β-Catenin in dendritic cells exerts opposite functions in cross-priming and maintenance of CD8+ T cells through regulation of IL-10

Proceedings of the National Academy of Sciences of the United States of America

Volumn 112, Issue 9, 2015, Pages 2823-2828

  Fu, Chunmei ^a   Liang, Xinjun ^a   Cui, Weiguo ^b   Ober Blöbaum, Julia L ^c   Vazzana, Joseph ^a   Shrikant, Protul A ^a,d   Lee, Kelvin P ^a   Clausen, Björn E ^c   Mellman, Ira ^e   Jiang, Aimin ^a  

^a ROSWELL PARK CANCER INSTITUTE   (United States)

^b BLOOD RESEARCH INSTITUTE   (United States)

^c JOHANNES GUTENBERG UNIVERSITY   (Germany)

^d MAYO CLINIC   (United States)

^e GENENTECH INC   (United States)

Author keywords

Beta catenin; CD8+ T cell immunity; Dendritic cells; IL 10; MTOR

Indexed keywords

BETA CATENIN; INTERLEUKIN 10; MAMMALIAN TARGET OF RAPAMYCIN; CANCER VACCINE; IL10 PROTEIN, MOUSE; MTOR PROTEIN, MOUSE; TARGET OF RAPAMYCIN KINASE;

ANIMAL CELL; ANIMAL EXPERIMENT; ARTICLE; CD8+ T LYMPHOCYTE; CELL EXPANSION; CELLULAR IMMUNITY; CONTROLLED STUDY; CROSS PRESENTATION; CYTOKINE PRODUCTION; DENDRITIC CELL; IMMUNOREGULATION; MOUSE; NONHUMAN; PRIORITY JOURNAL; PROTEIN FUNCTION; SIGNAL TRANSDUCTION; TUMOR IMMUNITY; UPREGULATION; VACCINATION; ANIMAL; GENETICS; IMMUNOLOGY; KNOCKOUT MOUSE; NEOPLASM; PATHOLOGY;

MUS;

ANIMALS; BETA CATENIN; CANCER VACCINES; CD8-POSITIVE T-LYMPHOCYTES; DENDRITIC CELLS; IMMUNITY, CELLULAR; INTERLEUKIN-10; MICE; MICE, KNOCKOUT; NEOPLASMS; TOR SERINE-THREONINE KINASES;

EID: 84924180359     PISSN: 00278424     EISSN: 10916490     Source Type: Journal    
DOI: 10.1073/pnas.1414167112     Document Type: Article

References (44)

1. Steinman RM, Hawiger D, Nussenzweig MC (2003) Tolerogenic dendritic cells. Annu Rev Immunol 21: 685-711.
2. Van den Bossche J, Malissen B, Mantovani A, De Baetselier P, Van Ginderachter JA (2012) Regulation and function of the E-cadherin/catenin complex in cells of the monocyte-macrophage lineage and DCs. Blood 119(7): 1623-1633.
3. Jiang A, et al. (2007) Disruption of E-cadherin-mediated adhesion induces a functionally distinct pathway of dendritic cell maturation. Immunity 27(4): 610-624.
4. Manicassamy S, et al. (2010) Activation of beta-catenin in dendritic cells regulates immunity versus tolerance in the intestine. Science 329(5993): 849-853.
5. + T cells. J Leukoc Biol 95(1): 179-190.
6. Palucka K, Banchereau J (2013) Dendritic-cell-based therapeutic cancer vaccines. Immunity 39(1): 38-48.
7. Melief CJ (2008) Cancer immunotherapy by dendritic cells. Immunity 29(3): 372-383.
8. Lin A, Schildknecht A, Nguyen LT, Ohashi PS (2010) Dendritic cells integrate signals from the tumor microenvironment to modulate immunity and tumor growth. Immunol Lett 127(2): 77-84.
9. Mellman I, Coukos G, Dranoff G (2011) Cancer immunotherapy comes of age. Nature 480(7378): 480-489.
10. Joffre OP, Segura E, Savina A, Amigorena S (2012) Cross-presentation by dendritic cells. Nat Rev Immunol 12(8): 557-569.
11. Wagner CS, Grotzke JE, Cresswell P (2012) Intracellular events regulating cross-presentation. Front Immunol 3: 138.
12. Curtsinger JM, Gerner MY, Lins DC, Mescher MF (2007) Signal 3 availability limits the CD8 T cell response to a solid tumor. J Immunol 178(11): 6752-6760.
13. Zhou J, Cheng P, Youn JI, Cotter MJ, Gabrilovich DI (2009) Notch and wingless signaling cooperate in regulation of dendritic cell differentiation. Immunity 30(6): 845-859.
14. Shortman K, Heath WR (2010) The CD8+ dendritic cell subset. Immunol Rev 234(1): 18-31.
15. Cui W, Joshi NS, Jiang A, Kaech SM (2009) Effects of Signal 3 during CD8 T cell priming: Bystander production of IL-12 enhances effector T cell expansion but promotes terminal differentiation. Vaccine 27(15): 2177-2187.
16. Woodland DL, Dutton RW (2003) Heterogeneity of CD4(+) and CD8(+) T cells. Curr Opin Immunol 15(3): 336-342.
17. Zhao F, et al. (2009) Activation of p38 mitogen-activated protein kinase drives dendritic cells to become tolerogenic in ret transgenic mice spontaneously developing melanoma. Clin Cancer Res 15(13): 4382-4390.
18. Haidinger M, et al. (2010) A versatile role of mammalian target of rapamycin in human dendritic cell function and differentiation. J Immunol 185(7): 3919-3931.
19. Ohtani M, et al. (2012) Cutting edge: mTORC1 in intestinal CD11c+ CD11b+ dendritic cells regulates intestinal homeostasis by promoting IL-10 production. J Immunol 188(10): 4736-4740.
20. Araki K, Ellebedy AH, Ahmed R (2011) TOR in the immune system. Curr Opin Cell Biol 23(6): 707-715.
21. Bonifaz LC, et al. (2004) In vivo targeting of antigens to maturing dendritic cells via the DEC-205 receptor improves T cell vaccination. J Exp Med 199(6): 815-824.
22. Agrawal S, Temsamani J, Galbraith W, Tang J (1995) Pharmacokinetics of antisense oligonucleotides. Clin Pharmacokinet 28(1): 7-16.
23. Groux H, Bigler M, de Vries JE, Roncarolo MG (1998) Inhibitory and stimulatory effects of IL-10 on human CD8+ T cells. J Immunol 160(7): 3188-3193.
24. Fujii S, Shimizu K, Shimizu T, Lotze MT (2001) Interleukin-10 promotes the maintenance of antitumor CD8(+) T-cell effector function in situ. Blood 98(7): 2143-2151.
25. Dercamp C, Chemin K, Caux C, Trinchieri G, Vicari AP (2005) Distinct and overlapping roles of interleukin-10 and CD25+ regulatory T cells in the inhibition of antitumor CD8 T-cell responses. Cancer Res 65(18): 8479-8486.
26. Kang SS, Allen PM (2005) Priming in the presence of IL-10 results in direct enhancement of CD8+ T cell primary responses and inhibition of secondary responses. J Immunol 174(9): 5382-5389.
27. Foulds KE, Rotte MJ, Seder RA (2006) IL-10 is required for optimal CD8 T cell memory following Listeria monocytogenes infection. J Immunol 177(4): 2565-2574.
28. Biswas PS, et al. (2007) Pathogen-specific CD8 T cell responses are directly inhibited by IL-10. J Immunol 179(7): 4520-4528.
29. Brooks DG, Lee AM, Elsaesser H, McGavern DB, Oldstone MB (2008) IL-10 blockade facilitates DNA vaccine-induced T cell responses and enhances clearance of persistent virus infection. J Exp Med 205(3): 533-541.
30. Brooks DG, Walsh KB, Elsaesser H, Oldstone MB (2010) IL-10 directly suppresses CD4 but not CD8 T cell effector and memory responses following acute viral infection. Proc Natl Acad Sci USA 107(7): 3018-3023.
31. Mumm JB, et al. (2011) IL-10 elicits IFNγ-dependent tumor immune surveillance. Cancer Cell 20(6): 781-796.
32. Cui W, Liu Y, Weinstein JS, Craft J, Kaech SM (2011) An interleukin-21-interleukin-10-STAT3 pathway is critical for functional maturation of memory CD8+ T cells. Immunity 35(5): 792-805.
33. Huang SM, et al. (2009) Tankyrase inhibition stabilizes axin and antagonizes Wnt signalling. Nature 461(7264): 614-620.
34. Moore KW, de Waal Malefyt R, Coffman RL, O'Garra A (2001) Interleukin-10 and the interleukin-10 receptor. Annu Rev Immunol 19: 683-765.
35. Banchereau J, et al. (2012) The differential production of cytokines by human Langerhans cells and dermal CD14(+) DCs controls CTL priming. Blood 119(24): 5742-5749.
36. Thomson AW, Turnquist HR, Raimondi G (2009) Immunoregulatory functions of mTOR inhibition. Nat Rev Immunol 9(5): 324-337.
37. Wang Y, Chi H (2014) mTOR signaling and dendritic cell biology. J Immunol Clin Res 2(1): 1015.
38. Wang Y, et al. (2013) Tuberous sclerosis 1 (Tsc1)-dependent metabolic checkpoint controls development of dendritic cells. Proc Natl Acad Sci USA 110(50):E4894-E4903.
39. Amiel E, et al. (2012) Inhibition of mechanistic target of rapamycin promotes dendritic cell activation and enhances therapeutic autologous vaccination in mice. J Immunol 189(5): 2151-2158.
40. Vander Lugt B, et al. (2011) TGF-β suppresses β-catenin-dependent tolerogenic activation program in dendritic cells. PLoS ONE 6(5): e20099.
41. Orr SJ, et al. (2013) LAB/NTAL facilitates fungal/PAMP-induced IL-12 and IFN-γ production by repressing β-catenin activation in dendritic cells. PLoS Pathog 9(5): e1003357.
42. Qian C, et al. (2013) Fas signal promotes the immunosuppressive function of regulatory dendritic cells via the ERK/β-catenin pathway. J Biol Chem 288(39): 27825-27835.
43. Shan M, et al. (2013) Mucus enhances gut homeostasis and oral tolerance by delivering immunoregulatory signals. Science 342(6157): 447-453.
44. Baur AS, et al. (2013) Denileukin diftitox (ONTAK) induces a tolerogenic phenotype in dendritic cells and stimulates survival of resting Treg. Blood 122(13): 2185-2194.