Materials-Based Approaches for Cancer Vaccination.

Therapeutic cancer vaccines offer the promise of stimulating the immune system to specifically eradicate tumor cells and establish long-term memory to prevent tumor recurrence. However, despite showing benign safety profiles and the ability to generate Ag-specific cellular responses, cancer vaccines have been hampered by modest clinical efficacy. Lessons learned from these studies have led to the emergence of innovative materials-based strategies that aim to boost the clinical activity of cancer vaccines. In this Brief Review, we provide an overview of the key elements needed for an effective vaccine-induced antitumor response, categorize current approaches to therapeutic cancer vaccination, and explore recent advances in materials-based strategies to potentiate cancer vaccines.

[1]  Yusheng Liu,et al.  Targeted delivery of liposomal chemoimmunotherapy for cancer treatment , 2022, Frontiers in Immunology.

[2]  F. Ginhoux,et al.  Systemic vaccination induces CD8+ T cells and remodels the tumor microenvironment , 2022, Cell.

[3]  I. Melero,et al.  Cancer vaccines: the next immunotherapy frontier , 2022, Nature Cancer.

[4]  Jing Chen,et al.  An in situ hydrogel-mediated chemo-immunometabolic cancer therapy , 2022, Nature Communications.

[5]  Aileen W. Li,et al.  A vaccine targeting resistant tumours by dual T cell plus NK cell attack , 2022, Nature.

[6]  Jin Gao,et al.  Engineering Bacterial Membrane Nanovesicles for Improved Therapies in Infectious Diseases and Cancer. , 2022, Advanced drug delivery reviews.

[7]  Aileen W. Li,et al.  Scaffold Vaccines for Generating Robust and Tunable Antibody Responses , 2022, Advanced Functional Materials.

[8]  Jordan A. Stinson,et al.  Intratumourally injected alum-tethered cytokines elicit potent and safer local and systemic anticancer immunity , 2021, Nature Biomedical Engineering.

[9]  B. Pulendran,et al.  Designing spatial and temporal control of vaccine responses , 2021, Nature Reviews Materials.

[10]  R. Brink,et al.  The unique biology of germinal center B cells. , 2021, Immunity.

[11]  Jianzhu Chen,et al.  In situ cancer vaccination using lipidoid nanoparticles , 2021, Science Advances.

[12]  B. Pulendran,et al.  Emerging concepts in the science of vaccine adjuvants , 2021, Nature reviews. Drug discovery.

[13]  D. Irvine,et al.  Exploiting albumin as a mucosal vaccine chaperone for robust generation of lung-resident memory T cells , 2021, Science Immunology.

[14]  S. Eisenbarth,et al.  Dendritic Cell Regulation of T Helper Cells. , 2021, Annual review of immunology.

[15]  P. Ott,et al.  Personal Neoantigen Vaccines for the Treatment of Cancer , 2021 .

[16]  C. Reis e Sousa,et al.  Dendritic Cells Revisited. , 2021, Annual review of immunology.

[17]  Rebecca L. Holden,et al.  Personal neoantigen vaccines induce persistent memory T cell responses and epitope spreading in patients with melanoma , 2021, Nature Medicine.

[18]  P. Ott,et al.  Advances in the development of personalized neoantigen-based therapeutic cancer vaccines , 2021, Nature Reviews Clinical Oncology.

[19]  P. Danaher,et al.  Flt3 ligand augments immune responses to anti-DEC-205-NY-ESO-1 vaccine through expansion of dendritic cell subsets , 2020, Nature Cancer.

[20]  Aileen W. Li,et al.  Biomaterial-based scaffold for in situ chemo-immunotherapy to treat poorly immunogenic tumors , 2020, Nature Communications.

[21]  Katie M. Campbell,et al.  304 Intratumoral injection of CMP-001, a toll-like receptor 9 (TLR9) agonist, in combination with pembrolizumab reversed programmed death receptor 1 (PD-1) blockade resistance in advanced melanoma , 2020 .

[22]  F. Ginhoux,et al.  Intravenous Nanoparticle Vaccination Generates Stem-Like TCF1+ Neoantigen-Specific CD8+ T Cells , 2020, Nature immunology.

[23]  J. Utikal,et al.  An RNA vaccine drives immunity in checkpoint-inhibitor-treated melanoma , 2020, Nature.

[24]  Aileen W. Li,et al.  Single‐Shot Mesoporous Silica Rods Scaffold for Induction of Humoral Responses Against Small Antigens , 2020, Advanced Functional Materials.

[25]  D. Irvine,et al.  Controlling timing and location in vaccines , 2020, Advanced Drug Delivery Reviews.

[26]  D. Irvine,et al.  Pharmacokinetic tuning of protein–antigen fusions enhances the immunogenicity of T-cell vaccines , 2020, Nature Biomedical Engineering.

[27]  C. Kojima,et al.  Carboxyl-, sulfonyl-, and phosphate-terminal dendrimers as a nanoplatform with lymph node targeting. , 2020, International journal of pharmaceutics.

[28]  H. Shu,et al.  Innate Immune Response to Cytoplasmic DNA: Mechanisms and Diseases. , 2019, Annual review of immunology.

[29]  D. Kong,et al.  Dual fluorescence imaging-guided programmed delivery of doxorubicin and CpG nanoparticles to modulate tumor microenvironment for effective chemo-immunotherapy. , 2019, Biomaterials.

[30]  Michele De Palma,et al.  Engineering dendritic cell vaccines to improve cancer immunotherapy , 2019, Nature Communications.

[31]  J. L. Santos,et al.  Physical and chemical profiles of nanoparticles for lymphatic targeting. , 2019, Advanced drug delivery reviews.

[32]  Jiasheng Tu,et al.  Mild photothermal therapy potentiates anti-PD-L1 treatment for immunologically cold tumors via an all-in-one and all-in-control strategy , 2019, Nature Communications.

[33]  S. Hohaus,et al.  Clinical and Antitumor Immune Responses in Relapsed/Refractory Follicular Lymphoma Patients after Intranodal Injections of IFNα-Dendritic Cells and Rituximab: a Phase I Clinical Trial , 2019, Clinical Cancer Research.

[34]  S. Thomas,et al.  Material design for lymph node drug delivery , 2019, Nature Reviews Materials.

[35]  Scott N. Mueller,et al.  T cell and dendritic cell interactions in lymphoid organs: More than just being in the right place at the right time , 2019, Immunological reviews.

[36]  M. Merad,et al.  Systemic clinical tumor regressions and potentiation of PD1 blockade with in situ vaccination , 2019, Nature Medicine.

[37]  Shuang Wang,et al.  Engineering Magnetosomes for High-Performance Cancer Vaccination , 2019, ACS central science.

[38]  Yu Qin,et al.  Co-delivery of antigen and dual agonists by programmed mannose-targeted cationic lipid-hybrid polymersomes for enhanced vaccination. , 2019, Biomaterials.

[39]  Sangdun Choi,et al.  Recent clinical trends in Toll‐like receptor targeting therapeutics , 2018, Medicinal research reviews.

[40]  Thanh Loc Nguyen,et al.  Mesoporous Silica as a Versatile Platform for Cancer Immunotherapy , 2018, Advanced materials.

[41]  S. Eisenbarth,et al.  Dendritic cell subsets in T cell programming: location dictates function , 2018, Nature Reviews Immunology.

[42]  R. Coffman,et al.  SD-101 in Combination with Pembrolizumab in Advanced Melanoma: Results of a Phase Ib, Multicenter Study. , 2018, Cancer discovery.

[43]  D. Mooney,et al.  Biomaterial-assisted targeted modulation of immune cells in cancer treatment , 2018, Nature Materials.

[44]  J. Borst,et al.  CD4+ T cell help in cancer immunology and immunotherapy , 2018, Nature Reviews Immunology.

[45]  E. Latz,et al.  Targeting the NLRP3 inflammasome in inflammatory diseases , 2018, Nature Reviews Drug Discovery.

[46]  Kai Yang,et al.  Combined local immunostimulatory radioisotope therapy and systemic immune checkpoint blockade imparts potent antitumour responses , 2018, Nature Biomedical Engineering.

[47]  W. Loging,et al.  Therapeutic Immune Modulation against Solid Cancers with Intratumoral Poly-ICLC: A Pilot Trial , 2018, Clinical Cancer Research.

[48]  Rebecca L. Holden,et al.  Enhancement of Peptide Vaccine Immunogenicity by Increasing Lymphatic Drainage and Boosting Serum Stability , 2018, Cancer Immunology Research.

[49]  Gordon D. Brown,et al.  C-type lectins in immunity and homeostasis , 2018, Nature Reviews Immunology.

[50]  Aileen W. Li,et al.  Injectable, Tough Alginate Cryogels as Cancer Vaccines , 2018, Advanced healthcare materials.

[51]  I. Taniuchi CD4 Helper and CD8 Cytotoxic T Cell Differentiation. , 2018, Annual review of immunology.

[52]  M. Gale,et al.  RIG-I and Other RNA Sensors in Antiviral Immunity. , 2018, Annual review of immunology.

[53]  S. Son,et al.  Elimination of established tumors with nanodisc-based combination chemoimmunotherapy , 2018, Science Advances.

[54]  Charles H. Yoon,et al.  Antibody-mediated inhibition of MICA and MICB shedding promotes NK cell–driven tumor immunity , 2018, Science.

[55]  J. Jeong,et al.  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 , 2018, ACS central science.

[56]  Ö. Türeci,et al.  Personalized vaccines for cancer immunotherapy , 2018, Science.

[57]  Michael S. Goldberg,et al.  Extended release of perioperative immunotherapy prevents tumor recurrence and eliminates metastases , 2018, Science Translational Medicine.

[58]  R. Dillman,et al.  Randomized phase II trial of autologous dendritic cell vaccines versus autologous tumor cell vaccines in metastatic melanoma: 5-year follow up and additional analyses , 2018, Journal of Immunotherapy for Cancer.

[59]  Aileen W. Li,et al.  A facile approach to enhance antigen response for personalized cancer vaccination , 2018, Nature Materials.

[60]  Aileen W. Li,et al.  Covalent Conjugation of Peptide Antigen to Mesoporous Silica Rods to Enhance Cellular Responses. , 2018, Bioconjugate chemistry.

[61]  Catherine J. Wu,et al.  Towards personalized, tumour-specific, therapeutic vaccines for cancer , 2017, Nature Reviews Immunology.

[62]  Xun Sun,et al.  Lymph node targeting strategies to improve vaccination efficacy , 2017, Journal of controlled release : official journal of the Controlled Release Society.

[63]  Ido D. Weiss,et al.  Albumin/vaccine nanocomplexes that assemble in vivo for combination cancer immunotherapy , 2017, Nature Communications.

[64]  R. A. van den Berg,et al.  Different Adjuvants Induce Common Innate Pathways That Are Associated with Enhanced Adaptive Responses against a Model Antigen in Humans , 2017, Front. Immunol..

[65]  J. Utikal,et al.  Personalized RNA mutanome vaccines mobilize poly-specific therapeutic immunity against cancer , 2017, Nature.

[66]  Charles H. Yoon,et al.  An immunogenic personal neoantigen vaccine for patients with melanoma , 2017, Nature.

[67]  Tian Zhang,et al.  Antigen-capturing nanoparticles improve the abscopal effect and cancer immunotherapy , 2017, Nature Nanotechnology.

[68]  Xun Sun,et al.  Tailoring polymeric hybrid micelles with lymph node targeting ability to improve the potency of cancer vaccines. , 2017, Biomaterials.

[69]  R. Förster,et al.  Dendritic cell migration in health and disease , 2016, Nature Reviews Immunology.

[70]  J. Moon,et al.  Designer vaccine nanodiscs for personalized cancer immunotherapy , 2016, Nature materials.

[71]  D. Mooney,et al.  Designing hydrogels for controlled drug delivery. , 2016, Nature reviews. Materials.

[72]  Özlem Türeci,et al.  Systemic RNA delivery to dendritic cells exploits antiviral defence for cancer immunotherapy , 2016, Nature.

[73]  W. Jiskoot,et al.  Synthetic long peptide-based vaccine formulations for induction of cell mediated immunity: A comparative study of cationic liposomes and PLGA nanoparticles. , 2016, Journal of controlled release : official journal of the Controlled Release Society.

[74]  P. Lizotte,et al.  In situ vaccination with cowpea mosaic virus nanoparticles suppresses metastatic cancer , 2015, Nature nanotechnology.

[75]  Michael Y. Gerner,et al.  In vivo characterization of the physicochemical properties of TLR agonist delivery that enhance vaccine immunogenicity , 2015, Nature Biotechnology.

[76]  Scott N. Mueller,et al.  Spatiotemporally Distinct Interactions with Dendritic Cell Subsets Facilitates CD4+ and CD8+ T Cell Activation to Localized Viral Infection. , 2015, Immunity.

[77]  S. Amigorena Helping the Help for CD8+ T Cell Responses , 2015, Cell.

[78]  Ting-Yu Shih,et al.  Injectable cryogel-based whole-cell cancer vaccines , 2015, Nature Communications.

[79]  Shinn-Jang Hwang,et al.  Efficacy of an adjuvanted herpes zoster subunit vaccine in older adults. , 2015, The New England journal of medicine.

[80]  J. Castle,et al.  Mutant MHC class II epitopes drive therapeutic immune responses to cancer , 2015, Nature.

[81]  S. Mitragotri,et al.  Elasticity of nanoparticles influences their blood circulation, phagocytosis, endocytosis, and targeting. , 2015, ACS nano.

[82]  Michael Y. Gerner,et al.  Strategically localized dendritic cells promote rapid T cell responses to lymph-borne particulate antigens. , 2015, Immunity.

[83]  Tae Jin Kim,et al.  Clearance of persistent HPV infection and cervical lesion by therapeutic DNA vaccine in CIN3 patients , 2014, Nature Communications.

[84]  S. Bertholet,et al.  Unleashing the potential of NOD- and Toll-like agonists as vaccine adjuvants , 2014, Proceedings of the National Academy of Sciences.

[85]  M. Dhodapkar,et al.  Induction of Antigen-Specific Immunity with a Vaccine Targeting NY-ESO-1 to the Dendritic Cell Receptor DEC-205 , 2014, Science Translational Medicine.

[86]  David J Mooney,et al.  Injectable, porous, and cell-responsive gelatin cryogels. , 2014, Biomaterials.

[87]  Gregory L. Szeto,et al.  Structure-based programming of lymph-node targeting in molecular vaccines , 2014, Nature.

[88]  M. Nussenzweig,et al.  Intestinal monocytes and macrophages are required for T cell polarization in response to Citrobacter rodentium , 2013, The Journal of experimental medicine.

[89]  A. Mackiewicz,et al.  Therapeutic gene modified cell based cancer vaccines. , 2013, Gene.

[90]  T. Cloughesy,et al.  Comparison of Glioma-associated Antigen Peptide-loaded Versus Autologous Tumor Lysate-loaded Dendritic Cell Vaccination in Malignant Glioma Patients , 2013, Journal of immunotherapy.

[91]  Giuseppe Del Giudice,et al.  The history of MF59® adjuvant: a phoenix that arose from the ashes , 2013, Expert review of vaccines.

[92]  D. Mooney,et al.  The efficacy of intracranial PLG-based vaccines is dependent on direct implantation into brain tissue. , 2011, Journal of controlled release : official journal of the Controlled Release Society.

[93]  D. Venzon,et al.  TLR3-Specific Double-Stranded RNA Oligonucleotide Adjuvants Induce Dendritic Cell Cross-Presentation, CTL Responses, and Antiviral Protection , 2011, The Journal of Immunology.

[94]  A. Oxenius,et al.  Type I IFN Substitutes for T Cell Help during Viral Infections , 2011, The Journal of Immunology.

[95]  D. Mooney,et al.  Biomaterial-Based Vaccine Induces Regression of Established Intracranial Glioma in Rats , 2011, Pharmaceutical Research.

[96]  S. H. van der Burg,et al.  Therapeutic cancer vaccines. , 2010, The Journal of clinical investigation.

[97]  S. Akira,et al.  The role of pattern-recognition receptors in innate immunity: update on Toll-like receptors , 2010, Nature Immunology.

[98]  J. Robinson,et al.  Biodegradable PLGA based nanoparticles for sustained regional lymphatic drug delivery. , 2010, Journal of pharmaceutical sciences.

[99]  S. H. van der Burg,et al.  Vaccination against HPV-16 oncoproteins for vulvar intraepithelial neoplasia. , 2009, The New England journal of medicine.

[100]  David J Mooney,et al.  In Situ Regulation of DC Subsets and T Cells Mediates Tumor Regression in Mice , 2009, Science Translational Medicine.

[101]  K. Sauer,et al.  IL-21 Is Required to Control Chronic Viral Infection , 2009, Science.

[102]  David J. Mooney,et al.  Infection-Mimicking Materials to Program Dendritic Cells In Situ , 2008, Nature materials.

[103]  Katrin Schwarz,et al.  Nanoparticles target distinct dendritic cell populations according to their size , 2008, European journal of immunology.

[104]  Samir Mitragotri,et al.  Role of target geometry in phagocytosis. , 2006, Proceedings of the National Academy of Sciences of the United States of America.

[105]  C. Figdor,et al.  Effective induction of naive and recall T-cell responses by targeting antigen to human dendritic cells via a humanized anti-DC-SIGN antibody. , 2005, Blood.

[106]  J. Nemunaitis,et al.  GM-CSF gene-transduced tumor vaccines. , 2005, Molecular therapy : the journal of the American Society of Gene Therapy.

[107]  R. Steinman,et al.  In Vivo Targeting of Antigens to Maturing Dendritic Cells via the DEC-205 Receptor Improves T Cell Vaccination , 2004, The Journal of experimental medicine.

[108]  Kouji Matsushima,et al.  Pivotal Role of Dendritic Cell–derived CXCL10 in the Retention of T Helper Cell 1 Lymphocytes in Secondary Lymph Nodes , 2002, The Journal of experimental medicine.

[109]  A. Sher,et al.  CD40 triggering of heterodimeric IL-12 p70 production by dendritic cells in vivo requires a microbial priming signal. , 2000, Immunity.

[110]  G. Dranoff,et al.  Advances in Therapeutic Cancer Vaccines. , 2016, Advances in immunology.