CTLA-4 is a direct target of Wnt/β-catenin signaling and is expressed in human melanoma tumors

Journal of Investigative Dermatology

Volumn 128, Issue 12, 2008, Pages 2870-2879

  Shah, Kavita V ^a   Chien, Andy J ^b   Yee, Cassian ^b,c   Moon, Randall T ^a  

^a UNIVERSITY OF WASHINGTON SCHOOL OF MEDICINE   (United States)

^b UNIVERSITY OF WASHINGTON   (United States)

^c USA   (United States)

Author keywords

[No Author keywords available]

Indexed keywords

BETA CATENIN; CYTOTOXIC T LYMPHOCYTE ANTIGEN 4; RECOMBINANT PROTEIN; TRANSCRIPTION FACTOR 7; WNT PROTEIN;

ARTICLE; CANCER CELL; CONTROLLED STUDY; HUMAN; HUMAN CELL; MELANOCYTE; MELANOMA; NUCLEOTIDE SEQUENCE; PRIORITY JOURNAL; PROTEIN EXPRESSION; PROTEIN TARGETING; TRANSCRIPTION INITIATION;

ANTIGENS, CD; BETA CATENIN; BINDING SITES; CELL LINE, TUMOR; CULTURE MEDIA, CONDITIONED; FLOW CYTOMETRY; GENE EXPRESSION REGULATION, NEOPLASTIC; HUMANS; MELANOMA; OLIGONUCLEOTIDE ARRAY SEQUENCE ANALYSIS; REVERSE TRANSCRIPTASE POLYMERASE CHAIN REACTION; SIGNAL TRANSDUCTION; SKIN NEOPLASMS; TRANSCRIPTION, GENETIC; WNT PROTEINS;

EID: 57349099365     PISSN: 0022202X     EISSN: 15231747     Source Type: Journal    
DOI: 10.1038/jid.2008.170     Document Type: Article

References (62)

1. Alegre ML, Noel PJ, Eisfelder BJ, Chuang E, Clark MR, Reiner SL et al. (1996) Regulation of surface and intracellular expression of CTLA4 on mouse T cells. J Immunol 157:4762-70
2. Alegre ML, Shiels H, Thompson CB, Gajewski TF (1998) Expression and function of CTLA-4 in Th1 and Th2 cells. J Immunol 161:3347-56
3. Angers S, Thorpe CJ, Biechele TL, Goldenberg SJ, Zheng N, MacCoss MJ et al. (2006) The KLHL12-Cullin-3 ubiquitin ligase negatively regulates the Wnt-beta-catenin pathway by targeting dishevelled for degradation. Nat Cell Biol 8:348-57
4. Anjos SM, Tessier MC, Polychronakos C (2004) Association of the cytotoxic T lymphocyte-associated antigen 4 gene with type 1 diabetes: evidence for independent effects of two polymorphisms on the same haplotype block. J Clin Endocrinol Metab 89:6257-65
5. Anna CH, Iida M, Sills RC, Devereux TR (2003) Expression of potential beta-catenin targets, cyclin D1, c-Jun, c-Myc, E-cadherin, and EGFR in chemically induced hepatocellular neoplasms from B6C3F1 mice. Toxicol Appl Pharmacol 190:135-45
6. Attia P, Phan GQ, Maker AV, Robinson MR, Quezado MM, Yang JC et al. (2005) Autoimmunity correlates with tumor regression in patients with metastatic melanoma treated with anti-cytotoxic T-lymphocyte antigen-4. J Clin Oncol 23:6043-53
7. Bittner M, Meltzer P, Chen Y, Jiang Y, Seftor E, Hendrix M et al. (2000) Molecular classification of cutaneous malignant melanoma by gene expression profiling. Nature 406:536-40
8. Chin L, Garraway LA, Fisher DE (2006) Malignant melanoma: genetics and therapeutics in the genomic era. Genes Dev 20:2149-82
9. Chistiakov DA, Savost'anov KV, Turakulov RI, Efremov IA, Demurov LM (2006) Genetic analysis and functional evaluation of the C/T(-318) and A/G(-1661) polymorphisms of the CTLA-4 gene in patients affected with Graves' disease. Clin Immunol 118:233-42
10. Chuang E, Alegre ML, Duckett CS, Noel PJ, Vander Heiden MG, Thompson CB (1997) Interaction of CTLA-4 with the clathrin-associated protein AP50 results in ligand-independent endocytosis that limits cell surface expression. J Immunol 159:144-51
11. Clevers H (2006) Wnt/beta-catenin signaling in development and disease. Cell 127:469-80
12. Contardi E, Palmisano GL, Tazzari PL, Martelli AM, Fala F, Fabbi M et al. (2005) CTLA-4 is constitutively expressed on tumor cells and can trigger apoptosis upon ligand interaction. Int J Cancer 117:538-50
13. Cummins DL, Cummins JM, Pantle H, Silverman MA, Leonard AL, Chanmugam A (2006) Cutaneous malignant melanoma. Mayo Clin Proc 81:500-7
14. Demunter A, Libbrecht L, Degreef H, De Wolf-Peeters C, van den Oord JJ (2002) Loss of membranous expression of beta-catenin is associated with tumor progression in cutaneous melanoma and rarely caused by exon 3 mutations. Mod Pathol 15:454-61
15. Dhawan P, Richmond A (2002) Role of CXCL1 in tumorigenesis of melanoma. J Leukoc Biol 72:9-18
16. Diepgen TL, Mahler V (2002) The epidemiology of skin cancer. Br J Dermatol 146(Suppl 61):1-6
17. Dissanayake SK, Wade M, Johnson CE, O'Connell MP, Leotlela PD, French AD et al. (2007) The Wnt5A/protein kinase C pathway mediates motility in melanoma cells via the inhibition of metastasis suppressors and initiation of an epithelial to mesenchymal transition. J Biol Chem 282:17259-71
18. Fallarino F, Grohmann U, Hwang KW, Orabona C, Vacca C, Bianchi R et al. (2003) Modulation of tryptophan catabolism by regulatory T cells. Nat Immunol 4:1206-12
19. Fecher LA, Cummings SD, Keefe MJ, Alani RM (2007) Toward a molecular classification of melanoma. J Clin Oncol 25:1606-20
20. Ghaderi A, Yeganeh F, Kalantari T, Talei AR, Pezeshki AM, Doroudchi M et al. (2004) Cytotoxic T lymphocyte antigen-4 gene in breast cancer. Breast Cancer Res Treat 86:1-7
21. Grohmann U, Orabona C, Fallarino F, Vacca C, Calcinaro F, Falorni A et al. (2002) CTLA-4-Ig regulates tryptophan catabolism in vivo. Nat Immunol 3:1097-101
22. Hurwitz AA, Foster BA, Kwon ED, Truong T, Choi EM, Greenberg NM et al. (2000) Combination immunotherapy of primary prostate cancer in a transgenic mouse model using CTLA-4 blockade. Cancer Res 60:2444-8
23. Iida T, Ohno H, Nakaseko C, Sakuma M, Takeda-Ezaki M, Arase H et al. (2000) Regulation of cell surface expression of CTLA-4 by secretion of CTLA-4-containing lysosomes upon activation of CD4+ T cells. J Immunol 165:5062-8
24. Kasper B, D'Hondt V, Vereecken P, Awada A (2007) Novel treatment strategies for malignant melanoma: a new beginning? Crit Rev Oncol Hematol 62:16-22
25. Kaykas A, Yang-Snyder J, Heroux M, Shah KV, Bouvier M, Moon RT (2004) Mutant Frizzled 4 associated with vitreoretinopathy traps wild-type Frizzled in the endoplasmic reticulum by oligomerization. Nat Cell Biol 6:52-8
26. Kohn AD, Moon RT (2005) Wnt and calcium signaling: beta-catenin- independent pathways. Cell Calcium 38:439-46
27. Krummel MF, Allison JP (1996) CTLA-4 engagement inhibits IL-2 accumulation and cell cycle progression upon activation of resting T cells. J Exp Med 183:2533-40
28. Kuphal S, Lodermeyer S, Bataille F, Schuierer M, Hoang BH, Bosserhoff AK (2006) Expression of Dickkopf genes is strongly reduced in malignant melanoma. Oncogene 25:5027-36
29. Larue L, Delmas V (2006) The WNT/Beta-catenin pathway in melanoma. Front Biosci 11:733-42
30. Laurent S, Palmisano GL, Martelli AM, Kato T, Tazzari PL, Pierri I et al. (2007) CTLA-4 expressed by chemoresistant, as well as untreated, myeloid leukaemia cells can be targeted with ligands to induce apoptosis. Br J Haematol 136:597-608
31. Leach DR, Krummel MF, Allison JP (1996) Enhancement of antitumor immunity by CTLA-4 blockade. Science 271:1734-6
32. Leotlela PD, Wade MS, Duray PH, Rhode MJ, Brown HF, Rosenthal DT et al. (2007) Claudin-1 overexpression in melanoma is regulated by PKC and contributes to melanoma cell motility. Oncogene 26:3846-56
33. Logan CY, Nusse R (2004) The Wnt signaling pathway in development and disease. Annu Rev Cell Dev Biol 20:781-810
34. Major MB, Camp ND, Berndt JD, Yi X, Goldenberg SJ, Hubbert C et al. (2007) Wilms tumor suppressor WTX negatively regulates WNT/beta-catenin signaling. Science 316:1043-6
35. Maker AV, Attia P, Rosenberg SA (2005) Analysis of the cellular mechanism of antitumor responses and autoimmunity in patients treated with CTLA-4 blockade. J Immunol 175:7746-54
36. Mandelbrot DA, Oosterwegel MA, Shimizu K, Yamada A, Freeman GJ, Mitchell RN et al. (2001) B7-dependent T-cell costimulation in mice lacking CD28 and CTLA4. J Clin Invest 107:881-7
37. Manenti S, Malecaze F, Chap H, Darbon JM (1998) Overexpression of the myristoylated alanine-rich C kinase substrate in human choroidal melanoma cells affects cell proliferation. Cancer Res 58:1429-34
38. Miller AJ, Mihm MC Jr (2006) Melanoma. N Engl J Med 355:51-65
39. Monne M, Piras G, Palmas A, Arru L, Murineddu M, Latte G et al. (2004) Cytotoxic T-lymphocyte antigen-4 (CTLA-4) gene polymorphism and susceptibility to non-Hodgkin's lymphoma. Am J Hematol 76:14-8
40. Munn DH, Sharma MD, Mellor AL (2004) Ligation of B7-1/B7-2 by human CD4+ T cells triggers indoleamine 2,3-dioxygenase activity in dendritic cells. J Immunol 172:4100-10
41. Murakami T, Toda S, Fujimoto M, Ohtsuki M, Byers HR, Etoh T et al. (2001) Constitutive activation of Wnt/beta-catenin signaling pathway in migration-active melanoma cells: role of LEF-1 in melanoma with increased metastatic potential. Biochem Biophys Res Commun 288:8-15
42. Pawlak E, Kochanowska IE, Frydecka I, Kielbinski M, Potoczek S, Bilinska M (2005) The soluble CTLA-4 receptor: a new marker in autoimmune diseases. Arch Immunol Ther Exp 53:336-41
43. Perkins D, Wang Z, Donovan C, He H, Mark D, Guan G et al. (1996) Regulation of CTLA-4 expression during T cell activation. J Immunol 156:4154-9
44. Pham K, Milovanovic T, Barr RJ, Truong T, Holcombe RF (2003) Wnt ligand expression in malignant melanoma: pilot study indicating correlation with histopathological features. Mol Pathol 56:280-5
45. Pistillo MP, Tazzari PL, Palmisano GL, Pierri I, Bolognesi A, Ferlito F et al. (2003) CTLA-4 is not restricted to the lymphoid cell lineage and can function as a target molecule for apoptosis induction of leukemic cells. Blood 101:202-9
46. Reifenberger J, Knobbe CB, Wolter M, Blaschke B, Schulte KW, Pietsch T et al. (2002) Molecular genetic analysis of malignant melanomas for aberrations of the WNT signaling pathway genes CTNNB1, APC, ICAT and BTRC. Int J Cancer 100:549-56
47. Rimm DL, Caca K, Hu G, Harrison FB, Fearon ER (1999) Frequent nuclear/ cytoplasmic localization of beta-catenin without exon 3 mutations in malignant melanoma. Am J Pathol 154:325-9
48. Rodolfo M, Daniotti M, Vallacchi V (2004) Genetic progression of metastatic melanoma. Cancer Lett 214:133-47
49. Rubinfeld B, Robbins P, El-Gamil M, Albert I, Porfiri E, Polakis P (1997) Stabilization of beta-catenin by genetic defects in melanoma cell lines. Science 275:1790-2
50. Sekiya T, Adachi S, Kohu K, Yamada T, Higuchi O, Furukawa Y et al. (2004) Identification of BMP and activin membrane-bound inhibitor (BAMBI), an inhibitor of transforming growth factor-beta signaling, as a target of the beta-catenin pathway in colorectal tumor cells. J Biol Chem 279:6840-6
51. Takahashi T, Tagami T, Yamazaki S, Uede T, Shimizu J, Sakaguchi N et al. (2000) Immunologic self-tolerance maintained by CD25(+)CD4(+) regulatory T cells constitutively expressing cytotoxic T lymphocyte-associated antigen 4. J Exp Med 192:303-10
52. Teft WA, Kirchhof MG, Madrenas J (2006) A molecular perspective of CTLA-4 function. Annu Rev Immunol 24:65-97
53. Tirapu I, Huarte E, Guiducci C, Arina A, Zaratiegui M, Murillo O et al. (2006) Low surface expression of B7-1 (CD80) is an immunoescape mechanism of colon carcinoma. Cancer Res 66:2442-50
54. van Elsas A, Hurwitz AA, Allison JP (1999) Combination immunotherapy of B16 melanoma using anti-cytotoxic T lymphocyte-associated antigen 4 (CTLA-4) and granulocyte/macrophage colony-stimulating factor (GMCSF)-producing vaccines induces rejection of subcutaneous and metastatic tumors accompanied by autoimmune depigmentation. J Exp Med 190:355-66
55. Veeman MT, Axelrod JD, Moon RT (2003) A second canon. Functions and mechanisms of beta-catenin-independent Wnt signaling. Dev Cell 5:367-77
56. Walunas TL, Bakker CY, Bluestone JA (1996) CTLA-4 ligation blocks CD28-dependent T cell activation. J Exp Med 183:2541-50
57. Wang HY, Wang RF (2007) Regulatory T cells and cancer. Curr Opin Immunol 19:217-23
58. Weeraratna AT (2005) A Wnt-er wonderland - the complexity of Wnt signaling in melanoma. Cancer Metastasis Rev 24:237-50
59. Weeraratna AT, Jiang Y, Hostetter G, Rosenblatt K, Duray P, Bittner M et al. (2002) Wnt5a signaling directly affects cell motility and invasion of metastatic melanoma. Cancer Cell 1:279-88
60. Willert K, Brown JD, Danenberg E, Duncan AW, Weissman IL, Reya T et al. (2003) Wnt proteins are lipid-modified and can act as stem cell growth factors. Nature 423:448-52
61. Worm J, Christensen C, Gronbaek K, Tulchinsky E, Guldberg P (2004) Genetic and epigenetic alterations of the APC gene in malignant melanoma. Oncogene 23:5215-26
62. Zheng C, Huang D, Liu L, Bjorkholm M, Holm G, Yi Q et al. (2001) Cytotoxic T-lymphocyte antigen-4 microsatellite polymorphism is associated with multiple myeloma. Br J Haematol 112:216-8