducible caspase 9-mediated suicide gene for MSC-based cancer gene therapy, Cancer Gene Ther., 26, 11, 10.1038/s41417-018-0034-1 Erkan, 2017, Extracellular vesicle-mediated suicide mRNA/protein delivery inhibits glioblastoma tumor growth in vivo, Cancer Gene Ther., 24, 38, 10.1038/cgt.2016.78 Kowalski, 2019, Delivering the messenger: advances in technologies for therapeutic mRNA delivery, Mol. Ther., 27, 710, 10.1016/j.ymthe.2019.02.012 Hajj, 2017, Tools for translation: non-viral materials for therapeutic mRNA delivery, Nat. Rev. Mater., 2, 1, 10.1038/natrevmats.2017.56 Patel, 2019, Inhaled nanoformulated mRNA polyplexes for protein production in lung epithelium, Adv. Mater., 31 Kaczmarek, 2018, Optimization of a degradable polymer–lipid nanoparticle for potent systemic delivery of mRNA to the lung endothelium and immune cells, Nano Lett., 18, 6449, 10.1021/acs.nanolett.8b02917 Oberli, 2017, Lipid nanoparticle assisted mRNA delivery for potent cancer immunotherapy, Nano Lett., 17, 1326, 10.1021/acs.nanolett.6b03329 Paunovska, 2019, Nanoparticles containing oxidized cholesterol deliver mRNA to the liver microenvironment at clinically relevant doses, Adv. Mater., 31 McKinlay, 2017, Charge-altering releasable transporters (CARTs) for the delivery and release of mRNA in living animals, Proc. Natl. Acad. Sci. U. S. A., 114, E448, 10.1073/pnas.1614193114 Haabeth, 2019, Local delivery of Ox40l, Cd80, and Cd86 mRNA kindles global anticancer immunity, Cancer Res., 79, 1624, 10.1158/0008-5472.CAN-18-2867 Yoshinaga, 2019, Bundling mRNA strands to prepare nano-assemblies with enhanced stability towards rnase for in vivo delivery, Angew. Chem. Int. Ed. Engl., 58, 11360, 10.1002/anie.201905203 Li, 2017, Structurally programmed assembly of translation initiation nanoplex for superior mRNA delivery, ACS Nano, 11, 2531, 10.1021/acsnano.6b08447 Li, 2017, Polyamine-mediated stoichiometric assembly of ribonucleoproteins for enhanced mRNA delivery, Angew. Chem. Int. Ed. Engl., 56, 13709, 10.1002/anie.201707466 Forterre, 2020, Extracellular vesicle-mediated in vitro transcribed mrna delivery for treatment of HER2+ breast cancer xenografts in mice by prodrug CB1954 without general toxicity, Mol. Cancer Ther., 19, 858, 10.1158/1535-7163.MCT-19-0928 Hoy, 2018, Patisiran: first global approval, Drugs, 78, 1625, 10.1007/s40265-018-0983-6 Zheng, 2018, Nanotechnology-nased strategies for siRNA brain delivery for disease therapy, Trends Biotechnol., 36, 562, 10.1016/j.tibtech.2018.01.006 Park, 2016, Pharmacokinetics and biodistribution of recently-developed siRNA nanomedicines, Adv. Drug Deliv. Rev., 104, 93, 10.1016/j.addr.2015.12.004 Kim, 2016, Recent progress in development of siRNA delivery vehicles for cancer therapy, Adv. Drug Deliv. Rev., 104, 61, 10.1016/j.addr.2016.06.011 Yin, 2016, Therapeutic genome editing by combined viral and non-viral delivery of CRISPR system components in vivo, Nat. Biotechnol., 34, 328, 10.1038/nbt.3471 Chen, 2019, A biodegradable nanocapsule delivers a Cas9 ribonucleoprotein complex for in vivo genome editing, Nat. Nanotechnol., 14, 974, 10.1038/s41565-019-0539-2 Liu, 2019, Fast and efficient CRISPR/Cas9 genome editing in vivo enabled by bioreducible lipid and messenger RNA nanoparticles, Adv. Mater., 31, 10.1002/adma.201902575 Xu, 2019, Development of 'CLAN' nanomedicine for nucleic acid therapeutics, Small, 15, 10.1002/smll.201900055 Guo, 2019, Therapeutic genome editing of triple-negative breast tumors using a noncationic and deformable nanolipogel, Proc. Natl. Acad. Sci. U. S. A., 116, 18295, 10.1073/pnas.1904697116 Wang, 2017, Genome editing for cancer therapy: delivery of Cas9 protein/sgRNA plasmid via a gold nanocluster/lipid core–shell nanocarrier, Adv. Sci., 4, 10.1002/advs.201700175 Mout, 2017, Direct cytosolic delivery of CRISPR/Cas9-ribonucleoprotein for efficient gene editing, ACS Nano, 11, 2452, 10.1021/acsnano.6b07600 Guo, 2018, Nanoparticle elasticity directs tumor uptake, Nat. Commun., 9, 130, 10.1038/s41467-017-02588-9 Yin, 2016, Therapeutic genome editing by combined viral and non-viral delivery of CRISPR system components in vivo, Nat. Biotechnol., 34, 328, 10.1038/nbt.3471 Maeder, 2019, Development of a gene-editing approach to restore vision loss in Leber congenital amaurosis type 10, Nat. Med., 25, 229, 10.1038/s41591-018-0327-9 De Ravin, 2017, CRISPR-Cas9 gene repair of hematopoietic stem cells from patients with X-linked chronic granulomatous disease, Sci. Transl. Med., 9, 10.1126/scitranslmed.aah3480 Irvine, 2020, Enhancing cancer immunotherapy with nanomedicine, Nat. Rev. Immunol., 20, 321, 10.1038/s41577-019-0269-6 Martin, 2020, Improving cancer immunotherapy using nanomedicines: progress, opportunities and challenges, Nat. Rev. Clin. Oncol., 17, 251, 10.1038/s41571-019-0308-z Goldberg, 2019, Improving cancer immunotherapy through nanotechnology, Nat. Rev. Cancer, 19, 587, 10.1038/s41568-019-0186-9 Chauhan, 2019, Reprogramming the microenvironment with tumor-selective angiotensin blockers enhances cancer immunotherapy, Proc. Natl. Acad. Sci. U. S. A., 116, 10674, 10.1073/pnas.1819889116 Zhang, 2018, Nanoparticle anchoring targets immune agonists to tumors enabling anti-cancer immunity without systemic toxicity, Nat. Commun., 9 Schmid, 2017, T cell-targeting nanoparticles focus delivery of immunotherapy to improve antitumor immunity, Nat. Commun., 8, 1747, 10.1038/s41467-017-01830-8 Rodell, 2018, TLR7/8-agonist-loaded nanoparticles promote the polarization of tumour-associated macrophages to enhance cancer immunotherapy, Nat. Biomed. Eng., 2, 578, 10.1038/s41551-018-0236-8 Chen, 2020, Intratumoral delivery of CCL25 enhances immunotherapy against triple-negative breast cancer by recruiting CCR9+ T cells, Sci. Adv., 6 Xu, 2020, Nano-puerarin regulates tumor microenvironment and facilitates chemo- and immunotherapy in murine triple negative breast cancer model, Biomaterials, 235, 10.1016/j.biomaterials.2020.119769 Chen, 2019, Blocking CXCR4 alleviates desmoplasia, increases T-lymphocyte infiltration, and improves immunotherapy in metastatic breast cancer, Proc. Natl. Acad. Sci. U. S. A., 116, 4558, 10.1073/pnas.1815515116 Billingsley, 2020, Ionizable lipid nanoparticle-mediated mRNA delivery for human CAR T cell engineering, Nano Lett., 20, 1578, 10.1021/acs.nanolett.9b04246 Olden, 2018, Cationic polymers for non-viral gene delivery to human T cells, J. Control. Release, 282, 140, 10.1016/j.jconrel.2018.02.043 Smith, 2017, In situ programming of leukaemia-specific T cells using synthetic DNA nanocarriers, Nat. Nanotechnol., 12, 813, 10.1038/nnano.2017.57 Tang, 2018, Enhancing T cell therapy through TCR-signaling-responsive nanoparticle drug delivery, Nat. Biotechnol., 36, 707, 10.1038/nbt.4181 Zhu, 2017, Intertwining DNA–RNA nanocapsules loaded with tumor neoantigens as synergistic nanovaccines for cancer immunotherapy, Nat. Commun., 8, 10.1038/s41467-017-01386-7 Kuai, 2017, Designer vaccine nanodiscs for personalized cancer immunotherapy, Nat. Mater., 16, 489, 10.1038/nmat4822 Shae, 2019, Endosomolytic polymersomes increase the activity of cyclic dinucleotide STING agonists to enhance cancer immunotherapy, Nat. Nanotechnol., 14, 269, 10.1038/s41565-018-0342-5 Min, 2017, Antigen-capturing nanoparticles improve the abscopal effect and cancer immunotherapy, Nat. Nanotechnol., 12, 877, 10.1038/nnano.2017.113 Chen, 2018, Clay nanoparticles elicit long-term immune responses by forming biodegradable depots for sustained antigen stimulation, Small, 14, 10.1002/smll.201704465 Kapadia, 2018, Extending antigen release from particulate vaccines results in enhanced antitumor immune response, J. Control. Release, 269, 393, 10.1016/j.jconrel.2017.11.020 Wiklander, 2019, Advances in therapeutic applications of extracellular vesicles, Sci. Transl. Med., 11, 10.1126/scitranslmed.aav8521 Xu, 2018, Extracellular vesicles in cancer – implications for future improvements in cancer care, Nat. Rev. Clin. Oncol., 15, 617, 10.1038/s41571-018-0036-9 Maas, 2017, Extracellular vesicles: unique intercellular delivery vehicles, Trends Cell Biol., 27, 172, 10.1016/j.tcb.2016.11.003 Pi, 2018, Nanoparticle orientation to control RNA loading and ligand display on extracellular vesicles for cancer regression, Nat. Nanotechnol., 13, 82, 10.1038/s41565-017-0012-z Yang, 2020, Large-scale generation of functional mRNA-encapsulating exosomes via cellular nanoporation, Nat. Biomed. Eng., 4, 69, 10.1038/s41551-019-0485-1 Nie, 2020, Use of lung-specific exosomes for miRNA-126 delivery in non-small cell lung cancer, Nanoscale, 12, 877, 10.1039/C9NR09011H Kim, 2017, Cancer-derived exosomes as a delivery platform of CRISPR/Cas9 confer cancer cell tropism-dependent targeting, J. Control. Release, 266, 8, 10.1016/j.jconrel.2017.09.013 Morishita, 2016, Exosome-based tumor antigens-adjuvant co-delivery utilizing genetically engineered tumor cell-derived exosomes with immunostimulatory CpG DNA, Biomaterials, 111, 55, 10.1016/j.biomaterials.2016.09.031 Garofalo, 2019, Extracellular vesicles enhance the targeted delivery of immunogenic oncolytic adenovirus and paclitaxel in immunocompetent mice, J. Control. Release, 294, 165, 10.1016/j.jconrel.2018.12.022 Hoshino, 2015, Tumour exosome integrins determine organotropic metastasis, Nature, 527, 329, 10.1038/nature15756 Morad, 2019, Brainwashed by extracellular vesicles: the role of extracellular vesicles in primary and metastatic brain tumour microenvironment, J. Extracell. Vesicles, 8, 10.1080/20013078.2019.1627164 Wang, 2019, Exosomes from M1-polarized macrophages enhance paclitaxel antitumor activity by activating macrophages-mediated inflammation, Theranostics, 9, 1714, 10.7150/thno.30716 O’Brien, 2015, miR-134 in extracellular vesicles reduces triple-negative breast cancer aggression and increases drug sensitivity, Oncotarget, 6, 32774, 10.18632/oncotarget.5192 Watson, 2016, Efficient production and enhanced tumor delivery of engineered extracellular vesicles, Biomaterials, 105, 195, 10.1016/j.biomaterials.2016.07.003 Lunavat, 2016, RNAi delivery by exosome-mimetic nanovesicles – implications for targeting c-Myc in cancer, Biomaterials, 102, 231, 10.1016/j.biomaterials.2016.06.024 Yang, 2016, Functional exosome-mimic for deliv ery of siRNA to cancer: in vitro and in vivo evaluation, J. Control. Release, 243, 160, 10.1016/j.jconrel.2016.10.008 Kooijmans, 2013, Electroporation-induced siRNA precipitation obscures the efficiency of siRNA loading into extracellular vesicles, J. Control. Release, 172, 229, 10.1016/j.jconrel.2013.08.014 Lamichhane, 2015, Exogenous DNA loading into extracellular vesicles via electroporation is size-dependent and enables limited gene delivery, Mol. Pharm., 12, 3650, 10.1021/acs.molpharmaceut.5b00364 Jeyaram, 2020, Enhanced loading of functional miRNA cargo via pH gradient modification of extracellular vesicles, Mol. Ther., 28, 975, 10.1016/j.ymthe.2019.12.007 Fuhrmann, 2015, Active loading into extracellular vesicles significantly improves the cellular uptake and photodynamic effect of porphyrins, J. Control. Release, 205, 35, 10.1016/j.jconrel.2014.11.029 Gao, 2018, Anchor peptide captures, targets, and loads exosomes of diverse origins for diagnostics and therapy, Sci. Transl. Med., 10, 10.1126/scitranslmed.aat0195 Piffoux, 2018, Modification of extracellular vesicles by fusion with liposomes for the design of personalized biogenic drug delivery systems, ACS Nano, 12, 6830, 10.1021/acsnano.8b02053 Reshke, 2020, Reduction of the therapeutic dose of silencing RNA by packaging it in extracellular vesicles via a pre-microRNA backbone, Nat. Biomed. Eng., 4, 52, 10.1038/s41551-019-0502-4 Sawada, 2020, Nanogel hybrid assembly for exosome intracellular delivery: effects on endocytosis and fusion by exosome surface polymer engineering, Biomater. Sci., 8, 619, 10.1039/C9BM01232J de Jong, 2019, Drug delivery with extracellular vesicles: from imagination to innovation, Acc. Chem. Res., 52, 1761, 10.1021/acs.accounts.9b00109 Smyth, 2015, Biodistribution and delivery efficiency of unmodified tumor-derived exosomes, J. Control. Release, 199, 145, 10.1016/j.jconrel.2014.12.013 Zhu, 2019, Embryonic stem cells-derived exosomes endowed with targeting properties as chemotherapeutics delivery vehicles for glioblastoma therapy, Adv. Sci., 6, 10.1002/advs.201801899 Kooijmans, 2016, PEGylated and targeted extracellular vesicles display enhanced cell specificity and circulation time, J. Control. Release, 224, 77, 10.1016/j.jconrel.2016.01.009 Alvarez-Erviti, 2011, Delivery of siRNA to the mouse brain by systemic injection of targeted exosomes, Nat. Biotechnol., 29, 341, 10.1038/nbt.1807 Kooijmans, 2016, Display of GPI-anchored anti-EGFR nanobodies on extracellular vesicles promotes tumour cell targeting, J. Extracell. Vesicles, 5, 10.3402/jev.v5.31053 Royo, 2019, Modification of the glycosylation of extracellular vesicles alters their biodistribution in mice, Nanoscale, 11, 1531, 10.1039/C8NR03900C Topol, 2019, High-performance medicine: the convergence of human and artificial intelligence, Nat. Med., 25, 44, 10.1038/s41591-018-0300-7 McKinney, 2020, International evaluation of an AI system for breast cancer screening, Nature, 577, 89, 10.1038/s41586-019-1799-6 Yamankurt, 2019, Exploration of the nanomedicine-design space with high-throughput screening and machine learning, Nat. Biomed. Eng., 3, 318, 10.1038/s41551-019-0351-1 Li, 2019, Design of self-assembly dipeptide hydrogels and machine learning via their chemical features, Proc. Natl. Acad. Sci. U. S. A., 116, 11259, 10.1073/pnas.1903376116 Han, 2019, Predicting physical stability of solid dispersions by machine learning techniques, J. Control. Release, 311, 16, 10.1016/j.jconrel.2019.08.030 Shamay, 2018, Quantitative self-assembly prediction yields targeted nanomedicines, Nat. Mater., 17, 361, 10.1038/s41563-017-0007-z Price, 2019, An in vitro assay and artificial intelligence approach to determine rate constants of nanomaterial–cell interactions, Sci. Rep., 9 Large, 2019, Advances in receptor-mediated, tumor-targeted drug delivery, Adv. Ther., 2 Alshaer, 2018, Aptamer-guided nanomedicines for anticancer drug delivery, Adv. Drug Deliv. Rev., 134, 122, 10.1016/j.addr.2018.09.011 Guo, 2019, Dual complementary liposomes inhibit triple-negative breast tumor progression and metastasis, Sci. Adv., 5, 10.1126/sciadv.aav5010 Ho, 2019, Artificial intelligence in nanomedicine, Nanoscale Horiz., 4, 365, 10.1039/C8NH00233A Zhang, 2017, Integrating evolutionary dynamics into treatment of metastatic castrate-resistant prostate cancer, Nat. Commun., 8, 10.1038/s41467-017-01968-5 Chmielecki, 2011, Optimization of dosing for EGFR-mutant non-small cell lung cancer with evolutionary cancer modeling, Sci. Transl. Med., 3, 90ra59, 10.1126/scitranslmed.3002356 Enriquez-Navas, 2016, Exploiting evolutionary principles to prolong tumor control in preclinical models of breast cancer, Sci. Transl. Med., 8, 327ra24, 10.1126/scitranslmed.aad7842 Wang, 2015, Mechanism-independent pptimization of combinatorial nanodiamond and unmodified drug delivery using a phenotypically driven platform technology, ACS Nano, 9, 3332, 10.1021/acsnano.5b00638 von Maltzahn, 2011, Nanoparticles that communicate in vivo to amplify tumour targeting, Nat. Mater., 10, 545, 10.1038/nmat3049