Regulation of β-catenin and connexin-43 expression: Targets for sphingolipids in colon cancer prevention

Molecular Nutrition and Food Research

Volumn 53, Issue 3, 2009, Pages 332-340

  Simon, Kirk W ^a   Roberts, Paul C ^b   Vespremi, Michael J ^a   Manchen, Steve ^a   Schmelz, Eva M ^b  

^a WAYNE STATE UNIVERSITY   (United States)

^b VIRGINIA POLYTECHNIC INSTITUTE AND STATE UNIVERSITY   (United States)

Author keywords

catenin; Bcl 2; Colon cancer prevention; Connexin 43; Sphingomyelin

Indexed keywords

BETA CATENIN; CARCINOGEN; CONNEXIN 43; DIMETHYLHYDRAZINE; MESSENGER RNA; SPHINGOMYELIN;

ANIMAL; APOPTOSIS; ARTICLE; CELL DIVISION; CHEMICALLY INDUCED DISORDER; CHEMISTRY; COLON TUMOR; DIET; DOWN REGULATION; DRUG EFFECT; FEMALE; GENE EXPRESSION REGULATION; GENETICS; IMMUNOHISTOCHEMISTRY; INTESTINE MUCOSA; MOUSE; PROGNOSIS; PROTO ONCOGENE; REVERSE TRANSCRIPTION POLYMERASE CHAIN REACTION; WESTERN BLOTTING;

ANIMALS; APOPTOSIS; BETA CATENIN; BLOTTING, WESTERN; CARCINOGENS; CELL DIVISION; COLONIC NEOPLASMS; CONNEXIN 43; DIET; DIMETHYLHYDRAZINES; DOWN-REGULATION; FEMALE; GENE EXPRESSION REGULATION; GENES, BCL-2; IMMUNOHISTOCHEMISTRY; INTESTINAL MUCOSA; MICE; PROGNOSIS; REVERSE TRANSCRIPTASE POLYMERASE CHAIN REACTION; RNA, MESSENGER; SPHINGOMYELINS;

ANIMALIA; MUS;

EID: 62749107624     PISSN: 16134125     EISSN: 16134133     Source Type: Journal    
DOI: 10.1002/mnfr.200800102     Document Type: Article

References (53)

1. Fearon, E. R., Vogelstein, B., A genetic model for colorectal tumorigenesis, Cell 1990, 61, 759-767.
2. Jen, J., Powell, S. M., Papdopoulos, N., Smith, K. J., et al., Molecular determinants of dysplasia in colorectal lesions, Cancer Res. 1994, 54, 5523-55262.
3. Kinzler, K. W., Vogelstein, B., Lessons from hereditary colorectal cancer, Cell 1996, 87, 159-170.
4. Cottrell, S., Bicknell, D., Kaklamanis, L., Bodmer, W. F., Molecular analysis of APC mutations in familial adenomatous polyposis and sporadic colon carcinomas, Lancet 1992, 340, 626-630.
5. Sparks, A. B., Morin, P. J., Vogelstein, B., Kinzler, K. W., Mutational analysis of the APC/beta-catenin/Tcf pathway in colorectal cancer, Cancer Res. 1998, 58, 1130-1134.
6. Takahashi, M., Mutoh, M., Kawamori, T., Sugimura, T., Wakabayashi, K., Altered β-catenin, inducible nitric oxide synthase and cyclooxygenase-2 in azoxymethane-induced rat colon carcinogenesis, Carcinogenesis 2000, 21, 1319-1327.
7. Otori, K., Konishi, M., Sugiyama, K., Hasebe, T., et al., Infrequent somatic mutation of the adenomatous polyposis coli gene in aberrant crypt foci of human colon tissue, Cancer 1998, 83, 896-900.
8. Schmelz, E. M., Sphingolipids and Chemoprevention, Front. Biosci. 2004, 9, 2632-2639.
9. Dillehay, D. L., Webb, S. K., Schmelz, E. M., Merrill, A. H., Jr., Dietary sphingomyelin inhibits 1,2-dimethylhydrazine-induced colon cancer in CF1 mice, J. Nutr. 1994, 124, 615-620.
10. Schmelz, E. M., Dillehay, D. L., Webb, S., Reiter, A., et al., 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. 1996, 56, 4936-4941.
11. Schmelz, E. M., Bushnev, A. B., Dillehay, D. L., Liotta, D. C., Merrill, A. H., Jr., Suppression of aberrant colonic crypt foci by synthetic sphingomyelins with saturated or unsaturated sphingoid base backbones, Nutr. Cancer 1997, 28, 81-85.
12. Schmelz, E. M., Dillehay, D. L., Sullards, M. C., Merrill, A. H., Jr., Colonic cell proliferation and aberrant crypt foci formation are inhibited by dairy glycosphingolipids in 1,2-dimethylhydrazine-treated CF1 mice, J. Nutr. 2000, 130, 522-527.
13. Lemonnier, L. A., Dillehay, D. L., Vespremi, M. J., Abrams, J., et al., Sphingomyelin in the suppression of colon tumors: Prevention versus intervention, Arch. Biochem. Biophys. 2003, 419, 129-138.
14. Schmelz, E. M., Roberts, P. C., Kustin, E. M., Lemonnier, L. A., et al., Modulation of intracellular β-catenin localization and intestinal tumorigenesis in vivo and in vitro by sphingolipids, Cancer Res. 2001, 61, 6723-6729.
15. Nilsson, A., Duan, R. D., Absorption and lipoprotein transport of sphingomyelin, J. Lipid Res. 2006, 47, 154-171.
16. Schmelz, E. M., Crall, K. L., LaRocque, R., Dillehay, D. L., Merrill, A. H., Jr., Uptake and metabolism of sphingolipids in isolated intestinal loops of mice, J. Nutr. 1994, 124, 702-712.
17. Nichenametla, S., South, E., Exon, J., Interaction of conjugated linoleic acid, sphingomyelin, and butyrate on formation of colonic aberrant crypt foci and immune functions in rats, J. Toxicol. Environ. Health 2004, 67, 469-481.
18. Graff, J. R., Herman, J. G., Lapidus, R. G., Chopra, H., et al., E-cadherin expression is silenced by DNA hypermethylation in human breast and prostate carcinomas, Cancer Res. 1995, 55, 5195-5199.
19. Husoy, T., Olstorn, H. B., Knutson, H. K., Loberg, E. M., et al., Truncated mouse adenomatous polyposis coli reduces connexin32 content and increases matrilysin secretion from Paneth cells, Eur. J. Cancer 2004, 40, 1599-1603.
20. American Institute of Nutrition, Report of the American Institute of Nutrition ad hoc committee on standards for nutritional studies, J. Nutr. 1977, 107, 1340-1348.
21. Weisburger, H., Fiala, E. S., in: H. Autrop, G. M. Williams (Eds.), Experimental Colon Carcinogenesis, CRC Press, Boca Raton 1982, pp. 27-50.
22. Efstathiou, J. A., Liu, D., Wheeler, J. M., Kim, H. C., et al., Mutated epithelial cadherin is associated with increased tumorigenicity and loss of adhesion and of responsiveness to the motogenic trefoil factor 2 in colon carcinoma cells, Proc. Natl. Acad. Sci. USA 1999, 96, 2316-21.
23. Wheeler, J., Kim, H., Efstathiou, J. M., Ilyas, M., et al., Hypermethylation of the promoter region of the E-cadherin gene (CDH1) in sporadic and ulcerative colitis associated colorectal cancer, Gut 2008, 48, 367-371.
24. Husoy, T., Cruciani, V., Knutson, H. K., Mikalsen, S. O., et al., Cells heterozygous for the ApcMin mutation have decreased gap junctional intercellular communication and connexin43 level, and reduced microtubule polymerization, Carcinogenesis 2003, 24, 643-650.
25. Chen, E. H., Kirsch, D. G., Clem, R. J., et al., Conversion of Bcl-2 to a Bax-like death effector by caspases, Science 1997, 278, 1966-1968.
26. Hannun, Y. A., Loomis, C. R., Merrill, A. H., Jr., Bell, R. M., Sphingosine inhibition of protein kinase C activity and of phorbol dibutyrate binding in vitro and in human platelets, J. Biol. Chem. 1986, 261, 12604-12609.
27. Murray, N. R., Davidson, L. A., Chapkin, R. S., Gustafson, W. C., et al., Overexpression of protein kinase C βII induces colonic hyperproliferation and increased sensitivity to colon carcinogenesis, J. Cell. Biol. 1999, 145, 699-711.
28. Nilsson, Å., Metabolism of sphingomyelin in the intestinal tract of the rat, Biochim. Biophys. Acta 1968, 76, 575-584.
29. Inomata, M., Ochiai, A., Akimoto, S., Kitano, S., Hirohashi, S., Alteration of beta-catenin expression in colonic epithelial cells of familial adenomatous polyposis patients, Cancer Res. 1996, 56, 2213-2217.
30. Kim, J. S., Crooks, H., Foxworth, A., Waldman, T., Proof-of-principle: oncogenic β-catenin is a valid molecular target for the development of pharmacological inhibitors, Mol. Cancer Ther. 2002, 1, 1355-1359.
31. Van de Wetering, M., Sancho, E., Verweij, C., de Lau, W., et al., The beta-catenin/TCF-4 complex imposes a crypt progenitor phenotype on colorectal cancer cells, Cell 2002, 111, 241-250.
32. Kaiser, S., Park, Y. K., Halberg, R. B., Yu, M., et al., Transcriptional recapitulation and subversion of embryonic colon development by mouse colon tumor models and human colon cancer, Genome Biol. 2007, 8, R131.
33. Symolon, H., Schmelz, E. M., Dillehay, D. L., Merrill, A. H., Jr., Dietary soy sphingolipids suppress tumorigenesis and gene expression in mouse models of colon cancer, J. Nutr. 2004, 134, 1157-1161.
34. Kroesen, B. J., Jacobs, S., Pettus, B. J., Sietsma, H., et al., BcR-induced apoptosis involves differential regulation of C16 and C24-ceramide formation and sphingolipid-dependent activation of the proteasome, J. Biol. Chem. 2003, 278, 14723-14731.
35. Dbaibo, G. S., Wolff, R. A., Obeid, L. M., Hannun, Y. A., Activation of a retinoblastoma-protein-dependent pathway by sphingosine, Biochem. J. 1995, 310, 453-459.
36. Alesse, E., Zazzeroni, F., Angelucci, A., Giannini, G., et al., The growth arrest and downregulation of c-myc transcription induced by ceramide are related events dependent on p21 induction, Rb underphosphorylation and E2F sequestering, Cell Death Differ. 1998, 5, 381-399.
37. Kim, D. S., Kim, S. Y., Kleuser, B., Schafer-Korting, M., et al., Sphingosine-1-phosphate inhibits human keratinocyte proliferation via Akt/protein kinase B inactivation, Cell Signal. 2004, 16, 89-95.
38. Mehta, P. P., Perez-Stable, C., Nadji, M., Mian, M., et al., Suppression of human prostate cancer cell growth by forced expression of connexin genes, Dev. Genet. 1999, 24, 91-110.
39. Zhang, Z. Q., Zhang, W., Wang, N. Q., Bani-Yaghoub, M., et al., Suppression of tumorigenicity of human lung carcinoma cells after transfection with connexin43, Carcinogenesis 1998, 19, 1889-1894.
40. van der Heyden, M. A., Rook, M. B., Hermans, M. M., Rijksen, G., et al., Identification of connexin43 as a functional target for Wnt signalling, J. Cell Sci. 1998, 111, 1741-1749.
41. Hernadez-Blazquez, F. J., Joazeiro, P. P., Omori, Y., Yamasaki, H., Control of intracellular movement of connexins by E-cadherin in murine skin papilloma cells, Exp. Cell. Res. 2001, 270, 235-247.
42. Nishimura, M., Saito, T., Yamasaki, H., Kudo, R., Suppression of gap junctional intercellular communication via 5′ CpG island methylation in promoter region of E-cadherin gene in endometrial cancer cells, Carcinogenesis 2003, 24, 1615-1623.
43. Roberts, P. C., Mottillo, E. P., Baxa, A. C., Heng, H. H., et al., Sequential molecular and cellular events during neoplastic progression: A mouse syngeneic ovarian cancer model, Neoplasia 2005, 7, 944-956.
44. Murray, N. R., Weems, C., Chen, L., Leon, J., et al., Protein kinase C betaII and TGFbetaRII in omega-3 fatty acid-mediated inhibition of colon carcinogenesis, J. Cell Biol. 2002, 157, 915-920.
45. Gökmen-Polar, Y., Murray, N. R., Velasco, M. A., Gatalica, Z., Fields, A. P., Elevated protein kinase C βII is an early promotive event in colon carcinogenesis, Cancer Res. 2001, 61, 1375-1381.
46. Zhang, J., Anastasiadis, P. Z., Liu, Y., Aubrey Thompson, E., Fields, A. P., Protein kinase C beta II induces cell invasion through a RAS/MEK-, PKC/RAC 1-dependent signaling pathway, J. Biol. Chem. 2004, 279, 22118-22123.
47. Mutanen, M., Pajari, A. M., Oikarinen, S. L., Beef induces and rye bran prevents the formation of intestinal polyps in Apc(Min) mice: Relation to beta-catenin and PKC isozymes, Carcinogenesis 2000, 21, 1167-1173.
48. Zhang, J., Alter, N., Reed, J. C., Borner, C., et al., Bcl-2 interrupts the ceramide-mediated pathway of cell death, Proc. Natl. Acad. Sci. USA 1996, 93, 5325-5328.
49. Hague, A., Moorghen, M., Hicks, D., Chapman, M., Paraskeva, C., Bcl-2 expression in human colorectal adenomas and carcinomas, Oncogene 1994, 9, 3367-3370.
50. Ofner, D., Riehemann, K., Maier, H., Riedmann, B., et al., Immunohistochemically detectable bcl-2 expression in colorectal carcinoma: Correlation with tumour stage and patient survival, Br. J. Cancer 1995, 72, 981-985.
51. Manne, U., Myers, R. B., Moron, C., et al., Prognostic significance of bcl-2 expression and p53 nuclear accumulation in colorectal adenocarcinoma, Int. J. Cancer 1997, 74, 346.
52. Hanson, C. J., Bootman, M. D., Distelhorst, C. W., Maraldi, T., Roderick, H. L., The cellular concentration of Bcl-2 determines its pro- or anti-apoptotic effect. Cell Calcium 2008, in press, DOI: 10.1016/j.ceca.2007.11.014.
53. Ruvolo, P. P., Clark, W., Mumby, M., et al., A functional role for the B56 alpha-subunit of protein phosphatase 2A in ceramide-mediated regulation of Bcl2 phosphorylation status and function, J. Biol. Chem. 2002, 277, 22847-22852.