Chemopreventive sphingadienes downregulate WNT signaling via a PP2A/Akt/GSK3β pathway in colon cancer

Carcinogenesis

Volumn 33, Issue 9, 2012, Pages 1726-1735

  Kumar, Ashok ^a   Pandurangan, Ashok K ^a   Lu, Fang ^a   Fyrst, Henrik ^a   Zhang, Meng ^a   Byun, Hoe Sup ^a   Bittman, Robert ^a   Saba, Julie D ^b  

^a CHILDREN S HOSPITAL OAKLAND RESEARCH INSTITUTE   (United States)

^b CITY UNIVERSITY OF NEW YORK   (United States)

Author keywords

[No Author keywords available]

Indexed keywords

ANTINEOPLASTIC AGENT; BETA CATENIN; MAMMALIAN TARGET OF RAPAMYCIN; PHOSPHATIDYLINOSITOL 3 KINASE; RAPAMYCIN; SPHINGADIENE; UNCLASSIFIED DRUG; WNT PROTEIN;

ANIMAL EXPERIMENT; ANIMAL MODEL; ANIMAL TISSUE; ANTINEOPLASTIC ACTIVITY; ARTICLE; CHEMOPROPHYLAXIS; COLON CANCER; COLON CARCINOGENESIS; CONTROLLED STUDY; DOWN REGULATION; GENE EXPRESSION; HUMAN; HUMAN CELL; LOW DRUG DOSE; MALE; MOUSE; NONHUMAN; ONCOGENE C MYC; PRIORITY JOURNAL; PROTEIN PHOSPHORYLATION;

AMP-ACTIVATED PROTEIN KINASES; ANTICARCINOGENIC AGENTS; CELL LINE, TUMOR; COLONIC NEOPLASMS; CYTOCHROME P-450 ENZYME SYSTEM; DOWN-REGULATION; GLYCOGEN SYNTHASE KINASE 3; HUMANS; PROTEIN PHOSPHATASE 2; PROTO-ONCOGENE PROTEINS C-AKT; RESPONSE ELEMENTS; SIGNAL TRANSDUCTION; SPHINGOLIPIDS; TUMOR SUPPRESSOR PROTEIN P53; WNT SIGNALING PATHWAY;

EID: 84865593352     PISSN: 01433334     EISSN: 14602180     Source Type: Journal    
DOI: 10.1093/carcin/bgs174     Document Type: Article

References (51)

1. Row, L.C. et al. (2007) Cerebrosides and tocopherol trimers from the seeds of Euryale ferox. J. Nat. Prod., 70, 1214-1217.
2. Sullards, M.C. et al. (2000) Structure determination of soybean and wheat glucosylceramides by tandem mass spectrometry. J. Mass Spectrom., 35, 347-353.
3. Fyrst, H. et al. (2008) Identification and characterization by electrospray mass spectrometry of endogenous Drosophila sphingadienes. J. Lipid Res., 49, 597-606.
4. Nilsson, A. et al. (2006) Absorption and lipoprotein transport of sphingomyelin. J. Lipid Res., 47, 154-171.
5. Fyrst, H. et al. (2009) Natural sphingadienes inhibit Akt-dependent signaling and prevent intestinal tumorigenesis. Cancer Res., 69, 9457-9464.
6. Moser, A. et al. (1990) A dominant mutation that predisposes to multiple intestinal neoplasia in the mouse. Science, 247, 322-324.
7. de Lau, W. et al. (2007) WNT signaling in the normal intestine and colorectal cancer. Front. Biosci., 12, 471-491.
8. Fuchs, S.Y. et al. (2005) Oncogenic beta-catenin signaling networks in colorectal cancer. Cell Cycle, 4, 1522-1539.
9. Satyamoorthy, K. et al. (2001) Insulin-like growth factor-1 induces survival and growth of biologically early melanoma cells through both the mitogen-activated protein kinase and beta-catenin pathways. Cancer Res., 61, 7318-7324.
10. Lovatt, M. et al. (2010) Stabilisation of beta-catenin downstream of T cell receptor signalling. PLoS One, 5, e12794.
11. McManus, E.J. et al. (2005) Role that phosphorylation of GSK3 plays in insulin and Wnt signalling defined by knockin analysis. EMBO J., 24, 1571-1583.
12. Oskouian, B. et al. (2006) Sphingosine-1-phosphate lyase potentiates apoptosis via p53- and p38-dependent pathways and is downregulated in colon cancer. Proc. Natl. Acad. Sci. U. S. A., 103, 17384-17389.
13. Ramaswamy, S. et al. (1999) Regulation of G1 progression by the PTEN tumor suppressor protein is linked to inhibition of the phosphatidylinositol 3-kinase/Akt pathway. Proc. Natl. Acad. Sci. U. S. A., 96, 2110-2115.
14. Chen, C.A. et al. (1988) Calcium phosphate-mediated gene transfer: a highly efficient transfection system for stably transforming cells with plasmid DNA. Biotechniques, 6, 632-638.
15. Veeman, M.T. et al. (2003) Zebrafish prickle, a modulator of noncanonical Wnt/Fz signaling, regulates gastrulation movements. Curr. Biol., 13, 680-685.
16. Chen, X. et al. (1999) Serum-induced expression of the cdc25A gene by relief of E2F-mediated repression. Mol. Cell. Biol., 19, 4695-4702.
17. Staal, F.J. et al. (2002) Wnt signals are transmitted through N-terminally dephosphorylated beta-catenin. EMBO Rep, 3, 63-68.
18. Kikuchi, A. et al. (2006) Regulation of Wnt signaling by protein-protein interaction and post-translational modifications. Exp. Mol. Med., 38, 1-10.
19. Cross, D.A. et al. (1995) Inhibition of glycogen synthase kinase-3 by insulin mediated by protein kinase B. Nature, 378, 785-789.
20. Hennessy, B.T. et al. (2005) Exploiting the PI3K/AKT pathway for cancer drug discovery. Nat Rev Drug Discov, 4, 988-1004.
21. Moran, A. et al. (2004) Apc deficiency is associated with increased Egfr activity in the intestinal enterocytes and adenomas of C57BL/6J-Min/+ mice. J. Biol. Chem., 279, 43261-43272.
22. Zoncu, R. et al. (2011) mTOR: from growth signal integration to cancer, diabetes and ageing. Nat Rev Mol Cell Biol, 12, 21-35.
23. Don, A.S. et al. (2011) Recent clinical trials of mTOR-targeted cancer therapies. Rev Recent Clin Trials, 6, 24-35.
24. Zolnierowicz, S. (2000) Type 2A protein phosphatase, the complex regulator of numerous signaling pathways. Biochem. Pharmacol., 60, 1225-1235.
25. Yang, J. et al. (2010) Functions of B56-containing PP2As in major developmental and cancer signaling pathways. Life Sci., 87, 659-666.
26. Jeon, K.I. et al. (2010) Ca2+/calmodulin-stimulated PDE1 regulates the beta-catenin/TCF signaling through PP2A B56 gamma subunit in proliferating vascular smooth muscle cells. FEBS J, 277, 5026-5039.
27. Zhang, W. et al. (2009) PR55 alpha, a regulatory subunit of PP2A, specifically regulates PP2A-mediated beta-catenin dephosphorylation. J. Biol. Chem., 284, 22649-22656.
28. Dobrowsky, R.T. et al. (1993) Ceramide activates heterotrimeric protein phosphatase 2A. J. Biol. Chem., 268, 15523-15530.
29. Ivaska, J. et al. (2002) Integrin alpha 2 beta 1 promotes activation of protein phosphatase 2A and dephosphorylation of Akt and glycogen synthase kinase 3 beta. Mol. Cell. Biol., 22, 1352-1359.
30. Powell, D.J. et al. (2003) Ceramide disables 3-phosphoinositide binding to the pleckstrin homology domain of protein kinase B (PKB)/Akt by a PKCzeta-dependent mechanism. Mol. Cell. Biol., 23, 7794-7808.
31. Abnet, C. et al. (2001) A cross-sectional study of human serum sphingolipids, diet and physiological parameters. J. Nutr., 131, 2748-2752.
32. Schmelz, E.M. et al. (1996) Sphingomyelin consumption suppresses aberrant colonic crypt foci and increases the proportion of adenomas versus adenocarcinomas in CF1 mice treated with 1, 2-dimethylhydrazine: implications for dietary sphingolipids and colon carcinogenesis. Cancer Res., 56, 4936-4941.
33. Ahn, E.H. et al. (2002) Sphingoid bases and ceramide induce apoptosis in HT-29 and HCT-116 human colon cancer cells. Exp Biol Med (Maywood), 227, 345-353.
34. Sweeney, E.A. et al. (1996) Sphingosine and its methylated derivative N, N-dimethylsphingosine (DMS) induce apoptosis in a variety of human cancer cell lines. Int. J. Cancer, 66, 358-366.
35. Lee, M.J. et al. (1999) Vascular endothelial cell adherens junction assembly and morphogenesis induced by sphingosine-1-phosphate. Cell, 99, 301-312.
36. Lee, H. et al. (2010) STAT3-induced S1PR1 expression is crucial for persistent STAT3 activation in tumors. Nat. Med., 16, 1421-1428.
37. Xia, P. et al. (2000) An oncogenic role of sphingosine kinase. Curr. Biol., 10, 1527-1530.
38. Kawamori, T. et al. (2006) Sphingosine kinase 1 is up-regulated in colon carcinogenesis. FASEB J., 20, 386-388.
39. Kawamori, T. et al. (2009) Role for sphingosine kinase 1 in colon carcinogenesis. FASEB J., 23, 405-414.
40. Chumanevich, A.A. et al. (2010) Suppression of colitis-driven colon cancer in mice by a novel small molecule inhibitor of sphingosine kinase. Carcinogenesis, 31, 1787-1793.
41. Sugawara, T. et al. (2010) Intestinal absorption of dietary maize glucosylceramide in lymphatic duct cannulated rats. J. Lipid Res., 51, 1761-1769.
42. Struckhoff, A.P. et al. (2004) Novel ceramide analogs as potential chemotherapeutic agents in breast cancer. J. Pharmacol. Exp. Ther., 309, 523-532.
43. Schmelz, E.M. et al. (2001) Modulation of intracellular beta-catenin localization and intestinal tumorigenesis in vivo and in vitro by sphingolipids. Cancer Res., 61, 6723-6729.
44. Symolon, H. et al. (2004) Dietary soy sphingolipids suppress tumorigenesis and gene expression in 1, 2-dimethylhydrazine-treated CF1 mice and ApcMin/+ mice. J. Nutr., 134, 1157-1161.
45. Lee, J.F. et al. (2006) Dual roles of tight junction-associated protein, zonula occludens-1, in sphingosine 1-phosphate-mediated endothelial chemotaxis and barrier integrity. J. Biol. Chem., 281, 29190-29200.
46. Paik, J.H. et al. (2004) Sphingosine 1-phosphate receptor regulation of N-cadherin mediates vascular stabilization. Genes Dev., 18, 2392-2403.
47. Singer, II et al. (2005) Sphingosine-1-phosphate agonists increase macrophage homing, lymphocyte contacts, and endothelial junctional complex formation in murine lymph nodes. J. Immunol., 175, 7151-7161.
48. Matsubara, S. et al. (2001) Expression of alpha-catenin in alpha-catenin-deficient cells increases resistance to sphingosine-induced apoptosis. J. Cell Biol., 154, 573-584.
49. Fujita, T. et al. (2004) Delta-catenin/NPRAP (neural plakophilin-related armadillo repeat protein) interacts with and activates sphingosine kinase 1. Biochem. J., 382, 717-723.
50. Ng, S.S. et al. (2009) Phosphatidylinositol 3-kinase signaling does not activate the wnt cascade. J. Biol. Chem., 284, 35308-35313.
51. Polakis, P. (2000) Wnt signaling and cancer. Genes Dev., 14, 1837-1851.