IFN-α as a vaccine adjuvant: recent insights into the mechanisms and perspectives for its clinical use

References

• Vilcek J. Fifty years of interferon research: aiming at a moving target. Immunity25(3), 343–348 (2006).
   PubMed Web of Science ®Google Scholar
• Belardelli F, Gresser I. The neglected role of type I interferon in the T cell response: implications for its clinical use. Immunol. Today17(8), 369–372 (1996).
   PubMedGoogle Scholar
• Belardelli F, Ferrantini M. Cytokines as a link between innate and adaptive antitumor immunity. Trends Immunol.23(4), 201–208 (2002).
   PubMed Web of Science ®Google Scholar
• Santini SM, Lapenta C, Logozzi M et al. Type I interferon as a powerful adjuvant for monocyte-derived dendritic cell development and activity in vitro and in Hu-PBL-SCID mice. J. Exp. Med.191(10), 1777–1788 (2000).
   PubMed Web of Science ®Google Scholar
• Rizza P, Moretti F, Belardelli F. Recent advances on the immunomodulatory effects of IFN-α: implications for cancer immunotherapy and autoimmunity. Autoimmunity43(3), 204–209 (2010).
   PubMed Web of Science ®Google Scholar
• Tovey MG, Lallemand C, Thyphronitis G. Adjuvant activity of type I interferons. Biol. Chem.389(5), 541–545 (2008).
   PubMed Web of Science ®Google Scholar
• Bracci L, La Sorsa V, Belardelli F, Proietti E. Type I interferons as vaccine adjuvants against infectious diseases and cancer. Expert Rev. Vaccines7(3), 373–381 (2008).
   PubMed Web of Science ®Google Scholar
• Toporovski R, Morrow MP, Weiner DB. Interferons as potential adjuvants in prophylactic vaccines. Expert. Opin. Biol. Ther.10(10), 1489–1500 (2010).
   PubMed Web of Science ®Google Scholar
• Iwasaki A, Medzhitov R. Regulation of adaptive immunity by the innate immune system. Science237(5963), 291–295 (2010).
   Google Scholar
• Tough DF, Borrow P, Sprent J. Induction of bystander T cell proliferation by viruses and type I interferon in vivo. Science272(5270), 1947–1950 (1996).
   PubMed Web of Science ®Google Scholar
• Sun S, Zhang X, Tough DF, Sprent J. Type I interferon-mediated stimulation of T cells by CpG DNA. J. Exp. Med.188(12), 2335–2342 (1998).
   PubMed Web of Science ®Google Scholar
• Le Bon A, Etchart N, Rossmann C et al. Cross-priming of CD8+ T cells stimulated by virus-induced type I interferon. Nat. Immunol.4(10), 1009–1015 (2003).
   PubMed Web of Science ®Google Scholar
• Siegal FP, Kadowaki N, Shodell M et al. The nature of the principal type I interferon-producing cells in human blood. Science284(5421), 1835–1837 (1999).
   PubMed Web of Science ®Google Scholar
• Cella M, Jarrossay D, Facchetti F et al. Plasmacytoid monocytes migrate to inflamed lymph nodes and produce large amounts of type I interferon. Nat. Med.5(8), 919–923 (1999).
   PubMed Web of Science ®Google Scholar
• Lande R, Gilliet M. Plasmacytoid dendritic cells: key players in the initiation and regulation of immune responses. Ann. NY Acad. Sci.1183, 89–103 (2010).
   PubMed Web of Science ®Google Scholar
• Fitzgerald-Bocarsly P, Dai J, Singh S. Plasmacytoid dendritic cells and type I IFN: 50 years of convergent history. Cytokine Growth Factor Rev.19(1), 3–19 (2008).
   PubMed Web of Science ®Google Scholar
• Gilliet M, Cao W, Liu YJ. Plasmacytoid dendritic cells: sensing nucleic acids in viral infection and autoimmune diseases. Nat. Rev. Immunol.8(8), 594–606 (2008).
   PubMed Web of Science ®Google Scholar
• Le Bon A, Schiavoni G, D’antigenostino G, Gresser I, Belardelli F, Tough DF. Type I interferons potently enhance humoral immunity and can promote isotype switching by stimulating dendritic cells in vivo. Immunity14(4), 461–470 (2001).
   PubMed Web of Science ®Google Scholar
• Paquette RL, Hsu NC, Kiertscher SM et al. Interferon-α and granulocyte-macrophage colony-stimulating factor differentiate peripheral blood monocytes into potent antigen-presenting cells. J. Leukoc. Biol.64(3), 358–367 (1998).
   PubMed Web of Science ®Google Scholar
• Blanco P, Palucka AK, Gill M, Pascual V, Banchereau J. Induction of dendritic cell differentiation by IFN-α in systemic lupus erythematosus. Science294(5546), 1540–1543 (2001).
   PubMed Web of Science ®Google Scholar
• Parlato S, Santini SM, Lapenta C et al. Expression of CCR-7, MIP-3β, and Th-1 chemokines in type I IFN-induced monocyte- derived dendritic cells: importance for the rapid acquisition of potent migratory and functional activities. Blood98(10), 3022–3029 (2001).
   PubMed Web of Science ®Google Scholar
• Santodonato L, D’antigenostino G, Nisini R et al. Monocyte-derived dendritic cells generated after a short-term culture with IFN-α and granulocyte-macrophage colony-stimulating factor stimulate a potent Epstein-Barr virus-specific CD8+ T cell response. J. Immunol.170(10), 5195–5202 (2003).
   PubMed Web of Science ®Google Scholar
• Lapenta C, Santini SM, Logozzi M et al. Potent immune response against HIV-1 and protection from virus challenge in hu-PBL-SCID mice immunized with inactivated-virus-pulsed dendritic cells generated in the presence of IFN-α. J. Exp. Med.198(2), 361–367 (2003).
   PubMed Web of Science ®Google Scholar
• Tosi D, Valenti R, Cova A et al. Role of cross-talk between IFN-α-induced monocyte-derived dendritic cells and NK cells in priming CD8+ T cell responses against human tumor antigens. J. Immunol.172(9), 5363–5370 (2004).
   PubMed Web of Science ®Google Scholar
• Lapenta C, Santini SM, Spada M et al. IFN-α-conditioned dendritic cells are highly efficient in inducing cross-priming CD8+ T-cells against exogenous viral antigens even in the absence of CD4+ T-cell help. Eur. J. Immunol.36(8), 2046–2060 (2006).
   PubMed Web of Science ®Google Scholar
• Gabriele L, Borghi P, Rozera C et al. IFN-α promotes the rapid differentiation of monocytes from patients with chronic myeloid leukemia into activated dendritic cells tuned to undergo full maturation after LPS treatment. Blood103(3), 980–987 (2004).
   PubMed Web of Science ®Google Scholar
• Salem ML, El-Naggar SA, Kadima A, Gillanders WE, Cole DJ. The adjuvant effects of the Toll-like receptor 3 ligand polyinosinic-cytidylic 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. Vaccine24(24), 5119–5132 (2006).
   PubMed Web of Science ®Google Scholar
• Stahl-Hennig C, Eisenblätter M, Jasny E et al. Synthetic double-stranded RNAs are adjuvants for the induction of T helper 1 and humoral immune responses to human papillomavirus in rhesus macaques. PLoS Pathog.5(4), e1000373 (2009).
   PubMed Web of Science ®Google Scholar
• Trumpfheller C, Caskey M, Nchinda G et al. The microbial mimic poly I:C induces durable and protective CD4+ T cell immunity together with a dendritic cell targeted vaccine. Proc. Natl Acad. Sci. USA105(7), 2574–2579 (2008).
   PubMed Web of Science ®Google Scholar
• Longhi MP, Trumpfheller C, Idoyaga J et al. Dendritic cells require a systemic type I interferon response to mature and induce CD4+ Th1 immunity with poly I:C as adjuvant. J. Exp. Med.206(7), 1589–1602 (2009).
   PubMed Web of Science ®Google Scholar
• Jongbloed SL, Kassianos AJ, McDonald KJ et al. Human CD141+ (BDCA-3)+ dendritic cells (DCs) represent a unique myeloid DC subset that cross-presents necrotic cell antigens. J. Exp. Med.207(6), 1247–1260 (2010).
   PubMed Web of Science ®Google Scholar
• Bachem A, Güttler S, Hartung E et al. Superior antigen cross-presentation and XCR1 expression define human CD11c+CD141+ cells as homologues of mouse CD8+ dendritic cells. J. Exp. Med.207(6), 1273–1281 (2010).
   PubMed Web of Science ®Google Scholar
• Poulin LF, Salio M, Griessinger E et al. Characterization of human DNGR-1+ BDCA3+ leukocytes as putative equivalents of mouse CD8α+ dendritic cells. J. Exp. Med.207(6), 1261–1271 (2010).
   PubMed Web of Science ®Google Scholar
• Crozat K, Guiton R, Contreras V et al. The XC chemokine receptor 1 is a conserved selective marker of mammalian cells homologous to mouse CD8α+ dendritic cells. J. Exp. Med.207(6), 1283–1292 (2010).
   PubMed Web of Science ®Google Scholar
• Shortman K, Heath WR. The CD8+ dendritic cell subset. Immunol. Rev.234(1), 18–31 (2010).
   PubMed Web of Science ®Google Scholar
• Pichlmair A, Reis e Sousa C. Innate recognition of viruses. Immunity27(3), 370–383 (2007).
   PubMed Web of Science ®Google Scholar
• Gaspari AA, Tyring SK, Rosen T. Beyond a decade of 5% imiquimod topical therapy. J. Drugs Dermatol.8(5), 467–474 (2009).
   PubMed Web of Science ®Google Scholar
• Rajagopal D, Paturel C, Morel Y, Uematsu S, Akira S, Diebold SS. Plasmacytoid dendritic cell-derived type I interferon is crucial for the adjuvant activity of Toll-like receptor 7 agonists. Blood115(10), 1949–1957 (2010).
   PubMed Web of Science ®Google Scholar
• Dondi E, Rogge L, Lutfalla G, Uze G, Pellegrini S. Down-modulation of responses to type I IFN upon T cell activation. J. Immunol.170(2), 749–756 (2003).
   PubMed Web of Science ®Google Scholar
• Chi B, Dickensheets HL, Spann KM et al.α and λ interferon together mediate suppression of CD4 T cells induced by respiratory syncytial virus. J. Virol.80(10), 5032–5040 (2006).
   PubMed Web of Science ®Google Scholar
• Le Bon A, Thompson C, Kamphuis E et al. Cutting edge: enhancement of antibody responses through direct stimulation of B and T cells by type I IFN. J. Immunol.176(4), 2074–2078 (2006).
   PubMed Web of Science ®Google Scholar
• Havenar-Daughton C, Kolumam GA, Murali-Krishna K. Cutting edge: the direct action of type I IFN on CD4 T cells is critical for sustaining clonal expansion in response to a viral but not a bacterial infection. J. Immunol.176(6), 3315–3319 (2006).
   PubMed Web of Science ®Google Scholar
• Krug A, Veeraswamy R, Pekosz A et al. Interferon-producing cells fail to induce proliferation of naive T cells but can promote expansion and T helper 1 differentiation of antigen-experienced unpolarized T cells. J. Exp. Med.197(7), 899–906 (2003).
   PubMed Web of Science ®Google Scholar
• Gallagher KM, Lauder S, Rees IW, Gallimore AM, Godkin AJ. Type I interferon (IFN α) acts directly on human memory CD4+ T cells altering their response to antigen. J. Immunol.183(5), 2915–2920 (2009).
   PubMed Web of Science ®Google Scholar
• Vila J, Isaacs JD, Anderson AE. Regulatory T cells and autoimmunity. Curr. Opin. Hematol.16(4), 274–279 (2009).
   PubMed Web of Science ®Google Scholar
• Pace L, Vitale S, Dettori B et al. APC activation by IFN-α decreases regulatory T cell and enhances Th cell functions. J. Immunol.184(11), 5969–5979 (2010).
   PubMed Web of Science ®Google Scholar
• Ascierto PA, Napolitano M, Celentano E et al. Regulatory T cell frequency in patients with melanoma with different disease stage and course, and modulating effects of high-dose interferon-α 2b treatment. J. Transl. Med.8, 76 (2010).
   PubMedGoogle Scholar
• Querec TD, Akondy RS, Lee EK et al. Systems biology approach predicts immunogenicity of the yellow fever vaccine in humans. Nat. Immunol.10(1), 116–125 (2009).
   PubMed Web of Science ®Google Scholar
• Gaucher D, Therrien R, Kettaf N et al. Yellow fever vaccine induces integrated multilineage and polyfunctional immune responses. J. Exp. Med.205(13), 3119–3131 (2008).
   PubMed Web of Science ®Google Scholar
• Le Bon A, Durand V, Kamphuis E et al. Direct stimulation of T cells by type I IFN enhances the CD8+ T cell response during cross-priming. J. Immunol.176(8), 4682–4689 (2006).
   PubMed Web of Science ®Google Scholar
• Proietti E, Bracci L, Puzelli S et al. Type I IFN as a natural adjuvant for a protective immune response: lessons from the influenza vaccine model. J. Immunol.169(1), 375–383 (2002).
   PubMed Web of Science ®Google Scholar
• Tovey MG, Lallemand C, Meritet JF, Maury C. Adjuvant activity of interferon α: mechanism(s) of action. Vaccine24(Suppl. 2), S2–46–47 (2006).
   PubMed Web of Science ®Google Scholar
• Bracci L, Canini I, Puzelli S et al. Type I IFN is a powerful mucosal adjuvant for a selective intranasal vaccination against influenza virus in mice and affects antigen capture at mucosal level. Vaccine23(23), 2994–3004 (2005).
   PubMed Web of Science ®Google Scholar
• Cull VS, Broomfield S, Bartlett EJ, Brekalo NL, James CM. Coimmunisation with type I IFN genes enhances protective immunity against cytomegalovirus and myocarditis in gB DNA-vaccinated mice. Gene Ther.9(20), 1369–1378 (2002).
   PubMed Web of Science ®Google Scholar
• Grob PJ, Joller-Jemelka HI, Binswanger U, Zaruba K, Descoeudres C, Fernex M. Interferon as an adjuvant for hepatitis B vaccination in non- and low-responder populations. Eur. J. Clin. Microbiol.3(3), 195–198 (1984).
   PubMedGoogle Scholar
• Stürchler D, Berger R, Etlinger H et al. Effects of interferons on immune response to a synthetic peptide malaria sporozoite vaccine in non-immune adults. Vaccine7(5), 457–461 (1989).
   PubMed Web of Science ®Google Scholar
• Goldwater PN. Randomized comparative trial of interferon-α versus placebo in hepatitis B vaccine non-responders and hyporesponders. Vaccine12(5), 410–414 (1994).
   PubMed Web of Science ®Google Scholar
• Rizza P, Capone I, Urbani F et al. Evaluation of the effects of human leukocyte IFN-α on the immune response to the HBV vaccine in healthy unvaccinated individuals. Vaccine26(8), 1038–1049 (2008).
   PubMed Web of Science ®Google Scholar
• Mennechet FJ, Uzè G. Interferon-l-treated dendritic cells specifically induce proliferation of FOXP3-expressing suppressor T cells. Blood107(11), 4417–4423 (2006).
   PubMed Web of Science ®Google Scholar
• Morrow MP, Pankhong P, Laddy DJ et al. Comparative ability of IL-12 and IL-28B to regulate Treg populations and enhance adaptive cellular immunity. Blood113(23), 5868–5877 (2009).
   PubMed Web of Science ®Google Scholar
• Miquilena-Colina ME, Lozano-Rodríguez T, García-Pozo L et al. Recombinant interferon-α2b improves immune response to hepatitis B vaccination in haemodialysis patients: results of a randomised clinical trial. Vaccine27(41), 5654–5660 (2009).
   PubMed Web of Science ®Google Scholar
• Eleftheriadis T, Antoniadi G, Liakopoulos V, Kartsios C, Stefanidis I. Disturbances of acquired immunity in hemodialysis patients. Semin. Dial.20(5), 440–451 (2007).
   PubMed Web of Science ®Google Scholar
• Sester U, Sester M, Hauk M, Kaul H, Köhler H, Girndt M. T-cell activation follows Th1 rather than Th2 in haemodialysis patients. Neprhol. Dial. Transplant.15(8), 1217–1223 (2000).
   PubMed Web of Science ®Google Scholar
• Launay O, Grabar S, Bloch F et al. Effect of sublingual administration of interferon-α on the immune response to influenza vaccination in institutionalized elderly individuals. Vaccine26(32), 4073–4079 (2008).
   PubMed Web of Science ®Google Scholar
• Couch RB, Atmar RL, Cate TR et al. Contrasting effects of type I interferon as a mucosal adjuvant for influenza vaccine in mice and humans. Vaccine27(39), 5344–5348 (2009).
   PubMed Web of Science ®Google Scholar
• Bracarda S, Eggermont AM, Samuelsson J. Redefining the role of interferon in the treatment of malignant diseases. Eur. J. Cancer.46(2), 284–297 (2010).
   PubMed Web of Science ®Google Scholar
• Ferrantini M, Belardelli F. Gene therapy of cancer with interferon: lessons from tumor models and perspectives for clinical applications. Semin. Cancer. Biol.10(2), 145–157 (2000).
   PubMed Web of Science ®Google Scholar
• Ferrantini M, Capone I, Belardelli F. Interferon-α and cancer: mechanisms of action and new perspectives of clinical use. Biochimie89(6–7), 884–893 (2007).
   PubMed Web of Science ®Google Scholar
• Sikora AG, Jaffarzad N, Hailemichael Y et al. IFN-α enhances peptide vaccine-induced CD8+ T cell numbers, effector function, and antitumor activity. J. Immunol.182(12), 7398–7407 (2009).
   PubMed Web of Science ®Google Scholar
• Hance KW, Rogers CJ, Zaharoff DA, Canter D, Schlom J, Greiner JW. The antitumor and immunoadjuvant effects of IFN-α in combination with recombinant poxvirus vaccines. Clin. Cancer Res.15(7), 2387–2396 (2009).
   PubMed Web of Science ®Google Scholar
• Gogas H, Ioannovich J, Dafni U et al. Prognostic significance of autoimmunity during treatment of melanoma with interferon. N. Engl. J. Med.354(7), 709–718 (2006).
   PubMed Web of Science ®Google Scholar
• Crow MK. Type I interferon in systemic lupus erythematosus. Curr. Top. Microbiol. Immunol.316, 359–386 (2007).
   PubMed Web of Science ®Google Scholar
• Banchereau J, Pascual V. Type I IFN in systemic lupus erythematosus and other autoimmune diseases. Immunity25(3), 383–392 (2006).
   PubMed Web of Science ®Google Scholar
• Koon H, Atkins M. Autoimmunity and immunotherapy of cancer. N. Engl. J. Med.354(7), 758–760 (2006).
   PubMed Web of Science ®Google Scholar
• Di Pucchio T, Pilla L, Capone I et al. Immunization of stage IV melanoma patients with Melan-A/MART-1 and gp100 peptides plus IFN-α results in the activation of specific CD8+ T cells and monocyte/dendritic cell precursors. Cancer Res.66(9), 4943–4951 (2006).
   PubMed Web of Science ®Google Scholar
• Kirkwood JM, Lee S, Moschos SJ et al. Immunogenicity and antitumor effects of vaccination with peptide vaccine+/-granulocyte-monocyte colony-stimulating factor and/or IFN-α2b in advanced metastatic melanoma: Eastern Cooperative Oncology Group Phase II Trial E1696. Clin. Cancer Res.15(4), 1443–1451 (2009).
   PubMed Web of Science ®Google Scholar
• Ziegler-Heitbrock L. The CD14+ CD16+ blood monocytes: their role in infection and inflammation. J. Leukoc. Biol.81(3), 584–592 (2007).
   PubMed Web of Science ®Google Scholar
• Krutzik SR, Tan B, Li H et al. TLR activation triggers the rapid differentiation of monocytes into macrophages and dendritic cells. Nat. Med.11(6), 653–660 (2005).
   PubMed Web of Science ®Google Scholar
• Mohty AM, Grob JJ, Mohty M, Richard MA, Olive D, Gaugler B. Induction of IP-10/CXCL10 secretion as an immunomodulatory effect of low-dose adjuvant interferon-α during treatment of melanoma. Immunobiology215(2), 113–123 (2010).
   PubMed Web of Science ®Google Scholar
• Nisticò P, Capone I, Palermo B et al. Chemotherapy enhances vaccine-induced antitumor immunity in melanoma patients. Int. J. Cancer.124(1), 130–139 (2009).
   PubMed Web of Science ®Google Scholar
• Steinman RM, Banchereau J. Taking dendritic cells into medicine. Nature449(7161), 419–426 (2007).
   PubMed Web of Science ®Google Scholar
• Parlato S, Romagnoli G, Spadaro F et al. LOX-1 as a natural IFN-α-mediated signal for apoptotic cell uptake and antigen presentation in dendritic cells. Blood115(8), 1554–1563 (2010).
   PubMed Web of Science ®Google Scholar
• Rouzaut A, Garasa S, Teijeira A et al. Dendritic cells adhere to and transmigrate across lymphatic endothelium in response to IFN-α. Eur. J. Immunol.40(11), 3054–3063 (2010).
   PubMed Web of Science ®Google Scholar
• Vermi W, Fisogni S, Salogni L et al. Spontaneous regression of highly immunogenic molluscum contagiosum virus (MCV)-induced skin lesions is associated with plasmacytoid dendritic cells and IFN-DC infiltration. J. Invest. Dermatol.131(2), 426–434 (2010).
   PubMed Web of Science ®Google Scholar
• Moschella F, Proietti E, Capone I, Belardelli F. Combination strategies for enhancing the efficacy of immunotherapy in cancer patients. Ann. NY Acad. Sci.1194, 169–178 (2010).
   PubMed Web of Science ®Google Scholar
• Locher C, Conforti R, Aymeric L et al. Desirable cell death during anticancer chemotherapy. Ann. NY Acad. Sci.1209, 99–108 (2010).
   PubMed Web of Science ®Google Scholar