Extranodal induction of therapeutic immunity in the tumor microenvironment after intratumoral delivery of Tbet gene-modified dendritic cells

Cancer Gene Therapy

Volumn 20, Issue 8, 2013, Pages 469-477

  Chen, L ^a   Taylor, J L ^a   Sabins, N C ^a   Lowe, D B ^a   Qu, Y ^a   You, Z ^a   Storkus, W J ^a,b  

^a UNIVERSITY OF PITTSBURGH SCHOOL OF MEDICINE   (United States)

^b UNIVERSITY OF PITTSBURGH CANCER INSTITUTE   (United States)

Author keywords

chemokines; dendritic cell; immunotherapy; sarcoma; T bet

Indexed keywords

DENDRITIC CELL VACCINE; GAMMA INTERFERON; INTERLEUKIN 12;

ANIMAL EXPERIMENT; ANIMAL MODEL; ANIMAL TISSUE; ANTINEOPLASTIC ACTIVITY; ARTICLE; CD8+ T LYMPHOCYTE; CONTROLLED STUDY; DENDRITIC CELL; DRUG DELIVERY SYSTEM; FEMALE; GENE THERAPY; HUMAN; HUMAN CELL; LYMPH NODE; MICROENVIRONMENT; MOUSE; NATURAL KILLER CELL; NONHUMAN; PRIORITY JOURNAL; SARCOMA; T LYMPHOCYTE; TUMOR IMMUNITY; TUMOR MICROENVIRONMENT; WILD TYPE;

MURINAE;

ANIMALS; CELL LINE, TUMOR; DENDRITIC CELLS; FEMALE; GENETIC THERAPY; IMMUNOTHERAPY, ADOPTIVE; MICE; MICE, INBRED C57BL; MICE, TRANSGENIC; SARCOMA; T-BOX DOMAIN PROTEINS; TRANSDUCTION, GENETIC; TUMOR MICROENVIRONMENT;

EID: 84882451371     PISSN: 09291903     EISSN: 14765500     Source Type: Journal    
DOI: 10.1038/cgt.2013.42     Document Type: Article

References (63)

1. Steinman RM. The dendritic cell system and its role in immunogenicity. Ann Rev Immunol 1991; 9: 271-296.
2. Mellman I, Steinman RM. Dendritic cells: specialized and regulated antigen processing machines. Cell 2001; 106: 255-258.
3. Steinman RM. Dendritic cells: understanding immunogenicity. Eur J Immunol 2007; 37(Suppl 1): S53-S60.
4. Anderson AE, Sayers BL, Haniffa MA, Swan DJ, Diboll J, Wang XN et al. Differential regulation of naive and memory CD4+ T cells by alternatively activated dendritic cells. J Leukoc Biol 2008; 84: 124-133.
5. Arens R, Schoenberger SP. Plasticity in programming of effector and memory CD8 T-cell formation. Immunol Rev 2010; 235: 190-205.
6. Watchmaker PB, Berk E, Muthuswamy R, Mailliard RB, Urban JA, Kirkwood JM et al. Independent regulation of chemokine responsiveness and cytolytic function versus CD8+ T cell expansion by dendritic cells. J Immunol 2010; 184: 591-597.
7. Steinman RM, Banchereau J. Taking dendritic cells into medicine. Nature 2007; 449: 419-426.
8. Cools N, Petrizzo A, Smits E, Buonaguro FM, Tornesello ML, Berneman Z et al. Dendritic cells in the pathogenesis and treatment of human diseases: a Janus Bifrons? Immunotherapy 2011; 3: 1203-1222.
9. Wu R, Forget MA, Chacon J, Bernatchez C, Haymaker C, Chen JQ et al. Adoptive T-cell therapy using autologous tumor-infiltrating lymphocytes for metastatic melanoma: current status and future outlook. Cancer J 2012; 18: 160-175.
10. Weber J, Atkins M, Hwu P, Radvanyi L, Sznol M, Yee C et al. Immunotherapy Task Force of the NCI Investigational Drug Steering Committee. White paper on adoptive cell therapy for cancer with tumor-infiltrating lymphocytes: a report of the CTEP subcommittee on adoptive cell therapy. Clin Cancer Res 2011; 17: 1664-1673.
11. Klebanoff CA, Gattinoni L, Restifo NP. CD8+ T-cell memory in tumor immunology and immunotherapy. Immunol Rev 2006; 211: 214-224.
12. Lazarevic V, Glimcher LH. T-bet in disease. Nat Immunol 2011; 12: 597-606.
13. Lipscomb MW, Chen L, Taylor JL, Goldbach C, Watkins SC, Kalinski P et al. Ectopic T-bet expression licenses dendritic cells for IL-12-independent priming of type 1 T cells in vitro. J Immunol 2009; 183: 7250-7258.
14. Qu Y, Chen L, Pardee AD, Taylor JL, Wesa AK, Storkus WJ. Intralesional delivery of dendritic cells engineered to express T-bet promotes protective type 1 immunity and the normalization of the tumor microenvironment. J Immunol 2010; 185: 2895-2902.
15. Wang Z, Divito SJ, Shufesky WJ, Sumpter T, Wang H, Tkacheva OA et al. Dendritic cell therapies in transplantation revisited: deletion of recipient DCs deters the effect of therapeutic DCs. Am J Transplant 2012; 12: 1398-1408.
16. Vignali DA, Kuchroo VK. IL-12 family cytokines: immunological playmakers. Nat Immunol 2012; 13: 722-728.
17. Cresswell P, Ackerman AL, Giodini A, Peaper DR, Wearsch PA. Mechanisms of MHC class I-restricted antigen processing and cross-presentation. Immunol Rev 2005; 207: 145-157.
18. Adam C, King S, Allgeier T, Braumüller H, Lüking C, Mysliwietz J et al. DC-NK cell cross talk as a novel CD4+ T-cell-independent pathway for antitumor CTL induction. Blood 2005; 106: 338-344.
19. Mailliard RB, Son YI, Redlinger R, Coates PT, Giermasz A, Morel PA et al. Dendritic cells mediate NK cell help for Th1 and CTL responses: two-signal requirement for the induction of NK cell helper function. J Immunol 2003; 171: 2366-2373.
20. McDonnell AM, Pro sser AC, van Bruggen I, Robinson BW, Currie AJ. CD8a+ DC are not the sole subset cross-presenting cell-associated tumor antigens from a solid tumor. Eur J Immunol 2010; 40: 1617-1627.
21. Heath WR, Belz GT, Behrens GM, Smith CM, Forehan SP, Parish IA et al. Crosspresentation, dendritic cell subsets, and the generation of immunity to cellular antigens. Immunol Rev 2004; 199: 9-26.
22. den Haan JM, Lehar SM, Bevan MJ. CD8+ but not CD8neg dendritic cells crossprime cytotoxic T cells in vivo. J Exp Med 2000; 192: 1685-1696.
23. Hildner K, Edelson BT, Purtha WE, Diamond M, Matsushita H, Kohyama M et al. Batf3 deficiency reveals a critical role for CD8a+ dendritic cells in cytotoxic T cell immunity. Science 2008; 322: 1097-1100.
24. Jang MH, Sougawa N, Tanaka T, Hirata T, Hiroi T, Tohya K et al. CCR7 is critically important for migration of dendritic cells in intestinal lamina propria to mesenteric lymph nodes. J Immunol 2006; 176: 803-810.
25. Bajan a S, Roach K, Turner S, Paul J, Kovats S. IRF4 promotes cutaneous dendritic cell migration to lymph nodes during homeostasis and inflammation. J Immunol 2012; 189: 3368-3377.
26. Yen JH, Kong W, Ganea D. IFN-b inhibits dendritic cell migration through STAT-1-mediated transcriptional suppression of CCR7 and matrix metalloproteinase 9. J Immunol 2010; 184: 3478-3486.
27. Olmos S, Stukes S, Ernst JD. Ectopic activation of Mycobacterium tuberculosisspecific CD4+ T cells in lungs of CCR7-/- mice. J Immunol 2010; 184: 895-901.
28. Feijoó E, Alfaro C, Mazzolini G, Serra P, Penũelas I, Arina A et al. Dendritic cells delivered inside human carcinomas are sequestered by interleukin-8. Int J Cancer 2005; 116: 275-281.
29. Fujiwara S, Wada H, Miyata H, Kawada J, Kawabata R, Nishikawa H et al. Clinical trial of the intratumoral administration of labeled DC combined with systemic chemotherapy for esophageal cancer. J Immunother 2012; 35: 513-521.
30. Feuerer M, Beckhove P, Garbi N, Mahnke Y, Limmer A, Hommel M et al. Bone marrow as a priming site for T-cell responses to blood-borne antigen. Nat Med 2003; 9: 1151-1157.
31. Smith AL, Fazekas de St Groth B. Antigen-pulsed CD8a+ dendritic cells generate an immune response after subcutaneous injection without homing to the draining lymph node. J Exp Med 1999; 189: 593-598.
32. Kirk CJ, Hartigan-O'Connor D, Mulé JJ. The dynamics of the T-cell antitumor response: chemokine-secreting dendritic cells can prime tumor-reactive T cells extranodally. Cancer Res 2001; 61: 8794-8802.
33. Zhu J, Jankovic D, Oler AJ, Wei G, Sharma S, Hu G et al. The transcription factor T-bet is induced by multiple pathways and prevents an endogenous Th2 cell program during Th1 cell responses. Immunity 2012; 37: 660-673.
34. Muthuswamy R, Mueller-Berghaus J, Haberkorn U, Reinhart TA, Schadendorf D, Kalinski P. PGE2 transiently enhances DC expression of CCR7 but inhibits the ability of DCs to produce CCL19 and attract naive T cells. Blood 2010; 116: 1454-1459.
35. Marelli-Berg FM, Cannella L, Dazzi F, Mirenda V. The highway code of T cell trafficking. J Pathol 2008; 214: 179-189.
36. Cose S, Brammer C, Khanna KM, Masopust D, Lefrancois L. Evidence that a significant number of naive T cells enter non-lymphoid organs as part of a normal migratory pathway. Eur J Immunol 2006; 36: 1423-1433.
37. Zippelius A, Bioley G, Le Gal FA, Rufer N, Brandes M, Batard P et al. Human thymus exports naive CD8 T cells that can home to nonlymphoid tissues. J Immunol 2004; 172: 2773-2777.
38. Lewis M, Tarlton JF, Cose S. Memory versus naive T-cell migration. Immunol Cell Biol 2008; 86: 226-231.
39. Bertolino P, Bowen DG, McCaughan GW, Fazekas de St Groth B. Antigenspecific primary activation of CD8+ T cells within the liver. J Immunol 2001; 166: 5430-5438.
40. Yu P, Lee Y, Liu W, Chin RK, Wang J, Wang Y et al. Priming of naive T cells inside tumors leads to eradication of established tumors. Nat Immunol 2004; 5: 141-149.
41. Igoucheva O, Grazzini M, Pidich A, Kemp DM, Larijani M, Farber M et al. Immunotargeting and eradication of orthotopic melanoma using a chemokineenhanced DNA vaccine. Gene Therapy 2013. doi:10.1038/gt.2013.17.
42. Robertson MJ. Role of chemokines in the biology of natural killer cells. J Leukoc Biol 2002; 71: 173-183.
43. Gustafsson K, Ingelsten M, Bergqvist L, Nyström J, Andersson B, Karlsson-Parra A. Recruitment and activation of natural killer cells in vitro by a human dendritic cell vaccine. Cancer Res 2008; 68: 5965-5971.
44. Inngjerdingen M, Damaj B, Maghazachi AA. Human NK cells express CC chemokine receptors 4 and 8 and respond to thymus and activation-regulated chemokine, macrophage-derived chemokine, and I-309. J Immunol 2000; 164: 4048-4054.
45. Vujanovic L, Ballard W, Thorne SH, Vujanovic NL, Butterfield LH. Adenovirusengineered human dendritic cells induce natural killer cell chemotaxis via CXCL8/IL-8 and CXCL10/IP-10. Oncoimmunology 2012; 1: 448-457.
46. Gustafsson K, Junevik K, Werlenius O, Holmgren S, Karlsson-Parra A, Andersson PO. Tumour-loaded a-type 1-polarized dendritic cells from patients with chronic lymphocytic leukaemia produce a superior NK-, NKT- and CD8+ T cell-attracting chemokine profile. Scand J Immunol 2011; 74: 318-326.
47. Messina JL, Fenstermacher DA, Eschrich S, Qu X, Berglund AE, Lloyd MC et al. 12-Chemokine gene signature identifies lymph node-like structures in melanoma: potential for patient selection for immunotherapy? Sci Rep 2012; 2: 765.
48. Morris MA, Ley K. Trafficking of natural killer cells. Curr Mol Med 2004; 4: 431-438.
49. Castellino F, Huang AY, Altan-Bonnet G, Stoll S, Scheinecker C, Germain RN. Chemokines enhance immunity by guiding naive CD8+ T cells to sites of CD4+ T cell-dendritic cell interaction. Nature 2006; 440: 890-895.
50. Coelho AL, Schaller MA, Benjamim CF, Orlofsky AZ, Hogaboam CM, Kunkel SL. The chemokine CCL6 promotes innate immunity via immune cell activation and recruitment. J Immunol 2007; 179: 5474-5482.
51. Semmling V, Lukacs-Kornek V, Thaiss CA, Quast T, Hochheiser K, Panzer U et al. Alternative cross-priming through CCL17-CCR4-mediated attraction of CTLs toward NKT cell-licensed DCs. Nat Immunol 2010; 11: 313-320.
52. Bernardini G, Sciumè G, Bosisio D, Morrone S, Sozzani S, Santoni A. CCL3 and CXCL12 regulate trafficking of mouse bone marrow NK cell subsets. Blood 2008; 111: 3626-3634.
53. Bai Z, Hayasaka H, Kobayashi M, Li W, Guo Z, Jang MH et al. CXC chemokine ligand 12 promotes CCR7-dependent naive T cell trafficking to lymph nodes and Peyer's patches. J Immunol 2009; 182: 1287-1295.
54. Henry CJ, Ornelles DA, Mitchell LM, Brzoza-Lewis KL, Hiltbold EM. IL-12 produced by dendritic cells augments CD8+ T cell activation through the production of the chemokines CCL1 and CCL17. J Immunol 2008; 181: 8576-8584.
55. Carbone E, Terrazzano G, Ruggiero G, Zanzi D, Ottaiano A, Manzo C et al. Recognition of autologous dendritic cells by human NK cells. Eur J Immunol 1999; 29: 4022-4029.
56. Wolfers J, Lozier A, Raposo G, Regnault A, Thé ry C, Masurier C et al. Tumor-derived exosomes are a source of shared tumor rejection antigens for CTL cross-priming. Nat Med 2001; 7: 297-303.
57. Cooper EH, Forbes MA, Hambling MH. Serum beta 2-microglobulin and C reactive protein concentrations in viral infections. J Clin Pathol 1984; 37: 1140-1143.
58. Hee CS, Beerbaum M, Loll B, Ballaschk M, Schmieder P, Uchanska-Ziegler B et al. Dynamics of free versus complexed b2-microglobulin and the evolution of interfaces in MHC class I molecules. Immunogenetics 2013; 65: 157-172.
59. Asano K, Nabeyama A, Miyake Y, Qiu CH, Kurita A, Tomura M et al. CD169-positive macrophages dominate antitumor immunity by crosspresenting dead cell-associated antigens. Immunity 2011; 34: 85-95.
60. Nishimura F, Dusak JE, Eguchi J, Zhu X, Gambotto A, Storkus WJ et al. Adoptive transfer of type 1 CTL mediates effective anti-central nervous system tumor response: critical roles of IFN-inducible protein-10. Cancer Res 2006; 66: 4478-4487.
61. Song S, Zhang K, You H, Wang J, Wang Z, Yan C et al. Significant anti-tumour activity of adoptively transferred T cells elicited by intratumoral dendritic cell vaccine injection through enhancing the ratio of CD8+ T cell/regulatory T cells in tumour. Clin Exp Immunol 2010; 162: 75-83.
62. Fujita M, Zhu X, Ueda R, Sasaki K, Kohanbash G, Kastenhuber ER et al. Effective immunotherapy against murine gliomas using type 1 polarizing dendritic cells-significant roles of CXCL10. Cancer Res 2009; 69: 1587-1595.
63. Pellegatta S, Poliani PL, Stucchi E, Corno D, Colombo CA, Orzan F et al. Intra-tumoral dendritic cells increase efficacy of peripheral vaccination by modulation of glioma microenvironment. Neuro Oncol 2010; 12: 377-388.