A new TLR2 agonist promotes cross-presentation by mouse and human antigen presenting cells

References

• Rappuoli R, Mandl CW, Black S, De Gregorio E. Vaccines for the twenty-first century society. Nature reviews Immunology 2011; 11:865-72; PMID:22051890
   PubMed Web of Science ®Google Scholar
• Wiesel M, Walton S, Richter K, Oxenius A. Virus-specific CD8 T cells: activation, differentiation and memory formation. APMIS 2009; 117:356-81; PMID:19400862; http://dx.doi.org/10.1111/j.1600-0463.2009.02459.x
   PubMed Web of Science ®Google Scholar
• Bevan MJ. Cross-priming for a secondary cytotoxic response to minor H antigens with H-2 congenic cells which do not cross-react in the cytotoxic assay. The Journal of experimental medicine 1976; 143:1283-8; PMID:1083422; http://dx.doi.org/10.1084/jem.143.5.1283
   PubMed Web of Science ®Google Scholar
• Rock KL, Shen L. Cross-presentation: underlying mechanisms and role in immune surveillance. Immunological reviews 2005; 207:166-83; PMID:16181335; http://dx.doi.org/10.1111/j.0105-2896.2005.00301.x
   PubMed Web of Science ®Google Scholar
• O'Neill D, Bhardwaj N. Exploiting dendritic cells for active immunotherapy of cancer and chronic infection. Methods Mol Med 2005; 109:1-18; PMID:15585909
   PubMedGoogle Scholar
• Bonifaz L, Bonnyay D, Mahnke K, Rivera M, Nussenzweig MC, Steinman RM. Efficient targeting of protein antigen to the dendritic cell receptor DEC-205 in the steady state leads to antigen presentation on major histocompatibility complex class I products and peripheral CD8+ T cell tolerance. J Exp Med 2002; 196:1627-38; PMID:12486105; http://dx.doi.org/10.1084/jem.20021598
   PubMed Web of Science ®Google Scholar
• Hoebe K, Janssen EM, Kim SO, Alexopoulou L, Flavell RA, Han J, Beutler B. Upregulation of costimulatory molecules induced by lipopolysaccharide and double-stranded RNA occurs by Trif-dependent and Trif-independent pathways. Nat Immunol 2003; 4:1223-9; PMID:14625548; http://dx.doi.org/10.1038/ni1010
   PubMed Web of Science ®Google Scholar
• Datta SK, Redecke V, Prilliman KR, Takabayashi K, Corr M, Tallant T, DiDonato J, Dziarski R, Akira S, Schoenberger SP, et al. A subset of Toll-like receptor ligands induces cross-presentation by bone marrow-derived dendritic cells. J Immunol 2003; 170:4102-10; PMID:12682240; http://dx.doi.org/10.4049/jimmunol.170.8.4102
   PubMed Web of Science ®Google Scholar
• Ishii KJ, Akira S. Toll or toll-free adjuvant path toward the optimal vaccine development. J Clin Immunol 2007; 27:363-71; PMID:17370119; http://dx.doi.org/10.1007/s10875-007-9087-x
   PubMed Web of Science ®Google Scholar
• Caproni E, Tritto E, Cortese M, Muzzi A, Mosca F, Monaci E, Baudner B, Seubert A, De Gregorio E. MF59 and Pam3CSK4 Boost Adaptive Responses to Influenza Subunit Vaccine through an IFN Type I-Independent Mechanism of Action. J Immunol 2012; PMID:22351935; http://dx.doi.org/10.4049/jimmunol.1101764
   PubMed Web of Science ®Google Scholar
• Steinhagen F, Kinjo T, Bode C, Klinman DM. TLR-based immune adjuvants. Vaccine 2011; 29:3341-55; PMID:20713100; http://dx.doi.org/10.1016/j.vaccine.2010.08.002
   PubMed Web of Science ®Google Scholar
• Schulz O, Diebold SS, Chen M, Naslund TI, Nolte MA, Alexopoulou L, Azuma YT, Flavell RA, Liljestrom P, Reis e Sousa C. Toll-like receptor 3 promotes cross-priming to virus-infected cells. Nature 2005; 433:887-92; PMID:15711573; http://dx.doi.org/10.1038/nature03326
   PubMed Web of Science ®Google Scholar
• Oh JZ, Kedl RM. The capacity to induce cross-presentation dictates the success of a TLR7 agonist-conjugate vaccine for eliciting cellular immunity. J Immunol 2010; 185:4602-8; PMID:20844205; http://dx.doi.org/10.4049/jimmunol.1001892
   PubMed Web of Science ®Google Scholar
• Speiser DE, Lienard D, Rufer N, Rubio-Godoy V, Rimoldi D, Lejeune F, Krieg AM, Cerottini JC, Romero P. Rapid and strong human CD8+ T cell responses to vaccination with peptide, IFA, and CpG oligodeoxynucleotide 7909. J Clin Invest 2005; 115:739-46; PMID:15696196; http://dx.doi.org/10.1172/JCI23373
   PubMed Web of Science ®Google Scholar
• Garcon N, Van Mechelen M. Recent clinical experience with vaccines using MPL- and QS-21-containing adjuvant systems. Exp Rev Vaccines 2011; 10:471-86; PMID:21506645; http://dx.doi.org/10.1586/erv.11.29
   PubMed Web of Science ®Google Scholar
• Prajeeth CK, Jirmo AC, Krishnaswamy JK, Ebensen T, Guzman CA, Weiss S, Constabel H, Schmidt RE, Behrens GM. The synthetic TLR2 agonist BPPcysMPEG leads to efficient cross-priming against co-administered and linked antigens. Eur J Immunol 2010; 40:1272-83; PMID:20213735; http://dx.doi.org/10.1002/eji.200939790
   PubMed Web of Science ®Google Scholar
• Chua BY, Pejoski D, Turner SJ, Zeng W, Jackson DC. Soluble proteins induce strong CD8+ T cell and antibody responses through electrostatic association with simple cationic or anionic lipopeptides that target TLR2. J Immunol 2011; 187:1692-701; PMID:21742967; http://dx.doi.org/10.4049/jimmunol.1100486
   PubMed Web of Science ®Google Scholar
• Shen KY, Song YC, Chen IH, Leng CH, Chen HW, Li HJ, Chong P, Liu SJ. Molecular mechanisms of TLR2-mediated antigen cross-presentation in dendritic cells. J Immunol 2014; 192:4233-41; PMID:24683188; http://dx.doi.org/10.4049/jimmunol.1302850
   PubMed Web of Science ®Google Scholar
• de Wit J, Souwer Y, Jorritsma T, Klaasse Bos H, ten Brinke A, Neefjes J, van Ham SM. Antigen-specific B cells reactivate an effective cytotoxic T cell response against phagocytosed Salmonella through cross-presentation. PloS One 2010; 5:e13016; PMID:20885961; http://dx.doi.org/10.1371/journal.pone.0013016
   PubMed Web of Science ®Google Scholar
• Jiang W, Lederman MM, Harding CV, Sieg SF. Presentation of soluble antigens to CD8+ T cells by CpG oligodeoxynucleotide-primed human naive B cells. J Immunol 2011; 186:2080-6; PMID:21239717; http://dx.doi.org/10.4049/jimmunol.1001869
   PubMed Web of Science ®Google Scholar
• Ritchie DS, Yang J, Hermans IF, Ronchese F. B-Lymphocytes activated by CD40 ligand induce an antigen-specific anti-tumour immune response by direct and indirect activation of CD8(+) T-cells. Scandinavian J Immunol 2004; 60:543-51; PMID:15584965; http://dx.doi.org/10.1111/j.0300-9475.2004.01517.x
   PubMed Web of Science ®Google Scholar
• Baschang G. Muramylpeptides and lipopeptides: Studies towards immunostimulants. Tetrahedron 1989; 45:6331-60; PMID:NOT_FOUND; http://dx.doi.org/10.1016/S0040-4020(01)89512-0
   PubMedGoogle Scholar
• Jin MS, Kim SE, Heo JY, Lee ME, Kim HM, Paik SG, Lee H, Lee JO. Crystal structure of the TLR1-TLR2 heterodimer induced by binding of a tri-acylated lipopeptide. Cell 2007; 130:1071-82; PMID:17889651; http://dx.doi.org/10.1016/j.cell.2007.09.008
   PubMed Web of Science ®Google Scholar
• Hogquist KA, Jameson SC, Heath WR, Howard JL, Bevan MJ, Carbone FR. T cell receptor antagonist peptides induce positive selection. Cell 1994; 76:17-27; PMID:8287475; http://dx.doi.org/10.1016/0092-8674(94)90169-4
   PubMed Web of Science ®Google Scholar
• Calabro S, Tortoli M, Baudner BC, Pacitto A, Cortese M, O'Hagan DT, De Gregorio E, Seubert A, Wack A. Vaccine adjuvants alum and MF59 induce rapid recruitment of neutrophils and monocytes that participate in antigen transport to draining lymph nodes. Vaccine 2011; 29:1812-23; PMID:21215831; http://dx.doi.org/10.1016/j.vaccine.2010.12.090
   PubMed Web of Science ®Google Scholar
• Belz GT, Smith CM, Eichner D, Shortman K, Karupiah G, Carbone FR, Heath WR. Cutting edge: conventional CD8 alpha+ dendritic cells are generally involved in priming CTL immunity to viruses. J Immunol 2004; 172:1996-2000; PMID:14764661; http://dx.doi.org/10.4049/jimmunol.172.4.1996
   PubMed Web of Science ®Google Scholar
• Shortman K, Heath WR. The CD8+ dendritic cell subset. Immunological reviews 2010; 234:18-31; PMID:20193009; http://dx.doi.org/10.1111/j.0105-2896.2009.00870.x
   PubMed Web of Science ®Google Scholar
• Heath WR, Carbone FR. Cross-presentation, dendritic cells, tolerance and immunity. Annu Rev Immunol 2001; 19:47-64; PMID:11244030; http://dx.doi.org/10.1146/annurev.immunol.19.1.47
   PubMed Web of Science ®Google Scholar
• Bachem A, Guttler S, Hartung E, Ebstein F, Schaefer M, Tannert A, Salama A, Movassaghi K, Opitz C, Mages HW, et al. Superior antigen cross-presentation and XCR1 expression define human CD11c+CD141+ cells as homologues of mouse CD8+ dendritic cells. J Exp Med 2010; 207:1273-81; PMID:20479115; http://dx.doi.org/10.1084/jem.20100348
   PubMed Web of Science ®Google Scholar
• Jongbloed SL, Kassianos AJ, McDonald KJ, Clark GJ, Ju X, Angel CE, Chen CJ, Dunbar PR, Wadley RB, Jeet V, et al. Human CD141+ (BDCA-3)+ dendritic cells (DCs) represent a unique myeloid DC subset that cross-presents necrotic cell antigens. J Exp Med 2010; 207:1247-60; PMID:20479116; http://dx.doi.org/10.1084/jem.20092140
   PubMed Web of Science ®Google Scholar
• den Haan JM, Bevan MJ. Constitutive versus activation-dependent cross-presentation of immune complexes by CD8(+) and CD8(−) dendritic cells in vivo. J Exp Med 2002; 196:817-27; PMID:12235214; http://dx.doi.org/10.1084/jem.20020295
   PubMed Web of Science ®Google Scholar
• Moron G, Rueda P, Casal I, Leclerc C. CD8alpha- CD11b+ dendritic cells present exogenous virus-like particles to CD8+ T cells and subsequently express CD8alpha and CD205 molecules. J Exp Med 2002; 195:1233-45; PMID:12021304; http://dx.doi.org/10.1084/jem.20011930
   PubMed Web of Science ®Google Scholar
• Billetta R, Filaci G, Zanetti M. Major histocompatibility complex class I-restricted presentation of influenza virus nucleoprotein peptide by B lymphoma cells harboring an antibody gene antigenized with the virus peptide. EurJ Immunol 1995; 25:776-83; PMID:7705408; http://dx.doi.org/10.1002/eji.1830250323
   PubMed Web of Science ®Google Scholar
• Zhong G, Reis e Sousa C, Germain RN. Antigen-unspecific B cells and lymphoid dendritic cells both show extensive surface expression of processed antigen-major histocompatibility complex class II complexes after soluble protein exposure in vivo or in vitro. J Exp Med 1997; 186:673-82; PMID:9271583; http://dx.doi.org/10.1084/jem.186.5.673
   PubMed Web of Science ®Google Scholar
• Constant SL. B lymphocytes as antigen-presenting cells for CD4+ T cell priming in vivo. J Immunol 1999; 162:5695-703; PMID:10229801
   PubMed Web of Science ®Google Scholar
• Evans DE, Munks MW, Purkerson JM, Parker DC. Resting B lymphocytes as APC for naive T lymphocytes: dependence on CD40 ligand/CD40. J Immunol 2000; 164:688-97; PMID:10623811; http://dx.doi.org/10.4049/jimmunol.164.2.688
   PubMed Web of Science ®Google Scholar
• Dougan SK, Ogata S, Hu CC, Grotenbreg GM, Guillen E, Jaenisch R, Ploegh HL. IgG1+ ovalbumin-specific B-cell transnuclear mice show class switch recombination in rare allelically included B cells. Proc Natl Acad Sci U S A 2012; 109:13739-44.
   PubMed Web of Science ®Google Scholar
• Harari A, Zimmerli SC, Pantaleo G. Cytomegalovirus (CMV)-specific cellular immune responses. Hum Immunol 2004; 65:500-6; PMID:15172450; http://dx.doi.org/10.1016/j.humimm.2004.02.012
   PubMed Web of Science ®Google Scholar
• Schulz O, Reis e Sousa C. Cross-presentation of cell-associated antigens by CD8alpha+ dendritic cells is attributable to their ability to internalize dead cells. Immunology 2002; 107:183-9; PMID:12383197; http://dx.doi.org/10.1046/j.1365-2567.2002.01513.x
   PubMed Web of Science ®Google Scholar
• Iyoda T, Shimoyama S, Liu K, Omatsu Y, Akiyama Y, Maeda Y, Takahara K, Steinman RM, Inaba K. The CD8+ dendritic cell subset selectively endocytoses dying cells in culture and in vivo. J Exp Med 2002; 195:1289-302; PMID:12021309; http://dx.doi.org/10.1084/jem.20020161
   PubMed Web of Science ®Google Scholar
• Crespo MI, Zacca ER, Nunez NG, Ranocchia RP, Maccioni M, Maletto BA, Pistoresi-Palencia MC, Moron G. TLR7 triggering with polyuridylic acid promotes cross-presentation in CD8alpha+ conventional dendritic cells by enhancing antigen preservation and MHC class I antigen permanence on the dendritic cell surface. J Immunol 2013; 190:948-60; PMID:23284054; http://dx.doi.org/10.4049/jimmunol.1102725
   PubMed Web of Science ®Google Scholar
• Browne EP. Regulation of B-cell responses by Toll-like receptors. Immunology 2012; 136:370-9; PMID:22444240; http://dx.doi.org/10.1111/j.1365-2567.2012.03587.x
   PubMed Web of Science ®Google Scholar
• Schreibelt G, Klinkenberg LJ, Cruz LJ, Tacken PJ, Tel J, Kreutz M, Adema GJ, Brown GD, Figdor CG, de Vries IJ. The C-type lectin receptor CLEC9A mediates antigen uptake and (cross-)presentation by human blood BDCA3+ myeloid dendritic cells. Blood 2012; 119:2284-92; PMID:22234694; http://dx.doi.org/10.1182/blood-2011-08-373944
   PubMed Web of Science ®Google Scholar
• Bonifaz LC, Bonnyay DP, Charalambous A, Darguste DI, Fujii S, Soares H, Brimnes MK, Moltedo B, Moran TM, Steinman RM. In vivo targeting of antigens to maturing dendritic cells via the DEC-205 receptor improves T cell vaccination. J Exp Med 2004; 199:815-24; PMID:15024047; http://dx.doi.org/10.1084/jem.20032220
   PubMed Web of Science ®Google Scholar
• Idoyaga J, Lubkin A, Fiorese C, Lahoud MH, Caminschi I, Huang Y, Rodriguez A, Clausen BE, Park CG, Trumpfheller C, et al. Comparable T helper 1 (Th1) and CD8 T-cell immunity by targeting HIV gag p24 to CD8 dendritic cells within antibodies to Langerin, DEC205, and Clec9A. Proceedings of the National Academy of Sciences of the United States of America 2011; 108:2384-9.
   Google Scholar
• Poulin LF, Salio M, Griessinger E, Anjos-Afonso F, Craciun L, Chen JL, Keller AM, Joffre O, Zelenay S, Nye E, et al. Characterization of human DNGR-1+ BDCA3+ leukocytes as putative equivalents of mouse CD8alpha+ dendritic cells. J Exp Med 2010; 207:1261-71; PMID:20479117; http://dx.doi.org/10.1084/jem.20092618
   PubMed Web of Science ®Google Scholar
• Cho HJ, Takabayashi K, Cheng PM, Nguyen MD, Corr M, Tuck S, Raz E. Immunostimulatory DNA-based vaccines induce cytotoxic lymphocyte activity by a T-helper cell-independent mechanism. Nat Biotechnol 2000; 18:509-14; PMID:10802617; http://dx.doi.org/10.1038/75365
   PubMed Web of Science ®Google Scholar
• Shirota H, Sano K, Hirasawa N, Terui T, Ohuchi K, Hattori T, Shirato K, Tamura G. Novel roles of CpG oligodeoxynucleotides as a leader for the sampling and presentation of CpG-tagged antigen by dendritic cells. J Immunol 2001; 167:66-74; PMID:11418633; http://dx.doi.org/10.4049/jimmunol.167.1.66
   PubMed Web of Science ®Google Scholar
• Ingulli E. Tracing tolerance and immunity in vivo by CFSE-labeling of administered cells. Methods Mol Biol 2007; 380:365-76; PMID:17876106; http://dx.doi.org/10.1007/978-1-59745-395-0_23
   PubMedGoogle Scholar