951
Views
10
CrossRef citations to date
0
Altmetric
Author's View

Radiation therapy combined with Listeria monocytogenes-based cancer vaccine synergize to enhance tumor control in the B16 melanoma model

, , &
Article: e29028 | Received 11 Mar 2014, Accepted 26 Apr 2014, Published online: 03 Jun 2014

References

  • Hodge JW, Garnett CT, Farsaci B, Palena C, Tsang KY, Ferrone S, Gameiro SR. Chemotherapy-induced immunogenic modulation of tumor cells enhances killing by cytotoxic T lymphocytes and is distinct from immunogenic cell death. Int J Cancer 2013; 133:624 - 36; http://dx.doi.org/10.1002/ijc.28070; PMID: 23364915
  • Zitvogel L, Galluzzi L, Smyth MJ, Kroemer G. Mechanism of action of conventional and targeted anticancer therapies: reinstating immunosurveillance. Immunity 2013; 39:74 - 88; http://dx.doi.org/10.1016/j.immuni.2013.06.014; PMID: 23890065
  • Lee Y, Auh SL, Wang Y, Burnette B, Wang Y, Meng Y, Beckett M, Sharma R, Chin R, Tu T, et al. Therapeutic effects of ablative radiation on local tumor require CD8+ T cells: changing strategies for cancer treatment. Blood 2009; 114:589 - 95; http://dx.doi.org/10.1182/blood-2009-02-206870; PMID: 19349616
  • Shiao SL, Coussens LM. The tumor-immune microenvironment and response to radiation therapy. J Mammary Gland Biol Neoplasia 2010; 15:411 - 21; http://dx.doi.org/10.1007/s10911-010-9194-9; PMID: 21161342
  • Takeshima T, Chamoto K, Wakita D, Ohkuri T, Togashi Y, Shirato H, Kitamura H, Nishimura T. Local radiation therapy inhibits tumor growth through the generation of tumor-specific CTL: its potentiation by combination with Th1 cell therapy. Cancer Res 2010; 70:2697 - 706; http://dx.doi.org/10.1158/0008-5472.CAN-09-2982; PMID: 20215523
  • Perez CA, Fu A, Onishko H, Hallahan DE, Geng L. Radiation induces an antitumour immune response to mouse melanoma. Int J RadiatBiol 2009; 85:1126 - 36; http://dx.doi.org/10.3109/09553000903242099; PMID: 19995238
  • Lugade AA, Sorensen EW, Gerber SA, Moran JP, Frelinger JG, Lord EM. Radiation-induced IFN-gamma production within the tumor microenvironment influences antitumor immunity. J Immunol 2008; 180:3132 - 9; http://dx.doi.org/10.4049/jimmunol.180.5.3132; PMID: 18292536
  • Santin AD, Hermonat PL, Ravaggi A, Chiriva-Internati M, Pecorelli S, Parham GP. Radiation-enhanced expression of E6/E7 transforming oncogenes of human papillomavirus-16 in human cervical carcinoma. Cancer 1998; 83:2346 - 52; http://dx.doi.org/10.1002/(SICI)1097-0142(19981201)83:11<2346::AID-CNCR14>3.0.CO;2-G; PMID: 9840534
  • Sharma A, Bode B, Wenger RH, Lehmann K, Sartori AA, Moch H, Knuth A, Boehmer Lv, Broek Mv. γ-Radiation promotes immunological recognition of cancer cells through increased expression of cancer-testis antigens in vitro and in vivo. PLoS One 2011; 6:e28217; http://dx.doi.org/10.1371/journal.pone.0028217; PMID: 22140550
  • Reits EA, Hodge JW, Herberts CA, Groothuis TA, Chakraborty M, Wansley EK, Camphausen K, Luiten RM, de Ru AH, Neijssen J, et al. Radiation modulates the peptide repertoire, enhances MHC class I expression, and induces successful antitumor immunotherapy. J Exp Med 2006; 203:1259 - 71; http://dx.doi.org/10.1084/jem.20052494; PMID: 16636135
  • Lugade AA, Moran JP, Gerber SA, Rose RC, Frelinger JG, Lord EM. Local radiation therapy of B16 melanoma tumors increases the generation of tumor antigen-specific effector cells that traffic to the tumor. J Immunol 2005; 174:7516 - 23; http://dx.doi.org/10.4049/jimmunol.174.12.7516; PMID: 15944250
  • Apetoh L, Ghiringhelli F, Tesniere A, Obeid M, Ortiz C, Criollo A, Mignot G, Maiuri MC, Ullrich E, Saulnier P, et al. Toll-like receptor 4-dependent contribution of the immune system to anticancer chemotherapy and radiotherapy. Nat Med 2007; 13:1050 - 9; http://dx.doi.org/10.1038/nm1622; PMID: 17704786
  • Wei S, Egenti MU, Teitz-Tennenbaum S, Zou W, Chang AE. Effects of tumor irradiation on host T-regulatory cells and systemic immunity in the context of adoptive T-cell therapy in mice. J Immunother 2013; 36:124 - 32; http://dx.doi.org/10.1097/CJI.0b013e31828298e6; PMID: 23377667
  • Billiard F, Buard V, Benderitter M, Linard C. Abdominal γ-radiation induces an accumulation of function-impaired regulatory T cells in the small intestine. Int J RadiatOncolBiolPhys 2011; 80:869 - 76; http://dx.doi.org/10.1016/j.ijrobp.2010.12.041; PMID: 21345609
  • Klug F, Prakash H, Huber PE, Seibel T, Bender N, Halama N, Pfirschke C, Voss RH, Timke C, Umansky L, et al. Low-dose irradiation programs macrophage differentiation to an iNOS⁺/M1 phenotype that orchestrates effective T cell immunotherapy. Cancer Cell 2013; 24:589 - 602; http://dx.doi.org/10.1016/j.ccr.2013.09.014; PMID: 24209604
  • Fenton BM, Lord EM, Paoni SF. Effects of radiation on tumor intravascular oxygenation, vascular configuration, development of hypoxia, and clonogenic survival. Radiat Res 2001; 155:360 - 8; http://dx.doi.org/10.1667/0033-7587(2001)155[0360:EOROTI]2.0.CO;2; PMID: 11175672
  • Barcellos-Hoff MH, Park C, Wright EG. Radiation and the microenvironment - tumorigenesis and therapy. Nat Rev Cancer 2005; 5:867 - 75; http://dx.doi.org/10.1038/nrc1735; PMID: 16327765
  • Park HJ, Griffin RJ, Hui S, Levitt SH, Song CW. Radiation-induced vascular damage in tumors: implications of vascular damage in ablative hypofractionated radiotherapy (SBRT and SRS). Radiat Res 2012; 177:311 - 27; http://dx.doi.org/10.1667/RR2773.1; PMID: 22229487
  • Formenti SC, Demaria S. Systemic effects of local radiotherapy. Lancet Oncol 2009; 10:718 - 26; http://dx.doi.org/10.1016/S1470-2045(09)70082-8; PMID: 19573801
  • Crittenden MR, Savage T, Cottam B, Bahjat KS, Redmond WL, Bambina S, Kasiewicz M, Newell P, Jackson AM, Gough MJ. The peripheral myeloid expansion driven by murine cancer progression is reversed by radiation therapy of the tumor. PLoS One 2013; 8:e69527; http://dx.doi.org/10.1371/journal.pone.0069527; PMID: 23936036
  • Seung SK, Curti B, Crittenden M, Urba W. Radiation and immunotherapy: Renewed allies in the war on cancer. Oncoimmunology 2012; 1:1645 - 7; http://dx.doi.org/10.4161/onci.21746; PMID: 23264923
  • Burnette B, Fu YX, Weichselbaum RR. The confluence of radiotherapy and immunotherapy. Front Oncol 2012; 2:143; http://dx.doi.org/10.3389/fonc.2012.00143; PMID: 23087904
  • Demaria S, Bhardwaj N, McBride WH, Formenti SC. Combining radiotherapy and immunotherapy: a revived partnership. Int J RadiatOncolBiolPhys 2005; 63:655 - 66; http://dx.doi.org/10.1016/j.ijrobp.2005.06.032; PMID: 16199306
  • Kalbasi A, June CH, Haas N, Vapiwala N. Radiation and immunotherapy: a synergistic combination. J Clin Invest 2013; 123:2756 - 63; http://dx.doi.org/10.1172/JCI69219; PMID: 23863633
  • Seung SK, Curti BD, Crittenden M, Walker E, Coffey T, Siebert JC, Miller W, Payne R, Glenn L, Bageac A, et al. Phase 1 study of stereotactic body radiotherapy and interleukin-2--tumor and immunological responses. SciTransl Med 2012; 4:37ra74; http://dx.doi.org/10.1126/scitranslmed.3003649; PMID: 22674552
  • Younes E, Haas GP, Dezso B, Ali E, Maughan RL, Kukuruga MA, Montecillo E, Pontes JE, Hillman GG. Local tumor irradiation augments the response to IL-2 therapy in a murine renal adenocarcinoma. Cell Immunol 1995; 165:243 - 51; http://dx.doi.org/10.1006/cimm.1995.1211; PMID: 7553889
  • Seetharam S, Staba MJ, Schumm LP, Schreiber K, Schreiber H, Kufe DW, Weichselbaum RR. Enhanced eradication of local and distant tumors by genetically produced interleukin-12 and radiation. Int J Oncol 1999; 15:769 - 73; PMID: 10493960
  • Lim JY, Gerber SA, Murphy SP, Lord EM. Type I interferons induced by radiation therapy mediate recruitment and effector function of CD8 T cells. Cancer ImmunolImmunother 2014; 63:259 - 71; PMID: 24357146
  • Mason KA, Ariga H, Neal R, Valdecanas D, Hunter N, Krieg AM, Whisnant JK, Milas L. Targeting toll-like receptor 9 with CpGoligodeoxynucleotides enhances tumor response to fractionated radiotherapy. Clin Cancer Res 2005; 11:361 - 9; PMID: 15671567
  • Chakravarty PK, Alfieri A, Thomas EK, Beri V, Tanaka KE, Vikram B, Guha C. Flt3-ligand administration after radiation therapy prolongs survival in a murine model of metastatic lung cancer. Cancer Res 1999; 59:6028 - 32; PMID: 10626784
  • Chen Z, Xia D, Bi X, Saxena A, Sidhu N, El-Gayed A, Xiang J. Combined radiation therapy and dendritic cell vaccine for treating solid tumors with liver micro-metastasis. J Gene Med 2005; 7:506 - 17; http://dx.doi.org/10.1002/jgm.692; PMID: 15580588
  • Jung S, Unutmaz D, Wong P, Sano G, De los Santos K, Sparwasser T, Wu S, Vuthoori S, Ko K, Zavala F, et al. In vivo depletion of CD11c+ dendritic cells abrogates priming of CD8+ T cells by exogenous cell-associated antigens. Immunity 2002; 17:211 - 20; http://dx.doi.org/10.1016/S1074-7613(02)00365-5; PMID: 12196292
  • Hamon M, Bierne H, Cossart P. Listeria monocytogenes: a multifaceted model. Nat Rev Microbiol 2006; 4:423 - 34; http://dx.doi.org/10.1038/nrmicro1413; PMID: 16710323
  • Brockstedt DG, Giedlin MA, Leong ML, Bahjat KS, Gao Y, Luckett W, Liu W, Cook DN, Portnoy DA, Dubensky TW Jr.. Listeria-based cancer vaccines that segregate immunogenicity from toxicity. ProcNatlAcadSci U S A 2004; 101:13832 - 7; http://dx.doi.org/10.1073/pnas.0406035101; PMID: 15365184
  • Starks H, Bruhn KW, Shen H, Barry RA, Dubensky TW, Brockstedt D, Hinrichs DJ, Higgins DE, Miller JF, Giedlin M, et al. Listeria monocytogenes as a vaccine vector: virulence attenuation or existing antivector immunity does not diminish therapeutic efficacy. J Immunol 2004; 173:420 - 7; http://dx.doi.org/10.4049/jimmunol.173.1.420; PMID: 15210801
  • Le DT, Brockstedt DG, Nir-Paz R, Hampl J, Mathur S, Nemunaitis J, Sterman DH, Hassan R, Lutz E, Moyer B, et al. A live-attenuated Listeria vaccine (ANZ-100) and a live-attenuated Listeria vaccine expressing mesothelin (CRS-207) for advanced cancers: phase I studies of safety and immune induction. Clin Cancer Res 2012; 18:858 - 68; http://dx.doi.org/10.1158/1078-0432.CCR-11-2121; PMID: 22147941
  • DungT. Le AW-G, Vincent Picozzi, Jr, Tim F. Greten, Todd S. Crocenzi, Gregory M. Springett, Michael Morse, Herbert Zeh, Deirdre Jill Cohen, Robert Lance Fine, Beth Onners, Jennifer N. Uram, Dan Laheru, Aimee Murphy, Justin Skoble, Ed Lemmens, John J. Grous, Thomas Dubensky, Dirk G. Brockstedt, Elizabeth M. Jaffee. A phase 2, randomized trial of GVAX pancreas and CRS-207 immunotherapy versus GVAX alone in patients with metastatic pancreatic adenocarcinoma: Updated results. 2014 ASCO Gastrointestinal Cancers Symposium. San Francisco, CA, 2014.
  • Kline J, Zhang L, Battaglia L, Cohen KS, Gajewski TF. Cellular and molecular requirements for rejection of B16 melanoma in the setting of regulatory T cell depletion and homeostatic proliferation. J Immunol 2012; 188:2630 - 42; http://dx.doi.org/10.4049/jimmunol.1100845; PMID: 22312128
  • Hannan R, Zhang H, Wallecha A, Singh R, Liu L, Cohen P, Alfieri A, Rothman J, Guha C. Combined immunotherapy with Listeria monocytogenes-based PSA vaccine and radiation therapy leads to a therapeutic response in a murine model of prostate cancer. Cancer ImmunolImmunother 2012; 61:2227 - 38; http://dx.doi.org/10.1007/s00262-012-1257-x; PMID: 22644735
  • Kärre K, Ljunggren HG, Piontek G, Kiessling R. Selective rejection of H-2-deficient lymphoma variants suggests alternative immune defence strategy. Nature 1986; 319:675 - 8; http://dx.doi.org/10.1038/319675a0; PMID: 3951539
  • Anfossi N, André P, Guia S, Falk CS, Roetynck S, Stewart CA, Breso V, Frassati C, Reviron D, Middleton D, et al. Human NK cell education by inhibitory receptors for MHC class I. Immunity 2006; 25:331 - 42; http://dx.doi.org/10.1016/j.immuni.2006.06.013; PMID: 16901727
  • Ljunggren HG, Kärre K. In search of the ‘missing self’: MHC molecules and NK cell recognition. Immunol Today 1990; 11:237 - 44; http://dx.doi.org/10.1016/0167-5699(90)90097-S; PMID: 2201309
  • Formenti SC, Demaria S. Radiation therapy to convert the tumor into an in situ vaccine. Int J RadiatOncolBiolPhys 2012; 84:879 - 80; http://dx.doi.org/10.1016/j.ijrobp.2012.06.020; PMID: 23078897
  • Brown JM, Koong AC. High-dose single-fraction radiotherapy: exploiting a new biology?. Int J RadiatOncolBiolPhys 2008; 71:324 - 5; http://dx.doi.org/10.1016/j.ijrobp.2008.02.003; PMID: 18474308
  • Chang JY, Liu YH, Zhu Z, Welsh JW, Gomez DR, Komaki R, Roth JA, Swisher SG. Stereotactic ablative radiotherapy: a potentially curable approach to early stage multiple primary lung cancer. Cancer 2013; 119:3402 - 10; http://dx.doi.org/10.1002/cncr.28217; PMID: 23798353
  • Fidler IJ. Selection of successive tumour lines for metastasis. Nat New Biol 1973; 242:148 - 9; http://dx.doi.org/10.1038/newbio242148a0; PMID: 4512654
  • Brown DM, Fisher TL, Wei C, Frelinger JG, Lord EM. Tumours can act as adjuvants for humoral immunity. Immunology 2001; 102:486 - 97; http://dx.doi.org/10.1046/j.1365-2567.2001.01213.x; PMID: 11328383
  • Sorensen EW, Gerber SA, Frelinger JG, Lord EM. IL-12 suppresses vascular endothelial growth factor receptor 3 expression on tumor vessels by two distinct IFN-gamma-dependent mechanisms. J Immunol 2010; 184:1858 - 66; http://dx.doi.org/10.4049/jimmunol.0903210; PMID: 20061409
  • Gerber SA, Pober JS. IFN-alpha induces transcription of hypoxia-inducible factor-1alpha to inhibit proliferation of human endothelial cells. J Immunol 2008; 181:1052 - 62; http://dx.doi.org/10.4049/jimmunol.181.2.1052; PMID: 18606657
  • Gerber SA, Sorensen EW, Sedlacek AL, Lim JY, Skrombolas D, Frelinger JG, Lord EM. Local expression of interleukin-2 by B16 melanoma cells results in decreased tumour growth and long-term tumour dormancy. Immunology 2013; 138:280 - 92; http://dx.doi.org/10.1111/imm.12037; PMID: 23198850

Reprints and Corporate Permissions

Please note: Selecting permissions does not provide access to the full text of the article, please see our help page How do I view content?

To request a reprint or corporate permissions for this article, please click on the relevant link below:

Academic Permissions

Please note: Selecting permissions does not provide access to the full text of the article, please see our help page How do I view content?

Obtain permissions instantly via Rightslink by clicking on the button below:

If you are unable to obtain permissions via Rightslink, please complete and submit this Permissions form. For more information, please visit our Permissions help page.