Molecular basis for the tissue specificity of β-catenin oncogenesis

Oncogene

Volumn 32, Issue 15, 2013, Pages 1901-1909

  Sharma, A ^a   Sen, J M ^a  

^a NATIONAL INSTITUTE ON AGING   (United States)

Author keywords

catenin; apoptosis; c Myc; hypocellular thymus; intestinal adenoma; p53

Indexed keywords

APC PROTEIN; BETA CATENIN; PROTEIN P53;

ANIMAL CELL; ANIMAL EXPERIMENT; ANIMAL MODEL; ANIMAL TISSUE; APOPTOSIS; ARTICLE; CANCER GROWTH; CANCER TISSUE; CARCINOGENESIS; CELL PROLIFERATION; COLON POLYPOSIS; CONTROLLED STUDY; GENE EXPRESSION; INTESTINE EPITHELIUM CELL; MOLECULAR BIOLOGY; MOUSE; NONHUMAN; ONCOGENE; PRIORITY JOURNAL; PROTEIN EXPRESSION; SENESCENCE; SIGNAL TRANSDUCTION; THYMOCYTE; THYMUS LYMPHOMA; TISSUE SPECIFICITY;

ADENOMATOUS POLYPOSIS COLI PROTEIN; ANIMALS; APOPTOSIS; BETA CATENIN; CELL AGING; CELL PROLIFERATION; CELL TRANSFORMATION, NEOPLASTIC; COLONIC NEOPLASMS; EPITHELIAL CELLS; GENE EXPRESSION REGULATION, NEOPLASTIC; INTESTINAL MUCOSA; INTESTINAL NEOPLASMS; INTESTINAL POLYPS; LYMPHOMA; MICE; MICE, INBRED C57BL; MICE, KNOCKOUT; ORGAN SPECIFICITY; PROTO-ONCOGENE PROTEINS C-MYC; SIGNAL TRANSDUCTION; THYMOCYTES; THYMUS NEOPLASMS; TUMOR SUPPRESSOR PROTEIN P53; WNT PROTEINS;

MUS;

EID: 84876100085     PISSN: 09509232     EISSN: 14765594     Source Type: Journal    
DOI: 10.1038/onc.2012.215     Document Type: Article

References (54)

1. Gregorieff A, Clevers H. Wnt signaling in the intestinal epithelium: from endoderm to cancer. Genes Dev 2005; 19: 877-890.
2. Korinek V, Barker N, Moerer P, van Donselaar E, Huls G, Peters PJ et al. Depletion of epithelial stem-cell compartments in the small intestine of mice lacking Tcf-4. Nat Genet 1998; 19: 379-383.
3. Ireland H, Kemp R, Houghton C, Howard L, Clarke AR, Sansom OJ et al. Inducible Cre-mediated control of gene expression in the murine gastrointestinal tract: effect of loss of beta-catenin. Gastroenterology 2004; 126: 1236-1246.
4. Kuhnert F, Davis CR, Wang HT, Chu P, Lee M, Yuan J et al. Essential requirement for Wnt signaling in proliferation of adult small intestine and colon revealed by adenoviral expression of Dickkopf-1. Proc Natl Acad Sci USA 2004; 101: 266-271.
5. Shibata H, Toyama K, Shioya H, Ito M, Hirota M, Hasegawa S et al. Rapid colorectal adenoma formation initiated by conditional targeting of the Apc gene. Science 1997; 278: 120-123.
6. Korinek V, Barker N, Morin PJ, van Wichen D, de Weger R, Kinzler KW et al. Constitutive transcriptional activation by a beta-catenin-Tcf complex in APC-/-colon carcinoma. Science 1997; 275: 1784-1787.
7. Sansom OJ, Reed KR, Hayes AJ, Ireland H, Brinkmann H, Newton IP et al. Loss of Apc in vivo immediately perturbs Wnt signaling, differentiation, and migration. Genes Dev 2004; 18: 1385-1390.
8. van de Wetering M, Sancho E, Verweij C, de Lau W, Oving I, Hurlstone A et al. The beta-catenin/TCF-4 complex imposes a crypt progenitor phenotype on colorectal cancer cells. Cell 2002; 111: 241-250.
9. Sansom OJ, Meniel VS, Muncan V, Phesse TJ, Wilkins JA, Reed KR et al. Myc deletion rescues Apc deficiency in the small intestine. Nature 2007; 446: 676-679.
10. Roose J, Huls G, van Beest M, Moerer P, van der Horn K, Goldschmeding R et al. Synergy between tumor suppressor APC and the beta-catenin-Tcf4 target Tcf1. Science 1999; 285: 1923-1926.
11. Polakis P. Wnt signaling and cancer. Genes Dev 2000; 14: 1837-1851.
12. Weerkamp F, van Dongen JJ, Staal FJ. Notch and Wnt signaling in T-lymphocyte development and acute lymphoblastic leukemia. Leukemia 2006; 20: 1197-1205.
13. Staal FJ, Langerak AW. Signaling pathways involved in the development of T-cell acute lymphoblastic leukemia. Haematologica 2008; 93: 493-497.
14. Serinsoz E, Neusch M, Busche G, Wasielewski R, Kreipe H, Bock O. Aberrant expression of beta-catenin discriminates acute myeloid leukaemia from acute lymphoblastic leukaemia. Br J Haematol 2004; 126: 313-319.
15. Dorfman DM, Greisman HA, Shahsafaei A. Loss of expression of the WNT/beta-catenin-signaling pathway transcription factors lymphoid enhancer factor-1 (LEF-1) and T cell factor-1 (TCF-1) in a subset of peripheral T cell lymphomas. Am J Pathol 2003; 162: 1539-1544.
16. Bellei B, Pacchiarotti A, Perez M, Faraggiana T. Frequent beta-catenin over-expression without exon 3 mutation in cutaneous lymphomas. Mod Pathol 2004; 17: 1275-1281.
17. Grigoryan T, Wend P, Klaus A, Birchmeier W. Deciphering the function of canonical Wnt signals in development and disease: conditional loss-and gain-of-function mutations of beta-catenin in mice. Genes Dev 2008; 22: 2308-2341.
18. Staal FJ, Meeldijk J, Moerer P, Jay P, van de Weerdt BC, Vainio S et al. Wnt signaling is required for thymocyte development and activates Tcf-1 mediated transcription. Eur J Immunol 2001; 31: 285-293.
19. Xu Y, Banerjee D, Huelsken J, Birchmeier W, Sen JM. Deletion of beta-catenin impairs T cell development. Nat Immunol 2003; 4: 1177-1182.
20. Xu Y, Sen J. Beta-catenin expression in thymocytes accelerates thymic involution. Eur J Immunol 2003; 33: 12-18.
21. Yu Q, Sharma A, Sen JM. TCF1 and beta-catenin regulate T cell development and function. Immunol Res 2010; 47: 45-55.
22. Xu M, Sharma A, Wiest DL, Sen JM. Pre-TCR-induced beta-catenin facilitates traversal through beta-selection. J Immunol 2009; 182: 751-758.
23. Xu M, Sharma A, Hossain MZ, Wiest DL, Sen JM. Sustained expression of pre-TCR induced beta-catenin in post-beta-selection thymocytes blocks T cell development. J Immunol 2009; 182: 759-765.
24. Xu M, Yu Q, Subrahmanyam R, Difilippantonio MJ, Ried T, Sen JM. Beta-catenin expression results in p53-independent DNA damage and oncogene-induced senescence in prelymphomagenic thymocytes in vivo. Mol Cell Biol 2008; 28: 1713-1723.
25. Moser AR, Pitot HC, Dove WF. A dominant mutation that predisposes to multiple intestinal neoplasia in the mouse. Science 1990; 247: 322-324.
26. Su LK, Kinzler KW, Vogelstein B, Preisinger AC, Moser AR, Luongo C et al. Multiple intestinal neoplasia caused by a mutation in the murine homolog of the APC gene. Science 1992; 256: 668-670.
27. Pajari AM, Rajakangas J, Paivarinta E, Kosma VM, Rafter J, Mutanen M. Promotion of intestinal tumor formation by inulin is associated with an accumulation of cytosolic beta-catenin in Min mice. Int J Cancer 2003; 106: 653-660.
28. Ignatenko NA, Holubec H, Besselsen DG, Blohm-Mangone KA, Padilla-Torres JL, Nagle RB et al. Role of c-Myc in intestinal tumorigenesis of the ApcMin/+ mouse. Cancer Biol Ther 2006; 5: 1658-1664.
29. Luongo C, Moser AR, Gledhill S, Dove WF. Loss of Apc + in intestinal adenomas from Min mice. Cancer Res 1994; 54: 5947-5952.
30. Ciofani M, Zuniga-Pflucker JC. A survival guide to early T cell development. Immunol Res 2006; 34: 117-132.
31. Gounari F, Chang R, Cowan J, Guo Z, Dose M, Gounaris E et al. Loss of adeno-matous polyposis coli gene function disrupts thymic development. Nat Immunol 2005; 6: 800-809.
32. Mulroy T, Xu Y, Sen JM. beta-Catenin expression enhances generation of mature thymocytes. Int Immunol 2003; 15: 1485-1494.
33. Damalas A, Kahan S, Shtutman M, Ben-Ze'ev A, Oren M. Deregulated beta-catenin induces a p53-and ARF-dependent growth arrest and cooperates with Ras in transformation. EMBO J 2001; 20: 4912-4922.
34. Reed KR, Meniel VS, Marsh V, Cole A, Sansom OJ, Clarke AR. A limited role for p53 in modulating the immediate phenotype of Apc loss in the intestine. BMC Cancer 2008; 8: 162.
35. Sansom OJ, Griffiths DF, Reed KR, Winton DJ, Clarke AR. Apc deficiency predisposes to renal carcinoma in the mouse. Oncogene 2005; 24: 8205-8210.
36. Cole AM, Ridgway RA, Derkits SE, Parry L, Barker N, Clevers H et al. p21 loss blocks senescence following Apc loss and provokes tumourigenesis in the renal but not the intestinal epithelium. EMBO Mol Med 2010; 2: 472-486.
37. Young NP, Jacks T. Tissue-specific p19Arf regulation dictates the response to oncogenic K-ras. Proc Natl Acad Sci USA 2010; 107: 10184-10189.
38. Reed KR, Athineos D, Meniel VS, Wilkins JA, Ridgway RA, Burke ZD et al. B-catenin deficiency, but not Myc deletion, suppresses the immediate phenotypes of APC loss in the liver. Proc Natl Acad Sci USA 2008; 105: 18919-18923.
39. Castrop J, van Wichen D, Koomans-Bitter M, van de Wetering M, de Weger R, van Dongen J et al. The human TCF-1 gene encodes a nuclear DNA-binding protein uniquely expressed in normal and neoplastic T-lineage lymphocytes. Blood 1995; 86: 3050-3059.
40. Tsutsui J, Moriyama M, Arima N, Ohtsubo H, Tanaka H, Ozawa M. Expression of cadherin-catenin complexes in human leukemia cell lines. J Biochem 1996; 120: 1034-1039.
41. Chung EJ, Hwang SG, Nguyen P, Lee S, Kim JS, Kim JW et al. Regulation of leukemic cell adhesion, proliferation, and survival by beta-catenin. Blood 2002; 100: 982-990.
42. Staal FJ, Burgering BM, van de Wetering M, Clevers HC. Tcf-1-mediated transcription in T lymphocytes: differential role for glycogen synthase kinase-3 in fibroblasts and T cells. Int Immunol 1999; 11: 317-323.
43. Prieve MG, Waterman ML. Nuclear localization and formation of beta-catenin-lymphoid enhancer factor 1 complexes are not sufficient for activation of gene expression. Mol Cell Biol 1999; 19: 4503-4515.
44. Groen RW, Oud ME, Schilder-Tol EJ, Overdijk MB, ten Berge D, Nusse R et al. Illegitimate WNT pathway activation by beta-catenin mutation or autocrine stimulation in T-cell malignancies. Cancer Res 2008; 68: 6969-6977.
45. Gounari F, Aifantis I, Khazaie K, Hoeflinger S, Harada N, Taketo MM et al. Somatic activation of beta-catenin bypasses pre-TCR signaling and TCR selection in thy-mocyte development. Nat Immunol 2001; 2: 863-869.
46. Coletta PL, Muller AM, Jones EA, Muhl B, Holwell S, Clarke D et al. Lymphode-pletion in the ApcMin/+ mouse model of intestinal tumorigenesis. Blood 2004; 103: 1050-1058.
47. Reya T, Clevers H. Wnt signalling in stem cells and cancer. Nature 2005; 434: 843-850.
48. Guo Z, Dose M, Kovalovsky D, Chang R, O'Neil J, Look AT et al. Beta-catenin stabilization stalls the transition from double-positive to single-positive stage and predisposes thymocytes to malignant transformation. Blood 2007; 109: 5463-5472.
49. Luis TC, Naber BA, Roozen PP, Brugman MH, de Haas EF, Ghazvini M et al. Canonical wnt signaling regulates hematopoiesis in a dosage-dependent fashion. Cell Stem Cell 2011; 9: 345-356.
50. You L, Xu Z, Punchihewa C, Jablons DM, Fujii N. Evaluation of a chemical library of small-molecule Dishevelled antagonists that suppress tumor growth by down-regulating T-cell factor-mediated transcription. Mol Cancer Ther 2008; 7: 1633-1638.
51. Gandhirajan RK, Staib PA, Minke K, Gehrke I, Plickert G, Schlosser A et al. Small molecule inhibitors of Wnt/beta-catenin/lef-1 signaling induces apoptosis in chronic lymphocytic leukemia cells in vitro and in vivo 2010. Neoplasia 12: 326-335.
52. Chen B, Dodge ME, Tang W, Lu J, Ma Z, Fan CW et al. Small molecule-mediated disruption of Wnt-dependent signaling in tissue regeneration and cancer. Nat Chem Biol 2009; 5: 100-107.
53. Tang X, Zhu Y, Han L, Kim AL, Kopelovich L, Bickers DR et al. CP-31398 restores mutant p53 tumor suppressor function and inhibits UVB-induced skin carcino-genesis in mice. J Clin Invest 2007; 117: 3753-3764.
54. Wiman KG. Pharmacological reactivation of mutant p53: from protein structure to the cancer patient 2010Oncogene 29: 4245-4252.