Inhibition of HIF-1α enhances anti-tumor effects of dendritic cell-based vaccination in a mouse model of breast cancer

Cancer Immunology, Immunotherapy

Volumn 65, Issue 10, 2016, Pages 1159-1167

  Kheshtchin, Nasim ^a   Arab, Samaneh ^b   Ajami, Maryam ^c   Mirzaei, Reza ^a   Ashourpour, Mahboubeh ^b   Mousavi, Neda ^d   Khosravianfar, Najmeh ^b   Jadidi Niaragh, Farhad ^b,d,e   Namdar, Afshin ^a   Noorbakhsh, Farshid ^a   Hadjati, Jamshid ^a  

^a TEHRAN UNIVERSITY OF MEDICAL SCIENCES   (Iran)

^b TEHRAN UNIVERSITY OF MEDICAL SCIENCES   (Iran)

^c TARBIAT MODARES UNIVERSITY   (Iran)

^d TABRIZ UNIVERSITY OF MEDICAL SCIENCES   (Iran)

^e TABRIZ UNIVERSITY OF MEDICAL SCIENCES   (Iran)

Author keywords

Cancer; Dendritic cell based immunotherapy; HIF 1 ; Hypoxia

Indexed keywords

4 [BIS(2 CHLOROETHYL)OXIDOAMINO]PHENYLALANINE; DENDRITIC CELL VACCINE; GAMMA INTERFERON; GRANZYME B; HYPOXIA INDUCIBLE FACTOR 1ALPHA; INTERLEUKIN 10; INTERLEUKIN 17; MESSENGER RNA; TRANSCRIPTION FACTOR FOXP3; VASCULOTROPIN; 2-AMINO-3-(4'-N,N-BIS(2-CHLOROETHYL)AMINO)PHENYLPROPIONIC ACID N-OXIDE; ANTINEOPLASTIC AGENT; CANCER VACCINE; FORKHEAD TRANSCRIPTION FACTOR; FOXP3 PROTEIN, MOUSE; HIF1A PROTEIN, MOUSE; MUSTARD GAS DERIVATIVE; PHENYLPROPIONIC ACID DERIVATIVE; VASCULOTROPIN A;

ANIMAL CELL; ANIMAL EXPERIMENT; ANIMAL MODEL; ANTINEOPLASTIC ACTIVITY; ARTICLE; BREAST CANCER; CANCER COMBINATION CHEMOTHERAPY; CANCER IMMUNIZATION; CANCER INHIBITION; CANCER REGRESSION; CANCER SURVIVAL; CD8+ T LYMPHOCYTE; CONTROLLED STUDY; CYTOKINE PRODUCTION; CYTOKINE RELEASE; CYTOTOXIC T LYMPHOCYTE; FEMALE; IN VIVO STUDY; LYMPHOCYTE FUNCTION; LYMPHOCYTE PROLIFERATION; MOUSE; NONHUMAN; PRIORITY JOURNAL; PROTEIN EXPRESSION; REGULATORY T LYMPHOCYTE; ADOPTIVE IMMUNOTHERAPY; ANIMAL; ANTAGONISTS AND INHIBITORS; BAGG ALBINO MOUSE; BREAST NEOPLASMS; CELL CULTURE; CELL PROLIFERATION; DENDRITIC CELL; GENETICS; HUMAN; IMMUNOLOGY; MAMMARY NEOPLASMS, ANIMAL; METABOLISM; MULTIMODALITY CANCER THERAPY; PROCEDURES; TRANSPLANTATION; TUMOR VOLUME;

ANIMALS; ANTINEOPLASTIC AGENTS; BREAST NEOPLASMS; CANCER VACCINES; CELL PROLIFERATION; CELLS, CULTURED; COMBINED MODALITY THERAPY; DENDRITIC CELLS; FEMALE; FORKHEAD TRANSCRIPTION FACTORS; HUMANS; HYPOXIA-INDUCIBLE FACTOR 1, ALPHA SUBUNIT; IMMUNOTHERAPY, ADOPTIVE; INTERFERON-GAMMA; MAMMARY NEOPLASMS, ANIMAL; MICE; MICE, INBRED BALB C; MUSTARD COMPOUNDS; PHENYLPROPIONATES; T-LYMPHOCYTES, CYTOTOXIC; TUMOR BURDEN; VASCULAR ENDOTHELIAL GROWTH FACTOR A;

EID: 84982972109     PISSN: 03407004     EISSN: 14320851     Source Type: Journal    
DOI: 10.1007/s00262-016-1879-5     Document Type: Article

References (31)

1. Brown JM, Wilson WR (2004) Exploiting tumour hypoxia in cancer treatment. Nat Rev Cancer 4:437–447
2. Rabinovich GA, Gabrilovich D, Sotomayor EM (2007) Immunosuppressive strategies that are mediated by tumor cells. Annu Rev Immunol 25:267–296
3. Facciabene A, Peng X, Hagemann IS, Balint K, Barchetti A, Wang LP et al (2011) Tumour hypoxia promotes tolerance and angiogenesis via CCL28 and T(reg) cells. Nature 475:226–230
4. Sitkovsky M, Lukashev D (2005) Regulation of immune cells by local-tissue oxygen tension: HIF1α and adenosine receptors. Nat Rev Immunol 5:712–721
5. Noman MZ, Benlalam H, Hasmim M, Chouaib S (2011) Cytotoxic T cells–stroma interactions. Bull Cancer 98:E19–E24
6. Noman MZ, Janji B, Kaminska B, Van Moer K, Pierson S, Przanowski P et al (2011) Blocking hypoxia-induced autophagy in tumors restores cytotoxic T-cell activity and promotes regression. Cancer Res 71:5976–5986
7. Noman MZ, Messai Y, Carre T, Akalay I, Meron M, Janji B et al (2011) Microenvironmental hypoxia orchestrating the cell stroma cross talk, tumor progression and antitumor response. Crit Rev Immunol 31:357–377
8. Semenza GL (2003) Targeting HIF-1 for cancer therapy. Nat Rev Cancer 3:721–732
9. Shi YH, Fang WG (2004) Hypoxia-inducible factor-1 in tumour angiogenesis. World J Gastroenterol 10:1082–1087
10. Semenza GL (2010) Defining the role of hypoxia-inducible factor 1 in cancer biology and therapeutics. Oncogene 29:625–634
11. Kim JW, Gao P, Dang CV (2007) Effects of hypoxia on tumor metabolism. Cancer Metastasis Rev 26:291–298
12. Wilson WR, Hay MP (2011) Targeting hypoxia in cancer therapy. Nat Rev Cancer 11:393–410
13. Koh MY, Spivak-Kroizman T, Venturini S, Welsh S, Williams RR, Kirkpatrick DL et al (2008) Molecular mechanisms for the activity of PX-478, an antitumor inhibitor of the hypoxia-inducible factor-1alpha. Mol Cancer Ther 7:90–100
14. Macpherson GR, Figg WD (2004) Small molecule-mediated anti-cancer therapy via hypoxia-inducible factor-1 blockade. Cancer Biol Ther 3:503–504
15. Welsh S, Williams R, Kirkpatrick L, Paine-Murrieta G, Powis G (2004) Antitumor activity and pharmacodynamic properties of PX-478, an inhibitor of hypoxia-inducible factor-1alpha. Mol Cancer Ther 3:233–244
16. Inaba K, Inaba M, Naito M, Steinman RM (1993) Dendritic cell progenitors phagocytose particulates, including bacillus Calmette-Guerin organisms, and sensitize mice to mycobacterial antigens in vivo. J Exp Med 178:479–488
17. Shi LZ, Wang R, Huang G, Vogel P, Neale G, Green DR et al (2011) HIF1α–dependent glycolytic pathway orchestrates a metabolic checkpoint for the differentiation of T H 17 and T reg cells. J Exp Med 208:1367–1376
18. Clambey ET, McNamee EN, Westrich JA, Glover LE, Campbell EL, Jedlicka P et al (2012) Hypoxia-inducible factor-1 alpha-dependent induction of FoxP3 drives regulatory T-cell abundance and function during inflammatory hypoxia of the mucosa. Proc Natl Acad Sci U S A 109:E2784–E2793
19. Takenaga K (2011) Angiogenic signaling aberrantly induced by tumor hypoxia. Front Biosci (Landmark Ed) 16:31–48
20. Noman MZ, Buart S, Van Pelt J, Richon C, Hasmim M, Leleu N et al (2009) The cooperative induction of hypoxia-inducible factor-1 alpha and STAT3 ring hypoxia induced an impairment of tumor susceptibility to CTL-mediated cell lysis. J Immunol 182:3510–3521
21. Eltzschig HK, Ibla JC, Furuta GT, Leonard MO, Jacobson KA, Enjyoji K et al (2003) Coordinated adenine nucleotide phosphohydrolysis and nucleoside signaling in posthypoxic endothelium: role of ectonucleotidases and adenosine A2B receptors. J Exp Med 198:783–796
22. Deaglio S, Dwyer KM, Gao W, Friedman D, Usheva A, Erat A et al (2007) Adenosine generation catalyzed by CD39 and CD73 expressed on regulatory T cells mediates immune suppression. J Exp Med 204:1257–1265
23. Zarek PE, Huang CT, Lutz ER, Kowalski J, Horton MR, Linden J et al (2008) A2A receptor signaling promotes peripheral tolerance by inducing T-cell anergy and the generation of adaptive regulatory T cells. Blood 111:251–259
24. Noman MZ, Desantis G, Janji B, Hasmim M, Karray S, Dessen P et al (2014) PD-L1 is a novel direct target of HIF-1, and its blockade under hypoxia enhanced MDSC-mediated T cell activation. J Exp Med 211:781–790
25. Caldwell CC, Kojima H, Lukashev D, Armstrong J, Farber M, Apasov SG et al (2001) Differential effects of physiologically relevant hypoxic conditions on T lymphocyte development and effector functions. J Immunol 167:6140–6149
26. Doedens AL, Phan AT, Stradner MH, Fujimoto JK, Nguyen JV, Yang E et al (2013) Hypoxia-inducible factors enhance the effector responses of CD8 + T cells to persistent antigen. Nat Immunol 14:1173–1182
27. Barsoum IB, Smallwood CA, Siemens DR, Graham CH (2014) A mechanism of hypoxia-mediated escape from adaptive immunity in cancer cells. Cancer Res 74:665–674
28. Noman MZ, Buart S, Romero P, Ketari S, Janji B, Mari B et al (2012) Hypoxia-inducible miR-210 regulates the susceptibility of tumor cells to lysis by cytotoxic T cells. Cancer Res 72:4629–4641
29. Thiel M, Caldwell CC, Kreth S, Kuboki S, Chen P, Smith P et al (2007) Targeted deletion of HIF-1alpha gene in T cells prevents their inhibition in hypoxic inflamed tissues and improves septic mice survival. PLoS ONE 2:e853
30. Sitkovsky MV (2009) T regulatory cells: hypoxia-adenosinergic suppression and re-direction of the immune response. Trends Immunol 30:102–108
31. Helft J, Böttcher J, Chakravarty P, Zelenay S, Huotari J et al (2015) GM-CSF mouse bone marrow cultures comprise a heterogeneous population of CD11c + MHCII + Macrophages and Dendritic Cells. Immunity 42:1197–1211