β-catenin promotes regulatory T-cell responses in tumors by inducing vitamin a metabolism in dendritic cells

Cancer Research

Volumn 75, Issue 4, 2015, Pages 656-665

  Hong, Yuan ^a   Manoharan, Indumathi ^a   Suryawanshi, Amol ^a   Majumdar, Tanmay ^a   Angus Hill, Melinda L ^b   Koni, Pandelakis A ^a   Manicassamy, Balaji ^c   Mellor, Andrew L ^a   Munn, David H ^a   Manicassamy, Santhakumar ^a,d  

^a MEDICAL COLLEGE OF GEORGIA   (United States)

^b UNIVERSITY OF UTAH   (United States)

^c UNIVERSITY OF CHICAGO   (United States)

^d AUGUSTA UNIVERSITY   (United States)

Author keywords

[No Author keywords available]

Indexed keywords

7,8 DIHYDRO 2 [4 (TRIFLUOROMETHYL)PHENYL] 5H THIOPYRANO[4,3 D]PYRIMIDIN 4 OL; ALCOHOL DEHYDROGENASE; ANTINEOPLASTIC AGENT; BETA CATENIN; CITRAL; DISULFIRAM; JW 55; RETINOIC ACID; RETINOL; UNCLASSIFIED DRUG; BASIC HELIX LOOP HELIX LEUCINE ZIPPER TRANSCRIPTION FACTOR; TCF4 PROTEIN, MOUSE;

ANIMAL CELL; ANIMAL EXPERIMENT; ANIMAL MODEL; ANIMAL TISSUE; ANTINEOPLASTIC ACTIVITY; ARTICLE; CANCER IMMUNOTHERAPY; CANCER INHIBITION; CONTROLLED STUDY; DENDRITIC CELL; ENZYME ACTIVITY; ENZYME INHIBITION; IMMUNOLOGICAL TOLERANCE; IN VIVO STUDY; LYMPHOCYTE DIFFERENTIATION; MALE; MELANOMA; MOUSE; NEOPLASM; NONHUMAN; PHENOTYPE; PROTEIN EXPRESSION; REGULATORY T LYMPHOCYTE; SIGNAL TRANSDUCTION; TUMOR MICROENVIRONMENT; VITAMIN METABOLISM; ANIMAL; CD8+ T LYMPHOCYTE; GENETICS; HUMAN; IMMUNOLOGY; METABOLISM; PATHOLOGY; TRANSGENIC MOUSE;

ANIMALS; BASIC HELIX-LOOP-HELIX LEUCINE ZIPPER TRANSCRIPTION FACTORS; BETA CATENIN; CD8-POSITIVE T-LYMPHOCYTES; DENDRITIC CELLS; HUMANS; MICE; MICE, TRANSGENIC; SIGNAL TRANSDUCTION; T-LYMPHOCYTES, REGULATORY; TUMOR MICROENVIRONMENT; VITAMIN A;

EID: 84923163439     PISSN: 00085472     EISSN: 15387445     Source Type: Journal    
DOI: 10.1158/0008-5472.CAN-14-2377     Document Type: Article

References (42)

1. Rabinovich GA, Gabrilovich D, Sotomayor EM. Immunosuppressive strategies that are mediated by tumor cells. Annu Rev Immunol 2007;25:267-96.
2. Chen DS, Mellman I. Oncology meets immunology: the cancer-immunity cycle. Immunity 2013;39:1-10.
3. 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.
4. Munn DH, Mellor AL. Indoleamine 2,3-dioxygenase and tumor-induced tolerance. J Clin Invest 2007;117:1147-54.
5. Palucka K, Banchereau J. Cancer immunotherapy via dendritic cells. Nat Rev Cancer 2012;12:265-77.
6. Hall JA, Grainger JR, Spencer SP, Belkaid Y. The role of retinoic acid in tolerance and immunity. Immunity 2011;35:13-22.
7. Manicassamy S, Pulendran B. Retinoic acid-dependent regulation of immune responses by dendritic cells and macrophages. Semin Immunol 2009;21:22-7.
8. Guo Y, Pino-Lagos K, Ahonen CA, Bennett KA, Wang J, Napoli JL, et al. A retinoic acid-rich tumor microenvironment provides clonal survival cues for tumor-specific CD8(+) T cells. Cancer Res 2012;72:5230-9.
9. Reya T, Clevers H. Wnt signalling in stem cells and cancer. Nature 2005; 434:843-50.
10. Alastalo TP, Li M, Perez Vde J, Pham D, Sawada H, Wang JK, et al. Disruption of PPARgamma/beta-catenin-mediated regulation of apelin impairs BMP-induced mouse and human pulmonary arterial EC survival. J Clin Invest 2011;121:3735-46.
11. Liu J, Wang H, Zuo Y, Farmer SR. Functional interaction between peroxisome proliferator-activated receptor gamma and beta-catenin. Mol Cell Biol 2006;26:5827-37.
12. Hoogeboom D, Essers MA, Polderman PE, Voets E, Smits LM, Burgering BM. Interaction of FOXO with beta-catenin inhibits beta-catenin/T cell factor activity. J Biol Chem 2008;283:9224-30.
13. Yan Y, Lackner MR. FOXO3a and beta-catenin co-localization: double trouble in colon cancer? Nat Med 2012;18:854-6.
14. Shah S, Islam MN, Dakshanamurthy S, Rizvi I, Rao M, Herrell R, et al. The molecular basis of vitamin D receptor and beta-catenin crossregulation. Mol Cell 2006;21:799-809.
15. Yang P, An H, Liu X, Wen M, Zheng Y, Rui Y, et al. The cytosolic nucleic acid sensor LRRFIP1 mediates the production of type I interferon via a beta-catenin-dependent pathway. Nat Immunol 2010;11:487-94.
16. Macheda ML, Stacker SA. Importance of Wnt signaling in the tumor stroma microenvironment. Curr Cancer Drug Targets 2008;8:454-65.
17. Klaus A, Birchmeier W. Wnt signalling and its impact on development and cancer. Nat Rev Cancer 2008;8:387-98.
18. Liang X, Fu C, Cui W, Ober-Blobaum JL, Zahner SP, Shrikant PA, et al. betacatenin mediates tumor-induced immunosuppression by inhibiting crosspriming of CD8(+) T cells. J Leukoc Biol 2014;95:179-90.
19. Manicassamy S, Reizis B, Ravindran R, Nakaya H, Salazar-Gonzalez RM, Wang YC, et al. Activation of beta-catenin in dendritic cells regulates immunity versus tolerance in the intestine. Science 2010;329:849-53.
20. Maretto S, Cordenonsi M, Dupont S, Braghetta P, Broccoli V, Hassan AB, et al. Mapping Wnt/beta-catenin signaling during mouse development and in colorectal tumors. Proc Natl Acad Sci U S A 2003;100:3299-304.
21. Brault V, Moore R, Kutsch S, Ishibashi M, Rowitch DH, McMahon AP, et al. Inactivation of the beta-catenin gene by Wnt1-Cre-mediated deletion results in dramatic brain malformation and failure of craniofacial development. Development 2001;128:1253-64.
22. CatonML, Smith-RaskaMR, Reizis B.Notch-RBP-J signaling controls the homeostasis of CD8- dendritic cells in the spleen. J Exp Med 2007;204:1653-64.
23. Angus-Hill ML, Elbert KM, Hidalgo J, CapecchiMR. T-cell factor 4 functions as a tumor suppressor whose disruption modulates colon cell proliferation and tumorigenesis. Proc Natl Acad Sci U S A 2011;108:4914-9.
24. Guadix JA, Ruiz-Villalba A, Lettice L, Velecela V,Munoz-Chapuli R,Hastie ND, et al. Wt1 controls retinoic acid signalling in embryonic epicardium through transcriptional activation of Raldh2. Development 2011;138:1093-7.
25. Sharma MD, Baban B, Chandler P, Hou DY, Singh N, Yagita H, et al. Plasmacytoid dendritic cells from mouse tumor-draining lymph nodes directly activate mature Tregs via indoleamine 2,3-dioxygenase. J Clin Invest 2007;117:2570-82.
26. Manicassamy S, Ravindran R, Deng J, Oluoch H, Denning TL, Kasturi SP, et al. Toll-like receptor 2-dependent induction of vitamin A-metabolizing enzymes in dendritic cells promotes T regulatory responses and inhibits autoimmunity. Nat Med 2009;15:401-9.
27. Manoharan I, Hong Y, Suryawanshi A, Angus-Hill ML, Sun Z, Mellor AL, et al. TLR2-dependent activation of beta-catenin pathway in dendritic cells induces regulatory responses and attenuates autoimmune inflammation. J Immunol 2014;193:4203-13.
28. Munn DH, Sharma MD, Hou D, Baban B, Lee JR, Antonia SJ, et al. Expression of indoleamine 2,3-dioxygenase by plasmacytoid dendritic cells in tumor-draining lymph nodes. J Clin Invest 2004;114:280-90.
29. Stern A, Wold AE, Ostman S. Neonatal mucosal immune stimulation by microbial superantigen improves the tolerogenic capacity of CD103(+) dendritic cells. PLoS One 2013;8:e75594.
30. Capietto AH, Kim S, Sanford DE, Linehan DC, Hikida M, Kumosaki T, et al. Down-regulation of PLCgamma2-beta-catenin pathway promotes activation and expansion of myeloid-derived suppressor cells in cancer. J Exp Med 2013;210:2257-71.
31. Ghosh HS, Cisse B, Bunin A, Lewis KL, Reizis B. Continuous expression of the transcription factor e2-2maintains the cell fate of mature plasmacytoid dendritic cells. Immunity 2010;33:905-16.
32. Jiang A, BloomO,OnoS, Cui W, Unternaehrer J, Jiang S, et al. Disruption of E-cadherin-mediated adhesion induces a functionally distinct pathway of dendritic cell maturation. Immunity 2007;27:610-24.
33. Oderup C, LaJevic M, Butcher EC. Canonical and noncanonical Wnt proteins program dendritic cell responses for tolerance. J Immunol 2013; 190:6126-34.
34. Huang SM, Mishina YM, Liu S, Cheung A, Stegmeier F, Michaud GA, et al. Tankyrase inhibition stabilizes axin and antagonizes Wnt signalling. Nature 2009;461:614-20.
35. Waaler J, Machon O, Tumova L, Dinh H, Korinek V, Wilson SR, et al. A novel tankyrase inhibitor decreases canonical Wnt signaling in colon carcinoma cells and reduces tumor growth in conditional APC mutant mice. Cancer Res 2012;72:2822-32.
36. Anastas JN, Moon RT. WNT signalling pathways as therapeutic targets in cancer. Nat Rev Cancer 2013;13:11-26.
37. Villablanca EJ, Wang S, de Calisto J, Gomes DC, Kane MA, Napoli JL, et al. MyD88 and retinoic acid signaling pathways interact to modulate gastrointestinal activities of dendritic cells. Gastroenterology 2011;141: 176-85.
38. Huang D, Du X. Crosstalk between tumor cells and microenvironment via Wnt pathway in colorectal cancer dissemination. World J Gastroenterol 2008;14:1823-7.
39. Larue L, Delmas V. The WNT/Beta-catenin pathway in melanoma. Front Biosci 2006;11:733-42.
40. Manicassamy S, Pulendran B. Dendritic cell control of tolerogenic responses. Immunol Rev 2011;241:206-27.
41. Jian H, Shen X, Liu I, Semenov M, He X, Wang XF. Smad3-dependent nuclear translocation of beta-catenin is required for TGF-beta1-induced proliferation of bone marrow-derived adult human mesenchymal stem cells. Genes Dev 2006;20:666-74.
42. Sato Y, Goto Y, Narita N, Hoon DS. Cancer cells expressing toll-like receptors and the tumor microenvironment. Cancer Microenviron 2009; 2 Suppl 1:205-14.