CD73-mediated adenosine production promotes stem cell-like properties in mouse Tc17 cells

Immunology

Volumn 146, Issue 4, 2015, Pages 582-594

  Flores Santibáñez, Felipe ^a   Fernández, Dominique ^a   Meza, Daniel ^a   Tejón, Gabriela ^a   Vargas, Leonardo ^a   Varela Nallar, Lorena ^b   Arredondo, Sebastián ^b   Guixé, Victoria ^a   Rosemblatt, Mario ^a,b,c   Bono, María Rosa ^a   Sauma, Daniela ^a  

^a UNIVERSITY OF CHILE   (Chile)

^b UNIVERSIDAD ANDRÉS BELLO   (Chile)

^c Fundacion Ciencia para la Vida   (Chile)

Author keywords

Adenosine; CD73; Cell differentiation; Stem cell; Tc17; Tumour immunology

Indexed keywords

5' NUCLEOTIDASE; ADENOSINE; ADENOSINE A2A RECEPTOR; GAMMA INTERFERON; GRANZYME B; INTERLEUKIN 17; INTERLEUKIN 7 RECEPTOR; L SELECTIN; LYMPHOID ENHANCER FACTOR 1; TRANSCRIPTION FACTOR 7; ADENOSINE PHOSPHATE; CYTOKINE;

ANIMAL CELL; ANIMAL EXPERIMENT; ANIMAL MODEL; ANIMAL TISSUE; ARTICLE; CD4+ T LYMPHOCYTE; CD8+ T LYMPHOCYTE; CONTROLLED STUDY; CYTOKINE PRODUCTION; DOWN REGULATION; LYMPHOCYTE DIFFERENTIATION; LYMPHOCYTE PROLIFERATION; MEMORY T LYMPHOCYTE; MOUSE; NONHUMAN; PHENOTYPE; PRIORITY JOURNAL; PROTEIN EXPRESSION; PROTEIN FUNCTION; SIGNAL TRANSDUCTION; STEM CELL; TUMOR MICROENVIRONMENT; ADOPTIVE TRANSFER; ANIMAL; BIOSYNTHESIS; CELL DIFFERENTIATION; CYTOLOGY; EXPERIMENTAL MELANOMA; IMMUNOLOGICAL MEMORY; IMMUNOLOGY; IMMUNOPHENOTYPING; METABOLISM; PATHOLOGY; T LYMPHOCYTE SUBPOPULATION; TRANSGENIC MOUSE; TUMOR ASSOCIATED LEUKOCYTE;

5'-NUCLEOTIDASE; ADENOSINE; ADENOSINE MONOPHOSPHATE; ADOPTIVE TRANSFER; ANIMALS; CD8-POSITIVE T-LYMPHOCYTES; CELL DIFFERENTIATION; CYTOKINES; DOWN-REGULATION; IMMUNOLOGIC MEMORY; IMMUNOPHENOTYPING; LYMPHOCYTES, TUMOR-INFILTRATING; MELANOMA, EXPERIMENTAL; MICE; MICE, TRANSGENIC; PHENOTYPE; STEM CELLS; T-LYMPHOCYTE SUBSETS;

EID: 84983159940     PISSN: 00192805     EISSN: 13652567     Source Type: Journal    
DOI: 10.1111/imm.12529     Document Type: Article

References (44)

1. Restifo NP, Dudley ME, Rosenberg SA. Adoptive immunotherapy for cancer: harnessing the T cell response. Nat Rev Immunol 2012; 12:269-81.
2. Rosenberg SA, Yang JC, Sherry RM, et al. Durable complete responses in heavily pretreated patients with metastatic melanoma using T-cell transfer immunotherapy. Clin Cancer Res 2011; 17:4550-7.
3. Crompton JG, Sukumar M, Restifo NP. Uncoupling T-cell expansion from effector differentiation in cell-based immunotherapy. Immunol Rev 2014; 257:264-76.
4. + T-cell adoptive immunotherapy for large established tumors in mice. Clin Cancer Res 2011; 17:5343-52.
5. Gattinoni L, Klebanoff CA, Restifo NP. Paths to stemness: building the ultimate antitumour T cell. Nat Rev Cancer 2012; 12:671-84.
6. Gattinoni L, Lugli E, Ji Y, et al. A human memory T cell subset with stem cell-like properties. Nat Med 2011; 17:1290-7.
7. + memory stem cells. Nat Med 2009; 15:808-13.
8. Croft M, Carter L, Swain SL, Dutton RW. Generation of polarized antigen-specific CD8 effector populations: reciprocal action of interleukin (IL)-4 and IL-12 in promoting type 2 versus type 1 cytokine profiles. J Exp Med 1994; 180:1715-28.
9. Hamada H, Garcia-Hernandez Mde L, Reome JB, et al. Tc17, a unique subset of CD8 T cells that can protect against lethal influenza challenge. J Immunol 2009; 182:3469-81.
10. + Tc17 cells with reduced cytotoxic activity. Eur J Immunol 2009; 39:1716-25.
11. Muranski P, Borman ZA, Kerkar SP, et al. Th17 cells are long lived and retain a stem cell-like molecular signature. Immunity 2011; 35:972-85.
12. + T cells display enhanced antitumor immunity. Blood 2009; 114:596-9.
13. Junger WG. Immune cell regulation by autocrine purinergic signalling. Nat Rev Immunol 2011; 11:201-12.
14. Antonioli L, Pacher P, Vizi ES, Hasko G. CD39 and CD73 in immunity and inflammation. Trends Mol Med 2013; 19:355-67.
15. + T cells. J Immunol 2005; 174:1073-80.
16. Su AI, Wiltshire T, Batalov S, et al. A gene atlas of the mouse and human protein-encoding transcriptomes. Proc Natl Acad Sci USA 2004; 101:6062-7.
17. + T cells in the tumor microenvironment. Cancer Res 2014; 74:7239-49.
18. Cekic C, Sag D, Day YJ, Linden J. Extracellular adenosine regulates naive T cell development and peripheral maintenance. J Exp Med 2013; 210:2693-706.
19. Regateiro FS, Howie D, Nolan KF, et al. Generation of anti-inflammatory adenosine by leukocytes is regulated by TGF-β. Eur J Immunol 2011; 41:2955-65.
20. Kryczek I, Zhao E, Liu Y, et al. Human TH17 cells are long-lived effector memory cells. Sci Transl Med 2011; 3:104ra0.
21. Chhabra A. Mitochondria-centric activation induced cell death of cytolytic T lymphocytes and its implications for cancer immunotherapy. Vaccine 2010; 28:4566-72.
22. + T cells. J Clin Invest 2005; 115:1616-26.
23. + T cells confer superior antitumor immunity compared with effector memory T cells. Proc Natl Acad Sci USA 2005; 102:9571-6.
24. Mueller SN, Gebhardt T, Carbone FR, Heath WR. Memory T cell subsets, migration patterns, and tissue residence. Annu Rev Immunol 2013; 31:137-61.
25. Chalmin F, Mignot G, Bruchard M, et al. Stat3 and Gfi-1 transcription factors control Th17 cell immunosuppressive activity via the regulation of ectonucleotidase expression. Immunity 2012; 36:362-73.
26. Crompton JG, Sukumar M, Roychoudhuri R, et al. Akt inhibition enhances expansion of potent tumor-specific lymphocytes with memory cell characteristics. Cancer Res 2015; 75:296-305.
27. Williams BA, Blay J, Hoskin DW. 2-Chloroadenosine stimulates granule exocytosis from mouse natural killer cells: evidence for signal transduction through a novel extracellular receptor. Exp Cell Res 1997; 233:187-97.
28. Csoka B, Himer L, Selmeczy Z, et al. Adenosine A2A receptor activation inhibits T helper 1 and T helper 2 cell development and effector function. FASEB J 2008; 22:3491-9.
29. Hasko G, Kuhel DG, Chen JF, et al. Adenosine inhibits IL-12 and TNF-α production via adenosine A2a receptor-dependent and independent mechanisms. FASEB J 2000; 14:2065-74.
30. Regateiro FS, Cobbold SP, Waldmann H. CD73 and adenosine generation in the creation of regulatory microenvironments. Clin Exp Immunol 2013; 171:1-7.
31. + Treg cells: hydrolysis of extracellular ATP and immune suppression. Blood 2007; 110:1225-32.
32. Deaglio S, Dwyer KM, Gao W, et al. Adenosine generation catalyzed by CD39 and CD73 expressed on regulatory T cells mediates immune suppression. J Exp Med 2007; 204:1257-65.
33. Vignali DA, Collison LW, Workman CJ. How regulatory T cells work. Nat Rev Immunol 2008; 8:523-32.
34. Beavis PA, Stagg J, Darcy PK, Smyth MJ. CD73: a potent suppressor of antitumor immune responses. Trends Immunol 2012; 33:231-7.
35. Stagg J, Beavis PA, Divisekera U, et al. CD73-deficient mice are resistant to carcinogenesis. Cancer Res 2012; 72:2190-6.
36. Stagg J, Divisekera U, McLaughlin N, et al. Anti-CD73 antibody therapy inhibits breast tumor growth and metastasis. Proc Natl Acad Sci USA 2010; 107:1547-52.
37. Stagg J, Smyth MJ. Extracellular adenosine triphosphate and adenosine in cancer. Oncogene 2010; 29:5346-58.
38. Wang L, Fan J, Thompson LF, et al. CD73 has distinct roles in nonhematopoietic and hematopoietic cells to promote tumor growth in mice. J Clin Invest 2011; 121:2371-82.
39. Yegutkin GG, Marttila-Ichihara F, Karikoski M, et al. Altered purinergic signaling in CD73-deficient mice inhibits tumor progression. Eur J Immunol 2011; 41:1231-41.
40. Szymczak-Workman AL, Workman CJ, Vignali DA. Cutting edge: regulatory T cells do not require stimulation through their TCR to suppress. J Immunol 2009; 182:5188-92.
41. Hand TW, Cui W, Jung YW, et al. Differential effects of STAT5 and PI3K/AKT signaling on effector and memory CD8 T-cell survival. Proc Natl Acad Sci USA 2010; 107:16601-6.
42. Kim EH, Sullivan JA, Plisch EH, et al. Signal integration by Akt regulates CD8 T cell effector and memory differentiation. J Immunol 2012; 188:4305-14.
43. Chatterjee S, Thyagarajan K, Kesarwani P, et al. Reducing CD73 expression by IL1β-programmed Th17 cells improves immunotherapeutic control of tumors. Cancer Res 2014; 74:6048-59.
44. Wilson JM, Kurtz CC, Black SG, et al. The A2B adenosine receptor promotes Th17 differentiation via stimulation of dendritic cell IL-6. J Immunol 2011; 186:6746-52.