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Erschienen in: Cancer Immunology, Immunotherapy 7/2015

01.07.2015 | Original Article

Engineering monocyte-derived dendritic cells to secrete interferon-α enhances their ability to promote adaptive and innate anti-tumor immune effector functions

verfasst von: Yannick Willemen, Johan M. J. Van den Bergh, Eva Lion, Sébastien Anguille, Vicky A. E. Roelandts, Heleen H. Van Acker, Steven D. I. Heynderickx, Barbara M. H. Stein, Marc Peeters, Carl G. Figdor, Viggo F. I. Van Tendeloo, I. Jolanda de Vries, Gosse J. Adema, Zwi N. Berneman, Evelien L. J. Smits

Erschienen in: Cancer Immunology, Immunotherapy | Ausgabe 7/2015

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Abstract

Dendritic cell (DC) vaccination has demonstrated potential in clinical trials as a new effective cancer treatment, but objective and durable clinical responses are confined to a minority of patients. Interferon (IFN)-α, a type-I IFN, can bolster anti-tumor immunity by restoring or increasing the function of DCs, T cells and natural killer (NK) cells. Moreover, type-I IFN signaling on DCs was found to be essential in mice for tumor rejection by the innate and adaptive immune system. Targeted delivery of IFN-α by DCs to immune cells could boost the generation of anti-tumor immunity, while avoiding the side effects frequently associated with systemic administration. Naturally circulating plasmacytoid DCs, major producers of type-I IFN, were already shown capable of inducing tumor antigen-specific T cell responses in cancer patients without severe toxicity, but their limited number complicates their use in cancer vaccination. In the present work, we hypothesized that engineering easily generated human monocyte-derived mature DCs to secrete IFN-α using mRNA electroporation enhances their ability to promote adaptive and innate anti-tumor immunity. Our results show that IFN-α mRNA electroporation of DCs significantly increases the stimulation of tumor antigen-specific cytotoxic T cell as well as anti-tumor NK cell effector functions in vitro through high levels of IFN-α secretion. Altogether, our findings mark IFN-α mRNA-electroporated DCs as potent inducers of both adaptive and innate anti-tumor immunity and pave the way for clinical trial evaluation in cancer patients.
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Literatur
2.
7.
Zurück zum Zitat Kirkwood J (2002) Cancer immunotherapy: the interferon-alpha experience. Semin Oncol 29:18–26PubMedCrossRef Kirkwood J (2002) Cancer immunotherapy: the interferon-alpha experience. Semin Oncol 29:18–26PubMedCrossRef
8.
Zurück zum Zitat Atzpodien J, Kirchner H, Rebmann U et al (2006) Interleukin-2/interferon-alpha2a/13-retinoic acid-based chemoimmunotherapy in advanced renal cell carcinoma: results of a prospectively randomised trial of the German Cooperative Renal Carcinoma Chemoimmunotherapy Group (DGCIN). Br J Cancer 95:463–469. doi:10.1038/sj.bjc.6603271 PubMedCentralPubMedCrossRef Atzpodien J, Kirchner H, Rebmann U et al (2006) Interleukin-2/interferon-alpha2a/13-retinoic acid-based chemoimmunotherapy in advanced renal cell carcinoma: results of a prospectively randomised trial of the German Cooperative Renal Carcinoma Chemoimmunotherapy Group (DGCIN). Br J Cancer 95:463–469. doi:10.​1038/​sj.​bjc.​6603271 PubMedCentralPubMedCrossRef
15.
18.
Zurück zum Zitat Okada H, Tsugawa T, Sato H et al (2004) Delivery of interferon-alpha transfected dendritic cells into central nervous system tumors enhances the antitumor efficacy of peripheral peptide-based vaccines. Cancer Res 64:5830–5838. doi:10.1158/0008-5472.can-04-0130 PubMedCrossRef Okada H, Tsugawa T, Sato H et al (2004) Delivery of interferon-alpha transfected dendritic cells into central nervous system tumors enhances the antitumor efficacy of peripheral peptide-based vaccines. Cancer Res 64:5830–5838. doi:10.​1158/​0008-5472.​can-04-0130 PubMedCrossRef
19.
Zurück zum Zitat Kuwashima N, Nishimura F, Eguchi J et al (2005) Delivery of dendritic cells engineered to secrete IFN-alpha into central nervous system tumors enhances the efficacy of peripheral tumor cell vaccines: dependence on apoptotic pathways. J Immunol 175:2730–2740PubMedCrossRef Kuwashima N, Nishimura F, Eguchi J et al (2005) Delivery of dendritic cells engineered to secrete IFN-alpha into central nervous system tumors enhances the efficacy of peripheral tumor cell vaccines: dependence on apoptotic pathways. J Immunol 175:2730–2740PubMedCrossRef
21.
Zurück zum Zitat Van Tendeloo VF, Ponsaerts P, Lardon F, Nijs G, Lenjou M, Van Broeckhoven C, Van Bockstaele DR, Berneman ZN (2001) Highly efficient gene delivery by mRNA electroporation in human hematopoietic cells: superiority to lipofection and passive pulsing of mRNA and to electroporation of plasmid cDNA for tumor antigen loading of dendritic cells. Blood 98:49–56PubMedCrossRef Van Tendeloo VF, Ponsaerts P, Lardon F, Nijs G, Lenjou M, Van Broeckhoven C, Van Bockstaele DR, Berneman ZN (2001) Highly efficient gene delivery by mRNA electroporation in human hematopoietic cells: superiority to lipofection and passive pulsing of mRNA and to electroporation of plasmid cDNA for tumor antigen loading of dendritic cells. Blood 98:49–56PubMedCrossRef
22.
Zurück zum Zitat Van Tendeloo VF, Ponsaerts P, Berneman ZN (2007) mRNA-based gene transfer as a tool for gene and cell therapy. Curr Opin Mol Ther 9:423–431PubMed Van Tendeloo VF, Ponsaerts P, Berneman ZN (2007) mRNA-based gene transfer as a tool for gene and cell therapy. Curr Opin Mol Ther 9:423–431PubMed
25.
Zurück zum Zitat Holtkamp S, Kreiter S, Selmi A, Simon P, Koslowski M, Huber C, Tureci O, Sahin U (2006) Modification of antigen-encoding RNA increases stability, translational efficacy, and T-cell stimulatory capacity of dendritic cells. Blood 108:4009–4017. doi:10.1182/blood-2006-04-015024 PubMedCrossRef Holtkamp S, Kreiter S, Selmi A, Simon P, Koslowski M, Huber C, Tureci O, Sahin U (2006) Modification of antigen-encoding RNA increases stability, translational efficacy, and T-cell stimulatory capacity of dendritic cells. Blood 108:4009–4017. doi:10.​1182/​blood-2006-04-015024 PubMedCrossRef
27.
Zurück zum Zitat Van Driessche A, Van de Velde AL, Nijs G, Braeckman T, Stein B, De Vries JM, Berneman ZN, Van Tendeloo VF (2009) Clinical-grade manufacturing of autologous mature mRNA-electroporated dendritic cells and safety testing in acute myeloid leukemia patients in a phase I dose-escalation clinical trial. Cytotherapy 11:653–668. doi:10.1080/14653240902960411 PubMedCrossRef Van Driessche A, Van de Velde AL, Nijs G, Braeckman T, Stein B, De Vries JM, Berneman ZN, Van Tendeloo VF (2009) Clinical-grade manufacturing of autologous mature mRNA-electroporated dendritic cells and safety testing in acute myeloid leukemia patients in a phase I dose-escalation clinical trial. Cytotherapy 11:653–668. doi:10.​1080/​1465324090296041​1 PubMedCrossRef
29.
Zurück zum Zitat Rubinstein M, Levy WP, Moschera JA, Lai CY, Hershberg RD, Bartlett RT, Pestka S (1981) Human leukocyte interferon: isolation and characterization of several molecular forms. Arch Biochem Biophys 210:307–318PubMedCrossRef Rubinstein M, Levy WP, Moschera JA, Lai CY, Hershberg RD, Bartlett RT, Pestka S (1981) Human leukocyte interferon: isolation and characterization of several molecular forms. Arch Biochem Biophys 210:307–318PubMedCrossRef
30.
Zurück zum Zitat Hobbs DS, Pestka S (1982) Purification and characterization of interferons from a continuous myeloblastic cell line. J Biol Chem 257:4071–4076PubMed Hobbs DS, Pestka S (1982) Purification and characterization of interferons from a continuous myeloblastic cell line. J Biol Chem 257:4071–4076PubMed
32.
Zurück zum Zitat Bonehill A, Tuyaerts S, Van Nuffel AM, Heirman C, Bos TJ, Fostier K, Neyns B, Thielemans K (2008) Enhancing the T-cell stimulatory capacity of human dendritic cells by co-electroporation with CD40L, CD70 and constitutively active TLR4 encoding mRNA. Mol Ther 16:1170–1180. doi:10.1038/mt.2008.77 PubMedCrossRef Bonehill A, Tuyaerts S, Van Nuffel AM, Heirman C, Bos TJ, Fostier K, Neyns B, Thielemans K (2008) Enhancing the T-cell stimulatory capacity of human dendritic cells by co-electroporation with CD40L, CD70 and constitutively active TLR4 encoding mRNA. Mol Ther 16:1170–1180. doi:10.​1038/​mt.​2008.​77 PubMedCrossRef
33.
Zurück zum Zitat Luft T, Pang KC, Thomas E, Hertzog P, Hart DN, Trapani J, Cebon J (1998) Type I IFNs enhance the terminal differentiation of dendritic cells. J Immunol 161:1947–1953PubMed Luft T, Pang KC, Thomas E, Hertzog P, Hart DN, Trapani J, Cebon J (1998) Type I IFNs enhance the terminal differentiation of dendritic cells. J Immunol 161:1947–1953PubMed
34.
Zurück zum Zitat Santini SM, Lapenta C, Logozzi M, Parlato S, Spada M, Di Pucchio T, Belardelli F (2000) 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 191:1777–1788PubMedCentralPubMedCrossRef Santini SM, Lapenta C, Logozzi M, Parlato S, Spada M, Di Pucchio T, Belardelli F (2000) 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 191:1777–1788PubMedCentralPubMedCrossRef
35.
Zurück zum Zitat Montoya M, Schiavoni G, Mattei F, Gresser I, Belardelli F, Borrow P, Tough DF (2002) Type I interferons produced by dendritic cells promote their phenotypic and functional activation. Blood 99:3263–3271PubMedCrossRef Montoya M, Schiavoni G, Mattei F, Gresser I, Belardelli F, Borrow P, Tough DF (2002) Type I interferons produced by dendritic cells promote their phenotypic and functional activation. Blood 99:3263–3271PubMedCrossRef
36.
Zurück zum Zitat Nguyen KB, Watford WT, Salomon R, Hofmann SR, Pien GC, Morinobu A, Gadina M, O’Shea JJ, Biron CA (2002) Critical role for STAT4 activation by type 1 interferons in the interferon-gamma response to viral infection. Science 297:2063–2066. doi:10.1126/science.1074900 PubMedCrossRef Nguyen KB, Watford WT, Salomon R, Hofmann SR, Pien GC, Morinobu A, Gadina M, O’Shea JJ, Biron CA (2002) Critical role for STAT4 activation by type 1 interferons in the interferon-gamma response to viral infection. Science 297:2063–2066. doi:10.​1126/​science.​1074900 PubMedCrossRef
37.
Zurück zum Zitat Curtsinger JM, Valenzuela JO, Agarwal P, Lins D, Mescher MF (2005) Type I IFNs provide a third signal to CD8 T cells to stimulate clonal expansion and differentiation. J. Immunol. 174:4465–4469PubMedCrossRef Curtsinger JM, Valenzuela JO, Agarwal P, Lins D, Mescher MF (2005) Type I IFNs provide a third signal to CD8 T cells to stimulate clonal expansion and differentiation. J. Immunol. 174:4465–4469PubMedCrossRef
38.
Zurück zum Zitat Spadaro F, Lapenta C, Donati S, Abalsamo L, Barnaba V, Belardelli F, Santini SM, Ferrantini M (2012) IFN-alpha enhances cross-presentation in human dendritic cells by modulating antigen survival, endocytic routing, and processing. Blood 119:1407–1417. doi:10.1182/blood-2011-06-363564 PubMedCrossRef Spadaro F, Lapenta C, Donati S, Abalsamo L, Barnaba V, Belardelli F, Santini SM, Ferrantini M (2012) IFN-alpha enhances cross-presentation in human dendritic cells by modulating antigen survival, endocytic routing, and processing. Blood 119:1407–1417. doi:10.​1182/​blood-2011-06-363564 PubMedCrossRef
39.
Zurück zum Zitat Nguyen KB, Salazar-Mather TP, Dalod MY, Van Deusen JB, Wei XQ, Liew FY, Caligiuri MA, Durbin JE, Biron CA (2002) Coordinated and distinct roles for IFN-alpha beta, IL-12, and IL-15 regulation of NK cell responses to viral infection. J Immunol 169:4279–4287PubMedCrossRef Nguyen KB, Salazar-Mather TP, Dalod MY, Van Deusen JB, Wei XQ, Liew FY, Caligiuri MA, Durbin JE, Biron CA (2002) Coordinated and distinct roles for IFN-alpha beta, IL-12, and IL-15 regulation of NK cell responses to viral infection. J Immunol 169:4279–4287PubMedCrossRef
40.
Zurück zum Zitat Mailliard RB, Son YI, Redlinger R, Coates PT, Giermasz A, Morel PA, Storkus WJ, Kalinski P (2003) Dendritic cells mediate NK cell help for Th1 and CTL responses: two-signal requirement for the induction of NK cell helper function. J Immunol 171:2366–2373PubMedCrossRef Mailliard RB, Son YI, Redlinger R, Coates PT, Giermasz A, Morel PA, Storkus WJ, Kalinski P (2003) Dendritic cells mediate NK cell help for Th1 and CTL responses: two-signal requirement for the induction of NK cell helper function. J Immunol 171:2366–2373PubMedCrossRef
41.
Zurück zum Zitat Swann JB, Hayakawa Y, Zerafa N, Sheehan KC, Scott B, Schreiber RD, Hertzog P, Smyth MJ (2007) Type I IFN contributes to NK cell homeostasis, activation, and antitumor function. J Immunol 178:7540–7549PubMedCrossRef Swann JB, Hayakawa Y, Zerafa N, Sheehan KC, Scott B, Schreiber RD, Hertzog P, Smyth MJ (2007) Type I IFN contributes to NK cell homeostasis, activation, and antitumor function. J Immunol 178:7540–7549PubMedCrossRef
44.
Zurück zum Zitat Jinushi M, Takehara T, Kanto T et al (2003) Critical role of MHC class I-related chain A and B expression on IFN-alpha-stimulated dendritic cells in NK cell activation: impairment in chronic hepatitis C virus infection. J Immunol 170:1249–1256PubMedCrossRef Jinushi M, Takehara T, Kanto T et al (2003) Critical role of MHC class I-related chain A and B expression on IFN-alpha-stimulated dendritic cells in NK cell activation: impairment in chronic hepatitis C virus infection. J Immunol 170:1249–1256PubMedCrossRef
45.
Zurück zum Zitat Elpek KG, Rubinstein MP, Bellemare-Pelletier A, Goldrath AW, Turley SJ (2010) Mature natural killer cells with phenotypic and functional alterations accumulate upon sustained stimulation with IL-15/IL-15Ralpha complexes. Proc Natl Acad Sci U S A 107:21647–21652. doi:10.1073/pnas.1012128107 PubMedCentralPubMedCrossRef Elpek KG, Rubinstein MP, Bellemare-Pelletier A, Goldrath AW, Turley SJ (2010) Mature natural killer cells with phenotypic and functional alterations accumulate upon sustained stimulation with IL-15/IL-15Ralpha complexes. Proc Natl Acad Sci U S A 107:21647–21652. doi:10.​1073/​pnas.​1012128107 PubMedCentralPubMedCrossRef
46.
Metadaten
Titel
Engineering monocyte-derived dendritic cells to secrete interferon-α enhances their ability to promote adaptive and innate anti-tumor immune effector functions
verfasst von
Yannick Willemen
Johan M. J. Van den Bergh
Eva Lion
Sébastien Anguille
Vicky A. E. Roelandts
Heleen H. Van Acker
Steven D. I. Heynderickx
Barbara M. H. Stein
Marc Peeters
Carl G. Figdor
Viggo F. I. Van Tendeloo
I. Jolanda de Vries
Gosse J. Adema
Zwi N. Berneman
Evelien L. J. Smits
Publikationsdatum
01.07.2015
Verlag
Springer Berlin Heidelberg
Erschienen in
Cancer Immunology, Immunotherapy / Ausgabe 7/2015
Print ISSN: 0340-7004
Elektronische ISSN: 1432-0851
DOI
https://doi.org/10.1007/s00262-015-1688-2

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