Tumor-infiltrating myeloid cells induce tumor cell resistance to cytotoxic T cells in mice

Journal of Clinical Investigation

Volumn 121, Issue 10, 2011, Pages 4015-4029

  Lu, Tangying ^a   Ramakrishnan, Rupal ^a   Altiok, Soner ^a   Youn, Je In ^a   Cheng, Pingyan ^a   Celis, Esteban ^a   Pisarev, Vladimir ^b,c   Sherman, Simon ^b   Sporn, Michael B ^d   Gabrilovich, Dmitry ^a  

^a H LEE MOFFITT CANCER CENTER AND RESEARCH INSTITUTE   (United States)

^b UNIVERSITY OF NEBRASKA MEDICAL CENTER   (United States)

^c RESEARCH CENTRE FOR MEDICAL GENETICS   (Russian Federation)

^d DARTMOUTH MEDICAL SCHOOL   (United States)

Author keywords

[No Author keywords available]

Indexed keywords

INTERLEUKIN 1BETA; PEROXYNITRITE;

ANIMAL CELL; ANIMAL EXPERIMENT; ANIMAL MODEL; ANIMAL TISSUE; ARTICLE; BONE MARROW CELL; BREAST CANCER; CELL INFILTRATION; CELL SURFACE; CELL VIABILITY; CYTOTOXIC T LYMPHOCYTE; HUMAN; HUMAN CELL; HUMAN TISSUE; INFLAMMATION; LUNG CANCER; MOUSE; NONHUMAN; PANCREAS CANCER; PRIORITY JOURNAL; PROTEIN EXPRESSION; PROTEIN PROCESSING; SUPPRESSOR CELL; TUMOR CELL;

ANIMALS; CARCINOMA, LEWIS LUNG; CELL LINE, TUMOR; FEMALE; HUMANS; INFLAMMATION MEDIATORS; INTERLEUKIN-1BETA; LYMPHOCYTES, TUMOR-INFILTRATING; MALE; MICE; MICE, INBRED C57BL; MICE, KNOCKOUT; MICE, TRANSGENIC; MOLSIDOMINE; MYELOID CELLS; NEOPLASMS, EXPERIMENTAL; PEROXYNITROUS ACID; T-LYMPHOCYTES, CYTOTOXIC; TUMOR ESCAPE;

EID: 80053421470     PISSN: 00219738     EISSN: 15588238     Source Type: Journal    
DOI: 10.1172/JCI45862     Document Type: Article

References (53)

1. Jandus C, Speiser D, Romero P. Recent advances and hurdles in melanoma immunotherapy. Pigment Cell Melanoma Res. 2009;22(6):711-723.
2. Lasaro MO, Ertl HC. Targeting inhibitory pathways in cancer immunotherapy. Curr Opin Immunol. 2010;22(3):385-390.
3. Sarnaik AA, Weber JS. Recent advances using anti- CTLA-4 for the treatment of melanoma. Cancer J. 2009;15(3):169-173.
4. Muranski P, Restifo NP. Adoptive immunotherapy of cancer using CD4(+) T cells. Curr Opin Immunol. 2009;21(2):200-208.
5. Rosenberg SA, Dudley ME. Adoptive cell therapy for the treatment of patients with metastatic melanoma. Curr Opin Immunol. 2009;21(2):233-240.
6. Gabrilovich DI, Hurwitz A, eds. Tumor Induced Immune Suppression: Mechanisms and Therapeutic Reversal. New York, New York, USA: Springer- Verlag; 2007.
7. Safwat A. The immunobiology of low-dose totalbody irradiation: more questions than answers. Radiat Res. 2000;153(5 pt 1):599-604. (Pubitemid 30252609)
8. Paulos CM, et al. Toll-like receptors in tumor immunotherapy. Clin Cancer Res. 2007;13(18 pt 1):5280-5289. (Pubitemid 47510351)
9. Coussens LM, Werb Z. Inflammation and cancer. Nature. 2002;420(6917):860-867. (Pubitemid 36019639)
10. Gabrilovich DI, Nagaraj S. Myeloid-derived suppressor cells as regulators of the immune system. Nat Rev Immunol. 2009;9(3):162-174.
11. Alvarez B, Radi R. Peroxynitrite reactivity with amino acids and proteins. Amino Acids. 2003; 25(3-4):295-311. (Pubitemid 38041267)
12. Vickers SM, MacMillan-Crow LA, Green M, Ellis C, Thompson JA. Association of increased immunostaining for inducible nitric oxide synthase and nitrotyrosine with fibroblast growth factor transformation in pancreatic cancer. Arch Surg. 1999; 134(3):245-251. (Pubitemid 29136006)
13. Cobbs CS, Whisenhunt TR, Wesemann DR, Harkins LE, van Meir EG, Samanta M. Inactivation of wild-type p53 protein function by reactive oxygen and nitrogen species in malignant glioma cells. Cancer Res. 2003;63(24):8670-8673. (Pubitemid 38064042)
14. Bentz BG, Haines GK 3rd, Radosevich JA. Increased protein nitrosylation in head and neck squamous cell carcinogenesis. Head Neck. 2000;22(1):64-70. (Pubitemid 30030671)
15. Kinnula VL, et al. Ultrastructural and chromosomal studies on manganese superoxide dismutase in malignant mesothelioma. Am J Respir Cell Mol Biol. 2004;31(2):147-153. (Pubitemid 39095444)
16. Kojima M, et al. Nitric oxide synthase expression and nitric oxide production in human colon carcinoma tissue. J Surg Oncol. 1999;70(4):222-229. (Pubitemid 29187907)
17. Nakamura Y, et al. Nitric oxide in breast cancer: induction of vascular endothelial growth factor-C and correlation with metastasis and poor prognosis. Clin Cancer Res. 2006;12(4):1201-1207. (Pubitemid 43342509)
18. Ekmekcioglu S, Ellerhorst J, Prieto V, Johnson M, Broemeling L, Grimm EA. Early detection and diagnosis tumor iNOS predicts poor survival for stage III melanoma patients. Int J Cancer. 2005;119(4):861-866. (Pubitemid 44051450)
19. Ahmed B, van Den Oord JJ. Expression of the inducible isoform of nitric oxide synthase in pigment cell lesions of the skin. Br J Dermatol. 2000; 142(3):432-440. (Pubitemid 30159063)
20. Masri FA, et al. Abnormalities in nitric oxide and its derivatives in lung cancer. Am J Respir Crit Care Med. 2005;172(5):597-605. (Pubitemid 41232971)
21. Vakkala M, Kahlos K, Lakari E, Paakko P, Kinnula V, Soini Y. Inducible nitric oxide synthase expression, apoptosis, and angiogenesis in in situ and invasive breast carcinomas. Clin Cancer Res. 2000; 6(6):2408-2416. (Pubitemid 30399209)
22. Rotondo R, et al. Arginase 2 is expressed by human lung cancer, but it neither induces immune suppression, nor affects disease progression. Int J Cancer. 2008;123(5):1108-1116.
23. Kono K, et al. Hydrogen peroxide secreted by tumor-derived macrophages down-modulates signal-transducing zeta molecules and inhibits tumor-specific T cell-and natural killer cell-mediated cytotoxicity. Eur J Immunol. 1996;26(6):1308-1313.
24. Aoe T, Okamoto Y, Saito T. Activated macrophages induce structural abnormalities of the T cell receptor- CD3 complex. J Exp Med. 1995;181(5):1881-1886.
25. Otsuji M, Kimura Y, Aoe T, Okamoto Y, Saito T. Oxidative stress by tumor-derived macrophages suppresses the expression of CD3 zeta chain of T-cell receptor complex and antigen-specific T-cell responses. Proc Natl Acad Sci U S A. 1996;93(23):13119-13124. (Pubitemid 26382779)
26. Schmielau J, Finn OJ. Activated granulocytes and granulocyte-derived hydrogen peroxide are the underlying mechanism of suppression of T-cell function in advanced cancer patients. Cancer Res. 2001; 61(12):4756-4760. (Pubitemid 32691887)
27. Bronte V, et al. Boosting antitumor responses of T lymphocytes infiltrating human prostate cancers. J Exp Med. 2005;201(8):1257-1268. (Pubitemid 40629069)
28. Nagaraj S, et al. Altered recognition of antigen is a novel mechanism of CD8+ T cell tolerance in cancer Nat Med. 2007;13(7):828-835. (Pubitemid 47038194)
29. Birnboim HC, Lemay AM, Lam DK, Goldstein R, Webb JR. Cutting edge: MHC class II-restricted peptides containing the inflammation-associated marker 3-nitrotyrosine evade central tolerance and elicit a robust cell-mediated immune response. J Immunol. 2003;171(2):528-532. (Pubitemid 36871356)
30. Hardy LL, Wick DA, Webb JR. Conversion of tyrosine to the inflammation-associated analog 3′-nitrotyrosine at either TCR- or MHC-contact positions can profoundly affect recognition of the MHC class Irestricted epitope of lymphocytic choriomeningitis virus glycoprotein 33 by CD8 T cells. J Immunol. 2008;180(9):5956-5962.
31. Overwijk WW, et al. Tumor regression and autoimmunity after reversal of a functionally tolerant state of self-reactive CD8+ T cells. J Exp Med. 2003;198(4):569-580. (Pubitemid 37040391)
32. Pisarev V, Yu B, Salup R, Sherman S, Altieri DC, Gabrilovich DI. Full-length dominant-negative survivin for cancer immunotherapy. Clin Cancer Res. 2003;9(17):6523-6533. (Pubitemid 38031841)
33. Wang B, et al. A single peptide-MHC complex positively selects a diverse and specific CD8 T cell repertoire. Science. 2009;326(5954):871-874.
34. Kusmartsev S, Nagaraj S, Gabrilovich DI. Tumor-associated CD8+ T cell tolerance induced by bone marrow-derived immature myeloid cells. J Immunol. 2005;175(7):4583-4592. (Pubitemid 41361997)
35. Splettstoesser WD, Schuff-Werner P. Oxidative stress in phagocytes - "the enemy within". Microsc Res Tech. 2002;57(6):441-455. (Pubitemid 34701145)
36. Corzo CA, et al. Mechanism regulating reactive oxygen species in tumor-induced myeloid-derived suppressor cells. J Immunol. 2009;182(9):5693- 5701.
37. Nagaraj S, et al. Anti-inflammatory triterpenoid blocks immune suppressive function of myeloid-derived suppressor cells and improves immune response in cancer. Clin Cancer Res. 2010; 16(6):1812-1823.
38. Dummer W, et al. T cell homeostatic proliferation elicits effective antitumor autoimmunity. J Clin Invest. 2002;110(2):185-192. (Pubitemid 34787355)
39. Wrzesinski C, et al. Increased intensity lymphodepletion enhances tumor treatment efficacy of adoptively transferred tumor-specific T cells. J Immunother. 2010;33(1):1-7.
40. Cho HI, Lee YR, Celis E. Interferon gamma limits the effectiveness of melanoma peptide vaccines. Blood. 2011;117(1):135-144.
41. Kusmartsev S, Nefedova Y, Yoder D, Gabrilovich DI. Antigen-specific inhibition of CD8+ T cell response by immature myeloid cells in cancer is mediated by reactive oxygen species. J Immunol. 2004; 172(2):989-999. (Pubitemid 38113758)
42. Lechner M, Lirk P, Rieder J. Inducible nitric oxide synthase (iNOS) in tumor biology: the two sides of the same coin. Semin Cancer Biol. 2005;15(4):277-289. (Pubitemid 41058773)
43. Bogdan C. Nitric oxide and the immune response. Nat Immunol. 2001;2(10):907-916. (Pubitemid 32976162)
44. Doedens AL, et al. Macrophage expression of hypoxia-inducible factor-1 alpha suppresses T-cell function and promotes tumor progression. Cancer Res. 2010;70(19):7465-7475.
45. Corzo CA, et al. HIF-1α regulates function and differentiation of myeloid-derived suppressor cells in the tumor microenvironment. J Exp Med. 2010; 207(11):2439-2453.
46. Apte RN, Voronov E. Is interleukin-1 a good or bad 'guy' in tumor immunobiology and immunotherapy? Immunol Rev. 2008;222:222-241. (Pubitemid 351430377)
47. Bunt SK, Sinha P, Clements VK, Leips J, Ostrand- Rosenberg S. Inflammation induces myeloidderived suppressor cells that facilitate tumor progression. J Immunol. 2006;176(1):284-290. (Pubitemid 43023273)
48. Liby KT, Yore MM, Sporn MB. Triterpenoids and rexinoids as multifunctional agents for the prevention and treatment of cancer. Nat Rev Cancer. 2007; 7(5):357-369. (Pubitemid 46652485)
49. Dinkova-Kostova AT, et al. Extremely potent triterpenoid inducers of the phase 2 response: correlations of protection against oxidant and inflammatory stress. Proc Natl Acad Sci U S A. 2005;102(12):4584-4589. (Pubitemid 40397155)
50. Yates MS, et al. Potent protection against aflatoxin-induced tumorigenesis through induction of Nrf2- regulated pathways by the triterpenoid 1-[2-cyano- 3-,12-dioxooleana-1,9(11)-dien-28-oyl]imidazole. Cancer Res. 2006;66(4):2488-2494.
51. Cho HI, Lee YR, Celis E. Interferon gamma limits the effectiveness of melanoma peptide vaccines. Blood. 2011;117(1):135-144.
52. Porgador A, Yewdell JW, Deng Y, Bennink JR, Germain RN. Localization, quantitation, and in situ detection of specific peptide-MHC class I complexes using a mAb. Immunity. Immunity. 1997;6(6):715.
53. Honda T, Rounds BV, Gribble GW, Suh N, Wang Y, Sporn MB. Design and synthesis of 2-cyano- 3,12-dioxoolean-1,9-dien-28-oic acid, a novel and highly active inhibitor of nitric oxide production in mouse macrophages. Bioorg Med Chem Lett. 1998; 8(19):2711-2714. (Pubitemid 28496657)