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Using nanoparticles for in situ vaccination against cancer: mechanisms and immunotherapy benefits

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Pages 18-33 | Received 05 May 2020, Accepted 23 Jul 2020, Published online: 10 Jan 2021

References

  • Abe BT, Shin DS, Mocholi E, et al. NFAT1 supports tumor-induced energy of CD4(+) T cells. Cancer Res. 2012;72:4642–4651.
  • Rabinovich GA, Gabrilovich D, Sotomayor EM. Immunosuppressive strategies that are mediated by tumor cells. Annu Rev Immunol. 2007;25:267–296.
  • Zamarin D, Ricca JM, Sadekova S, et al. PD-L1 in tumor microenvironment mediates resistance to oncolytic immunotherapy. J Clin Invest. 2018;128:1413–1428.
  • Wei SC, Anang NAAS, Sharma R, et al. Combination anti-CTLA-4 plus anti-PD-1 checkpoint blockade utilizes cellular mechanisms partially distinct from monotherapies. Proc Natl Acad Sci U S A. 2019;116:22699–22709.
  • Zamarin D, Holmgaard RB, Subudhi SK, et al. Localized oncolytic virotherapy overcomes systemic tumor resistance to immune checkpoint blockade immunotherapy. Sci Transl Med. 2014;6:226ra32.
  • Morello S, Capone M, Sorrentino C, et al. Soluble CD73 as biomarker in patients with metastatic melanoma patients treated with nivolumab. J Transl Med. 2017;15:244.
  • Deinlein T, Wolf IH, Rainer B, et al. Treatment of primary and metastatic multifocal mucosal melanoma of the oral cavity with imatinib. Case Rep Oncol. 2017;10:558–563.
  • Neelapu SS, Locke FL, Bartlett NL, et al. Axicabtagene ciloleucel CAR T-cell therapy in refractory large B-cell lymphoma. N Engl J Med. 2017;377:2531–2544.
  • Raje N, Berdeja J, Lin Y, et al. Anti-BCMA CAR T-cell therapy bb2121 in relapsed or refractory multiple myeloma. N Engl J Med. 2019;380:1726–1737.
  • Cohen AD, Garfall AL, Stadtmauer EA, et al. B cell maturation antigen-specific CAR T cells are clinically active in multiple myeloma. J Clin Invest. 2019;129:2210–2221.
  • Andtbacka RHI, Amatruda T, Nemunaitis J, et al. Biodistribution, shedding, and transmissibility of the oncolytic virus talimogene laherparepvec in patients with melanoma. EBioMed. 2019;47:89–97.
  • Franke V, Berger DMS, Klop WMC, et al. High response rates for T-VEC in early metastatic melanoma (stage IIIB/C-IVM1a). Int J Cancer. 2019;145:974–978.
  • Jiang J, Zhou H, Ni C, et al. Immunotherapy in pancreatic cancer: new hope or mission impossible?. Cancer Lett. 2019;445:57–64.
  • Hammerich L, Binder A, Brody JD. In situ vaccination: cancer immunotherapy both personalized and off-the-shelf. Mol Oncol. 2015;9:1966–1981.
  • Mi Y, Smith CC, Yang F, et al. A dual immunotherapy nanoparticle improves T-cell activation and cancer immunotherapy. Adv Mater Weinheim. 2018;30:e1706098.
  • Singh M, Khong H, Dai Z, et al. Effective innate and adaptive antimelanoma immunity through localized TLR7/8 activation. J Immunol. 2014;193:4722–4731.
  • Fakhari A, Nugent S, Elvecrog J, et al. Thermosensitive gel-based formulation for intratumoral delivery of toll-like receptor 7/8 dual agonist, MEDI9197. J Pharm Sci. 2017;106:2037–2045.
  • Brody JD, Ai WZ, Czerwinski DK, et al. In situ vaccination with a TLR9 agonist induces systemic lymphoma regression: a phase I/II study. J Clin Oncol. 2010;28:4324–4332.
  • Wang S, Campos J, Gallotta M, et al. Intratumoral injection of a CpG oligonucleotide reverts resistance to PD-1 blockade by expanding multifunctional CD8+ T cells. Proc Natl Acad Sci U S A. 2016;113:E7240–E7249.
  • Sagiv-Barfi I, Czerwinski DK, Levy S, et al. Eradication of spontaneous malignancy by local immunotherapy. Sci Transl Med. 2018;10:eaan4488.
  • Kwong B, Liu H, Irvine DJ. Induction of potent anti-tumor responses while eliminating systemic side effects via liposome-anchored combinatorial immunotherapy. Biomaterials. 2011;32:5134–5147.
  • Hewakuruppu YL, Dombrovsky LA, Chen C, et al. Plasmonic "pump-probe" method to study semi-transparent nanofluids. Appl Opt. 2013;52:6041–6050.
  • Baetke SC, Lammers T, Kiessling F. Applications of nanoparticles for diagnosis and therapy of cancer. Br J Radiol. 2015;88:20150207.
  • Barenholz Y. Doxil®-the first FDA-approved nano-drug: lessons learned. J Control Release. 2012;160:117–134.
  • Elahi-Gedwillo KY, Carlson M, Zettervall J, et al. Antifibrotic therapy disrupts stromal barriers and modulates the immune landscape in pancreatic ductal adenocarcinoma. Cancer Res. 2019;79:372–386.
  • Zhou S, Zhang T, Peng B, et al. Targeted delivery of epirubicin to tumor-associated macrophages by sialic acid-cholesterol conjugate modified liposomes with improved antitumor activity. Int J Pharm. 2017;523:203–216.
  • Mielgo A, Schmid MC. Impact of tumour associated macrophages in pancreatic cancer. BMB Rep. 2013;46:131–138.
  • Grivennikov SI, Wang K, Mucida D, et al. Adenoma-linked barrier defects and microbial products drive IL-23/IL-17-mediated tumour growth. Nature. 2012;491:254–258.
  • Kong L, Zhou Y, Bu H, et al. Deletion of interleukin-6 in monocytes/macrophages suppresses the initiation of hepatocellular carcinoma in mice. J Exp Clin Cancer Res. 2016;35:131.
  • Bicho A, Peça IN, Roque ACA, et al. Anti-CD8 conjugated nanoparticles to target mammalian cells expressing CD8. Int J Pharm. 2010;399:80–86.
  • Horwitz DA, Bickerton S, Koss M, et al. Suppression of murine lupus by CD4+ and CD8+ Treg cells induced by T cell-targeted nanoparticles loaded with interleukin-2 and transforming growth factor β. Arthritis Rheumatol. 2019;71:632–640.
  • Schmid D, Park CG, Hartl CA, et al. T cell-targeting nanoparticles focus delivery of immunotherapy to improve antitumor immunity. Nat Commun. 2017;8:1747.
  • Sacchetti C, Rapini N, Magrini A, et al. In vivo targeting of intratumor regulatory T cells using PEG-modified single-walled carbon nanotubes. Bioconjug Chem. 2013;24:852–858.
  • Ou W, Thapa RK, Jiang L, et al. Regulatory T cell-targeted hybrid nanoparticles combined with immuno-checkpoint blockage for cancer immunotherapy. J Control Release. 2018;281:84–96.
  • Cruz LJ, Rosalia RA, Kleinovink JW, et al. Targeting nanoparticles to CD40, DEC-205 or CD11c molecules on dendritic cells for efficient CD8(+) T cell response: a comparative study. J Control Release. 2014;192:209–218.
  • Rosalia RA, Cruz LJ, van Duikeren S, et al. CD40-targeted dendritic cell delivery of PLGA-nanoparticle vaccines induce potent anti-tumor responses. Biomaterials. 2015;40:88–97.
  • Raghuwanshi D, Mishra V, Suresh MR, et al. A simple approach for enhanced immune response using engineered dendritic cell targeted nanoparticles. Vaccine. 2012;30:7292–7299.
  • Hu G, Guo M, Xu J, et al. Nanoparticles targeting macrophages as potential clinical therapeutic agents against cancer and inflammation. Front Immunol. 2019;10:1998.
  • Liu Y, Hardie J, Zhang X, et al. Effects of engineered nanoparticles on the innate immune system. Semin Immunol. 2017;34:25–32.
  • Oh WK, Kim S, Choi M, et al. Cellular uptake, cytotoxicity, and innate immune response of silica-titania hollow nanoparticles based on size and surface functionality. ACS Nano. 2010;4:5301–5313.
  • Jia J, Zhang Y, Xin Y, et al. Interactions between nanoparticles and dendritic cells: from the perspective of cancer immunotherapy. Front Oncol. 2018;8:404.
  • Shima F, Akagi T, Akashi M. Effect of hydrophobic side chains in the induction of immune responses by nanoparticle adjuvants consisting of amphiphilic poly(γ-glutamic acid). Bioconjug Chem. 2015;26:890–898.
  • Moyano DF, Goldsmith M, Solfiell DJ, et al. Nanoparticle hydrophobicity dictates immune response. J Am Chem Soc. 2012;134:3965–3967.
  • Oh JY, Kim HS, Palanikumar L, et al. Cloaking nanoparticles with protein corona shield for targeted drug delivery. Nat Commun. 2018;9:4548.
  • Saha K, Rahimi M, Yazdani M, et al. Regulation of macrophage recognition through the interplay of nanoparticle surface functionality and protein corona. ACS Nano. 2016;10:4421–4430.
  • Settanni G, Zhou J, Suo T, et al. Protein corona composition of poly(ethylene glycol)- and poly(phosphoester)-coated nanoparticles correlates strongly with the amino acid composition of the protein surface. Nanoscale. 2017;9:2138–2144.
  • Gref R, Lück M, Quellec P, et al. Stealth' corona-core nanoparticles surface modified by polyethylene glycol (PEG): influences of the corona (PEG chain length and surface density) and of the core composition on phagocytic uptake and plasma protein adsorption. Colloids Surf B Biointerf. 2000;18:301–313.
  • Xiao W, Lin J, Li M, et al. Prolonged in vivo circulation time by zwitterionic modification of magnetite nanoparticles for blood pool contrast agents. Contrast Media Mol Imaging. 2012;7:320–327.
  • Moyano DF, Liu Y, Ayaz F, et al. Immunomodulatory effects of coated gold nanoparticles in LPS-stimulated in vitro and in vivo murine model systems. Chem. 2016;1:320–327.
  • Kato Y, Ozawa S, Miyamoto C, et al. Acidic extracellular microenvironment and cancer. Cancer Cell Int. 2013;13:89.
  • Wu L, Zhang Y, Li Z, et al. "Sweet" architecture-dependent uptake of glycocalyx-mimicking nanoparticles based on biodegradable aliphatic polyesters by macrophages. J Am Chem Soc. 2017;139:14684–14692.
  • Morris ZS, Guy EI, Werner LR, et al. Tumor-specific inhibition of in situ vaccination by distant untreated tumor sites. Cancer Immunol Res. 2018;6:825–834.
  • Iyoda T, Yamasaki S, Kawamura M, et al. Optimal therapeutic strategy using antigen-containing liposomes selectively delivered to antigen-presenting cells. Cancer Sci. 2019;110:875–887.
  • Jain S, Tran TH, Amiji M. Macrophage repolarization with targeted alginate nanoparticles containing IL-10 plasmid DNA for the treatment of experimental arthritis. Biomaterials. 2015;61:162–177.
  • Wang Y, Lin YX, Qiao SL, et al. Polymeric nanoparticles promote macrophage reversal from M2 to M1 phenotypes in the tumor microenvironment. Biomaterials. 2017;112:153–163.
  • Mahon OR, Browe DC, Gonzalez-Fernandez T, et al. Nano-particle mediated M2 macrophage polarization enhances bone formation and MSC osteogenesis in an IL-10 dependent manner. Biomaterials. 2020;239:119833.
  • Wang AZ, Langer R, Farokhzad OC. Nanoparticle delivery of cancer drugs. Annu Rev Med. 2012;63:185–198.
  • Amidi M, de Raad M, Crommelin DJ, et al. Antigen-expressing immunostimulatory liposomes as a genetically programmable synthetic vaccine. Syst Synth Biol. 2011;5:21–31.
  • Kanaoka E, Takahashi K, Yoshikawa T, et al. A novel and simple type of liposome carrier for recombinant interleukin-2. J Pharm Pharmacol. 2001;53:295–302.
  • Kanaoka E, Takahashi K, Yoshikawa T, et al. Continuous release of interleukin-2 from liposomal IL-2 (mixture of interleukin-2 and liposomes) after subcutaneous administration to mice. Drug Dev Ind Pharm. 2003;29:1149–1153.
  • Anderson PM, et al. Depot characteristics and biodistribution of interleukin-2 liposomes: importance of route of administration. J Immunother. 1992;12:19–31.
  • Sethuraman SN, Singh MP, Patil G, et al. Novel calreticulin-nanoparticle in combination with focused ultrasound induces immunogenic cell death in melanoma to enhance antitumor immunity. Theranostics. 2020;10:3397–3412.
  • Meraz IM, Savage DJ, Segura-Ibarra V, et al. Adjuvant cationic liposomes presenting MPL and IL-12 induce cell death, suppress tumor growth, and alter the cellular phenotype of tumors in a murine model of breast cancer. Mol Pharm. 2014;11:3484–3491.
  • Francian A, Namen S, Stanley M, et al. Intratumoral delivery of antigen with complement C3-bound liposomes reduces tumor growth in mice. Nanomedicine. 2019;18:326–335.
  • Nomura T, Koreeda N, Yamashita F, et al. Effect of particle size and charge on the disposition of lipid carriers after intratumoral injection into tissue-isolated tumors. Pharm Res. 1998;15:128–132.
  • Harrington KJ, Rowlinson-Busza G, Syrigos KN, et al. Pegylated liposomes have potential as vehicles for intratumoral and subcutaneous drug delivery. Clin Cancer Res. 2000;6:2528–2537.
  • Kato K, Omura H, Ishitani R, et al. Cyclic GMP-AMP as an endogenous second messenger in innate immune signaling by cytosolic DNA. Annu Rev Biochem. 2017;86:541–566.
  • Koshy ST, Cheung AS, Gu L, et al. Liposomal delivery enhances immune activation by STING agonists for cancer immunotherapy. Adv Biosyst. 2017;1:1600013.
  • Liu Y, Crowe WN, Wang L, et al. An inhalable nanoparticulate STING agonist synergizes with radiotherapy to confer long-term control of lung metastases. Nat Commun. 2019;10:5108.
  • Cubillos-Ruiz JR, Engle X, Scarlett UK, et al. Polyethylenimine-based siRNA nanocomplexes reprogram tumor-associated dendritic cells via TLR5 to elicit therapeutic antitumor immunity. J Clin Invest. 2009;119:2231–2244.
  • He W, Liang P, Guo G, et al. Re-polarizing myeloid-derived suppressor cells (MDSCs) with cationic polymers for cancer immunotherapy. Sci Rep. 2016;6:24506.
  • Nikitczuk KP, Schloss RS, Yarmush ML, et al. PLGA-polymer encapsulating tumor antigen and CpG DNA administered into the tumor microenvironment elicits a systemic antigen-specific IFN-γ response and enhances survival. J Cancer Ther. 2013;4:280–290.
  • Da Silva CG, Camps MGM, Li TMWY, et al. Effective chemoimmunotherapy by co-delivery of doxorubicin and immune adjuvants in biodegradable nanoparticles. Theranostics. 2019;9:6485–6500.
  • Min Y, Roche KC, Tian S, et al. Antigen-capturing nanoparticles improve the abscopal effect and cancer immunotherapy. Nat Nanotechnol. 2017;12:877–882.
  • Han HD, Byeon Y, Jang JH, et al. In vivo stepwise immunomodulation using chitosan nanoparticles as a platform nanotechnology for cancer immunotherapy. Sci Rep. 2016;6:38348.
  • Li X, Min M, Du N, et al. Chitin, chitosan, and glycated chitosan regulate immune responses: the novel adjuvants for cancer vaccine. Clin Dev Immunol. 2013; 2013:387023.
  • Zaharoff DA, Rogers CJ, Hance KW, et al. Chitosan solution enhances both humoral and cell-mediated immune responses to subcutaneous vaccination. Vaccine. 2007;25:2085–2094.
  • Tahamtan A, Barati M, Tabarraei A, et al. Antitumor immunity induced by genetic immunization with chitosan nanoparticle formulated adjuvanted for HPV-16 E7 DNA vaccine. Iran J Immunol. 2018;15:269–280.
  • Kim TH, Jin H, Kim HW, et al. Mannosylated chitosan nanoparticle-based cytokine gene therapy suppressed cancer growth in BALB/c mice bearing CT-26 carcinoma cells. Mol Cancer Ther. 2006;5:1723–1732.
  • Zaharoff DA, Hance KW, Rogers CJ, et al. Intratumoral immunotherapy of established solid tumors with chitosan/IL-12. J Immunother. 2010;33:697–705.
  • Zaharoff DA, Hoffman BS, Hooper HB, et al. Intravesical immunotherapy of superficial bladder cancer with chitosan/interleukin-12. Cancer Res. 2009;69:6192–6199.
  • Guo L, Yan DD, Yang D, et al. Combinatorial photothermal and immuno cancer therapy using chitosan-coated hollow copper sulfide nanoparticles. ACS Nano. 2014;8:5670–5681.
  • Fogli S, Montis C, Paccosi S, et al. Inorganic nanoparticles as potential regulators of immune response in dendritic cells. Nanomedicine (Lond). 2017;12:1647–1660.
  • Tsai YS, Chen YH, Cheng PC, et al. TGF-β1 conjugated to gold nanoparticles results in protein conformational changes and attenuates the biological function. Small. 2013;9:2119–2128.
  • Nam J, Son S, Ochyl LJ, et al. Chemo-photothermal therapy combination elicits anti-tumor immunity against advanced metastatic cancer. Nat Commun. 2018;9:1074.
  • Cha BG, Jeong JH, Kim J. Extra-large pore mesoporous silica nanoparticles enabling co-delivery of high amounts of protein antigen and toll-like receptor 9 agonist for enhanced cancer vaccine efficacy. ACS Cent Sci. 2018;4:484–492.
  • Hong X, Zhong X, Du G, et al. The pore size of mesoporous silica nanoparticles regulates their antigen delivery efficiency. Sci Adv. 2020;6:eaaz4462.
  • Chen L, Liu J, Zhang Y, et al. The toxicity of silica nanoparticles to the immune system. Nanomedicine (Lond). 2018;13:1939–1962.
  • An M, Yu C, Xi J, et al. Induction of necrotic cell death and activation of STING in the tumor microenvironment via cationic silica nanoparticles leading to enhanced antitumor immunity. Nanoscale. 2018;10:9311–9319.
  • Zhang Y, Chen H, Wang H, et al. A synergistic cancer immunotherapy nano-system for preventing tumor growth. Chem Eng J. 2020;380:122472.
  • Chen Q, Xu L, Liang C, et al. Photothermal therapy with immune-adjuvant nanoparticles together with checkpoint blockade for effective cancer immunotherapy. Nat Commun. 2016;7:13193.
  • Chen PM, Pan WY, Wu CY, et al. Modulation of tumor microenvironment using a TLR-7/8 agonist-loaded nanoparticle system that exerts low-temperature hyperthermia and immunotherapy for in situ cancer vaccination. Biomaterials. 2020;230:119629.
  • Mühlberger M, Janko C, Unterweger H, et al. Functionalization of T lymphocytes with citrate-coated superparamagnetic iron oxide nanoparticles for magnetically controlled immune therapy. Int J Nanomed. 2019;14:8421–8432.
  • Yang Y, Tang J, Abbaraju PL, et al. Hybrid nanoreactors: enabling an off-the-shelf strategy for concurrently enhanced chemo-immunotherapy. Angew Chem Int Ed Engl. 2018;57:11764–11769.
  • Zhang N, Song J, Liu Y, et al. Photothermal therapy mediated by phase-transformation nanoparticles facilitates delivery of anti-PD1 antibody and synergizes with antitumor immunotherapy for melanoma. J Control Release. 2019;306:15–28.
  • Lu S, Neoh KG, Huang C, et al. Polyacrylamide hybrid nanogels for targeted cancer chemotherapy via co-delivery of gold nanoparticles and MTX. J Colloid Interf Sci. 2013;412:46–55.
  • Chen Q, Wang C, Zhang X, et al. In situ sprayed bioresponsive immunotherapeutic gel for post-surgical cancer treatment. Nat Nanotechnol. 2019;14:89–97.
  • Hoopes PJ, Wagner RJ, Duval K, et al. Treatment of canine oral melanoma with nanotechnology-based immunotherapy and radiation. Mol Pharm. 2018;15:3717–3722.
  • Ito A, Tanaka K, Honda H, et al. Complete regression of mouse mammary carcinoma with a size greater than 15 mm by frequent repeated hyperthermia using magnetite nanoparticles. J Biosci Bioeng. 2003;96:364–369.
  • Chen W, Qin M, Chen X, et al. Combining photothermal therapy and immunotherapy against melanoma by polydopamine-coated Al2O3 nanoparticles. Theranostics. 2018;8:2229–2241.
  • Cano-Mejia J, Bookstaver ML, Sweeney EE, et al. Prussian blue nanoparticle-based antigenicity and adjuvanticity trigger robust antitumor immune responses against neuroblastoma. Biomater Sci. 2019;7:1875–1887.
  • Ito A, Matsuoka F, Honda H, et al. Antitumor effects of combined therapy of recombinant heat shock protein 70 and hyperthermia using magnetic nanoparticles in an experimental subcutaneous murine melanoma. Cancer Immunol Immunother. 2004;53:26–32.
  • Zhang X, Wu F, Men K, et al. Modified Fe3O4 magnetic nanoparticle delivery of CpG inhibits tumor growth and spontaneous pulmonary metastases to enhance immunotherapy. Nanoscale Res Lett. 2018;13:240.
  • Toraya-Brown S, Sheen MR, Zhang P, et al. Local hyperthermia treatment of tumors induces CD8(+) T cell-mediated resistance against distal and secondary tumors. Nanomedicine. 2014;10:1273–1285.
  • Zhou Z, Zhang B, Zai W, et al. Perfluorocarbon nanoparticle-mediated platelet inhibition promotes intratumoral infiltration of T cells and boosts immunotherapy. Proc Natl Acad Sci U S A. 2019;116:11972–11977.
  • Steinmetz NF. Viral nanoparticles as platforms for next-generation therapeutics and imaging devices. Nanomedicine. 2010;6:634–641.
  • Miermont A, Barnhill H, Strable E, et al. Cowpea mosaic virus capsid: a promising carrier for the development of carbohydrate based antitumor vaccines. Chemistry. 2008;14:4939–4947.
  • Wang C, Beiss V, Steinmetz NF. Cowpea mosaic virus nanoparticles and empty virus-like particles show distinct but overlapping immunostimulatory properties. J Virol. 2019;93:e00129-19.
  • Murray AA, Wang C, Fiering S, et al. In situ vaccination with cowpea vs tobacco mosaic virus against melanoma. Mol Pharm. 2018;15:3700–3716.
  • Lizotte PH, Wen AM, Sheen MR, et al. In situ vaccination with cowpea mosaic virus nanoparticles suppresses metastatic cancer. Nat Nanotechnol. 2016;11:295–303.
  • Kerstetter-Fogle A, et al. Plant virus-like particle in situ vaccine for intracranial glioma immunotherapy. Cancers (Basel). 2019;11:515.
  • Wang C, Steinmetz NF. CD47 blockade and cowpea mosaic virus nanoparticle in situ vaccination triggers phagocytosis and tumor killing. Adv Healthc Mater. 2019;8:e1801288.
  • Czapar AE, Tiu BDB, Veliz FA, et al. Slow-release formulation of cowpea mosaic virus for in situ vaccine delivery to treat ovarian cancer. Adv Sci (Weinh). 2018;5:1700991–1700991.
  • Shukla S, Wang C, Beiss V, et al. Antibody response against cowpea mosaic viral nanoparticles improves in situ vaccine efficacy in ovarian cancer. ACS Nano . 2020;14:2994–3003.
  • Lee KL, Murray AA, Le DHT, et al. Combination of plant virus nanoparticle-based in situ vaccination with chemotherapy potentiates antitumor response. Nano Lett. 2017;17:4019–4028.
  • Lebel MÈ, Chartrand K, Tarrab E, et al. Potentiating cancer immunotherapy using papaya mosaic virus-derived nanoparticles. Nano Lett. 2016;16:1826–1832.
  • Pokorski JK, Steinmetz NF. The art of engineering viral nanoparticles. Mol Pharm. 2011;8:29–43.
  • Farley MM, Hu B, Margolin W, et al. Minicells, back in fashion. J Bacteriol. 2016;198:1186–1195.
  • MacDiarmid JA, Mugridge NB, Weiss JC, et al. Bacterially derived 400 nm particles for encapsulation and cancer cell targeting of chemotherapeutics. Cancer Cell. 2007;11:431–445.
  • Schwechheimer C, Kuehn MJ. Outer-membrane vesicles from Gram-negative bacteria: biogenesis and functions. Nat Rev Microbiol. 2015;13:605–619.
  • Jivrajani M, Nivsarkar M. Ligand-targeted bacterial minicells: futuristic nano-sized drug delivery system for the efficient and cost effective delivery of shRNA to cancer cells. Nanomedicine. 2016;12:2485–2498.
  • Zhang Y, Ji W, He L, et al. E. coli nissle 1917-derived minicells for targeted delivery of chemotherapeutic drug to hypoxic regions for cancer therapy. Theranostics. 2018;8:1690–1705.
  • Tsuji S, Chen X, Hancock B, et al. Preclinical evaluation of VAX-IP, a novel bacterial minicell-based biopharmaceutical for nonmuscle invasive bladder cancer. Mol Ther Oncolytics. 2016;3:16004–16004.
  • MacDiarmid JA, Langova V, Bailey D, et al. Targeted doxorubicin delivery to brain tumors via minicells: proof of principle using dogs with spontaneously occurring tumors as a model. PLoS One. 2016;11:e0151832.
  • MacDiarmid JA, Madrid-Weiss J, Amaro-Mugridge NB, et al. Bacterially-derived nanocells for tumor-targeted delivery of chemotherapeutics and cell cycle inhibitors. Cell Cycle. 2007;6:2099–2105.
  • Solomon BJ, Desai J, Rosenthal M, et al. A first-time-in-human phase I clinical trial of bispecific antibody-targeted, paclitaxel-packaged bacterial minicells. PLoS One. 2015;10:e0144559.
  • Carleton HA, Lara-Tejero M, Liu X, et al. Engineering the type III secretion system in non-replicating bacterial minicells for antigen delivery. Nat Commun. 2013;4:1590–1590.
  • Hancock BM, McGuire KL, Tsuji S, et al. A single intravesical instillation of VAX014 inhibits orthotopic superficial bladder tumor implantation to increase survival. Anticancer Res. 2016;36:6243–6248.
  • Karagiannis ED, Anderson DG. Minicells overcome tumor drug-resistance. Nat Biotechnol. 2009;27:620–621.
  • Singh MP, Sethuraman SN, Ritchey J, et al. In-situ vaccination using focused ultrasound heating and anti-CD-40 agonistic antibody enhances T-cell mediated local and abscopal effects in murine melanoma. Int J Hyperthermia. 2019;36:64–73.
  • Beg S, Kawish SM, Panda SK, et al. Nanomedicinal strategies as efficient therapeutic interventions for delivery of cancer vaccines. Semin Cancer Biol. 2019.
  • Zhang R, Billingsley MM, Mitchell MJ. Biomaterials for vaccine-based cancer immunotherapy. J Control Release. 2018;292:256–276.
  • Young JK, Figueroa ER, Drezek RA. Tunable nanostructures as photothermal theranostic agents. Ann Biomed Eng. 2012;40:438–459.
  • Zhang Z, Wang J, Chen C. Near-infrared light-mediated nanoplatforms for cancer thermo-chemotherapy and optical imaging. Adv Mater Weinheim. 2013;25:3869–3880.
  • Zhou F, Li X, Naylor MF, et al. InCVAX-a novel strategy for treatment of late-stage, metastatic cancers through photoimmunotherapy induced tumor-specific immunity. Cancer Lett. 2015;359:169–177.
  • Zhang Z, Wang J, Nie X, et al. Near infrared laser-induced targeted cancer therapy using thermoresponsive polymer encapsulated gold nanorods. J Am Chem Soc. 2014;136:7317–7326.
  • Wang C, Xu L, Liang C, et al. Immunological responses triggered by photothermal therapy with carbon nanotubes in combination with anti-CTLA-4 therapy to inhibit cancer metastasis. Adv Mater Weinheim. 2014;26:8154–8162.
  • Bear AS, Kennedy LC, Young JK, et al. Elimination of metastatic melanoma using gold nanoshell-enabled photothermal therapy and adoptive T cell transfer. PloS One. 2013;8:e69073.
  • Cano-Mejia J, Burga RA, Sweeney EE, et al. Prussian blue nanoparticle-based photothermal therapy combined with checkpoint inhibition for photothermal immunotherapy of neuroblastoma. Nanomedicine. 2017;13:771–781.
  • Duval KEA, Vernice NA, Wagner RJ, et al. Immunogenetic effects of low dose (CEM43 30) magnetic nanoparticle hyperthermia and radiation in melanoma cells. Int J Hyperthermia. 2019;36:37–46.
  • Ito A, Shinkai M, Honda H, et al. Heat shock protein 70 expression induces antitumor immunity during intracellular hyperthermia using magnetite nanoparticles. Cancer Immunol Immunother. 2003;52:80–88.
  • Tanaka K, Ito A, Kobayashi T, et al. Intratumoral injection of immature dendritic cells enhances antitumor effect of hyperthermia using magnetic nanoparticles. Int J Cancer. 2005;116:624–633.
  • Kobayashi T, Kakimi K, Nakayama E, et al. Antitumor immunity by magnetic nanoparticle-mediated hyperthermia. Nanomedicine (Lond)). 2014;9:1715–1726.
  • Oei AL, Korangath P, Mulka K, et al. Enhancing the abscopal effect of radiation and immune checkpoint inhibitor therapies with magnetic nanoparticle hyperthermia in a model of metastatic breast cancer. Int J Hyperthermia. 2019;36:47–63.
  • Ranjan A, Jacobs GC, Woods DL, et al. Image-guided drug delivery with magnetic resonance guided high intensity focused ultrasound and temperature sensitive liposomes in a rabbit Vx2 tumor model. J Controlled Release. 2012;158:487–494.
  • Ektate K, Munteanu MC, Ashar H, et al. Chemo-immunotherapy of colon cancer with focused ultrasound and Salmonella-laden temperature sensitive liposomes (thermobots). Sci Rep. 2018;8:13062.
  • VanOsdol J, Ektate K, Ramasamy S, et al. Sequential HIFU heating and nanobubble encapsulation provide efficient drug penetration from stealth and temperature sensitive liposomes in colon cancer. J Control Release. 2017;247:55–63.
  • Skalina KA, Singh S, Chavez CG, et al. Low intensity focused ultrasound (LOFU)-mediated acoustic immune priming and ablative radiation therapy for in situ tumor vaccines. Sci Rep. 2019;9:15516.
  • Silvestrini MT, Ingham ES, Mahakian LM, et al. Priming is key to effective incorporation of image-guided thermal ablation into immunotherapy protocols. JCI Insight. 2017;2:e90521.
  • Eranki A, Farr N, Partanen A, et al. Boiling histotripsy lesion characterization on a clinical magnetic resonance imaging-guided high intensity focused ultrasound system. PloS ONE. 2017;12:e0173867.
  • Suzuki R, Namai E, Oda Y, et al. Cancer gene therapy by IL-12 gene delivery using liposomal bubbles and tumoral ultrasound exposure. J Control Release. 2010;142:245–250.
  • Chen YL, Wang CY, Yang FY, et al. Synergistic effects of glycated chitosan with high-intensity focused ultrasound on suppression of metastases in a syngeneic breast tumor model. Cell Death Dis. 2014;5:e1178.
  • Wei SC, Duffy CR, Allison JP. Fundamental mechanisms of immune checkpoint blockade therapy. Cancer Discov. 2018;8:1069–1086.
  • Francis DM, Thomas SN. Progress and opportunities for enhancing the delivery and efficacy of checkpoint inhibitors for cancer immunotherapy. Adv Drug Deliv Rev. 2017;114:33–42.
  • Barrueto L, Caminero F, Cash L, et al. Resistance to checkpoint inhibition in cancer immunotherapy. Transl Oncol. 2020;13:100738.
  • Ajina R, Zahavi DJ, Zhang YW, et al. Overcoming malignant cell-based mechanisms of resistance to immune checkpoint blockade antibodies. Semin Cancer Biol. 2019;65:28–37.
  • Gong J, Hendifar A, Tuli R, et al. Combination systemic therapies with immune checkpoint inhibitors in pancreatic cancer: overcoming resistance to single-agent checkpoint blockade. Clin Transl Med. 2018;7:32.
  • Fay AP, Antonarakis ES. Blocking the PD-1/PD-L1 axis in advanced prostate cancer: are we moving in the right direction?. Ann Transl Med. 2019;7:S7.
  • Luo L, Zhu C, Yin H, et al. Laser immunotherapy in combination with perdurable PD-1 blocking for the treatment of metastatic tumors. ACS Nano. 2018;12:7647–7662.
  • Tselikas L, de Baere T, Isoardo T, et al. Pickering emulsions with ethiodized oil and nanoparticles for slow release of intratumoral anti-CTLA4 immune checkpoint antibodies. J Immunother Cancer. 2020;8:e000579.