3,573
Views
61
CrossRef citations to date
0
Altmetric
Original Research

Oncolytic adenoviruses coated with MHC-I tumor epitopes increase the antitumor immunity and efficacy against melanoma

, , , , , , , , , , , , , & show all
Article: e1105429 | Received 14 Jul 2015, Accepted 04 Oct 2015, Published online: 08 Apr 2016

References

  • Bischoff JR, Kirn DH, Williams A, Heise C, Horn S, Muna M, Ng L, Nye JA, Sampson-Johannes A, Fattaey A et al. An adenovirus mutant that replicates selectively in p53-deficient human tumor cells. Science 1996; 274:373-6; PMID:8832876; http://dx.doi.org/10.1126/science.274.5286.373
  • Heise C, Hermiston T, Johnson L, Brooks G, Sampson-Johannes A, Williams A, Hawkins L, Kirn D. An adenovirus E1A mutant that demonstrates potent and selective systemic anti-tumoral efficacy. Nat Med 2000; 6:1134-9; PMID:11017145; http://dx.doi.org/10.1038/80474
  • Zhang SN, Choi IK, Huang JH, Yoo JY, Choi KJ, Yun CO. Optimizing DC vaccination by combination with oncolytic adenovirus coexpressing IL-12 and GM-CSF. Mol Ther 2011; 19:1558-68; PMID:21468000; http://dx.doi.org/10.1038/mt.2011.29
  • Seiler MP, Gottschalk S, Cerullo V, Ratnayake M, Mane VP, Clarke C, Palmer DJ, Ng P, Rooney CM, Lee B. Dendritic cell function after gene transfer with adenovirus-calcium phosphate co-precipitates. Mol Ther 2007; 15:386-92; PMID:17235318; http://dx.doi.org/10.1038/sj.mt.6300029
  • Cerullo V, Pesonen S, Diaconu I, Escutenaire S, Arstila PT, Ugolini M, Nokisalmi P, Raki M, Laasonen L, Sarkioja M et al. Oncolytic adenovirus coding for granulocyte macrophage colony-stimulating factor induces antitumoral immunity in cancer patients. Cancer Res 2010; 70:4297-309; PMID:20484030; http://dx.doi.org/10.1158/0008-5472.CAN-09-3567
  • Cerullo V, Diaconu I, Kangasniemi L, Rajecki M, Escutenaire S, Koski A, Romano V, Rouvinen N, Tuuminen T, Laasonen L et al. Immunological effects of low-dose cyclophosphamide in cancer patients treated with oncolytic adenovirus. Mol Ther 2011; 19:1737-46; PMID:21673660; http://dx.doi.org/10.1038/mt.2011.113
  • Choi IK, Li Y, Oh E, Kim J, Yun CO. Oncolytic adenovirus expressing IL-23 and p35 elicits IFN-gamma- and TNF-alpha-co-producing T cell-mediated antitumor immunity. PLoS One 2013; 8:e67512; PMID:23844018; http://dx.doi.org/10.1371/journal.pone.0067512
  • Hirvinen M, Rajecki M, Kapanen M, Parviainen S, Rouvinen-Lagerstrom N, Diaconu I, Nokisalmi P, Tenhunen M, Hemminki A, Cerullo V. Immunological effects of a tumor necrosis factor alpha-armed oncolytic adenovirus. Hum Gene Ther 2015; 26(3):134-44; PMID:25557131; http://dx.doi.org/10.1089/hum.2014.069
  • Diaconu I, Cerullo V, Hirvinen ML, Escutenaire S, Ugolini M, Pesonen SK, Bramante S, Parviainen S, Kanerva A, Loskog AS et al. Immune response is an important aspect of the antitumor effect produced by a CD40L-encoding oncolytic adenovirus. Cancer Res 2012; 72:2327-38; PMID:22396493; http://dx.doi.org/10.1158/0008-5472.CAN-11-2975
  • Liljenfeldt L, Dieterich LC, Dimberg A, Mangsbo SM, Loskog AS. CD40L gene therapy tilts the myeloid cell profile and promotes infiltration of activated T lymphocytes. Cancer Gene Ther 2014; 21:95-102; PMID:24481488; http://dx.doi.org/10.1038/cgt.2014.2
  • Pesonen S, Diaconu I, Cerullo V, Escutenaire S, Raki M, Kangasniemi L, Nokisalmi P, Dotti G, Guse K, Laasonen L et al. Integrin targeted oncolytic adenoviruses Ad5-D24-RGD and Ad5-RGD-D24-GMCSF for treatment of patients with advanced chemotherapy refractory solid tumors. Int J Cancer 2012; 130:1937-47; PMID:21630267; http://dx.doi.org/10.1002/ijc.26216
  • Koski A, Kangasniemi L, Escutenaire S, Pesonen S, Cerullo V, Diaconu I, Nokisalmi P, Raki M, Rajecki M, Guse K et al. Treatment of cancer patients with a serotype 5/3 chimeric oncolytic adenovirus expressing GMCSF. Mol Ther 2010; 18:1874-84; PMID:20664527; http://dx.doi.org/10.1038/mt.2010.161
  • Sorensen MR, Holst PJ, Pircher H, Christensen JP, Thomsen AR. Vaccination with an adenoviral vector encoding the tumor antigen directly linked to invariant chain induces potent CD4(+) T-cell-independent CD8(+) T-cell-mediated tumor control. Eur J Immunol 2009; 39:2725-36; PMID:19637230; http://dx.doi.org/10.1002/eji.200939543
  • Nwanegbo E, Vardas E, Gao W, Whittle H, Sun H, Rowe D, Robbins PD, Gambotto A. Prevalence of neutralizing antibodies to adenoviral serotypes 5 and 35 in the adult populations of The Gambia, South Africa, and the United States. Clin Diagn Lab Immunol 2004; 11:351-7; PMID:15013987; http://dx.doi.org/10.1128/CDLI.11.2.351–357.2004
  • Zaiss AK, Machado HB, Herschman HR. The influence of innate and pre-existing immunity on adenovirus therapy. J Cell Biochem 2009; 108:778-90; PMID:19711370; http://dx.doi.org/10.1002/jcb.22328
  • Fasbender A, Zabner J, Chillon M, Moninger TO, Puga AP, Davidson BL, Welsh MJ. Complexes of adenovirus with polycationic polymers and cationic lipids increase the efficiency of gene transfer in vitro and in vivo. J Biol Chem 1997; 272:6479-89; PMID:9045673; http://dx.doi.org/10.1074/jbc.272.10.6479
  • Moore MW, Carbone FR, Bevan MJ. Introduction of soluble protein into the class I pathway of antigen processing and presentation. Cell 1988; 54:777-85; PMID:3261634; http://dx.doi.org/10.1016/S0092-8674(88)91043-4
  • Deng Y, Gibbs J, Bacik I, Porgador A, Copeman J, Lehner P, Ortmann B, Cresswell P, Bennink JR, Yewdell JW. Assembly of MHC class I molecules with biosynthesized endoplasmic reticulum-targeted peptides is inefficient in insect cells and can be enhanced by protease inhibitors. J Immunol 1998; 161:1677-85; PMID:9712031
  • Cerullo V, Diaconu I, Romano V, Hirvinen M, Ugolini M, Escutenaire S, Holm SL, Kipar A, Kanerva A, Hemminki A. An oncolytic adenovirus enhanced for toll-like receptor 9 stimulation increases antitumor immune responses and tumor clearance. Mol Ther 2012; 20:2076-86; PMID:22828500; http://dx.doi.org/10.1038/mt.2012.137
  • Overwijk WW, Tsung A, Irvine KR, Parkhurst MR, Goletz TJ, Tsung K, Carroll MW, Liu C, Moss B, Rosenberg SA et al. gp100/pmel 17 is a murine tumor rejection antigen: induction of “self”-reactive, tumoricidal T cells using high-affinity, altered peptide ligand. J Exp Med 1998; 188:277-86; PMID:9670040; http://dx.doi.org/10.1084/jem.188.2.277
  • Overwijk WW, Restifo NP. B16 as a mouse model for human melanoma. Curr Protoc Immunol 2001; Chapter 20:Unit 20 1; PMID:18432774; http://dx.doi.org/10.1002/0471142735.im2001s39
  • Vacchelli E, Eggermont A, Fridman WH, Galon J, Zitvogel L, Kroemer G, Galluzzi L. Trial Watch: Immunostimulatory cytokines. Oncoimmunology 2013; 2:e24850; PMID:24073369; http://dx.doi.org/10.4161/onci.24850
  • Aranda F, Vacchelli E, Eggermont A, Galon J, Sautes-Fridman C, Tartour E, Zitvogel L, Kroemer G, Galluzzi L. Trial Watch: Peptide vaccines in cancer therapy. Oncoimmunology 2013; 2:e26621; PMID:24498550; http://dx.doi.org/10.4161/onci.26621
  • Aranda F, Vacchelli E, Obrist F, Eggermont A, Galon J, Herve Fridman W, Cremer I, Tartour E, Zitvogel L, Kroemer G et al. Trial Watch: Adoptive cell transfer for anticancer immunotherapy. Oncoimmunology 2014; 3:e28344; PMID:25050207; http://dx.doi.org/10.4161/onci.28344
  • Topalian SL, Hodi FS, Brahmer JR, Gettinger SN, Smith DC, McDermott DF, Powderly JD, Carvajal RD, Sosman JA, Atkins MB et al. Safety, activity, and immune correlates of anti-PD-1 antibody in cancer. N Engl J Med 2012; 366:2443-54; PMID:22658127; http://dx.doi.org/10.1056/NEJMoa1200690
  • Nigatu AS, Vupputuri S, Flynn N, Neely BJ, Ramsey JD. Evaluation of cell-penetrating peptide/adenovirus particles for transduction of CAR-negative cells. J Pharm Sci 2013; 102:1981-93; PMID:23592439; http://dx.doi.org/10.1002/jps.23556
  • Heath WR, Carbone FR. Cross-presentation in viral immunity and self-tolerance. Nat Rev Immunol 2001; 1:126-34; PMID:11905820; http://dx.doi.org/10.1038/35100512
  • Joffre OP, Segura E, Savina A, Amigorena S. Cross-presentation by dendritic cells. Nat Rev Immunol 2012; 12:557-69; PMID:22790179; http://dx.doi.org/10.1038/nri3254
  • Ma X, Serna A, Xu RH, Sigal LJ. The amino acid sequences flanking an antigenic determinant can strongly affect MHC class I cross-presentation without altering direct presentation. J Immunol 2009; 182:4601-7; PMID:19342634; http://dx.doi.org/10.4049/jimmunol.0803806
  • Capasso C, Garofalo M, Hirvinen M, Cerullo V. The evolution of adenoviral vectors through genetic and chemical surface modifications. Viruses 2014; 6:832-55; PMID:24549268; http://dx.doi.org/10.3390/v6020832
  • Wonganan P, Croyle MA. PEGylated Adenoviruses: From Mice to Monkeys. Viruses 2010; 2:468-502; PMID:21994645; http://dx.doi.org/10.3390/v2020468
  • Clapp T, Siebert P, Chen D, Jones Braun L. Vaccines with aluminum-containing adjuvants: optimizing vaccine efficacy and thermal stability. J Pharm Sci 2011; 100:388-401; PMID:20740674; http://dx.doi.org/10.1002/jps.22284
  • Li KY, Peers-Adams A, Win SJ, Scullion S, Wilson M, Young VL, Jennings P, Ward VK, Baird MA, Young SL. Antigen Incorporated In Virus-like Particles Is Delivered to Specific Dendritic Cell Subsets That Induce An Effective Antitumor Immune Response In Vivo. J Immunother 2013; 36:11-9; PMID:23211625; http://dx.doi.org/10.1097/CJI.0b013e3182787f5e
  • Matsushita H, Vesely MD, Koboldt DC, Rickert CG, Uppaluri R, Magrini VJ, Arthur CD, White JM, Chen YS, Shea LK et al. Cancer exome analysis reveals a T-cell-dependent mechanism of cancer immunoediting. Nature 2012; 482:400-4; PMID:22318521; http://dx.doi.org/10.1038/nature10755
  • Andersen BM, Ohlfest JR. Increasing the efficacy of tumor cell vaccines by enhancing cross priming. Cancer Lett 2012; 325:155-64; PMID:22809568; http://dx.doi.org/10.1016/j.canlet.2012.07.012
  • Walter S, Weinschenk T, Stenzl A, Zdrojowy R, Pluzanska A, Szczylik C, Staehler M, Brugger W, Dietrich PY, Mendrzyk R et al. Multipeptide immune response to cancer vaccine IMA901 after single-dose cyclophosphamide associates with longer patient survival. Nat Med 2012; 18(8):1254-61; PMID:22842478; http://dx.doi.org/10.1038/nm.2883
  • Carretero R, Romero JM, Ruiz-Cabello F, Maleno I, Rodriguez F, Camacho FM, Real LM, Garrido F, Cabrera T. Analysis of HLA class I expression in progressing and regressing metastatic melanoma lesions after immunotherapy. Immunogenetics 2008; 60:439-47; PMID:18545995; http://dx.doi.org/10.1007/s00251-008-0303-5
  • Ito H, Aoki H, Kuhnel F, Kondo Y, Kubicka S, Wirth T, Iwado E, Iwamaru A, Fujiwara K, Hess KR et al. Autophagic cell death of malignant glioma cells induced by a conditionally replicating adenovirus. J Natl Cancer Inst 2006; 98:625-36; PMID:16670388; http://dx.doi.org/10.1093/jnci/djj161
  • Liikanen I, Ahtiainen L, Hirvinen ML, Bramante S, Cerullo V, Nokisalmi P, Hemminki O, Diaconu I, Pesonen S, Koski A et al. Oncolytic adenovirus with temozolomide induces autophagy and antitumor immune responses in cancer patients. Mol Ther 2013; 21:1212-23; PMID:23546299; http://dx.doi.org/10.1038/mt.2013.51
  • Biosynthesis. Peptide Property Calculator Version 3.1. 612 East Main Street Lewisville, TX 75057 Bio-Synthesis Inc.
  • Kanerva A, Zinn KR, Chaudhuri TR, Lam JT, Suzuki K, Uil TG, Hakkarainen T, Bauerschmitz GJ, Wang M, Liu B et al. Enhanced therapeutic efficacy for ovarian cancer with a serotype 3 receptor-targeted oncolytic adenovirus. Mol Ther 2003; 8:449-58; PMID:12946318; http://dx.doi.org/10.1016/S1525-0016(03)00200-4