Pro-inflammatory chitosan/poly(γ-glutamic acid) nanoparticles modulate human antigen-presenting cells phenotype and revert their pro-invasive capacity

Shiao, 2011, Immune microenvironments in solid tumors: new targets for therapy, Genes Dev.., 25, 2559, 10.1101/gad.169029.111 de Visser, 2006, Paradoxical roles of the immune system during cancer development, Nat. Rev. Cancer, 6, 24, 10.1038/nrc1782 Coussens, 2002, Inflammation and cancer, Nature, 420, 860, 10.1038/nature01322 Talmadge, 2007, Inflammatory cell infiltration of tumors: Jekyll or Hyde, Cancer Metastasis Rev., 26, 373, 10.1007/s10555-007-9072-0 Rutkowski, 2012, Anti-tumor immunity: myeloid leukocytes control the immune landscape, Cell. Immunol., 278, 21, 10.1016/j.cellimm.2012.06.014 Rabinovich, 2007, Immunosuppressive strategies that are mediated by tumor cells, Annu. Rev. Immunol., 25, 267, 10.1146/annurev.immunol.25.022106.141609 Mosser, 2008, Exploring the full spectrum of macrophage activation, Nat. Rev. Immunol., 8, 958, 10.1038/nri2448 Shurin, 2006, Intratumoral cytokines/chemokines/growth factors and tumor infiltrating dendritic cells: friends or enemies?, Cancer Metastasis Rev., 25, 333, 10.1007/s10555-006-9010-6 Mantovani, 2006, Role of tumor-associated macrophages in tumor progression and invasion, Cancer Metastasis Rev., 25, 315, 10.1007/s10555-006-9001-7 Condeelis, 2006, Macrophages: obligate partners for tumor cell migration, invasion, and metastasis, Cell, 124, 263, 10.1016/j.cell.2006.01.007 Zhang, 2012, Prognostic significance of tumor-associated macrophages in solid tumor: a meta-analysis of the literature, PLoS One, 7, e50946, 10.1371/journal.pone.0050946 Murray, 2014, Macrophage activation and polarization: nomenclature and experimental guidelines, Immunity, 41, 14, 10.1016/j.immuni.2014.06.008 F.O. Martinez, S. Gordon. The M1 and M2 paradigm of macrophage activation: time for reassessment. F1000Prime Rep, 2014, 6, 13. Jetten, 2014, Anti-inflammatory M2, but not pro-inflammatory M1 macrophages promote angiogenesis in vivo, Angiogenesis, 17, 109, 10.1007/s10456-013-9381-6 Mantovani, 2002, Macrophage polarization: tumor-associated macrophages as a paradigm for polarized M2 mononuclear phagocytes, Trends Immunol., 23, 549, 10.1016/S1471-4906(02)02302-5 Schmieder, 2012, Differentiation and gene expression profile of tumor-associated macrophages, Semin. Cancer Biol., 22, 289, 10.1016/j.semcancer.2012.02.002 Ma, 2016, Tumor cell-derived microparticles polarize M2 tumor-associated macrophages for tumor progression, Oncoimmunology, 5, e1118599, 10.1080/2162402X.2015.1118599 Cardoso, 2014, Macrophages stimulate gastric and colorectal cancer invasion through EGFR Y(1086), c-Src, Erk1/2 and Akt phosphorylation and smallGTPase activity, Oncogene, 33, 2123, 10.1038/onc.2013.154 Gutkin, 2014, Clinical evaluation of systemic and local immune responses in cancer: time for integration, Cancer Immunol. Immunother., 63, 45, 10.1007/s00262-013-1480-0 Ma, 2013, Dendritic cells in the cancer microenvironment, J. Cancer, 4, 36, 10.7150/jca.5046 Palucka, 2013, Dendritic-cell-based therapeutic cancer vaccines, Immunity, 39, 38, 10.1016/j.immuni.2013.07.004 Tang, 2013, Anti-tumour strategies aiming to target tumour-associated macrophages, Immunology, 138, 93, 10.1111/imm.12023 Mantovani, 2017, Tumour-associated macrophages as treatment targets in oncology, Nat. Rev. Clin. Oncol., 10.1038/nrclinonc.2016.217 Tuettenberg, 2016, Myeloid cells as orchestrators of the tumor microenvironment: novel targets for nanoparticular cancer therapy, Nanomedicine (Lond.), 11, 2735, 10.2217/nnm-2016-0208 Kuai, 2016, Designer vaccine nanodiscs for personalized cancer immunotherapy, Nat. Mater. Chen, 2016, Photothermal therapy with immune-adjuvant nanoparticles together with checkpoint blockade for effective cancer immunotherapy, Nat. Commun., 7, 13193, 10.1038/ncomms13193 van Broekhoven, 2004, Targeting dendritic cells with antigen-containing liposomes: a highly effective procedure for induction of antitumor immunity and for tumor immunotherapy, Cancer Res., 64, 4357, 10.1158/0008-5472.CAN-04-0138 Zanganeh, 2016, Iron oxide nanoparticles inhibit tumour growth by inducing pro-inflammatory macrophage polarization in tumour tissues, Nat. Nanotechnol., 11, 986, 10.1038/nnano.2016.168 Cardoso, 2015, An interferon-gamma-delivery system based on chitosan/poly(gamma-glutamic acid) polyelectrolyte complexes modulates macrophage-derived stimulation of cancer cell invasion in vitro, Acta Biomater., 23, 157, 10.1016/j.actbio.2015.05.022 Cheung, 2015, Chitosan: an update on potential biomedical and pharmaceutical applications, Mar. Drugs, 13, 5156, 10.3390/md13085156 Carroll, 2016, The Vaccine adjuvant chitosan promotes cellular immunity via DNA sensor cGAS-STING-dependent induction of type i interferons, Immunity, 44, 597, 10.1016/j.immuni.2016.02.004 Buescher, 2007, Microbial biosynthesis of polyglutamic acid biopolymer and applications in the biopharmaceutical, biomedical and food industries, Crit. Rev. Biotechnol., 27, 1, 10.1080/07388550601166458 Pereira, 2012, Biosynthesis of highly pure poly-gamma-glutamic acid for biomedical applications, J. Mater. Sci. – Mater. Med., 23, 1583, 10.1007/s10856-012-4639-x Goncalves, 2015, Macrophage response to chitosan/poly-(gamma-glutamic acid) nanoparticles carrying an anti-inflammatory drug, J. Mater. Sci. - Mater. Med., 26, 167, 10.1007/s10856-015-5496-1 Teixeira, 2016, R.M. Goncalves. Anti-inflammatory Chitosan/Poly-gamma-glutamic acid nanoparticles control inflammation while remodeling extracellular matrix in degenerated intervertebral disc, Acta Biomater., 42, 168, 10.1016/j.actbio.2016.06.013 Antunes, 2011, Layer-by-layer self-assembly of chitosan and poly(gamma-glutamic acid) into polyelectrolyte complexes, Biomacromolecules, 12, 4183, 10.1021/bm2008235 Hopken, 2005, The ratio between dendritic cells and T cells determines the outcome of their encounter: proliferation versus deletion, Eur. J. Immunol., 35, 2851, 10.1002/eji.200526298 Upham, 1997, Selective inhibition of T cell proliferation but not expression of effector function by human alveolar macrophages, Thorax, 52, 786, 10.1136/thx.52.9.786 Palucka, 2012, Cancer immunotherapy via dendritic cells, Nat. Rev. Cancer, 12, 265, 10.1038/nrc3258 Solinas, 2009, Tumor-associated macrophages (TAM) as major players of the cancer-related inflammation, J. Leukoc. Biol., 86, 1065, 10.1189/jlb.0609385 Zanetti, 2015, Tapping CD4 T cells for cancer immunotherapy: the choice of personalized genomics, J. Immunol., 194, 2049, 10.4049/jimmunol.1402669 Oliveira, 2012, Chitosan drives anti-inflammatory macrophage polarisation and pro-inflammatory dendritic cell stimulation, Eur. Cells Mater., 24, 136, 10.22203/eCM.v024a10 Cardoso, 2015, Matrix metalloproteases as maestros for the dual role of LPS- and IL-10-stimulated macrophages in cancer cell behaviour, BMC Cancer, 15, 456, 10.1186/s12885-015-1466-8 Mori, 2012, The vaccine adjuvant alum inhibits IL-12 by promoting PI3 kinase signaling while chitosan does not inhibit IL-12 and enhances Th1 and Th17 responses, Eur. J. Immunol., 42, 2709, 10.1002/eji.201242372 Lin, 2014, Chitosan as an adjuvant-like substrate for dendritic cell culture to enhance antitumor effects, Biomaterials, 35, 8867, 10.1016/j.biomaterials.2014.07.014 Matsuo, 2011, Intranasal immunization with poly(gamma-glutamic acid) nanoparticles entrapping antigenic proteins can induce potent tumor immunity, J. Control. Release, 152, 310, 10.1016/j.jconrel.2011.03.009 Yoshikawa, 2008, Nanoparticles built by self-assembly of amphiphilic gamma-PGA can deliver antigens to antigen-presenting cells with high efficiency: a new tumor-vaccine carrier for eliciting effector T cells, Vaccine, 26, 1303, 10.1016/j.vaccine.2007.12.037 Lin, 2007, Preparation and characterization of nanoparticles shelled with chitosan for oral insulin delivery, Biomacromolecules, 8, 146, 10.1021/bm0607776 Corinti, 2001, Regulatory activity of autocrine IL-10 on dendritic cell functions, J. Immunol., 166, 4312, 10.4049/jimmunol.166.7.4312 Kelsall, 1996, Interleukin-12 production by dendritic cells. The role of CD40-CD40L interactions in Th1 T-cell responses, Ann. N. Y. Acad. Sci., 795, 116, 10.1111/j.1749-6632.1996.tb52660.x Trumpfheller, 2008, The microbial mimic poly IC induces durable and protective CD4+ T cell immunity together with a dendritic cell targeted vaccine, Proc. Natl. Acad. Sci. U.S.A., 105, 2574, 10.1073/pnas.0711976105 Guy, 2007, The perfect mix: recent progress in adjuvant research, Nat. Rev. Microbiol., 5, 505, 10.1038/nrmicro1681 Uto, 2009, Modulation of innate and adaptive immunity by biodegradable nanoparticles, Immunol. Lett., 125, 46, 10.1016/j.imlet.2009.05.008 Uto, 2007, Targeting of antigen to dendritic cells with poly(gamma-glutamic acid) nanoparticles induces antigen-specific humoral and cellular immunity, J. Immunol., 178, 2979, 10.4049/jimmunol.178.5.2979 Villiers, 2009, From secretome analysis to immunology: chitosan induces major alterations in the activation of dendritic cells via a TLR4-dependent mechanism, Mol. Cell. Proteomics, 8, 1252, 10.1074/mcp.M800589-MCP200 Bueter, 2014, Spectrum and mechanisms of inflammasome activation by chitosan, J. Immunol., 192, 5943, 10.4049/jimmunol.1301695 Kowal, 2011, CD163 and its role in inflammation, Folia Histochem. Cytobiol., 49, 365, 10.5603/FHC.2011.0052 Barbosa, 2010, Evaluation of the effect of the degree of acetylation on the inflammatory response to 3D porous chitosan scaffolds, J. Biomed. Mater. Res. A, 93, 20 Vasconcelos, 2013, Macrophage polarization following chitosan implantation, Biomaterials, 34, 9952, 10.1016/j.biomaterials.2013.09.012 Jain, 2015, Macrophage repolarization with targeted alginate nanoparticles containing IL-10 plasmid DNA for the treatment of experimental arthritis, Biomaterials, 61, 162, 10.1016/j.biomaterials.2015.05.028 He, 2016, Re-polarizing Myeloid-derived Suppressor Cells (MDSCs) with Cationic Polymers for Cancer Immunotherapy, Sci Rep, 6, 24506, 10.1038/srep24506 Mantovani, 2015, The interaction of anticancer therapies with tumor-associated macrophages, J. Exp. Med., 212, 435, 10.1084/jem.20150295 Zaharoff, 2007, Chitosan solution enhances both humoral and cell-mediated immune responses to subcutaneous vaccination, Vaccine, 25, 2085, 10.1016/j.vaccine.2006.11.034 Zaharoff, 2007, Chitosan solution enhances the immunoadjuvant properties of GM-CSF, Vaccine, 25, 8673, 10.1016/j.vaccine.2007.10.037