Systemic tolerance mediated by melanoma brain tumors is reversible by radiotherapy and vaccination

Clinical Cancer Research

Volumn 22, Issue 5, 2016, Pages 1161-1172

  Jackson, Christopher M ^a   Kochel, Christina M ^a   Nirschl, Christopher J ^a   Durham, Nicholas M ^a,e   Ruzevick, Jacob ^a   Alme, Angela ^a   Francica, Brian J ^a   Elias, Jimmy ^a   Daniels, Andrew ^a   Dubensky, Thomas W ^b   Lauer, Peter ^b   Brockstedt, Dirk G ^b   Baxi, Emily G ^c   Calabresi, Peter A ^c   Taube, Janis M ^a,c   Pardo, Carlos A ^c   Brem, Henry ^a,d   Pardoll, Drew M ^a   Lim, Michael ^a   Drake, Charles G ^a,f  

^a JOHNS HOPKINS UNIVERSITY   (United States)

^b Aduro BioTech Inc   (United States)

^c JOHNS HOPKINS UNIVERSITY SCHOOL OF MEDICINE   (United States)

^d Johns Hopkins University   (United States)

^e MEDIMMUNE   (United States)

^f JOHNS HOPKINS UNIVERSITY   (United States)

Author keywords

[No Author keywords available]

Indexed keywords

CANCER ANTIBODY; CD3 ANTIBODY; CYTOKINE; MELANOMA ANTIGEN; MONOCLONAL ANTIBODY; OVALBUMIN; TRANSFORMING GROWTH FACTOR BETA; TUMOR ANTIGEN;

ADOPTIVE TRANSFER; ANIMAL CELL; ANIMAL EXPERIMENT; ANIMAL MODEL; ANIMAL TISSUE; ANTIGEN SPECIFICITY; ARTICLE; BRAIN METASTASIS; BRAIN TUMOR; CANCER GROWTH; CANCER IMMUNIZATION; CANCER IMMUNOTHERAPY; CANCER RADIOTHERAPY; CANCER SURVIVAL; CD8+ T LYMPHOCYTE; CEREBROSPINAL FLUID; CONTROLLED STUDY; CYTOTOXICITY; EFFECTOR CELL; FEMALE; FLOW CYTOMETRY; IMMUNE RESPONSE; IMMUNOCHEMISTRY; IMMUNOLOGICAL TOLERANCE; IMMUNOPHENOTYPING; IN VIVO STUDY; LISTERIA MONOCYTOGENES; MELANOMA; MELANOMA B16; MICROGLIA; MOUSE; NONHUMAN; PATHOLOGY; PRIORITY JOURNAL; REGULATORY T LYMPHOCYTE; TUMOR CELL INOCULATION; TUMOR GROWTH; TUMOR LOCALIZATION; TUMOR REGRESSION; TUMOR VOLUME; ANIMAL; ANTAGONISTS AND INHIBITORS; BLOOD; BRAIN NEOPLASMS; CENTRAL NERVOUS SYSTEM NEOPLASMS; CYTOTOXIC T LYMPHOCYTE; HUMAN; IMMUNOLOGY; MELANOMA, EXPERIMENTAL; RADIATION RESPONSE; VACCINATION;

ANIMALS; ANTIGENS, NEOPLASM; BRAIN NEOPLASMS; CD8-POSITIVE T-LYMPHOCYTES; CENTRAL NERVOUS SYSTEM NEOPLASMS; FEMALE; HUMANS; IMMUNE TOLERANCE; MELANOMA, EXPERIMENTAL; MICE; MICROGLIA; T-LYMPHOCYTES, CYTOTOXIC; TRANSFORMING GROWTH FACTOR BETA; VACCINATION;

EID: 84962218955     PISSN: 10780432     EISSN: 15573265     Source Type: Journal    
DOI: 10.1158/1078-0432.CCR-15-1516     Document Type: Article

References (55)

1. Patchell RA. The management of brain metastases. Cancer Treat Rev 2003;29:533-40.
2. Jackson CM, Lim M, Drake CG. Immunotherapy for brain cancer: recent progress and future promise. Clin Cancer Res 2014;20:3651-9.
3. Ellsworth S, Balmanoukian A, Kos F, Nirschl CJ, Nirschl TR, Grossman SA, et al. Sustained CD4(+) T cell-driven lymphopenia without a compensatory IL-7/IL-15 response among high-grade glioma patients treated with radiation and temozolomide. Oncoimmunology 2014;3:e27357.
4. Grossman SA, Ye X, Lesser G, Sloan A, Carraway H, Desideri S, et al. Immunosuppression in patients with high-grade gliomas treated with radiation and temozolomide. Clin Cancer Res 2011;17:5473-80.
5. Ransohoff RM, Kivisäkk P, Kidd G. Three or more routes for leukocyte migration into the central nervous system. Nat Rev Immunol 2003; 3:569-81.
6. Ransohoff RM, Brown MA. Innate immunity in the central nervous system. J Clin Invest 2012;122:1164-71.
7. Biollaz G, Bernasconi L, Cretton C, Püntener U, Frei K, Fontana A, et al. Sitespecific anti-tumor immunity: differences in DC function, TGF-b production and numbers of intratumoral Foxp3+ Treg. Eur J Immunol 2009;39:1323-33.
8. Seliger B, Wollscheid U, Momburg F, Blankenstein T, Huber C. Characterization of the major histocompatibility complex class I deficiencies in B16 melanoma cells. Cancer Res 2001;61:1095-9.
9. Zeng J, See AP, Phallen J, Jackson CM, Belcaid Z, Ruzevick J, et al. Anti- PD-1 blockade and stereotactic radiation produce long-term survival in mice with intracranial gliomas. Int J Radiat Oncol Biol Phys 2013; 86:343-9.
10. Andrews DW, Scott CB, Sperduto PW, Flanders AE, Gaspar LE, Schell MC, et al. Whole brain radiation therapy with or without stereotactic radiosurgery boost for patients with one to three brain metastases: phase III results of the RTOG 9508 randomised trial. Lancet 2004; 363:1665-72.
11. Lauer P, Chow MYN, Loessner MJ, Portnoy DA, Calendar R. Construction, characterization, and use of two Listeria monocytogenes site-specific phage integration vectors. J Bacteriol 2002;184:4177-86.
12. Hirano F, Kaneko K, Tamura H, Dong H, Wang S, Ichikawa M, et al. Blockade of B7-H1 and PD-1 by monoclonal antibodies potentiates cancer therapeutic immunity. Cancer Res 2005;65:1089-96.
13. Oehen S, Brduscha-Riem K. Differentiation of naive CTL to effector and memory CTL: correlation of effector function with phenotype and cell division. J Immunol 1998;161:5338-46.
14. Staveley-O'Carroll K, Sotomayor E, Montgomery J, Borrello I, Hwang L, Fein S, et al. Induction of antigen-specific T cell anergy: an early event in the course of tumor progression. Proc Natl Acad Sci U S A 1998; 95:1178-83.
15. Overwijk WW, Tsung A, Irvine KR, Parkhurst MR, Goletz TJ, Tsung K, 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.
16. Dobrzanski MJ, Reome JB, Hollenbaugh JA, Dutton RW. Tc1 and Tc2 effector cell therapy elicit long-term tumor immunity by contrasting mechanisms that result in complementary endogenous type 1 antitumor responses. J Immunol 2004;172:1380-90.
17. Louveau A, Smirnov I, Keyes TJ, Eccles JD, Rouhani SJ, Peske JD, et al. Structural and functional features of central nervous system lymphatic vessels. Nature 2015;523:337-41.
18. Ransohoff RM, Cardona AE. The myeloid cells of the central nervous system parenchyma. Nature 2010;468:253-62.
19. Blattman JN, Antia R, Sourdive DJD, Wang X, Kaech SM, Murali-Krishna K, et al. Estimating the precursor frequency of naive antigen-specific CD8 T cells. J Exp Med 2002;195:657-64.
20. Brockstedt DG, Bahjat KS, Giedlin MA, Liu W, Leong M, Luckett W, et al. Killed but metabolically active microbes: a new vaccine paradigm for eliciting effector T-cell responses and protective immunity. Nat Med 2005;11:853-60.
21. Jakowlew SB. Transforming growth factor-β in cancer and metastasis. Cancer Metastasis Rev 2006;25:435-57.
22. Diaz-Valdes N, Basagoiti M, Dotor J, Aranda F, Monreal I, Riezu-Boj JI, et al. Induction of monocyte chemoattractant protein-1 and interleukin-10 by TGF 1 in melanoma enhances tumor infiltration and immunosuppression. Cancer Res 2011;71:812-21.
23. Bueno L, de Alwis DP, Pitou C, Yingling J, Lahn M, Glatt S, et al. Semimechanistic modelling of the tumour growth inhibitory effects of LY2157299, a new type I receptor TGF-beta kinase antagonist, in mice. Eur J Cancer 2008;44:142-50.
24. Curiel TJ. Regulatory T cells and treatment of cancer. Curr Opin Immunol 2008;20:241-6.
25. Persa E, Balogh A, Sáfrány G, Lumniczky K. The effect of ionizing radiation on regulatory T cells in health and disease. Cancer Lett 2015; 368:252-61.
26. Weide B, Richter S, Büttner P, Leiter U, Forschner A, Bauer J, et al. Serum S100B, lactate dehydrogenase and brain metastasis are prognostic factors in patients with distant melanoma metastasis and systemic therapy. Soyer HP, editor. PLoS One 2013;8:e81624.
27. Ma MW, Qian M, Lackaye DJ, Berman RS, Shapiro RL, Pavlick AC, et al. Challenging the current paradigm of melanoma progression: brain metastasis as isolated first visceral site. Neuro Oncol 2012;14:849-58.
28. Na S-Y, Hermann A, Sanchez-Ruiz M, Storch A, Deckert M, Hünig T. Oligodendrocytes enforce immune tolerance of the uninfected brain by purging the peripheral repertoire of autoreactive CD8+ T cells. Immunity 2012;37:134-46.
29. Lesniak MS, Gabikian P, Tyler BM, Pardoll DM, Brem H. Dexamethasone mediated inhibition of local IL-2 immunotherapy is dose dependent in experimental brain tumors. J Neurooncol 2004;70:23-8.
30. Gros A, Robbins PF, Yao X, Li YF, Turcotte S, Tran E, et al. PD-1 identifies the patient-specific CD8+ tumor-reactive repertoire infiltrating human tumors. J Clin Invest 2014;124:2246-59.
31. Gabrilovich DI,Ostrand-Rosenberg S, Bronte V. Coordinated regulation of myeloid cells by tumours. Nat Rev Immunol 2012;12:253-68.
32. Komohara Y, Ohnishi K, Kuratsu J, Takeya M. Possible involvement of the M2 anti-inflammatory macrophage phenotype in growth of human gliomas. J Pathol 2008;216:15-24.
33. Massagué J. TGFβ signalling in context. Nat Rev Mol Cell Biol 2012; 13:616-30.
34. Zhou X, Spittau B, Krieglstein K. TGFb signalling plays an important role in IL4-induced alternative activation of microglia. J Neuroinflammation 2012;9:210.
35. Young KH, Newell P, Cottam B, Friedman D, Savage T, Baird JR, et al. TGF inhibition prior to hypofractionated radiation enhances efficacy in preclinical models. Cancer Immunol Res 2014;2:1011-22.
36. Jia W, Jackson-Cook C, Graf MR. Tumor-infiltrating, myeloid-derived suppressor cells inhibit T cell activity by nitric oxide production in an intracranial rat glioma + vaccination model. J Neuroimmunol 2010; 223:20-30.
37. Yoshimura K, Jain A, Allen HE, Laird LS, Chia CY, Ravi S, et al. Selective targeting of antitumor immune responses with engineered live-attenuated Listeria monocytogenes. Cancer Res 2006;66:1096-104.
38. Pan ZK, Ikonomidis G, Lazenby A, Pardoll D, Paterson Y. A recombinant Listeria monocytogenes vaccine expressing a model tumour antigen protects mice against lethal tumour cell challenge and causes regression of established tumours. Nat Med 1995;1:471-7.
39. Maciag PC, Radulovic S, Rothman J. The first clinical use of a liveattenuated Listeria monocytogenes vaccine: a phase I safety study of Lm-LLO-E7 in patients with advanced carcinoma of the cervix. Vaccine 2009;27:3975-83.
40. Le DT, Brockstedt DG, Nir-Paz R, Hampl J, Mathur S, Nemunaitis J, 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.
41. Prins RM, Bruhn KW, Craft N, Lin JW, Kim C-H, Odesa SK, et al. Central nervous system tumor immunity generated by a recombinant listeria monocytogenes vaccine targeting tyrosinase related protein-2 and realtime imaging of intracranial tumor burden. Neurosurgery 2006;58: 169-78.
42. Drake CG. Molecular determinants of radiation Response. In:DeWeese TL, Laiho M, editors. New York, NY: Springer New York; 2011. p. 251-63.
43. Postow MA, Callahan MK, Barker CA, Yamada Y, Yuan J, Kitano S, et al. Immunologic correlates of the abscopal effect in a patient with melanoma. N Engl J Med 2012;366:925-31.
44. Parker JJ, Jones JC, Strober S, Knox SJ. Characterization of direct radiationinduced immune function and molecular signaling changes in an antigen presenting cell line. Clin Immunol 2013;148:44-55.
45. Demaria S, Ng B, Devitt ML, Babb JS, Kawashima N, Liebes L, et al. Ionizing radiation inhibition of distant untreated tumors (abscopal effect) is immune mediated. Int J Radiat Oncol Biol Phys 2004;58:862-70.
46. Demaria S, Kawashima N, Yang AM, Devitt ML, Babb JS, Allison JP, et al. Immune-mediated inhibition of metastases after treatment with local radiation and CTLA-4 blockade in a mouse model of breast cancer. Clin Cancer Res 2005;11:728-34.
47. Newcomb EW, Demaria S, Lukyanov Y, Shao Y, Schnee T, Kawashima N, et al. The combination of ionizing radiation and peripheral vaccination produces long-term survival of mice bearing established invasive GL261 gliomas. Clin Cancer Res 2006;12:4730-7.
48. Curran MA, Montalvo W, Yagita H, Allison JP. PD-1 and CTLA-4 combination blockade expands infiltrating T cells and reduces regulatory T and myeloid cells within B16 melanoma tumors. Proc Natl Acad Sci 2010; 107:4275-80.
49. Tarhini AA, Edington H, Butterfield LH, Lin Y, Shuai Y, Tawbi H, et al. Immune monitoring of the circulation and the tumor microenvironment in patients with regionally advanced melanoma receiving neoadjuvant ipilimumab. Chatenoud L, editor. PLoS One 2014;9:e87705.
50. Rizvi NA, Hellmann MD, Snyder A, Kvistborg P, Makarov V, Havel JJ, et al. Cancer immunology. Mutational landscape determines sensitivity to PD-1 blockade in non-small cell lung cancer. Science 2015;348:124-8.
51. Perret R, Sierro SR, Botelho NK, Corgnac S, Donda A, Romero P. Adjuvants that improve the ratio of antigen-specific effector to regulatory T cells enhance tumor immunity. Cancer Res 2013;73:6597-608.
52. Formenti SC, Demaria S. Systemic effects of local radiotherapy. Lancet Oncol 2009;10:718-26.
53. Li B, Simmons A, Du T, Lin C, Moskalenko M, Gonzalez-Edick M, et al. Allogeneic GM-CSF-secreting tumor cell immunotherapies generate potent anti-tumor responses comparable to autologous tumor cell immunotherapies. Clin Immunol 2009;133:184-97.
54. Hodi FS, O'Day SJ, McDermott DF, Weber RW, Sosman JA, Haanen JB, et al. Improved survival with ipilimumab in patients withmetastatic melanoma. N Engl J Med 2010;363:711-23.
55. Gibney GT, Kudchadkar RR, DeConti RC, Thebeau MS, Czupryn MP, Tetteh L, et al. Safety, correlative markers, and clinical results of adjuvant nivolumab in combination with vaccine in resected high-risk metastatic melanoma. Clin Cancer Res 2015;21:712-20.