Inherent and tumor-driven immune tolerance in the prostate microenvironment impairs natural killer cell antitumor activity

Cancer Research

Volumn 76, Issue 8, 2016, Pages 2153-2165

  Pasero, Christine ^a,b   Gravis, Gwenaëlle ^b   Guerin, Mathilde ^b   Granjeaud, Samuel ^a   Thomassin Piana, Jeanne ^b   Rocchi, Palma ^a,b   Paciencia Gros, Maria ^b   Poizat, Flora ^b   Bentobji, Mélanie ^b   Azario Cheillan, Francine ^b   Walz, Jochen ^b   Salem, Naji ^b   Brunelle, Serge ^b   Moretta, Alessandro ^c   Olive, Daniel ^a,b,d  

^a AIX MARSEILLE UNIVERSITY   (France)

^b INSTITUT PAOLI CALMETTES   (France)

^c UNIVERSITY OF GENOA   (Italy)

^d AIX MARSEILLE UNIVERSITY   (France)

Author keywords

[No Author keywords available]

Indexed keywords

CD16 ANTIGEN; CD56 ANTIGEN; NATURAL CYTOTOXICITY TRIGGERING RECEPTOR 1; NATURAL KILLER CELL RECEPTOR NKG2D; PROSTATE SPECIFIC ANTIGEN; PROTEIN ILT2; PROTEIN LILRB1; TRANSFORMING GROWTH FACTOR BETA1; TUMOR PROTEIN; UNCLASSIFIED DRUG; CYTOKINE;

AGED; ANTINEOPLASTIC ACTIVITY; ARTICLE; CANCER PROGNOSIS; CANCER TISSUE; CELL MEDIATED CYTOTOXICITY; CELLULAR IMMUNITY; CLINICAL ARTICLE; COCULTURE; CONTROLLED STUDY; DOWN REGULATION; HUMAN; HUMAN CELL; HUMAN TISSUE; IMMUNOLOGICAL TOLERANCE; IMMUNOPHENOTYPING; LYMPHOCYTIC INFILTRATION; MALE; MOLECULAR RECOGNITION; NATURAL KILLER CELL; PRIORITY JOURNAL; PROSTATE CANCER CELL LINE; PROSTATE TUMOR; TUMOR MICROENVIRONMENT; CYTOTOXICITY; IMMUNOLOGY; METABOLISM; METASTASIS; PATHOLOGY; PROSPECTIVE STUDY; TUMOR CELL LINE;

CELL LINE, TUMOR; CYTOKINES; CYTOTOXICITY, IMMUNOLOGIC; HUMANS; IMMUNE TOLERANCE; KILLER CELLS, NATURAL; MALE; NEOPLASM METASTASIS; PROSPECTIVE STUDIES; PROSTATIC NEOPLASMS; TUMOR MICROENVIRONMENT;

EID: 84971006847     PISSN: 00085472     EISSN: 15387445     Source Type: Journal    
DOI: 10.1158/0008-5472.CAN-15-1965     Document Type: Article

References (49)

1. Jemal A, Murray T, Ward E, Samuels A, Tiwari RC, Ghafoor A, et al. Cancer statistics, 2005. CA Cancer J Clin 2005;55:10-30.
2. May KFJr, Gulley JL, Drake CG, Dranoff G, Kantoff PW. Prostate cancer immunotherapy. Clin Cancer Res 2011;17:5233-8.
3. Fridman WH, Pages F, Sautes-Fridman C, Galon J. The immune contexture in human tumours: impact on clinical outcome. Nat Rev Cancer 2012;12:298-306.
4. Vivier E, Tomasello E, Baratin M, Walzer T, Ugolini S. Functions of natural killer cells. Nat Immunol 2008;9:503-10.
5. Guerra N, Tan YX, Joncker NT, Choy A, Gallardo F, Xiong N, et al. NKG2Ddeficientmice are defective in tumor surveillance in models of spontaneous malignancy. Immunity 2008;28:571-80.
6. Imai K, Matsuyama S, Miyake S, Suga K, Nakachi K. Natural cytotoxic activity of peripheral-blood lymphocytes and cancer incidence: an 11-year follow-up study of a general population. Lancet 2000;356:1795-9.
7. Hanna J, Bechtel P, Zhai Y, Youssef F, McLachlan K, Mandelboim O. Novel insights on human NK cells' immunological modalities revealed by gene expression profiling. J Immunol 2004;173:6547-63.
8. Moretta A, Bottino C, Vitale M, Pende D, Cantoni C, Mingari MC, et al. Activating receptors and coreceptors involved in human natural killer cellmediated cytolysis. Annu Rev Immunol 2001;19:197-223.
9. Rabinovich GA, Gabrilovich D, Sotomayor EM. Immunosuppressive strategies that are mediated by tumor cells. Annu Rev Immunol 2007;25:267-96.
10. Balsamo M, Scordamaglia F, Pietra G, Manzini C, Cantoni C, Boitano M, et al. Melanoma-associated fibroblasts modulate NK cell phenotype and antitumor cytotoxicity. Proc Natl Acad Sci U S A 2009;106:20847-52.
11. Costello RT, Sivori S, Marcenaro E, Lafage-Pochitaloff M, Mozziconacci MJ, Reviron D, et al. Defective expression and function of natural killer celltriggering receptors in patients with acute myeloid leukemia. Blood 2002;99:3661-7.
12. Mamessier E, Sylvain A, Thibult ML, Houvenaeghel G, Jacquemier J, Castellano R, et al. Human breast cancer cells enhance self tolerance by promoting evasion from NK cell antitumor immunity. J Clin Invest 2011;121:3609-22.
13. Mamessier E, Sylvain A, Bertucci F, Castellano R, Finetti P, Houvenaeghel G, et al. Human breast tumor cells induce self-tolerance mechanisms to avoid NKG2D-mediated andDNAM-mediatedNKcell recognition. Cancer Res 2011;71:6621-32.
14. Platonova S, Cherfils-Vicini J, Damotte D, Crozet L, Vieillard V, Validire P, et al. Profound coordinated alterations of intratumoral NK cell phenotype and function in lung carcinoma. Cancer Res 2011; 71:5412-22.
15. Gillard-Bocquet M, Caer C, Cagnard N, Crozet L, Perez M, Fridman WH, et al. Lung tumor microenvironment induces specific gene expression signature in intratumoral NK cells. Front Immunol 2013;4:19.
16. Carrega P, Morandi B, Costa R, Frumento G, Forte G, Altavilla G, et al. Natural killer cells infiltrating human nonsmall-cell lung cancer are enriched in CD56 bright CD16(-) cells and display an impaired capability to kill tumor cells. Cancer 2008;112:863-75.
17. Rocca YS, Roberti MP, Arriaga JM, Amat M, Bruno L, Pampena MB, et al. Altered phenotype in peripheral blood and tumor-associatedNKcells from colorectal cancer patients. Innate Immun 2013;19:76-85.
18. Schleypen JS, Baur N, Kammerer R, Nelson PJ, Rohrmann K, Grone EF, et al. Cytotoxic markers and frequency predict functional capacity of natural killer cells infiltrating renal cell carcinoma. Clin Cancer Res 2006;12:718-25.
19. Rusakiewicz S, Semeraro M, Sarabi M, Desbois M, Locher C, Mendez R, et al. Immune infiltrates are prognostic factors in localized gastrointestinal stromal tumors. Cancer Res 2013;73:3499-510.
20. Delahaye NF, Rusakiewicz S, Martins I,Menard C, Roux S, Lyonnet L, et al. Alternatively spliced NKp30 isoforms affect the prognosis of gastrointestinal stromal tumors. Nat Med 2011;17:700-7.
21. Arnon TI, Markel G, Bar-Ilan A, Hanna J, Fima E, Benchetrit F, et al. Harnessing soluble NK cell killer receptors for the generation of novel cancer immune therapy. PLoS One 2008;3:e2150.
22. Gannon PO, Poisson AO, Delvoye N, Lapointe R,Mes-Masson AM, Saad F. Characterization of the intra-prostatic immune cell infiltration in androgen-deprived prostate cancer patients. J Immunol Methods 2009;348:9-17.
23. Bjorkstrom NK, Riese P, Heuts F, Andersson S, Fauriat C, Ivarsson MA, et al. Expression patterns of NKG2A, KIR, and CD57 define a process of CD56dim NK-cell differentiation uncoupled from NK-cell education. Blood 2010;116:3853-64.
24. Lopez-Verges S, Milush JM, Pandey S, York VA, Arakawa-Hoyt J, Pircher H, et al. CD57 defines a functionally distinct population of mature NK cells in the human CD56dimCD16+NK-cell subset. Blood 2010; 116:3865-74.
25. Bryceson YT, Fauriat C, Nunes JM, Wood SM, Bjorkstrom NK, Long EO, et al. Functional analysis of human NK cells by flow cytometry. Methods Mol Biol 2010;612:335-52.
26. Mamessier E, Pradel LC, Thibult ML, Drevet C, Zouine A, Jacquemier J, et al. Peripheral blood NK cells from breast cancer patients are tumor-induced composite subsets. J Immunol 2013;190:2424-36.
27. Carrega P, Bonaccorsi I, Di Carlo E, Morandi B, Paul P, Rizzello V, et al. CD56(bright)perforin(low) noncytotoxic human NK cells are abundant in both healthy and neoplastic solid tissues and recirculate to secondary lymphoid organs via afferent lymph. J Immunol 2014;192:3805-15.
28. Flavell RA, Sanjabi S, Wrzesinski SH, Licona-Limon P. The polarization of immune cells in the tumour environment by TGFbeta. Nat Rev Immunol 2010;10:554-67.
29. Reis ST, Pontes-Junior J, Antunes AA, Sousa-Canavez JM, Abe DK, Cruz JA, et al. Tgf-beta1 expression as a biomarker of poor prognosis in prostate cancer. Clinics 2011;66:1143-7.
30. Keskin DB, Allan DS, Rybalov B, Andzelm MM,Stern JN, Kopcow HD, et al. TGFbeta promotes conversion of CD16+peripheral blood NK cells into CD16-NKcells with similarities to decidualNKcells. Proc Natl Acad SciUS A 2007;104:3378-83.
31. Allan DS, Rybalov B, Awong G, Zuniga-Pflucker JC, Kopcow HD, Carlyle JR, et al. TGF-beta affects development and differentiation of human natural killer cell subsets. Eur J Immunol 2010;40:2289-95.
32. Holtan SG, Creedon DJ, Thompson MA, Nevala WK, Markovic SN. Expansion of CD16-negative natural killer cells in the peripheral blood of patients with metastatic melanoma. Clin Dev Immunol 2011;2011: 316314.
33. Castriconi R, Cantoni C, Della Chiesa M, Vitale M, Marcenaro E, Conte R, et al. Transforming growth factor beta 1 inhibits expression of NKp30 and NKG2D receptors: consequences for the NK-mediated killing of dendritic cells. Proc Natl Acad Sci U S A 2003;100:4120-5.
34. Morris JC, Tan AR, Olencki TE, Shapiro GI, Dezube BJ, Reiss M, et al. Phase I study of GC1008 (fresolimumab): a human anti-transforming growth factor-beta (TGFbeta) monoclonal antibody in patients with advanced malignant melanoma or renal cell carcinoma. PLoS One 2014;9:e90353.
35. Pietra G, Manzini C, Rivara S, Vitale M, Cantoni C, Petretto A, et al. Melanoma cells inhibit natural killer cell function by modulating the expression of activating receptors and cytolytic activity. Cancer Res 2012;72:1407-15.
36. McGilvray RW, Eagle RA, Watson NF, Al-Attar A, Ball G, Jafferji I, et al. NKG2D ligand expression in human colorectal cancer reveals associations with prognosis and evidence for immunoediting. Clin Cancer Res 2009;15:6993-7002.
37. Carlsten M, Baumann BC, Simonsson M, Jadersten M, Forsblom AM, Hammarstedt C, et al. Reduced DNAM-1 expression on bone marrow NK cells associated with impaired killing of CD34+blasts in myelodysplastic syndrome. Leukemia 2010;24:1607-16.
38. Carlsten M, Norell H, Bryceson YT, Poschke I, Schedvins K, Ljunggren HG, et al. Primary human tumor cells expressing CD155 impair tumor targeting by down-regulating DNAM-1 on NK cells. J Immunol 2009;183:4921-30.
39. Koo KC, Shim DH, Yang CM, Lee SB, Kim SM, Shin TY, et al. Reduction of the CD16(-)CD56bright NK cell subset precedes NK cell dysfunction in prostate cancer. PLoS One 2013;8:e78049.
40. Horton NC, Mathew PA. NKp44 and natural cytotoxicity receptors as damage-associated molecular pattern recognition receptors. Front Immunol 2015;6:31.
41. Wu JD, Higgins LM, Steinle A, Cosman D, Haugk K, Plymate SR. Prevalent expression of the immunostimulatory MHC class I chainrelated molecule is counteracted by shedding in prostate cancer. J Clin Invest 2004;114:560-8.
42. Liu G, Lu S,Wang X, Page ST, Higano CS, Plymate SR, et al. Perturbation of NK cell peripheral homeostasis accelerates prostate carcinoma metastasis. J Clin Invest 2013;123:4410-22.
43. Crane CA, Austgen K, Haberthur K, Hofmann C, Moyes KW, Avanesyan L, et al. Immune evasion mediated by tumor-derived lactate dehydrogenase induction of NKG2D ligands on myeloid cells in glioblastoma patients. Proc Natl Acad Sci U S A 2014;111:12823-8.
44. Pasero C, Gravis G, Granjeaud S, Guerin M, Thomassin-Piana J, Rocchi P, et al. Highly effective NK cells are associated with good prognosis in patients with metastatic prostate cancer. Oncotarget 2015;6:14360-73.
45. Fong L, Carroll P, Weinberg V, Chan S, Lewis J, Corman J, et al. Activated lymphocyte recruitment into the tumor microenvironment following preoperative sipuleucel-T for localized prostate cancer. J Natl Cancer Inst 2014;106.doi:10.1093/jnci/dju268.
46. Miller AM, Lundberg K, Ozenci V, Banham AH, Hellstrom M, Egevad L, et al. CD4+CD25high T cells are enriched in the tumor and peripheral blood of prostate cancer patients. J Immunol 2006;177: 7398-405.
47. Sfanos KS, Bruno TC, Maris CH, Xu L, Thoburn CJ, DeMarzo AM, et al. Phenotypic analysis of prostate-infiltrating lymphocytes reveals TH17 and Treg skewing. Clin Cancer Res 2008;14:3254-61.
48. Anderson MJ, Shafer-Weaver K, Greenberg NM, Hurwitz AA. Tolerization of tumor-specific T cells despite efficient initial priming in a primary murine model of prostate cancer. J Immunol 2007;178: 1268-76.
49. Shafer-Weaver KA, Anderson MJ, Stagliano K, Malyguine A, Greenberg NM, Hurwitz AA. Cutting edge: tumor-specific CD8+T cells infiltrating prostatic tumors are induced to become suppressor cells. J Immunol 2009; 183:4848-52.