Oral delivery of tumor microparticle vaccines activates NOD2 signaling pathway in ileac epithelium rendering potent antitumor T cell immunity

References

• Prensner JR, Chinnaiyan AM. The emergence of lncRNAs in cancer biology. Cancer Discov 2011; 1:391-407; PMID:22096659; http://dx.doi.org/10.1158/2159-8290.cd-11-0209
   PubMed Web of Science ®Google Scholar
• Hanash S.. Integrated global profiling of cancer. Nat Rev Cancer 2004; 4:638-44; PMID:15286743; http://dx.doi.org/10.1038/nrc1414
   PubMed Web of Science ®Google Scholar
• Hubbell JA, Thomas SN, Swartz MA. Materials engineering for immunomodulation. Nature 2009; 462:449-60; PMID:19940915; http://dx.doi.org/10.1038/nature08604
   PubMed Web of Science ®Google Scholar
• Best SR, Peng S, Juang CM, Hung CF, Hannaman D, Saunders JR, Wu TC, Pai SI. Administration of HPV DNA vaccine via electroporation elicits the strongest CD8+ T cell immune responses compared to intramuscular injection and intradermal gene gun delivery. Vaccine 2009; 27:5450-9; PMID:19622402; http://dx.doi.org/10.1016/j.vaccine.2009.07.005
   PubMed Web of Science ®Google Scholar
• Buchan S, Gronevik E, Mathiesen I, King CA, Stevenson FK, Rice J. Electroporation as a “prime/boost” strategy for naked DNA vaccination against a tumor antigen. J Immunol 2005; 174:6292-8; PMID:15879128; http://dx.doi.org/10.4049/jimmunol.174.10.6292
   PubMed Web of Science ®Google Scholar
• Perez-Lopez A, Behnsen J, Nuccio SP, Raffatellu M. Mucosal immunity to pathogenic intestinal bacteria. Nat Rev Immunol 2016; 16:135-48; PMID:26898110; http://dx.doi.org/10.1038/nri.2015.17
   PubMed Web of Science ®Google Scholar
• Lycke N.. Recent progress in mucosal vaccine development: potential and limitations. Nat Rev Immunol 2012; 12:592-605; PMID:22828912; http://dx.doi.org/10.1038/nri3251
   PubMed Web of Science ®Google Scholar
• Holmgren J, Svennerholm AM. Vaccines against mucosal infections. Curr Opin Immunol 2012; 24:343-53; PMID:22580196; http://dx.doi.org/10.1016/j.coi.2012.03.014
   PubMed Web of Science ®Google Scholar
• Holmgren J, Czerkinsky C. Mucosal immunity and vaccines. Nat Med 2005; 11:S45-53; PMID:15812489; http://dx.doi.org/10.1038/nm1213
   PubMed Web of Science ®Google Scholar
• Mitragotri S.. Immunization without needles. Nat Rev Immunol 2005; 5:905-16; PMID:16239901; http://dx.doi.org/10.1038/nri1728
   PubMed Web of Science ®Google Scholar
• Cai X, Chiu YH, Chen ZJ. The cGAS-cGAMP-STING pathway of cytosolic DNA sensing and signaling. Mol Cell 2014; 54:289-96; PMID:24766893; http://dx.doi.org/10.1016/j.molcel.2014.03.040
   PubMed Web of Science ®Google Scholar
• Kroemer G, Galluzzi L, Kepp O, Zitvogel L. Immunogenic cell death in cancer therapy. Annu Rev Immunol 2013; 31:51-72; PMID:23157435; http://dx.doi.org/10.1146/annurev-immunol-032712-100008
   PubMed Web of Science ®Google Scholar
• Diamond MS, Kinder M, Matsushita H, Mashayekhi M, Dunn GP, Archambault JM, Lee H, Arthur CD, White JM, Kalinke U et al. Type I interferon is selectively required by dendritic cells for immune rejection of tumors. J Exp Med 2011; 208:1989-2003; PMID:21930769; http://dx.doi.org/10.1084/jem.20101158
   PubMed Web of Science ®Google Scholar
• Koshy ST, Mooney DJ. Biomaterials for enhancing anti-cancer immunity. Curr Opin Biotech 2016; 40:1-8; PMID:26896596; http://dx.doi.org/10.1016/j.copbio.2016.02.001
   PubMed Web of Science ®Google Scholar
• Irvine DJ, Swartz MA, Szeto GL. Engineering synthetic vaccines using cues from natural immunity. Nat Mater 2013; 12:978-90; PMID:24150416; http://dx.doi.org/10.1038/nmat3775
   PubMed Web of Science ®Google Scholar
• Fitzgerald KA, Rowe DC, Barnes BJ, Caffrey DR, Visintin A, Latz E, Monks B, Pitha PM, Golenbock DT. LPS-TLR4 signaling to IRF-3/7 and NF-κB involves the toll adapters TRAM and TRIF. J Exp Med 2003; 198:1043-55; PMID:14517278; http://dx.doi.org/10.1084/jem.20031023
   PubMed Web of Science ®Google Scholar
• Hornung V, Latz E. Intracellular DNA recognition. Nat Rev Immunol 2010; 10:123-30; PMID:20098460; http://dx.doi.org/10.1038/nri2690
   PubMed Web of Science ®Google Scholar
• Herber DL, Cao W, Nefedova Y, Novitskiy SV, Nagaraj S, Tyurin VA, Corzo A, Cho HI, Celis E, Lennox B et al. Lipid accumulation and dendritic cell dysfunction in cancer. Nat Med 2010; 16:880-6; PMID:20622859; http://dx.doi.org/10.1038/nm.2172
   PubMed Web of Science ®Google Scholar
• Dhodapkar MV, Dhodapkar KM, Palucka AK. Interactions of tumor cells with dendritic cells: balancing immunity and tolerance. Cell Death Differ 2008; 15:39-50; PMID:17948027; http://dx.doi.org/10.1038/sj.cdd.4402247
   PubMed Web of Science ®Google Scholar
• Zhang Y, Zhang R, Zhang H, Liu J, Yang Z, Xu P, Cai W, Lu G, Cui M, Schwendener RA et al. Microparticles released by Listeria monocytogenes-infected macrophages are required for dendritic cell-elicited protective immunity. Cell Mol Immunol 2012; 9:489-96; PMID:23064105; http://dx.doi.org/10.1038/cmi.2012.33
   PubMed Web of Science ®Google Scholar
• Zhang H, Tang K, Zhang Y, Ma R, Ma J, Li Y, Luo S, Liang X, Ji T, Gu Z et al. Cell-free tumor microparticle vaccines stimulate dendritic cells via cGAS/STING signaling. Cancer Immunol Res 2015; 3:196-205; PMID:25477253; http://dx.doi.org/10.1158/2326-6066.cir-14-0177
   PubMed Web of Science ®Google Scholar
• Zhang H, Huang B. Tumor cell-derived microparticles: a new form of cancer vaccine. Oncoimmunology 2015; 4:e1017704; PMID:26405568; http://dx.doi.org/10.1080/2162402x.2015.1017704
   PubMed Web of Science ®Google Scholar
• Chatterjee D, Chaudhuri K. Vibrio cholerae O395 outer membrane vesicles modulate intestinal epithelial cells in a NOD1 protein-dependent manner and induce dendritic cell-mediated Th2/Th17 cell responses. J Biol Chem 2013; 288:4299-309; PMID:23275338; http://dx.doi.org/10.1074/jbc.M112.408302
   PubMed Web of Science ®Google Scholar
• Motta V, Soares F, Sun T, Philpott DJ. NOD-like receptors: versatile cytosolic sentinels. Physiol Rev 2015; 95:149-78; PMID:25540141; http://dx.doi.org/10.1152/physrev.00009.2014
   PubMed Web of Science ®Google Scholar
• Strober W, Murray PJ, Kitani A, Watanabe T. Signalling pathways and molecular interactions of NOD1 and NOD2. Nat Rev Immunol 2006; 6:9-20; PMID:16493424; http://dx.doi.org/10.1038/nri1747
   PubMed Web of Science ®Google Scholar
• Tang K, Zhang Y, Zhang H, Xu P, Liu J, Ma J, Lv M, Li D, Katirai F, Shen GX et al. Delivery of chemotherapeutic drugs in tumour cell-derived microparticles. Nat Commun 2012; 3:1282; PMID:23250412; http://dx.doi.org/10.1038/ncomms2282
   PubMed Web of Science ®Google Scholar
• Ma J, Zhang Y, Tang K, Zhang H, Yin X, Li Y, Xu P, Sun Y, Ma R, Ji T et al. Reversing drug resistance of soft tumor-repopulating cells by tumor cell-derived chemotherapeutic microparticles. Cell Res 2016; 26:713-27; PMID:27167569; http://dx.doi.org/10.1038/cr.2016.53
   PubMed Web of Science ®Google Scholar
• Ran L, Tan X, Li Y, Zhang H, Ma R, Ji T, Dong W, Tong T, Liu Y, Chen D et al. Delivery of oncolytic adenovirus into the nucleus of tumorigenic cells by tumor microparticles for virotherapy. Biomaterials 2016; 89:56-66; PMID:26950165; http://dx.doi.org/10.1016/j.biomaterials.2016.02.025
   PubMed Web of Science ®Google Scholar
• Li D, Jia H, Zhang H, Lv M, Liu J, Zhang Y, Huang T, Huang B. TLR4 signaling induces the release of microparticles by tumor cells that regulate inflammatory cytokine IL-6 of macrophages via microRNA let-7b. Oncoimmunology 2012; 1:687-93; PMID:22934260; http://dx.doi.org/10.4161/onci.19854
   PubMed Web of Science ®Google Scholar
• Ma J, Cai W, Zhang Y, Huang C, Zhang H, Liu J, Tang K, Xu P, Katirai F, Zhang J et al. Innate immune cell-derived microparticles facilitate hepatocarcinoma metastasis by transferring integrin αMβ2 to tumor cells. J Immunol 2013; 191:3453-61; PMID:23956429; http://dx.doi.org/10.4049/jimmunol.1300171
   PubMed Web of Science ®Google Scholar
• Tang K, Liu J, Yang Z, Zhang B, Zhang H, Huang C, Ma J, Shen GX, Ye D, Huang B. Microparticles mediate enzyme transfer from platelets to mast cells: a new pathway for lipoxin A4 biosynthesis. Biochem Bioph Res Co 2010; 400:432-6; PMID:20801099; http://dx.doi.org/10.1016/j.bbrc.2010.08.095
   PubMed Web of Science ®Google Scholar
• Del Conde I, Shrimpton CN, Thiagarajan P, Lopez JA. Tissue-factor-bearing microvesicles arise from lipid rafts and fuse with activated platelets to initiate coagulation. Blood 2005; 106:1604-11; PMID:15741221; http://dx.doi.org/10.1182/blood-2004-03-1095
   PubMed Web of Science ®Google Scholar
• Johansson ME, Hansson GC. Microbiology. Keeping bacteria at a distance. Science 2011; 334:182-3; PMID:21998374; http://dx.doi.org/10.1126/science.1213909
   PubMed Web of Science ®Google Scholar
• Johansson ME, Sjovall H, Hansson GC. The gastrointestinal mucus system in health and disease. Nat Rev Gastro Hepa 2013; 10:352-61; PMID:23478383; http://dx.doi.org/10.1038/nrgastro.2013.35
   PubMed Web of Science ®Google Scholar
• Pelaseyed T, Bergstrom JH, Gustafsson JK, Ermund A, Birchenough GM, Schutte A, van der Post S, Svensson F, Rodríguez-Piñeiro AM, Nyström EE et al. The mucus and mucins of the goblet cells and enterocytes provide the first defense line of the gastrointestinal tract and interact with the immune system. Immunol Rev 2014; 260:8-20; PMID:24942678; http://dx.doi.org/10.1111/imr.12182
   PubMed Web of Science ®Google Scholar
• Ermund A, Schutte A, Johansson ME, Gustafsson JK, Hansson GC. Studies of mucus in mouse stomach, small intestine, and colon. I. Gastrointestinal mucus layers have different properties depending on location as well as over the Peyer's patches. Am J Physiol-Gastr L 2013; 305:G341-7; PMID:23832518; http://dx.doi.org/10.1152/ajpgi.00046.2013
   PubMed Web of Science ®Google Scholar
• Pabst O, Mowat AM. Oral tolerance to food protein. Mucosal Immunol 2012; 5:232-9; PMID:22318493; http://dx.doi.org/10.1038/mi.2012.4
   PubMed Web of Science ®Google Scholar
• Poonam P.. The biology of oral tolerance and issues related to oral vaccine design. Curr Pharm Design 2007; 13:2001-7; PMID:17627533; http://dx.doi.org/10.2174/138161207781039814
   PubMed Web of Science ®Google Scholar
• Goto Y, Ivanov II. Intestinal epithelial cells as mediators of the commensal-host immune crosstalk. Immunol Cell Biol 2013; 91:204-14; PMID:23318659; http://dx.doi.org/10.1038/icb.2012.80
   PubMed Web of Science ®Google Scholar
• Hershberg RM, Mayer LF. Antigen processing and presentation by intestinal epithelial cells - polarity and complexity. Immunol Today 2000; 21:123-8; PMID:10689299; http://dx.doi.org/10.1016/S0167-5699(99)01575-3
   PubMedGoogle Scholar
• Shakhar G, Lindquist RL, Skokos D, Dudziak D, Huang JH, Nussenzweig MC, Dustin ML. Stable T cell-dendritic cell interactions precede the development of both tolerance and immunity in vivo. Nat Immunol 2005; 6:707-14; PMID:15924144; http://dx.doi.org/10.1038/ni1210
   PubMed Web of Science ®Google Scholar
• Steinman RM, Banchereau J. Taking dendritic cells into medicine. Nature 2007; 449:419-26; PMID:17898760; http://dx.doi.org/10.1038/nature06175
   PubMed Web of Science ®Google Scholar
• Palucka K, Banchereau J. Cancer immunotherapy via dendritic cells. Nat Rev Cancer 2012; 12:265-77; PMID:22437871; http://dx.doi.org/10.1038/nrc3258
   PubMed Web of Science ®Google Scholar
• Kim D, Kim YG, Seo SU, Kim DJ, Kamada N, Prescott D, Philpott DJ, Rosenstiel P, Inohara N, Núñez G. Nod2-mediated recognition of the microbiota is critical for mucosal adjuvant activity of cholera toxin. Nat Med 2016; 22:524-30; PMID:27064448; http://dx.doi.org/10.1038/nm.4075
   PubMed Web of Science ®Google Scholar
• Yin Y, Qin T, Wang X, Lin J, Yu Q, Yang Q. CpG DNA assists the whole inactivated H9N2 influenza virus in crossing the intestinal epithelial barriers via transepithelial uptake of dendritic cell dendrites. Mucosal Immunol 2015; 8:799-814; PMID:25492476; http://dx.doi.org/10.1038/mi.2014.110
   PubMed Web of Science ®Google Scholar
• Holmgren J, Adamsson J, Anjuere F, Clemens J, Czerkinsky C, Eriksson K, Flach CF, George-Chandy A, Harandi AM, Lebens M et al. Mucosal adjuvants and anti-infection and anti-immunopathology vaccines based on cholera toxin, cholera toxin B subunit and CpG DNA. Immunol Lett 2005; 97:181-8; PMID:15752556; http://dx.doi.org/10.1016/j.imlet.2004.11.009
   PubMed Web of Science ®Google Scholar
• Gutzeit C, Magri G, Cerutti A. Intestinal IgA production and its role in host-microbe interaction. Immunol Rev 2014; 260:76-85; PMID:24942683; http://dx.doi.org/10.1111/imr.12189
   PubMed Web of Science ®Google Scholar
• Peterson LW, Artis D. Intestinal epithelial cells: regulators of barrier function and immune homeostasis. Nat Rev Immunol 2014; 14:141-53; PMID:24566914; http://dx.doi.org/10.1038/nri3608
   PubMed Web of Science ®Google Scholar
• Ferreira VH, Dizzell S, Nazli A, Kafka JK, Mueller K, Nguyen PV, Tremblay MJ, Cochrane A, Kaushic C. Medroxyprogesterone acetate regulates HIV-1 uptake and transcytosis but not replication in primarygenital epithelial cells, resulting in enhanced T-cell infection. J Infect Dis 2015; 211:1745-56; PMID:25538276; http://dx.doi.org/10.1093/infdis/jiu832
   PubMed Web of Science ®Google Scholar
• Skoufias DA, Wilson L. Mechanism of inhibition of microtubule polymerization by colchicine: inhibitory potencies of unliganded colchicine and tubulin-colchicine complexes. Biochemistry 1992; 31:738-46; PMID:1731931; http://dx.doi.org/10.1021/bi00118a015
   PubMed Web of Science ®Google Scholar