Consumption of high-fat diet induces tumor progression and epithelial-mesenchymal transition of colorectal cancer in a mouse xenograft model

Journal of Nutritional Biochemistry

Volumn 23, Issue 10, 2012, Pages 1302-1313

  Tang, Feng Yao ^a   Pai, Man Hui ^b   Chiang, En Pei Isabel ^c  

^a CHINA MEDICAL UNIVERSITY   (Taiwan)

^b TAIPEI MEDICAL UNIVERSITY   (Taiwan)

^c NATIONAL CHUNG HSING UNIVERSITY   (Taiwan)

Author keywords

Colorectal cancer; Cyclooxygenase 2; Epithelial mesenchymal transition; High fat diet; Histone deacetylase

Indexed keywords

BETA CATENIN; CELL NUCLEUS ANTIGEN; CYCLIN D1; CYCLOOXYGENASE 2; HISTONE DEACETYLASE; MAMMALIAN TARGET OF RAPAMYCIN; MITOGEN ACTIVATED PROTEIN KINASE; PHOSPHATIDYLINOSITOL 3 KINASE; PROTEIN KINASE B; PROTEIN P21; TRANSCRIPTION FACTOR RELA;

ANIMAL EXPERIMENT; ANIMAL MODEL; ANIMAL TISSUE; ARTICLE; CELL PROLIFERATION; COLORECTAL CANCER; DISEASE MODEL; ENZYME ACTIVITY; ENZYME INDUCTION; EPITHELIAL MESENCHYMAL TRANSITION; FAT INTAKE; INFLAMMATION; INTRACELLULAR SIGNALING; LIPID DIET; MOUSE; NONHUMAN; PROTEIN EXPRESSION; TUMOR GROWTH; TUMOR XENOGRAFT;

ANIMALS; BETA CATENIN; CADHERINS; CELL PROLIFERATION; COLORECTAL NEOPLASMS; CYCLIN D1; CYCLIN-DEPENDENT KINASE INHIBITOR P21; CYCLOOXYGENASE 2; DIET, HIGH-FAT; DISEASE MODELS, ANIMAL; EPITHELIAL-MESENCHYMAL TRANSITION; FEMALE; GENE EXPRESSION REGULATION, NEOPLASTIC; HT29 CELLS; HUMANS; MICE; MICE, INBRED BALB C; MITOGEN-ACTIVATED PROTEIN KINASES; NF-KAPPA B; PHOSPHATIDYLINOSITOL 3-KINASE; PROTO-ONCOGENE PROTEINS C-AKT; SIGNAL TRANSDUCTION; TOR SERINE-THREONINE KINASES; UP-REGULATION; VIMENTIN;

EID: 84866330700     PISSN: 09552863     EISSN: 18734847     Source Type: Journal    
DOI: 10.1016/j.jnutbio.2011.07.011     Document Type: Article

References (53)

1. Jemal A., Siegel R., Xu J., Ward E. Cancer statistics, 2010. CA Cancer J Clin 2010, 60:277-300.
2. Meyerhardt J.A., Niedzwiecki D., Hollis D., Saltz L.B., Hu F.B., Mayer R.J., et al. Association of dietary patterns with cancer recurrence and survival in patients with stage III colon cancer. JAMA 2007, 298:754-764.
3. Slattery M.L., Boucher K.M., Caan B.J., Potter J.D., Ma K.N. Eating patterns and risk of colon cancer. Am J Epidemiol 1998, 148:4-16.
4. Slattery M.L., Potter J.D., Duncan D.M., Berry T.D. Dietary fats and colon cancer: assessment of risk associated with specific fatty acids. Int J Cancer 1997, 73:670-677.
5. Larue L., Bellacosa A. Epithelial-mesenchymal transition in development and cancer: role of phosphatidylinositol 3' kinase/AKT pathways. Oncogene 2005, 24:7443-7454.
6. Lipsky P.E. Role of cyclooxygenase-1 and -2 in health and disease. Am J Orthop (Belle Mead NJ) 1999, 28:8-12.
7. Loboda A., Nebozhyn M.V., Watters J.W., Buser C.A., Shaw P.M., Huang P.S., et al. EMT is the dominant program in human colon cancer. BMC Med Genomics 2011, 4:9.
8. Castro-Carpeno J., Belda-Iniesta C., Casado S.E., Hernandez A.E., Feliu B.J., Gonzalez B.M. EGFR and colon cancer: a clinical view. Clin Transl Oncol 2008, 10:6-13.
9. Johnson S.M., Gulhati P., Rampy B.A., Han Y., Rychahou P.G., Doan H.Q., et al. Novel expression patterns of PI3K/Akt/mTOR signaling pathway components in colorectal cancer. J Am Coll Surg 2010, 210:767-768.
10. Lu Z., Cox-Hipkin M.A., Windsor W.T., Boyapati A. 3-Phosphoinositide-dependent protein kinase-1 regulates proliferation and survival of cancer cells with an activated mitogen-activated protein kinase pathway. Mol Cancer Res 2010, 8:421-432.
11. Morgensztern D., McLeod H.L. PI3K/Akt/mTOR pathway as a target for cancer therapy. Anticancer Drugs 2005, 16:797-803.
12. Petroulakis E., Mamane Y., Le Bacquer O., Shahbazian D., Sonenberg N. mTOR signaling: implications for cancer and anticancer therapy. Br J Cancer 2006, 94:195-199.
13. Raufman J.P., Shant J., Guo C.Y., Roy S., Cheng K. Deoxycholyltaurine rescues human colon cancer cells from apoptosis by activating EGFR-dependent PI3K/Akt signaling. J Cell Physiol 2008, 215:538-549.
14. Baldassarre G., Nicoloso M.S., Schiappacassi M., Chimienti E., Belletti B. Linking inflammation to cell cycle progression. Curr Pharm Des 2004, 10:1653-1666.
15. Prescott S.M., Fitzpatrick F.A. Cyclooxygenase-2 and carcinogenesis. Biochim Biophys Acta 2000, 1470:M69-M78.
16. McCubrey J.A., Steelman L.S., Chappell W.H., Abrams S.L., Wong E.W., Chang F., et al. Roles of the Raf/MEK/ERK pathway in cell growth, malignant transformation and drug resistance. Biochim Biophys Acta 2007, 1773:1263-1284.
17. Arber N., Doki Y., Han E.K., Sgambato A., Zhou P., Kim N.H., et al. Antisense to cyclin D1 inhibits the growth and tumorigenicity of human colon cancer cells. Cancer Res 1997, 57:1569-1574.
18. Qiao L., Shiff S.J., Rigas B. Sulindac sulfide inhibits the proliferation of colon cancer cells: diminished expression of the proliferation markers PCNA and Ki-67. Cancer Lett 1997, 115:229-234.
19. Tetsu O., McCormick F. Beta-catenin regulates expression of cyclin D1 in colon carcinoma cells. Nature 1999, 398:422-426.
20. Zhao J.H., Luo Y., Jiang Y.G., He D.L., Wu C.T. Knockdown of beta-catenin through shRNA cause a reversal of EMT and metastatic phenotypes induced by HIF-1alpha. Cancer Invest 2011, 29(6):377-382.
21. Kanwar S.S., Yu Y., Nautiyal J., Patel B.B., Majumdar A.P. The Wnt/beta-catenin pathway regulates growth and maintenance of colonospheres. Mol Cancer 2010, 9:212.
22. Agarwal C., Singh R.P., Dhanalakshmi S., Tyagi A.K., Tecklenburg M., Sclafani R.A., et al. Silibinin upregulates the expression of cyclin-dependent kinase inhibitors and causes cell cycle arrest and apoptosis in human colon carcinoma HT-29 cells. Oncogene 2003, 22:8271-8282.
23. Cayrol C., Knibiehler M., Ducommun B. p21 binding to PCNA causes G1 and G2 cell cycle arrest in p53-deficient cells. Oncogene 1998, 16:311-320.
24. Wilson A.J., Byun D.S., Nasser S., Murray L.B., Ayyanar K., Arango D., et al. HDAC4 promotes growth of colon cancer cells via repression of p21. Mol Biol Cell 2008, 19:4062-4075.
25. Hitomi T., Matsuzaki Y., Yokota T., Takaoka Y., Sakai T. p15(INK4b) in HDAC inhibitor-induced growth arrest. FEBS Lett 2003, 554:347-350.
26. Zupkovitz G., Grausenburger R., Brunmeir R., Senese S., Tischler J., Jurkin J., et al. The cyclin-dependent kinase inhibitor p21 is a crucial target for histone deacetylase 1 as a regulator of cellular proliferation. Mol Cell Biol 2010, 30:1171-1181.
27. Wendt M.K., Taylor M.A., Schiemann B.J., Schiemann W.P. Downregulation of epithelial cadherin is required to initiate metastatic outgrowth of breast cancer. Mol Biol Cell 2011, 22:2423-2435.
28. Serova M., Astorgues-Xerri L., Bieche I., Albert S., Vidaud M., Benhadji K.A., et al. Epithelial-to-mesenchymal transition and oncogenic Ras expression in resistance to the protein kinase Cbeta inhibitor enzastaurin in colon cancer cells. Mol Cancer Ther 2010, 9:1308-1317.
29. Mandal M., Myers J.N., Lippman S.M., Johnson F.M., Williams M.D., Rayala S., et al. Epithelial to mesenchymal transition in head and neck squamous carcinoma: association of Src activation with E-cadherin down-regulation, vimentin expression, and aggressive tumor features. Cancer 2008, 112:2088-2100.
30. Bracke M.E., Van Roy F.M., Mareel M.M. The E-cadherin/catenin complex in invasion and metastasis. Curr Top Microbiol Immunol 1996, 213:123-161.
31. Birchmeier W., Behrens J. Cadherin expression in carcinomas: role in the formation of cell junctions and the prevention of invasiveness. Biochim Biophys Acta 1994, 1198:11-26.
32. Maier H.J., Schmidt-Strassburger U., Huber M.A., Wiedemann E.M., Beug H., Wirth T. NF-kappaB promotes epithelial-mesenchymal transition, migration and invasion of pancreatic carcinoma cells. Cancer Lett 2010, 295:214-228.
33. van Zijl F., Zulehner G., Petz M., Schneller D., Kornauth C., Hau M., et al. Epithelial-mesenchymal transition in hepatocellular carcinoma. Future Oncol 2009, 5:1169-1179.
34. Cai Z., Wang Q., Zhou Y., Zheng L., Chiu J.F., He Q.Y. Epidermal growth factor-induced epithelial-mesenchymal transition in human esophageal carcinoma cells-a model for the study of metastasis. Cancer Lett 2010, 296:88-95.
35. Bates R.C. Colorectal cancer progression: integrin alphavbeta6 and the epithelial-mesenchymal transition (EMT). Cell Cycle 2005, 4:1350-1352.
36. Spaderna S., Schmalhofer O., Hlubek F., Berx G., Eger A., Merkel S., et al. A transient, EMT-linked loss of basement membranes indicates metastasis and poor survival in colorectal cancer. Gastroenterology 2006, 131:830-840.
37. Jung J.W., Hwang S.Y., Hwang J.S., Oh E.S., Park S., Han I.O. Ionising radiation induces changes associated with epithelial-mesenchymal transdifferentiation and increased cell motility of A549 lung epithelial cells. Eur J Cancer 2007, 43:1214-1224.
38. Schneider M.R., Dahlhoff M., Horst D., Hirschi B., Trulzsch K., Muller-Hocker J., et al. A key role for E-cadherin in intestinal homeostasis and Paneth cell maturation. PLoS One 2010, 5:e14325.
39. Satelli A., Li S. Vimentin in cancer and its potential as a molecular target for cancer therapy. Cell Mol Life Sci 2011, 68:3033-3046.
40. Zhang W., Wang J., Zou B., Sardet C., Li J., Lam C.S., et al. Four and a half LIM protein 2 (FHL2) negatively regulates the transcription of E-cadherin through interaction with Snail1. Eur J Cancer 2011, 47:121-130.
41. Joyce T., Cantarella D., Isella C., Medico E., Pintzas A. A molecular signature for epithelial to mesenchymal transition in a human colon cancer cell system is revealed by large-scale microarray analysis. Clin Exp Metastasis 2009, 26:569-587.
42. Roger L., Jullien L., Gire V., Roux P. Gain of oncogenic function of p53 mutants regulates E-cadherin expression uncoupled from cell invasion in colon cancer cells. J Cell Sci 2010, 123:1295-1305.
43. Jang T.J., Jeon K.H., Jung K.H. Cyclooxygenase-2 expression is related to the epithelial-to-mesenchymal transition in human colon cancers. Yonsei Med J 2009, 50:818-824.
44. Honma N., Genda T., Matsuda Y., Yamagiwa S., Takamura M., Ichida T., et al. MEK/ERK signaling is a critical mediator for integrin-induced cell scattering in highly metastatic hepatocellular carcinoma cells. Lab Invest 2006, 86:687-696.
45. Ray R.M., Vaidya R.J., Johnson L.R. MEK/ERK regulates adherens junctions and migration through Rac1. Cell Motil Cytoskeleton 2007, 64:143-156.
46. Tang F.Y., Chiang E.P., Chung J.G., Lee H.Z., Hsu C.Y. S-allylcysteine modulates the expression of E-cadherin and inhibits the malignant progression of human oral cancer. J Nutr Biochem 2009, 20:1013-1020.
47. Neal C.L., McKeithen D., Odero-Marah V.A. Snail negatively regulates cell adhesion to extracellular matrix and integrin expression via the MAPK pathway in prostate cancer cells. Cell Adh Migr 2011, 5.
48. Chen X., Halberg R.B., Burch R.P., Dove W.F. Intestinal adenomagenesis involves core molecular signatures of the epithelial-mesenchymal transition. J Mol Histol 2008, 39:283-294.
49. Hong K.O., Kim J.H., Hong J.S., Yoon H.J., Lee J.I., Hong S.P., et al. Inhibition of Akt activity induces the mesenchymal-to-epithelial reverting transition with restoring E-cadherin expression in KB and KOSCC-25B oral squamous cell carcinoma cells. J Exp Clin Cancer Res 2009, 28:28.
50. Khasawneh J., Schulz M.D., Walch A., Rozman J., Hrabed A., Klingenspor M., et al. Inflammation and mitochondrial fatty acid beta-oxidation link obesity to early tumor promotion. Proc Natl Acad Sci U S A 2009, 106:3354-3359.
51. Bi X., Pohl N.M., Yin Z., Yang W. Loss of JNK2 increases intestinal tumor susceptibility in Apc1638+/- mice with dietary modulation. Carcinogenesis 2011, 32:584-588.
52. Honma K., Mochizuki K., Goda T. Inductions of histone H3 acetylation at lysine 9 on SGLT1 gene and its expression by feeding mice a high carbohydrate/fat ratio diet. Nutrition 2009, 25:40-44.
53. Yorita S., Mochizuki K., Goda T. Induction of histone acetylation on the sucrase-isomaltase gene in the postnatal rat jejunum. Biosci Biotechnol Biochem 2009, 73:933-935.