Fusion of the dendritic cell-targeting chemokine mip3α to melanoma antigen gp100 in a therapeutic dna vaccine significantly enhances immunogenicity and survival in a mouse melanoma model

Journal for ImmunoTherapy of Cancer

Volumn 4, Issue 1, 2016, Pages

  Gordy, James T ^a   Luo, Kun ^a   Zhang, Hong ^a   Biragyn, Arya ^b   Markham, Richard B ^a  

^a JOHNS HOPKINS BLOOMBERG SCHOOL OF PUBLIC HEALTH   (United States)

^b NATIONAL INSTITUTE ON AGING   (United States)

Author keywords

B16 Melanoma; Chemokine antigen fusion; DNA Vaccine; Gp100; In vivo electroporation; MIP3 , MIP3alpha, or CCL20; Therapeutic cancer vaccine

Indexed keywords

DNA VACCINE; HYBRID PROTEIN; MACROPHAGE INFLAMMATORY PROTEIN 3ALPHA; MELANOCYTE PROTEIN PMEL 17;

ANIMAL CELL; ANIMAL MODEL; ANIMAL TISSUE; ARTICLE; CONTROLLED STUDY; ELECTROPORATION; ENZYME LINKED IMMUNOSORBENT ASSAY; FEMALE; FLOW CYTOMETRY; GENETIC TRANSFECTION; HUMAN; HUMAN CELL; IMMUNOGENICITY; LYMPHOCYTE DEPLETION; MELANOMA; MOUSE; NONHUMAN; PRIORITY JOURNAL; SURVIVAL; TUMOR ASSOCIATED LEUKOCYTE; TUMOR GROWTH; TUMOR VOLUME; WESTERN BLOTTING;

EID: 85006698902     PISSN: None     EISSN: 20511426     Source Type: Journal    
DOI: 10.1186/s40425-016-0189-y     Document Type: Article

References (46)

1. Eggermont AMM, Maio M, Robert C. Immune checkpoint inhibitors in melanoma provide the cornerstones for curative therapies. Semin Oncol. 2015;42:429-35.
2. Overwijk W, Wang E, Marincola F, Rammensee H-G, Restifo N. Mining the mutanome: developing highly personalized Immunotherapies based on mutational analysis of tumors. J Immuno Ther Cancer. 2013;1:11.
3. Hacohen N, Fritsch E, Carter T, Lander E. Getting personal with neoantigen-based therapeutic cancer vaccines. Cancer Immunol Res. 2013;1:11-5.
4. Small EJ, Schellhammer PF, Higano CS, Redfern CH, Nemunaitis JJ, Valone FH, Verjee SS, Jones LA, Hershberg RM. Placebo-controlled phase III trial of immunologic therapy with sipuleucel-T (APC8015) in patients with metastatic, asymptomatic hormone refractory prostate cancer. J Clin Oncol. 2006;24:3089-94.
5. Ali OA, Lewin SA, Dranoff G, Mooney DJ. Vaccines combined with immune checkpoint antibodies promote cytotoxic T-cell activity and tumor eradication. Cancer Immunol Res. 2016;4:95-100.
6. Liu M. DNA vaccines: an historical perspective and view to the future. Immunol Rev. 2011;239:62-84.
7. Tagawa S, Lee P, Snively J, Boswell W, Ounpraseuth S, Lee S, Hickingbottom B, Smith J, Johnson D, Weber J. Phase I study of intranodal delivery of a plasmid DNA vaccine for patients with Stage IV melanoma. Cancer. 2003;98:144-54.
8. Conry RM, Curiel DT, Strong TV, Moore SE, Allen KO, Barlow DL, Shaw DR, LoBuglio AF. Safety and immunogenicity of a DNA vaccine encoding carcinoembryonic antigen and hepatitis B surface antigen in colorectal carcinoma patients. Clin Cancer Res. 2002;8:2782-7.
9. Liu MA, Ulmer JB. Human clinical trials of plasmid DNA vaccines. Adv Genet. 2005;55:25-40.
10. Senovilla L, Vacchelli E, Garcia P, Eggermont A, Fridman W, Galon J, Zitvogel L, Kroemer G, Galluzzi L. Trial watch. OncoImmunology. 2013;2:e23803.
11. Rice J, Ottensmeier C, Stevenson F. DNA vaccines: precision tools for activating effective immunity against cancer. Nat Rev Cancer. 2008;8:108-20.
12. Davis BS, Chang GJ, Cropp B, Roehrig JT, Martin DA, Mitchell CJ, Bowen R, Bunning ML. West Nile virus recombinant DNA vaccine protects mouse and horse from virus challenge and expresses in vitro a noninfectious recombinant antigen that can be used in enzyme-linked immunosorbent assays. J Virol. 2001;75:4040-7.
13. Anderson ED, Mourich DV, Fahrenkrug SC, LaPatra S, Shepherd J, Leong JA. Genetic immunization of rainbow trout (Oncorhynchus mykiss) against infectious hematopoietic necrosis virus. Mol Marine Biol Biotechnol. 1996;5:114-22.
14. Bergman PJ, McKnight J, Novosad A, Charney S, Farrelly J, Craft D, Wulderk M, Jeffers Y, Sadelain M, Hohenhaus AE, Segal N, Gregor P, Engelhorn M, Riviere I, Houghton AN, Wolchok JD. Long-term survival of dogs with advanced malignant melanoma after DNA vaccination with xenogeneic human tyrosinase: a phase I trial. Clin Cancer Res. 2003;9:1284-90.
15. Chen J, Fang F, Li X, Chang H, Chen Z. Protection against influenza virus infection in BALB/c mice immunized with a single dose of neuraminidase-expressing DNAs by electroporation. Vaccine. 2005;23:4322-8.
16. Medi BM, Hoselton S, Marepalli RB, Singh J. Skin targeted DNA vaccine delivery using electroporation in rabbits. I: efficacy. Int J Pharm. 2005;294:53-63.
17. Otten G, Schaefer M, Doe B, Liu H, Srivastava I, Zur Megede J, O'Hagan D, Donnelly J, Widera G, Rabussay D, Lewis MG, Barnett S, Ulmer JB. Enhancement of DNA vaccine potency in rhesus macaques by electroporation. Vaccine. 2004;22:2489-93.
18. Tollefsen S, Vordermeier M, Olsen I, Storset AK, Reitan LJ, Clifford D, Lowrie DB, Wiker HG, Huygen K, Hewinson G, Mathiesen I, Tjelle TE. DNA injection in combination with electroporation: a novel method for vaccination of farmed ruminants. Scand J Immunol. 2003;57:229-38.
19. Ahlén G, Söderholm J, Tjelle T, Kjeken R, Frelin L, Höglund U, Blomberg P, Fons M, Mathiesen I, Sällberg M. In vivo electroporation enhances the immunogenicity of hepatitis C virus nonstructural 3/4A DNA by increased local DNA uptake, protein expression, inflammation, and infiltration of CD3+ T cells. J Immunol. 2007;179:4741-53.
20. Liu J, Kjeken R, Mathiesen I, Barouch D. Recruitment of antigen-presenting cells to the site of inoculation and augmentation of human immunodeficiency virus type 1 DNA vaccine immunogenicity by in vivo electroporation. J Virol. 2008;82:5643-9.
21. Babiuk S, Baca-Estrada ME, Foldvari M, Middleton DM, Rabussay D, Widera G, Babiuk LA. Increased gene expression and inflammatory cell infiltration caused by electroporation are both important for improving the efficacy of DNA vaccines. J Biotechnol. 2004;110:1-10.
22. Person R, Bodles-Brakhop AM, Pope MA, Brown PA, Khan AS, Draghia-Akli R. Growth hormone-releasing hormone plasmid treatment by electroporation decreases offspring mortality over three pregnancies. Mol Ther. 2008;16:1891-7.
23. Vasan S, Hurley A, Schlesinger SJ, Hannaman D. In vivo electroporation enhances the immunogenicity of an HIV-1 DNA vaccine candidate in healthy volunteers. PLoS One. 2011;6:e19252.
24. Low L, Mander A, McCann K, Dearnaley D. DNA vaccination with electroporation induces increased antibody responses in patients with prostate cancer. Hum Gene Ther. 2009;20:1269-78.
25. Loudon PT, Yager EJ, Lynch DT, Narendran A, Stagnar C, Franchini AM, Fuller JT, White PA, Nyuandi J, Wiley CA, Murphey-Corb M, Fuller DH. GM-CSF increases mucosal and systemic immunogenicity of an H1N1 influenza DNA vaccine administered into the epidermis of non-human primates. PLoS One. 2010;5:e11021.
26. Zheng Q, Fan D, Gao N, Chen H, Wang J, Ming Y, Li J, An J. Evaluation of a DNA vaccine candidate expressing prM-E-NS1 antigens of dengue virus serotype 1 with or without granulocyte-macrophage colony-stimulating factor (GM-CSF) in immunogenicity and protection. Vaccine. 2011;29:763-71.
27. Rodríguez AM, Pascutti MFF, Maeto C, Falivene J, Holgado MPP, Turk G, Gherardi MMM. IL-12 and GM-CSF in DNA/MVA immunizations against HIV-1 CRF12_BF Nef induced T-cell responses with an enhanced magnitude, breadth and quality. PLoS One. 2012;7:e37801.
28. Lapteva N, Huang XF. CCL5 as an adjuvant for cancer immunotherapy. Expert Opin Biol Ther. 2010;10:725-33.
29. Nguyen-Hoai T, Hohn O, Vu MD, Baldenhofer G, Sayed Ahmed MS, Dörken B, Norley S, Lipp M, Pezzutto A, Westermann J. CCL19 as an adjuvant for intradermal gene gun immunization in a Her2/neu mouse tumor model: improved vaccine efficacy and a role for B cells as APC. Cancer Gene Ther. 2012;19:880-7.
30. Luo K, Zhang H, Zavala F, Biragyn A, Espinosa D, Markham R. Fusion of antigen to a dendritic cell targeting chemokine combined with adjuvant yields a malaria DNA vaccine with enhanced protective capabilities. PLoS One. 2014;9:e90413.
31. Biragyn A, Schiavo R, Olkhanud P, Sumitomo K, King A, McCain M, Indig FE, Almanzar G, Baatar D. Tumor-associated embryonic antigen-expressing vaccines that target CCR6 elicit potent CD8+ T cell-mediated protective and therapeutic antitumor immunity. J Immunol. 2007;179:1381-8.
32. Biragyn A, Ruffini P, Coscia M, Harvey L, Neelapu S, Baskar S, Wang J-M, Kwak L. Chemokine receptor-mediated delivery directs self-tumor antigen efficiently into the class II processing pathway in vitro and induces protective immunity in vivo. Blood. 2004;104:1961-9.
33. Schiavo R, Baatar D, Olkhanud P, Indig F, Restifo N, Taub D, Biragyn A. Chemokine receptor targeting efficiently directs antigens to MHC class I pathways and elicits antigen-specific CD8+ T-cell responses. Blood. 2006;107:4597-605.
34. Guo J, Fan M, Sun J, Jia R. Fusion of antigen to chemokine CCL20 or CXCL13 strategy to enhance DNA vaccine potency. Int Immunopharmacol. 2009;9:925930.
35. Song R, Liu S, Leong KW. Effects of MIP-1 alpha, MIP-3 alpha, and MIP-3 beta on the induction of HIV Gag-specific immune response with DNA vaccines. Mol Ther. 2007;15:1007-15.
36. Oppenheim JJ, Biragyn A, Kwak LW, Yang D. Roles of antimicrobial peptides such as defensins in innate and adaptive immunity. Ann Rheum Dis. 2003;62 Suppl 2:ii17-21.
37. Coscia M, Biragyn A. Cancer immunotherapy with chemoattractant peptides. Semin Cancer Biol. 2004;14:209218.
38. Biragyn A, Tani K, Grimm M, Weeks S, Kwak L. Genetic fusion of chemokines to a self tumor antigen induces protective, T-cell dependent antitumor immunity. Nat Biotechnol. 1999;17:253-8.
39. Biragyn A, Surenhu M, Yang D, Ruffini PA, Haines BA, Klyushnenkova E, Oppenheim JJ, Kwak LW. Mediators of innate immunity that target immature, but not mature, dendritic cells induce antitumor immunity when genetically fused with nonimmunogenic tumor antigens. J Immunol. 2001;167:6644-53.
40. Ma K, Xu W, Shao X, Yanyue, Hu L, Xu H, Yuan Z, Zheng X, Xiong S. Coimmunization with RANTES plasmid polarized Th1 immune response against hepatitis B virus envelope via recruitment of dendritic cells. Antiviral Res. 2007;76:140-9.
41. Miguel A, Herrero M, Sendra L, Botella R, Algás R, Sánchez M, Aliño S. Comparative antitumor effect of preventive versus therapeutic vaccines employing B16 melanoma cells genetically modified to express GM-CSF and B7.2 in a Murine Model. Toxins. 2012;4:1058-81.
42. Yan J, Pankhong P, Shin TH, Obeng-Adjei N, Morrow MP, Walters JN, Khan AS, Sardesai NY, Weiner DB. Highly optimized DNA vaccine targeting human telomerase reverse transcriptase stimulates potent antitumor immunity. Cancer Immunol Res. 2013;1:179-89.
43. Tuthill RJ, Unger JM, Liu PY, Flaherty LE, Sondak VK. Risk assessment in localized primary cutaneous melanoma. Am J Clin Pathol. 2002;118:504-11.
44. Haabeth OA, Tveita AA, Fauskanger M, Schjesvold F, Lorvik KB, Hofgaard PO, Omholt H, Munthe LA, Dembic Z, Corthay A, Bogen B. How Do CD4(+) T cells detect and eliminate tumor cells that either lack or express MHC class II molecules Front Immunol. 2014;5:174.
45. Igoucheva O, Grazzini M, Pidich A, Kemp DM, Larijani M, Farber M, Lorton J, Rodeck U, Alexeev V. Immunotargeting and eradication of orthotopic melanoma using a chemokine-enhanced DNA vaccine. Gene Ther. 2013;20:939-48.
46. Castle J, Kreiter S, Diekmann J, Löwer M, van de Roemer N, de Graaf J, Selmi A, Diken M, Boegel S, Paret C, Koslowski M, Kuhn A, Britten C, Huber C, Türeci Ö, Sahin U. Exploiting the mutanome for tumor vaccination. Cancer Res. 2012;72:1081-91.