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

OncoImmunology

Volumn 3, Issue 6, 2014, Pages

  Lim, Joanne Y H ^a   Brockstedt, Dirk G ^b   Lord, Edith M ^a   Gerber, Scott A ^a  

^a UNIVERSITY OF ROCHESTER MEDICAL CENTER   (United States)

^b Aduro BioTech Inc   (United States)

Author keywords

Anti tumor immune response; B16 melanoma; Immunotherapy; Listeria monocytogenes based vaccine; Radiation therapy

Indexed keywords

CANCER VACCINE; GAMMA INTERFERON; GRANZYME B; LISTERIA MONOCYTOGENES OVALBUMIN CANCER VACCINE; OKT 8; OVALBUMIN; UNCLASSIFIED DRUG;

ADAPTIVE IMMUNITY; ANIMAL CELL; ANIMAL EXPERIMENT; ANIMAL MODEL; ANIMAL TISSUE; ARTICLE; CANCER CONTROL; CANCER GROWTH; CANCER IMMUNOTHERAPY; CANCER INHIBITION; CANCER RADIOTHERAPY; CD8+ T LYMPHOCYTE; CONTROLLED STUDY; DRUG EFFICACY; FEMALE; IMMUNE RESPONSE; LISTERIA MONOCYTOGENES; LYMPHOCYTE PROLIFERATION; MELANOMA; MOUSE; NATURAL KILLER CELL; NONHUMAN; RADIATION DOSE; T LYMPHOCYTE ACTIVATION;

EID: 84906500190     PISSN: 21624011     EISSN: 2162402X     Source Type: Journal    
DOI: 10.4161/onci.29028     Document Type: Article

References (50)

1. 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 Cancer2013; 133:624-36; PMID:23364915; http://dx.doi. org/10.1002/ijc.28070
2. Zitvoge IL, Galluzzi L, Smyth MJ, Kroemer G. Mechanism of action of conventional and targeted anticancer therapies: reinstating immunosurveillance. Immunity2013; 39:74-88; PMID:23890065; http://dx.doi.org/10.1016/j.immuni.2013.06.014
3. 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. Blood2009; 114:589-95; PMID:19349616; http://dx.doi.org/10.1182/blood-2009-02-206870
4. Shiao SL, Coussens LM. The tumor-immune microenvironment and response to radiation therapy.J Mammary Gland Biol Neoplasia2010; 15:411-21; PMID:21161342; http://dx.doi.org/10.1007/ s10911-010-9194-9
5. 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 Res2010; 70:2697-706; PMID:20215523; http://dx.doi. org/10.1158/0008-5472.CAN-09-2982
6. Perez CA, Fu A, Onishko H, Hallahan DE, Geng L. Radiation induces an antitumour immune response to mouse melanoma.Int J RadiatBiol2009; 85:1126-36; PMID:19995238; http://dx.doi. org/10.3109/09553000903242099
7. Lugade AA, Sorensen EW, Gerber SA, Moran JP, Frelinger JG, Lord EM. Radiation-induced IFNgamma production within the tumor microenvironment influences antitumor immunity.J Immunol2008; 180:3132-9; PMID:18292536; http://dx.doi.org/10.4049/jimmunol.180.5.3132
8. Santin AD, Hermonat PL, Ravaggi A, Chiriva-Internati M, Pecorelli S, Parham GP. Radiationenhanced expression of E6/E7 transforming oncogenes of human papillomavirus-16 in human cervical carcinoma.Cancer1998; 83:2346-52; PMID:9840534; http://dx.doi.org/10.1002/ (SICI)1097-0142(19981201)83:11<2346::AIDCNCR14> 3.0.CO;2-G
9. 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 One2011; 6:e28217; PMID:22140550; http://dx.doi. org/10.1371/journal.pone.0028217
10. 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 Med2006; 203:1259-71; PMID:16636135; http://dx.doi.org/10.1084/ jem.20052494
11. 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 Immunol2005; 174:7516-23; PMID:15944250; http://dx.doi.org/10.4049/ jimmunol.174.12.7516
12. 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 Med2007; 13:1050-9; PMID:17704786; http://dx.doi. org/10.1038/nm1622
13. 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 Immunother2013; 36:124-32; PMID:23377667; http://dx.doi.org/10.1097/CJI.0b013e31828298e6
14. 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 Radiat Oncol Biol Phys2011; 80:869-76; PMID:21345609; http://dx.doi.org/10.1016/j. ijrobp.2010.12.041
15. 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 Cell2013; 24:589-602; PMID:24209604; http://dx.doi.org/10.1016/j.ccr.2013.09.014
16. Fenton BM, Lord EM, Paoni SF. Effects of radiation on tumor intravascular oxygenation, vascular configuration, development of hypoxia, and clonogenic survival.Radiat Res2001; 155:360-8; PMID:11175672; http://dx.doi. org/10.1667/0033-7587(2001)155[0360:EOROTI] 2.0.CO;2
17. Barcellos-Hoff MH, Park C, Wright EG. Radiation and the microenvironment - tumorigenesis and therapy. Nat Rev Cancer2005; 5:867-75; PMID:16327765; http://dx.doi.org/10.1038/nrc1735
18. 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 Res2012; 177:311-27; PMID:22229487; http:// dx.doi.org/10.1667/RR2773.1
19. Formenti SC, Demaria S. Systemic effects of local radiotherapy.Lancet Oncol2009; 10:718-26; PMID:19573801; http://dx.doi.org/10.1016/ S1470-2045(09)70082-8
20. 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 One2013; 8:e69527; PMID:23936036; http:// dx.doi.org/10.1371/journal.pone.0069527
21. Seung SK, Curti B, Crittenden M, Urba W. Radiation and immunotherapy: Renewed allies in the war on cancer.Oncoimmunology2012; 1:1645-7; PMID:23264923; http://dx.doi.org/10.4161/ onci.21746
22. Burnette B, Fu YX, Weichselbaum RR. The confluence of radiotherapy and immunotherapy.Front Oncol2012; 2:143; PMID:23087904; http://dx.doi. org/10.3389/fonc.2012.00143
23. Demaria S, Bhardwaj N, McBride WH, Formenti SC. Combining radiotherapy and immunotherapy: a revived partnership.Int J RadiatOncolBiolPhys2005; 63:655-66; PMID:16199306; http://dx.doi. org/10.1016/j.ijrobp.2005.06.032
24. Kalbasi A, June CH, Haas N, Vapiwala N. Radiation and immunotherapy: a synergistic combination.J Clin Invest2013; 123:2756-63; PMID:23863633; http://dx.doi.org/10.1172/JCI69219
25. 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 Med2012; 4:37ra74; PMID:22674552; http://dx.doi.org/10.1126/scitranslmed.3003649
26. 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 Immunol1995; 165:243-51; PMID:7553889; http:// dx.doi.org/10.1006/cimm.1995.1211
27. 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 Oncol1999; 15:769-73; PMID:10493960
28. 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 ImmunolImmunother2014;63:259-71 PMID:24357146
29. 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 Res2005; 11:361-9; PMID:15671567
30. 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 Res1999; 59:6028-32; PMID:10626784
31. 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 Med2005; 7:506-17; PMID:15580588; http://dx.doi.org/10.1002/ jgm.692
32. 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.Immunity2002; 17:211-20; PMID:12196292; http://dx.doi.org/10.1016/ S1074-7613(02)00365-5
33. Hamon M, Bierne H, Cossart P. Listeria monocytogenes: a multifaceted model.Nat Rev Microbiol2006; 4:423-34; PMID:16710323; http://dx.doi. org/10.1038/nrmicro1413
34. 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 A2004; 101:13832-7; PMID:15365184; http://dx.doi.org/10.1073/ pnas.0406035101
35. 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 Immunol2004; 173:420-7; PMID:15210801; http://dx.doi.org/10.4049/ jimmunol.173.1.420
36. 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 Res2012; 18:858-68; PMID:22147941; http://dx.doi.org/10.1158/1078-0432.CCR-11-2121
37. Dung T. 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.
38. 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 Immunol2012; 188:2630-42; PMID:22312128; http://dx.doi.org/10.4049/jimmunol.1100845
39. Hannan R, Zhang H, Wallecha A, Singh R, Liu L, Cohen P, Alfieri A, Rothman J, Guha C. Combined immunotherapy with Listeria monocytogenesbased PSA vaccine and radiation therapy leads to a therapeutic response in a murine model of prostate cancer.Cancer ImmunolImmunother2012; 61:2227-38; PMID:22644735; http://dx.doi.org/10.1007/ s00262-012-1257-x
40. Kärre K, Ljunggren HG, Pionte kG, Kiessling R. Selective rejection of H-2-deficient lymphoma variants suggests alternative immune defence strategy. Nature1986; 319:675-8; PMID:3951539; http:// dx.doi.org/10.1038/319675a0
41. 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.Immunity2006; 25:331-42; PMID:16901727; http://dx.doi. org/10.1016/j.immuni.2006.06.013
42. Ljunggren HG, Kärre K. In search of the 'missing self ': MHC molecules and NK cell recognition.Immunol Today1990; 11:237-44; PMID:2201309; http:// dx.doi.org/10.1016/0167-5699(90)90097-S
43. Formenti SC, Demaria S. Radiation therapy to convert the tumor into an in situ vaccine. Int J RadiatOncolBiolPhys2012; 84:879-80; PMID:23078897; http://dx.doi.org/10.1016/j. ijrobp.2012.06.020
44. Brown JM, Koong AC. High-dose single-fraction radiotherapy: exploiting a new biology?Int J RadiatOncolBiolPhys2008; 71:324-5; PMID:18474308; http://dx.doi.org/10.1016/j. ijrobp.2008.02.003
45. 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.Cancer2013; 119:3402-10; PMID:23798353; http://dx.doi. org/10.1002/cncr.28217
46. Fidler IJ. Selection of successive tumour lines for metastasis.Nat New Biol1973; 242:148-9; PMID:4512654; http://dx.doi.org/10.1038/ newbio242148a0
47. Brown DM, Fisher TL, Wei C, Frelinger JG, Lord EM. Tumours can act as adjuvants for humoral immunity. Immunology2001; 102:486-97; PMID:11328383; http://dx.doi.org/10.1046/j.1365-2567.2001.01213.x
48. 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 Immunol2010; 184:1858-66; PMID:20061409; http://dx.doi.org/10.4049/jimmunol.0903210
49. GerberSA, PoberJS. IFN-alpha induces transcription of hypoxia-inducible factor-1alpha to inhibit proliferation of human endothelial cells.J Immunol2008; 181:1052-62; PMID:18606657; http://dx.doi. org/10.4049/jimmunol.181.2.1052
50. 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.Immunology2013; 138:280-92; PMID:23198850; http://dx.doi.org/10.1111/ imm.12037