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

Human Vaccines and Immunotherapeutics

Volumn 11, Issue 8, 2015, Pages 2038-2050

  Santone, Melissa ^a   Aprea, Susanna ^a   Wu, Tom Y H ^b   Cooke, Michael P ^b   Mbow, M Lamine ^c,e   Valiante, Nicholas M ^c   Rush, James S ^b,d,f   Dougan, Stephanie ^d   Avalos, Ana ^d   Ploegh, Hidde ^d   De Gregorio, Ennio ^a   Buonsanti, Cecilia ^a   D’Oro, Ugo ^a  

^a NOVARTIS VACCINES AND DIAGNOSTICS   (Italy)

^b Genomics Institute of Novartis Research Foundation (GNF)   (United States)

^c GLAXOSMITHKLINE   (United States)

^d WHITEHEAD INSTITUTE FOR BIOMEDICAL RESEARCH   (United States)

^e BOEHRINGER INGELHEIM PHARMACEUTICALS INC   (United States)

^f NOVARTIS PHARMA AG   (Switzerland)

Author keywords

B cells; Cross presentation priming; Cytotoxic T cells; Dendritic cells; Vaccination

Indexed keywords

CYTOMEGALOVIRUS ANTIGEN PP65; OVALBUMIN; RECOMBINANT ANTIGEN; SMALL MOLECULE IMMUNE POTENTIATOR; TOLL LIKE RECEPTOR AGONIST; UNCLASSIFIED DRUG; CANCER VACCINE; CYTOKINE; IMMUNOLOGICAL ADJUVANT; TLR2 PROTEIN, HUMAN; TLR2 PROTEIN, MOUSE; TOLL LIKE RECEPTOR 2;

ANIMAL CELL; ANIMAL EXPERIMENT; ANIMAL MODEL; ANTIGEN PRESENTING CELL; ARTICLE; B LYMPHOCYTE; BONE MARROW DERIVED DENDRITIC CELL; CD8+ T LYMPHOCYTE; CONTROLLED STUDY; CROSS PRESENTATION; ENZYME LINKED IMMUNOSORBENT ASSAY; FEMALE; FLOW CYTOMETRY; HUMAN; HUMAN CELL; MOUSE; NONHUMAN; THYMIDINE INCORPORATION ASSAY; AGONISTS; ANIMAL; BAGG ALBINO MOUSE; C57BL MOUSE; CELL PROLIFERATION; CYTOTOXICITY; DISEASE MODEL; IMMUNOLOGY; METABOLISM; NEOPLASMS, EXPERIMENTAL; SECRETION (PROCESS); TRANSGENIC MOUSE;

ADJUVANTS, IMMUNOLOGIC; ANIMALS; ANTIGEN-PRESENTING CELLS; CANCER VACCINES; CD8-POSITIVE T-LYMPHOCYTES; CELL PROLIFERATION; CROSS-PRIMING; CYTOKINES; CYTOTOXICITY, IMMUNOLOGIC; DISEASE MODELS, ANIMAL; FEMALE; MICE, INBRED BALB C; MICE, INBRED C57BL; MICE, TRANSGENIC; NEOPLASMS, EXPERIMENTAL; OVALBUMIN; TOLL-LIKE RECEPTOR 2;

EID: 84944456273     PISSN: 21645515     EISSN: 2164554X     Source Type: Journal    
DOI: 10.1080/21645515.2015.1027467     Document Type: Article

References (49)

1. 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
2. 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
3. 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
4. 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
5. 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
6. 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
7. Hoebe K, Janssen EM, Kim SO, Alexopoulou L, Flavell RA, Han J, Beutler B. Upregulation of costimulatory molecules induced by lipopolysaccharide and doublestranded RNA occurs by Trif-dependent and Trif-independent pathways. Nat Immunol 2003; 4:1223-9; PMID:14625548; http://dx. doi. org/10. 1038/ni1010
8. 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 Tolllike 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
9. 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
10. 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
11. 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
12. 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 crosspriming to virus-infected cells. Nature 2005; 433:887- 92; PMID:15711573; http://dx. doi. org/10. 1038/ nature03326
13. 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
14. 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
15. 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
16. 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
17. 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
18. 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
19. 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
20. 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
21. Ritchie DS, Yang J, Hermans IF, Ronchese F. B-Lymphocytes activated by CD40 ligand induce an antigenspecific 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
22. 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
23. 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
24. 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
25. 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
26. 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
27. 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
28. 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
29. 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
30. 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
31. 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
32. 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
33. 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
34. Zhong G, Reis e Sousa C, Germain RN. Antigenunspecific B cells and lymphoid dendritic cells both show extensive surface expression of processed antigenmajor 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
35. Constant SL. B lymphocytes as antigen-presenting cells for CD4+ T cell priming in vivo. J Immunol 1999; 162:5695-703; PMID:10229801
36. 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
37. Dougan SK, Ogata S, Hu CC, Grotenbreg GM, Guillen E, Jaenisch R, Ploegh HL. IgG1+ ovalbuminspecific 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.
38. 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
39. Schulz O, Reis e Sousa C. Cross-presentation of cellassociated 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
40. 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
41. 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
42. Browne EP. Regulation of B-cell responses by Tolllike receptors. Immunology 2012; 136:370-9; PMID:22444240; http://dx. doi. org/10. 1111/j. 1365- 2567. 2012. 03587. x
43. 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
44. 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
45. 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.
46. 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
47. Cho HJ, Takabayashi K, Cheng PM, Nguyen MD, Corr M, Tuck S, Raz E. Immunostimulatory DNAbased 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
48. 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
49. 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