Melanoma-derived Wnt5a promotes local dendritic-cell expression of IDO and immunotolerance: Opportunities for pharmacologic enhancement of immunotherapy

Cancer Immunology Research

Volumn 3, Issue 9, 2015, Pages 1082-1095

  Holtzhausen, Alisha ^a   Zhao, Fei ^a   Evans, Kathy S ^a   Tsutsui, Masahito ^a   Orabona, Ciriana ^b   Tyler, Douglas S ^a,c   Hanks, Brent A ^a  

^a DUKE UNIVERSITY   (United States)

^b UNIVERSITY OF PERUGIA   (Italy)

^c UNIVERSITY OF TEXAS MEDICAL BRANCH   (United States)

Author keywords

[No Author keywords available]

Indexed keywords

ACYLTRANSFERASE; ANTINEOPLASTIC AGENT; BETA CATENIN; C 59; CYTOTOXIC T LYMPHOCYTE ANTIGEN 4 ANTIBODY; IMMUNOMODULATING AGENT; INDOLEAMINE 2,3 DIOXYGENASE; UNCLASSIFIED DRUG; WNT5A PROTEIN; 2-(4-(2-METHYLPYRIDIN-4-YL)PHENYL)-N-(4-(PYRIDIN-3-YL)PHENYL)ACETAMIDE; BENZENEACETAMIDE DERIVATIVE; CTNNB1 PROTEIN, HUMAN; CYTOTOXIC T LYMPHOCYTE ANTIGEN 4; MEMBRANE PROTEIN; MONOCLONAL ANTIBODY; ONCOPROTEIN; PORCN PROTEIN, HUMAN; PYRIDINE DERIVATIVE; WNT PROTEIN; WNT5A PROTEIN, HUMAN;

ANIMAL CELL; ANIMAL EXPERIMENT; ANIMAL MODEL; ARTICLE; CANCER GROWTH; CANCER IMMUNOTHERAPY; CARCINOGENESIS; CELL DIFFERENTIATION; CELLULAR IMMUNITY; CONTROLLED STUDY; DENDRITIC CELL; GENE EXPRESSION; GENE SILENCING; HUMAN; HUMAN CELL; IMMUNOLOGICAL TOLERANCE; IMMUNOSURVEILLANCE; MELANOMA; MOUSE; NONHUMAN; PROGRESSION FREE SURVIVAL; PROTEIN EXPRESSION; REGULATORY T LYMPHOCYTE; SENTINEL LYMPH NODE; SIGNAL TRANSDUCTION; TUMOR MICROENVIRONMENT; ANIMAL; ANTAGONISTS AND INHIBITORS; CANCER TRANSPLANTATION; CELL COMMUNICATION; DISEASE COURSE; DRUG EFFECTS; ENZYMOLOGY; IMMUNOLOGY; IMMUNOTHERAPY; INBRED MOUSE STRAIN; LYMPH NODE; METABOLISM; MOLECULARLY TARGETED THERAPY; PATHOLOGY; PHYSIOLOGY; PROCEDURES; TRANSGENIC MOUSE; TUMOR CELL LINE;

ANIMALS; ANTIBODIES, MONOCLONAL; BENZENEACETAMIDES; BETA CATENIN; CELL COMMUNICATION; CELL LINE, TUMOR; CTLA-4 ANTIGEN; DENDRITIC CELLS; DISEASE PROGRESSION; HUMANS; IMMUNE TOLERANCE; IMMUNOTHERAPY; INDOLEAMINE-PYRROLE 2,3,-DIOXYGENASE; LYMPH NODES; MELANOMA; MEMBRANE PROTEINS; MICE, INBRED STRAINS; MICE, TRANSGENIC; MOLECULAR TARGETED THERAPY; NEOPLASM TRANSPLANTATION; PROTO-ONCOGENE PROTEINS; PYRIDINES; SIGNAL TRANSDUCTION; T-LYMPHOCYTES, REGULATORY; WNT PROTEINS; WNT-5A PROTEIN;

EID: 84962023214     PISSN: 23266066     EISSN: 23266074     Source Type: Journal    
DOI: 10.1158/2326-6066.CIR-14-0167     Document Type: Article

References (53)

1. Banchereau J, Steinman R. Dendritic cells and the control of immunity. Nature 1998;392:245-52.
2. Enk A, Jonuleit H, Saloga J, Knop J. Dendritic cells as mediators of tumor-induced tolerance in metastatic melanoma. Int J Cancer 1997;73:309-16.
3. Watkins SK, Zhu Z, Riboldi E, Shafer-Weaver KA, Stagliano KE, Sklavos MM, et al. FOXO3 programs tumor-associated DCs to become tolerogenic in human and murine prostate cancer. J Clin Invest 2011;121:1361-72.
4. Scarlett UK, Rutkowski MR, Rauwerdink AM, Fields J, Escovar-Fadul X, Baird J, et al. Ovarian cancer progression is controlled by phenotypic changes in dendritic cells. J Exp Med 2012;209:495-506.
5. 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.
6. Munn DH, Zhou M, Attwood JT, Bondarev I, Conway SJ, Marshall B, et al. Prevention of allogeneic fetal rejection by tryptophan catabolism. Science 1998;281:1191-3.
7. Sharma MD, Baban B, Chandler PR, Hou D-Y, 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.
8. Belladonna ML, Volpi C, Bianchi R, Vacca C, Orabona C, Pallotta MT, et al. Cutting edge: autocrine TGF-beta sustains default tolerogenesis by IDO-competent dendritic cells. J Immunol 2008;181:5194-8.
9. Hodi FS, O'Day SJ, McDermott DF, Weber RW, Sosman JA, Haanen JB, et al. Improved survivalwith ipilimumab in patients with metastatic melanoma. N Engl J Med 2010;363:711-23.
10. Topalian SL, Hodi FS, Brahmer JR, Gettinger SN, Smith DC, McDermott DF, et al. Safety, activity, and immune correlates of anti-PD-1 antibody in cancer. N Engl J Med 2012;366:2443-54.
11. Jiang A, Bloom O, Ono S, 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.
12. 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.
13. Valencia J, Hernandez-Lopez C, Martinez VG, Hidalgo L, Zapata AG, Vicente A, et al. Wnt5a skews dendritic cell differentiation to an unconventional phenotype with tolerogenic features. J Immunol 2011;187:4129-39.
14. Oderup C, La Jevic M, Butcher EC. Canonical and noncanonical Wnt proteins program dendritic cell responses for tolerance. J Immunol 2013;190:6126-34.
15. O'Connell MP, Weeraratna AT. Hear the Wnt Ror: how melanoma cells adjust to changes in Wnt. Pigment Cell Melanoma Res 2009;22:724-39.
16. Weeraratna AT, Jiang Y, Hostetter G, Rosenblatt K, Duray P, Bittner M, et al. Wnt5a signaling directly affects cell motility and invasion of metastatic melanoma. Cancer Cell 2002;1:279-88.
17. Da Forno PD, Pringle JH, Hutchinson P, Osborn J, Huang Q, Potter L, et al. WNT5A expression increases duringmelanoma progression and correlates with outcome. Clin Cancer Res 2008;14:5825-32.
18. Bittner M, Meltzer P, Chen Y, Jiang Y, Seftor E, Hendrix M, et al. Molecular classification of cutaneous malignant melanoma by gene expression profiling. Nature 2000;406:536-40.
19. Dankort D, Curley DP, Cartlidge RA, Nelson B, Karnezis AN, Damsky WE Jr, et al. Braf (V600E) cooperates with Pten loss to induce metastatic melanoma. Nat Genet 2009;41:544-52.
20. Clevers H, Nusse R. Wnt/beta-catenin signaling and disease. Cell 2012;149:1192-205.
21. Mii Y, Taira M. Secreted Frizzled-related proteins enhance the diffusion of Wnt ligands and expand their signalling range. Development 2009;136:4083-8.
22. Mulligan KA, Fuerer C, Ching W, Fish M, Willert K, Nusse R. Secreted Wingless-interacting molecule (Swim) promotes long-range signaling by maintaining Wingless solubility. Proc Natl Acad Sci U S A 2012;109:370-7.
23. Ono M, Yin P, Navarro A, Moravek MB, Coon JSt, Druschitz SA, et al. Paracrine activation of WNT/beta-catenin pathway in uterine leiomyoma stem cells promotes tumor growth. Proc Natl Acad Sci U S A 2013;110:17053-8.
24. Sun Y, Campisi J, Higano C, Beer TM, Porter P, Coleman I, et al. Treatment-induced damage to the tumor microenvironment promotes prostate cancer therapy resistance through WNT16B. Nat Med 2012;18:1359-68.
25. Ring L, Perobner I, Karow M, Jochum M, Neth P, Faussner A. Reporter gene HEK 293 cells and WNT/Frizzled fusion proteins as tools to study WNT signaling pathways. Biol Chem 2011;392:1011-20.
26. Augustine CK, Toshimitsu H, Jung SH, Zipfel PA, Yoo JS, Yoshimoto Y, et al. Sorafenib, a multikinase inhibitor, enhances the response of melanoma to regional chemotherapy. Mol Cancer Ther 2010;9:2090-101.
27. Inaba K, Inaba M, Romani N, Aya H, Deguchi M, Ikehara S, et al. Generation of large numbers of dendritic cells from mouse bone marrow cultures supplemented with granulocyte/macrophage colony-stimulating factor. J Exp Med 1992;176:1693-702.
28. Nair S, Archer GE, Tedder TF. Isolation and generation of human dendritic cells. Curr Prot Immunol 2012;7:7.32.1-7.32.23(suppl 99).
29. Yue EW, Douty B, Wayland B, Bower M, Liu X, Leffet L, et al. Discovery of potent competitive inhibitors of indoleamine 2, 3-dioxygenase with in vivo pharmacodynamic activity and efficacy in a mouse melanoma model. J Med Chem 2009;52:7364-7.
30. Sheridan JT, Gilmore RC, Watson MJ, Archer CB, Tarran R. 17beta-Estradiol inhibits phosphorylation of stromal interaction molecule 1 (STIM1) protein: implication for store-operated calcium entry and chronic lung diseases. J Biol Chem 2013;288:33509-18.
31. Pallotta MT, Orabona C, Volpi C, Vacca C, Belladonna ML, Bianchi R, et al. Indoleamine 2, 3-dioxygenase is a signaling protein in long-term tolerance by dendritic cells. Nat Immunol 2011;12:870-8.
32. Ferrer-Vaquer A, Piliszek A, Tian G, Aho RJ, Dufort D, Hadjantonakis AK. A sensitive and bright single-cell resolution live imaging reporter of Wnt/ss-catenin signaling in the mouse. BMC Dev Biol 2010;10:121.
33. Soichot M, Hennart B, Al Saabi A, Leloire A, Froguel P, Levy-Marchal C, et al. Identification of a variable number of tandem repeats polymorphism and characterization of LEF-1 response elements in the promoter of the IDO1 gene. PLoS ONE 2011;6:e25470.
34. Muller AJ, Du Hadaway JB, Donover PS, Sutanto-Ward E, Prendergast G. Inhibition of indoleamine 2, 3-dioxygenase, an immunoregulatory target of the cancer suppression gene, Bin1, potentiates cancer chemotherapy. Nat Med 2005;11:312-9.
35. Braun D, Longman RS, Albert ML. A two-step induction of indoleamine 2, 3 dioxygenase (IDO) activity during dendritic-cell maturation. Blood 2005;106:2375-81.
36. Kikuchi A, Yamamoto H, Sato A, Matsumoto S. Wnt5a: its signalling, functions and implication in diseases. Acta Physiol 2012;204:17-33.
37. Mikels AJ, Nusse R. Purified Wnt5a protein activates or inhibits betacatenin-TCF signaling depending on receptor context. PLoS Biol 2006;4:e115.
38. Van Amerongen R, Fuerer C, Mizutani M, Nusse R. Wnt5a can both activate and repress Wnt/beta-catenin signaling during mouse embryonic development. Dev Biol 2012;369:101-14.
39. 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.
40. Wawrzak D, Metioui M, Willems E, Hendrickx M, De Genst E, Leyns L. Wnt3a binds to several sFRPs in the nanomolar range. Biochem Biophys Res Commun 2007;357:1119-23.
41. Yamada A, Iwata T, Yamato M, Okano T, Izumi Y. Diverse functions of secreted frizzled-related proteins in the osteoblastogenesis of human multipotent mesenchymal stromal cells. Biomaterials 2013;34:3270-8.
42. Blumenthal A, Ehlers S, Lauber J, Buer J, Lange C, Goldmann T, et al. The Wingless homolog WNT5A and its receptor Frizzled-5 regulate inflammatory responses of human mononuclear cells induced by microbial stimulation. Blood 2006;108:965-73.
43. Dhodapkar MV, Dhodapkar KM, Palucka AK. Interactions of tumor cells with dendritic cells: balancing immunity and tolerance. Cell Death Differ 2008;15:39-50.
44. Ma Y, Shurin GV, Peiyuan Z, Shurin MR. Dendritic cells in the cancer microenvironment. J Cancer 2013;4:36-44.
45. Holtzhausen A, Evans K, Siska P, Rathmell J, Hanks BA. Combinatorial TGF-beta signaling blockade and anti-CTLA-4 antibodyimmunotherapy in a murine BRAF (V600E)-PTEN-/-transgenic model of melanoma. J Clin Oncol 32: (5s), 2014(suppl; abstr 3011).
46. Hanks BA, Holtzhausen A, Jamieson R, Gimpel P, Campbell O, Sun L, et al. Type III TGF-b receptor downregulation generates an immunotolerant tumor microenvironment. J Clin Invest 2013;123:3925-40.
47. Carmon KS, Loose DS. Development of a bioassay for detection of Wntbinding affinities for individual frizzled receptors. Anal Biochem 2010;401:288-94.
48. Spranger S, Spaapen RM, Zha Y, Williams J, Meng Y, Ha TT, et al. Upregulation of PD-L1, IDO, and T (regs) in the melanoma tumor microenvironment is driven by CD8 (+) T cells. Sci Transl Med 2013;5:200ra116.
49. Holmgaard RB, Zamarin D, Munn DH, Wolchok JD, Allison JP. Indoleamine 2, 3-dioxygenase is a critical resistance mechanism in antitumor T cell immunotherapy targeting CTLA-4. J Exp Med 2013;210:1389-402.
50. Lum L, Clevers H. Cell biology. The unusual case of Porcupine. Science 2012;337:922-3.
51. Liu J, Pan S, Hsieh MH, Ng N, Sun F, Wang T, et al. Targeting Wnt-driven cancer through the inhibition of Porcupine by LGK974. Proc Natl Acad Sci U S A 2013;110:20224-9.
52. Proffitt KD, Madan B, Ke Z, Pendharkar V, Ding L, Lee MA, et al. Pharmacological inhibition of the Wnt acyltransferase PORCN prevents growth of WNT-driven mammary cancer. Cancer Res 2013;73:502-7.
53. Hong Y, Manoharan I, Suryawanshi A, Majumdar T, Angus-Hill ML, Koni PA, et al. Beta-catenin promotes regulatory t-cell responses in tumors by inducing vitamin a metabolism in dendritic cells. Cancer Res 2015;75:656-65.