Coadministration of polyinosinic: Polycytidylic acid and immunostimulatory complexes modifies antigen processing in dendritic cell subsets and enhances HIV gag-specific T cell immunity

Journal of Immunology

Volumn 191, Issue 10, 2013, Pages 5085-5096

  Quinn, Kylie M ^a   Yamamoto, Ayako ^a   Costa, Andreia ^a,c   Darrah, Patricia A ^a   Lindsay, Ross W B ^a,d   Hegde, Sonia T ^a,e   Johnson, Teresa R ^a,f   Flynn, Barbara J ^a   Loré, Karin ^a,b   Seder, Robert A ^a  

^a NATIONAL INSTITUTE OF ALLERGY AND INFECTIOUS DISEASES   (United States)

^b KAROLINSKA INSTITUTE   (Sweden)

^c Fred Hutchinson Cancer Research Center   (United States)

^d INTERNATIONAL AIDS VACCINE INITIATIVE   (United States)

^e CENTERS FOR DISEASE CONTROL AND PREVENTION   (United States)

^f GenVec   (United States)

Author keywords

[No Author keywords available]

Indexed keywords

GAG PROTEIN; GAMMA INTERFERON; IMMUNOLOGICAL ADJUVANT; INTERLEUKIN 2; INTERLEUKIN 7 RECEPTOR; ISCOM; POLYINOSINIC POLYCYTIDYLIC ACID; TUMOR NECROSIS FACTOR; INTERLEUKIN 7 RECEPTOR ALPHA; T BOX TRANSCRIPTION FACTOR; T-BOX TRANSCRIPTION FACTOR TBX21; TUMOR NECROSIS FACTOR ALPHA;

ANIMAL CELL; ANIMAL EXPERIMENT; ANIMAL MODEL; ANIMAL TISSUE; ANTIGEN PRESENTATION; ARTICLE; CD4+ T LYMPHOCYTE; CD8+ T LYMPHOCYTE; CELL DEATH; CELLULAR IMMUNITY; CONTROLLED STUDY; CYTOKINE PRODUCTION; DENDRITIC CELL; DRUG FORMULATION; LISTERIA MONOCYTOGENES; MOUSE; NONHUMAN; PRIORITY JOURNAL; PROTEIN DEGRADATION; PROTEIN SECRETION; PROTEIN TRANSPORT; VACCINIA VIRUS; ANIMAL; BAGG ALBINO MOUSE; BIOSYNTHESIS; C57BL MOUSE; DRUG EFFECTS; IMMUNOLOGY; LISTERIOSIS; METABOLISM; VACCINIA;

ANIMALS; ANTIGEN PRESENTATION; CD4-POSITIVE T-LYMPHOCYTES; CD8-POSITIVE T-LYMPHOCYTES; DENDRITIC CELLS; GAG GENE PRODUCTS, HUMAN IMMUNODEFICIENCY VIRUS; INTERFERON-GAMMA; INTERLEUKIN-2; INTERLEUKIN-7 RECEPTOR ALPHA SUBUNIT; ISCOMS; LISTERIA MONOCYTOGENES; LISTERIOSIS; MICE; MICE, INBRED BALB C; MICE, INBRED C57BL; POLY I-C; T-BOX DOMAIN PROTEINS; TUMOR NECROSIS FACTOR-ALPHA; VACCINIA; VACCINIA VIRUS;

EID: 84887457989     PISSN: 00221767     EISSN: 15506606     Source Type: Journal    
DOI: 10.4049/jimmunol.1301730     Document Type: Article

References (74)

1. Kwong, P. D., J. R. Mascola, and G. J. Nabel. 2012. The changing face of HIV vaccine research. J. Int. AIDS Soc. 15:17407.
2. Hansen, S. G., J. C. Ford, M. S. Lewis, A. B. Ventura, C. M. Hughes, L. Coyne-Johnson, N. Whizin, K. Oswald, R. Shoemaker, T. Swanson, et al. 2011. Profound early control of highly pathogenic SIV by an effector memory T-cell vaccine. Nature 473:523-527.
3. Epstein, J. E., K. Tewari, K. E. Lyke, B. K. L. Sim, P. F. Billingsley, M. B. Laurens, A. Gunasekera, S. Chakravarty, E. R. James, M. Sedegah, et al. 2011. Live attenuated malaria vaccine designed to protect through hepatic CD8? T cell immunity. Science 334:475-480.
4. Abel, B., M. Tameris, N. Mansoor, S. Gelderbloem, J. Hughes, D. Abrahams, L. Makhethe, M. Erasmus, M. De Kock, L. Van Der Merwe, et al. 2010. The novel tuberculosis vaccine, AERAS-402, induces robust and polyfunctional CD4+ and CD8+ T cells in adults. Am. J. Respir. Crit. Care Med. 181:1407-1417.
5. Coffman, R. L., A. Sher, and R. A. Seder. 2010. Vaccine adjuvants: putting innate immunity to work. Immunity 33:492-503.
6. Longhi, M. P., C. Trumpfheller, J. Idoyaga, M. Caskey, I. Matos, C. Kluger, A. M. Salazar, M. Colonna, and R. M. Steinman. 2009. Dendritic cells require a systemic type I interferon response to mature and induce CD4+ Th1 immunity with poly IC as adjuvant. J. Exp. Med. 206:1589-1602.
7. Flynn, B. J., K. Kastenmüller, U. Wille-Reece, G. D. Tomaras, M. Alam, R. W. Lindsay, A. M. Salazar, B. Perdiguero, C. E. Gomez, R. Wagner, et al. 2011. Immunization with HIV Gag targeted to dendritic cells followed by recombinant New York vaccinia virus induces robust T-cell immunity in nonhuman primates. Proc. Natl. Acad. Sci. USA 108:7131-7136.
8. Drane, D., E. Maraskovsky, R. Gibson, S. Mitchell, M. Barnden, A. Moskwa, D. Shaw, B. Gervase, S. Coates, M. Houghton, and R. Basser. 2009. Priming of CD4+ and CD8+ T cell responses using a HCV core ISCOMATRIX vaccine: a phase I study in healthy volunteers. Hum. Vaccin. 5:151-157.
9. Pedersen, G. K., A. S. Madhun, L. Breakwell, K. Hoschler, H. Sjursen, R. D. Pathirana, J. Goudsmit, and R. J. Cox. 2012. T-helper 1 cells elicited by H5N1 vaccination predict seroprotection. J. Infect. Dis. 206:158-166.
10. Offermann, M. K., J. Zimring, K. H. Mellits, M. K. Hagan, R. Shaw, R. M. Medford, M. B. Mathews, S. Goodbourn, and R. Jagus. 1995. Activation of the double-stranded-RNA-activated protein kinase and induction of vascular cell adhesion molecule-1 by poly (I).poly (C) in endothelial cells. Eur. J. Biochem. 232:28-36.
11. Alexopoulou, L., A. C. Holt, R. Medzhitov, and R. A. Flavell. 2001. Recognition of double-stranded RNA and activation of NF-kappaB by Toll-like receptor 3. Nature 413:732-738.
12. Yoneyama, M., M. Kikuchi, T. Natsukawa, N. Shinobu, T. Imaizumi, M. Miyagishi, K. Taira, S. Akira, and T. Fujita. 2004. The RNA helicase RIG-I has an essential function in double-stranded RNA-induced innate antiviral responses. Nat. Immunol. 5:730-737.
13. Kato, H., O. Takeuchi, E. Mikamo-Satoh, R. Hirai, T. Kawai, K. Matsushita, A. Hiiragi, T. S. Dermody, T. Fujita, and S. Akira. 2008. Length-dependent recognition of double-stranded ribonucleic acids by retinoic acid-inducible gene-I and melanoma differentiation-associated gene 5. J. Exp. Med. 205:1601-1610.
14. Kato, H., O. Takeuchi, S. Sato, M. Yoneyama, M. Yamamoto, K. Matsui, S. Uematsu, A. Jung, T. Kawai, K. J. Ishii, et al. 2006. Differential roles of MDA5 and RIG-I helicases in the recognition of RNA viruses. Nature 441:101-105.
15. Edwards, A. D., S. S. Diebold, E. M. C. Slack, H. Tomizawa, H. Hemmi, T. Kaisho, S. Akira, and C. Reis E Sousa. 2003. Toll-like receptor expression in murine DC subsets: lack of TLR7 expression by CD8 alpha+ DC correlates with unresponsiveness to imidazoquinolines. Eur. J. Immunol. 33:827-833.
16. Jelinek, I., J. N. Leonard, G. E. Price, K. N. Brown, A. Meyer-Manlapat, P. K. Goldsmith, Y. Wang, D. Venzon, S. L. Epstein, and D. M. Segal. 2011. TLR3-specific double-stranded RNA oligonucleotide adjuvants induce dendritic cell cross-presentation, CTL responses, and antiviral protection. J. Immunol. 186:2422-2429.
17. Kang, D.-C., R. V. Gopalkrishnan, L. Lin, A. Randolph, K. Valerie, S. Pestka, and P. B. Fisher. 2004. Expression analysis and genomic characterization of human melanoma differentiation associated gene-5, mda-5: a novel type I interferon-responsive apoptosis-inducing gene. Oncogene 23:1789-1800.
18. Wang, Y., M. Cella, S. Gilfillan, and M. Colonna. 2010. Cutting edge: polyinosinic:polycytidylic acid boosts the generation of memory CD8 T cells through melanoma differentiation-associated protein 5 expressed in stromal cells. J. Immunol. 184:2751-2755.
19. Salem, M. L., S. A. El-Naggar, A. Kadima, W. E. Gillanders, and D. J. Cole. 2006. The adjuvant effects of the Toll-like receptor 3 ligand polyinosiniccytidylic acid poly (I:C) on antigen-specific CD8+ T cell responses are partially dependent on NK cells with the induction of a beneficial cytokine milieu. Vaccine 24:5119-5132.
20. Tewari, K., B. J. Flynn, S. B. Boscardin, K. Kastenmueller, A. M. Salazar, C. A. Anderson, V. Soundarapandian, A. Ahumada, T. Keler, S. L. Hoffman, et al. 2010. Poly (I:C) is an effective adjuvant for antibody and multi-functional CD4+ T cell responses to Plasmodium falciparum circumsporozoite protein (CSP) and aDEC-CSP in non human primates. Vaccine 28:7256-7266.
21. Datta, S. K., V. Redecke, K. R. Prilliman, K. Takabayashi, M. Corr, T. Tallant, J. Di Donato, R. Dziarski, S. Akira, S. P. Schoenberger, and E. Raz. 2003. A subset of Toll-like receptor ligands induces cross-presentation by bone marrowderived dendritic cells. J. Immunol. 170:4102-4110.
22. Drane, D., C. Gittleson, J. Boyle, and E. Maraskovsky. 2007. ISCOMATRIX adjuvant for prophylactic and therapeutic vaccines. Expert Rev. Vaccines 6:761-772.
23. Behboudi, S., B. Morein, and B. Rönnberg. 1995. Isolation and quantification of Quillaja saponaria Molina saponins and lipids in iscom-matrix and iscoms. Vaccine 13:1690-1696.
24. Villacres-Eriksson, M., M. Bergström-Mollaoglu, H. Kåberg, K. Lövgren, and B. Morein. 1993. The induction of cell-associated and secreted IL-1 by iscoms, matrix or micelles in murine splenic cells. Clin. Exp. Immunol. 93:120-125.
25. Duewell, P., U. Kisser, K. Heckelsmiller, S. Hoves, P. Stoitzner, S. Koernig, A. B. Morelli, B. E. Clausen, M. Dauer, A. Eigler, et al. 2011. ISCOMATRIX adjuvant combines immune activation with antigen delivery to dendritic cells in vivo leading to effective cross-priming of CD8+ T cells. J. Immunol. 187:55-63.
26. Maloy, K. J., A. M. Donachie, and A. M. Mowat. 1995. Induction of Th1 and Th2 CD4+ T cell responses by oral or parenteral immunization with ISCOMS. Eur. J. Immunol. 25:2835-2841.
27. Maraskovsky, E., M. Schnurr, N. S. Wilson, N. C. Robson, J. Boyle, and D. Drane. 2009. Development of prophylactic and therapeutic vaccines using the ISCOMATRIX adjuvant. Immunol. Cell Biol. 87:371-376.
28. Schnurr, M., M. Orban, N. C. Robson, A. Shin, H. Braley, D. Airey, J. Cebon, E. Maraskovsky, and S. Endres. 2009. ISCOMATRIX adjuvant induces efficient cross-presentation of tumor antigen by dendritic cells via rapid cytosolic antigen delivery and processing via tripeptidyl peptidase II. J. Immunol. 182:1253-1259.
29. Napolitani, G., A. Rinaldi, F. Bertoni, F. Sallusto, and A. Lanzavecchia. 2005. Selected Toll-like receptor agonist combinations synergistically trigger a T helper type 1-polarizing program in dendritic cells. Nat. Immunol. 6:769-776.
30. Kasturi, S. P., I. Skountzou, R. A. Albrecht, D. Koutsonanos, T. Hua, H. I. Nakaya, R. Ravindran, S. Stewart, M. Alam, M. Kwissa, et al. 2011. Programming the magnitude and persistence of antibody responses with innate immunity. Nature 470:543-547.
31. Nordly, P., F. Rose, D. Christensen, H. M. Nielsen, P. Andersen, E. M. Agger, and C. Foged. 2011. Immunity by formulation design: induction of high CD8+ T-cell responses by poly (I:C) incorporated into the CAF01 adjuvant via a double emulsion method. J. Control. Release 150:307-317.
32. Zaks, K., M. Jordan, A. Guth, K. Sellins, R. Kedl, A. Izzo, C. Bosio, and S. Dow. 2006. Efficient immunization and cross-priming by vaccine adjuvants containing TLR3 or TLR9 agonists complexed to cationic liposomes. J. Immunol. 176:7335-7345.
33. Jacobs, C., P. Duewell, K. Heckelsmiller, J. Wei, F. Bauernfeind, J. Ellermeier, U. Kisser, C. A. Bauer, M. Dauer, A. Eigler, et al. 2011. An ISCOM vaccine combined with a TLR9 agonist breaks immune evasion mediated by regulatory T cells in an orthotopic model of pancreatic carcinoma. Int. J. Cancer 128:897-907.
34. Sundling, C., M. N. E. Forsell, S. O'Dell, Y. Feng, B. Chakrabarti, S. S. Rao, K. Loré, J. R. Mascola, R. T. Wyatt, I. Douagi, and G. B. Karlsson Hedestam. 2010. Soluble HIV-1 Env trimers in adjuvant elicit potent and diverse functional B cell responses in primates. J. Exp. Med. 207:2003-2017.
35. Wille-Reece, U., B. J. Flynn, K. Loré, R. A. Koup, R. M. Kedl, J. J. Mattapallil, W. R. Weiss, M. Roederer, and R. A. Seder. 2005. HIV Gag protein conjugated to a Toll-like receptor 7/8 agonist improves the magnitude and quality of Th1 and CD8+ T cell responses in nonhuman primates. Proc. Natl. Acad. Sci. USA 102:15190-15194.
36. Wille-Reece, U., B. J. Flynn, K. Loré, R. A. Koup, A. P. Miles, A. Saul, R. M. Kedl, J. J. Mattapallil, W. R. Weiss, M. Roederer, and R. A. Seder. 2006. Toll-like receptor agonists influence the magnitude and quality of memory T cell responses after prime-boost immunization in nonhuman primates. J. Exp. Med. 203:1249-1258.
37. Quinn, K. M., A. Da Costa, A. Yamamoto, D. Berry, R. W. B. Lindsay, P. A. Darrah, L. Wang, C. Cheng, W.-P. Kong, J. G. D. Gall, et al. 2013. Comparative analysis of the magnitude, quality, phenotype, and protective capacity of simian immunodeficiency virus gag-specific CD8+ T cells following human-, simian-, and chimpanzee-derived recombinant adenoviral vector immunization. J. Immunol. 190:2720-2735.
38. Mata, M., P. J. Travers, Q. Liu, F. R. Frankel, and Y. Paterson. 1998. The MHC class I-restricted immune response to HIV-gag in BALB/c mice selects a single epitope that does not have a predictable MHC-binding motif and binds to Kd through interactions between a glutamine at P3 and pocket D. J. Immunol. 161:2985-2993.
39. Kastenmüller, K., U. Wille-Reece, R. W. B. Lindsay, L. R. Trager, P. A. Darrah, B. J. Flynn, M. R. Becker, M. C. Udey, B. E. Clausen, B. Z. Igyarto, et al. 2011. Protective T cell immunity in mice following protein-TLR7/8 agonist-conjugate immunization requires aggregation, type I IFN, and multiple DC subsets. J. Clin. Invest. 121:1782-1796.
40. Joshi, N. S., W. Cui, A. Chandele, H. K. Lee, D. R. Urso, J. Hagman, L. Gapin, and S. M. Kaech. 2007. Inflammation directs memory precursor and short-lived effector CD8 (+) T cell fates via the graded expression of T-bet transcription factor. Immunity 27:281-295.
41. Kaech, S. M., J. T. Tan, E. J. Wherry, B. T. Konieczny, C. D. Surh, and R. Ahmed. 2003. Selective expression of the interleukin 7 receptor identifies effector CD8 T cells that give rise to long-lived memory cells. Nat. Immunol. 4:1191-1198.
42. Obar, J. J., E. R. Jellison, B. S. Sheridan, D. A. Blair, Q.-M. Pham, J. M. Zickovich, and L. Lefrançois. 2011. Pathogen-induced inflammatory environment controls effector and memory CD8+ T cell differentiation. J. Immunol. 187:4967-4978.
43. Intlekofer, A. M., N. Takemoto, E. J. Wherry, S. A. Longworth, J. T. Northrup, V. R. Palanivel, A. C. Mullen, C. R. Gasink, S. M. Kaech, J. D. Miller, et al. 2005. Effector and memory CD8+ T cell fate coupled by T-bet and eomesodermin. Nat. Immunol. 6:1236-1244.
44. Darrah, P. A., D. T. Patel, P. M. De Luca, R. W. B. Lindsay, D. F. Davey, B. J. Flynn, S. T. Hoff, P. Andersen, S. G. Reed, S. L. Morris, et al. 2007. Multifunctional TH1 cells define a correlate of vaccine-mediated protection against Leishmania major. Nat. Med. 13:843-850.
45. Betts, M. R., M. C. Nason, S. M. West, S. C. De Rosa, S. A. Migueles, J. Abraham, M. M. Lederman, J. M. Benito, P. A. Goepfert, M. Connors, et al. 2006. HIV nonprogressors preferentially maintain highly functional HIV-specific CD8+ T cells. Blood 107:4781-4789.
46. Murray, P. J., and S. T. Smale. 2012. Restraint of inflammatory signaling by interdependent strata of negative regulatory pathways. Nat. Immunol. 13:916-924.
47. Darrah, P. A., S. T. Hegde, D. T. Patel, R. W. B. Lindsay, L. Chen, M. Roederer, and R. A. Seder. 2010. IL-10 production differentially influences the magnitude, quality, and protective capacity of Th1 responses depending on the vaccine platform. J. Exp. Med. 207:1421-1433.
48. Jankovic, D., D. G. Kugler, and A. Sher. 2010. IL-10 production by CD4+ effector T cells: a mechanism for self-regulation. Mucosal Immunol. 3:239-246.
49. Ghoreschi, K., A. Laurence, X.-P. Yang, C. M. Tato, M. J. McGeachy, J. E. Konkel, H. L. Ramos, L. Wei, T. S. Davidson, N. Bouladoux, et al. 2010. Generation of pathogenic T (H) 17 cells in the absence of TGF-β signalling. Nature 467:967-971.
50. Yu, H., X. Jiang, C. Shen, K. P. Karunakaran, J. Jiang, N. L. Rosin, and R. C. Brunham. 2010. Chlamydia muridarum T-cell antigens formulated with the adjuvant DDA/TDB induce immunity against infection that correlates with a high frequency of gamma interferon (IFN-gamma)/tumor necrosis factor alpha and IFN-gamma/interleukin-17 double-positive CD4+ T cells. Infect. Immun. 78:2272-2282.
51. Shah, J. A., P. A. Darrah, D. R. Ambrozak, T. N. Turon, S. Mendez, J. Kirman, C.-Y. Wu, N. Glaichenhaus, and R. A. Seder. 2003. Dendritic cells are responsible for the capacity of CpG oligodeoxynucleotides to act as an adjuvant for protective vaccine immunity against Leishmania major in mice. J. Exp. Med. 198:281-291.
52. Santambrogio, L., A. K. Sato, G. J. Carven, S. L. Belyanskaya, J. L. Strominger, and L. J. Stern. 1999. Extracellular antigen processing and presentation by immature dendritic cells. Proc. Natl. Acad. Sci. USA 96:15056-15061.
53. Daro, E., B. Pulendran, K. Brasel, M. Teepe, D. Pettit, D. H. Lynch, D. Vremec, L. Robb, K. Shortman, H. J. McKenna, et al. 2000. Polyethylene glycol-modified GM-CSF expands CD11b (high) CD11c (high) but notCD11b (low) CD11c (high) murine dendritic cells in vivo: a comparative analysis with Flt3 ligand. J. Immunol. 165:49-58.
54. Hildner, K., B. T. Edelson, W. E. Purtha, M. Diamond, H. Matsushita, M. Kohyama, B. Calderon, B. U. Schraml, E. R. Unanue, M. S. Diamond, et al. 2008. Batf3 deficiency reveals a critical role for CD8alpha+ dendritic cells in cytotoxic T cell immunity. Science 322:1097-1100.
55. Edelson, B. T., W. Kc, R. Juang, M. Kohyama, L. A. Benoit, P. A. Klekotka, C. Moon, J. C. Albring, W. Ise, D. G. Michael, et al. 2010. Peripheral CD103+ dendritic cells form a unified subset developmentally related to CD8alpha+ conventional dendritic cells. J. Exp. Med. 207:823-836.
56. Allan, R. S., J. Waithman, S. Bedoui, C. M. Jones, J. A. Villadangos, Y. Zhan, A. M. Lew, K. Shortman, W. R. Heath, and F. R. Carbone. 2006. Migratory dendritic cells transfer antigen to a lymph node-resident dendritic cell population for efficient CTL priming. Immunity 25:153-162.
57. Bedoui, S., P. G. Whitney, J. Waithman, L. Eidsmo, L. Wakim, I. Caminschi, R. S. Allan, M. Wojtasiak, K. Shortman, F. R. Carbone, et al. 2009. Crosspresentation of viral and self antigens by skin-derived CD103+ dendritic cells. Nat. Immunol. 10:488-495.
58. Henri, S., L. F. Poulin, S. Tamoutounour, L. Ardouin, M. Guilliams, B. De Bovis, E. Devilard, C. Viret, H. Azukizawa, A. Kissenpfennig, and B. Malissen. 2010. CD207+ CD103+ dermal dendritic cells cross-present keratinocyte-derived antigens irrespective of the presence of Langerhans cells. J. Exp. Med. 207:189-206.
59. Park, H., L. Adamson, T. Ha, K. Mullen, S. I. Hagen, A. Nogueron, A. W. Sylwester, M. K. Axthelm, A. Legasse, M. Piatak, Jr., et al. 2013. Polyinosinic-polycytidylic acid is the most effective TLR adjuvant for SIV Gag protein-induced T cell responses in nonhuman primates. J. Immunol. 190:4103-4115.
60. Caskey, M., F. Lefebvre, A. Filali-Mouhim, M. J. Cameron, J.-P. Goulet, E. K. Haddad, G. Breton, C. Trumpfheller, S. Pollak, I. Shimeliovich, et al. 2011. Synthetic double-stranded RNA induces innate immune responses similar to a live viral vaccine in humans. J. Exp. Med. 208:2357-2366.
61. The RTS, S Clinical Trials Partnership. 2012. A phase 3 trial of RTS, S/AS01 malaria vaccine in African infants. N. Engl. J. Med. 367:2284-2295.
62. Spadaro, F., C. Lapenta, S. Donati, L. Abalsamo, V. Barnaba, F. Belardelli, S. M. Santini, and M. Ferrantini. 2012. IFN-α enhances cross-presentation in human dendritic cells by modulating antigen survival, endocytic routing, and processing. Blood 119:1407-1417.
63. Kuchtey, J., P. J. Chefalo, R. C. Gray, L. Ramachandra, and C. V. Harding. 2005. Enhancement of dendritic cell antigen cross-presentation by CpG DNA involves type I IFN and stabilization of class I MHC mRNA. J. Immunol. 175:2244-2251.
64. Culshaw, S., O. R. Millington, J. M. Brewer, and I. B. McInnes. 2008. Murine neutrophils present class II restricted antigen. Immunol. Lett. 118:49-54.
65. Beauvillain, C., Y. Delneste, M. Scotet, A. Peres, H. Gascan, P. Guermonprez, V. Barnaba, and P. Jeannin. 2007. Neutrophils efficiently cross-prime naive T cells in vivo. Blood 110:2965-2973.
66. Abadie, V., E. Badell, P. Douillard, D. Ensergueix, P. J. M. Leenen, M. Tanguy, L. Fiette, S. Saeland, B. Gicquel, and N. Winter. 2005. Neutrophils rapidly migrate via lymphatics after Mycobacterium bovis BCG intradermal vaccination and shuttle live bacilli to the draining lymph nodes. Blood 106:1843-1850.
67. Abadie, V., O. Bonduelle, D. Duffy, C. Parizot, B. Verrier, and B. Combadière. 2009. Original encounter with antigen determines antigen-presenting cell imprinting of the quality of the immune response in mice. PLoS One 4:e8159.
68. Mempel, T. R., S. E. Henrickson, and U. H. Von Andrian. 2004. T-cell priming by dendritic cells in lymph nodes occurs in three distinct phases. Nature 427:154-159.
69. Henrickson, S. E., T. R. Mempel, I. B. Mazo, B. Liu, M. N. Artyomov, H. Zheng, A. Peixoto, M. P. Flynn, B. Senman, T. Junt, et al. 2008. T cell sensing of antigen dose governs interactive behavior with dendritic cells and sets a threshold for T cell activation. Nat. Immunol. 9:282-291.
70. Badovinac, V. P., and J. T. Harty. 2007. Manipulating the rate of memory CD8+ T cell generation after acute infection. J. Immunol. 179:53-63.
71. Curtsinger, J. M., C. S. Schmidt, A. Mondino, D. C. Lins, R. M. Kedl, M. K. Jenkins, and M. F. Mescher. 1999. Inflammatory cytokines provide a third signal for activation of naive CD4+ and CD8+ T cells. J. Immunol. 162:3256-3262.
72. Zhang, X., S. Sun, I. Hwang, D. F. Tough, and J. Sprent. 1998. Potent and selective stimulation of memory-phenotype CD8+ T cells in vivo by IL-15. Immunity 8:591-599.
73. Tough, D. F., X. Zhang, and J. Sprent. 2001. An IFN-gamma-dependent pathway controls stimulation of memory phenotype CD8+ T cell turnover in vivo by IL-12, IL-18, and IFN-gamma. J. Immunol. 166:6007-6011.
74. Madera, R. F., J. P. Wang, and D. H. Libraty. 2011. The combination of early and rapid type I IFN, IL-1α, and IL-1b production are essential mediators of RNA-like adjuvant driven CD4+ Th1 responses. PLoS One 6:e29412.