Antiproliferative effect of conjugated linoleic acid in caco-2 cells: Involvement of PPARγ and APC/β-catenin pathways

Chemico-Biological Interactions

Volumn 169, Issue 2, 2007, Pages 110-121

  Bozzo, Francesca ^a   Bocca, Claudia ^a   Colombatto, Sebastiano ^a   Miglietta, Antonella ^a  

^a UNIVERSITY OF TURIN   (Italy)

Author keywords

Catenin; APC; Caco 2; CLA; PPAR ; Proliferation

Indexed keywords

ACTIN; APC PROTEIN; BETA CATENIN; CONJUGATED LINOLEIC ACID; PEROXISOME PROLIFERATOR ACTIVATED RECEPTOR; PEROXISOME PROLIFERATOR ACTIVATED RECEPTOR GAMMA; TUBULIN;

ACTIN FILAMENT; ARTICLE; CELL DIFFERENTIATION; CELL PROLIFERATION; CELL STRAIN CACO 2; COLON CARCINOGENESIS; COLON POLYPOSIS; CONTROLLED STUDY; HUMAN; HUMAN CELL; PROTEIN PHOSPHORYLATION;

BETA CATENIN; BLOTTING, WESTERN; CACO-2 CELLS; CADHERINS; CELL PROLIFERATION; FLUORESCENT ANTIBODY TECHNIQUE, INDIRECT; GENES, APC; HUMANS; LINOLEIC ACID; PHOSPHORYLATION; PPAR GAMMA; PROTO-ONCOGENE PROTEINS C-MYC;

EID: 34547145925     PISSN: 00092797     EISSN: None     Source Type: Journal    
DOI: 10.1016/j.cbi.2007.05.010     Document Type: Article

References (60)

1. Calle E.E., Rodriguez C., Walker-Thurmond K., and Thun M.J. Overweight, obesity, and mortality from cancer in a prospectively studied cohort of U.S. adults. N. Engl. J. Med. 348 (2003) 1625-1638
2. Mutanen M., Pajari A.M., and Oikarinen S.I. Beef induces and rye bran prevents the formation of intestinal polyps in Apc(Min) mice: relation to β-catenin and PKC isozymes. Carcinogenesis 21 (2000) 1167-1173
3. Kallay E., Bareis P., Bajna E., Kriwanek S., Bonner E., Toyokuni S., and Cross H.S. Vitamin D receptor activity and prevention of colonic hyperproliferation and oxidative stress. Food Chem. Toxicol. 40 (2002) 1191-1196
4. Bhattacharya A., Banu J., Rahman M., Causey J., and Fernandes G. Biological effects of conjugated linoleic acids in health and disease. J. Nutr. Biochem. 17 (2006) 789-810
5. L.A. Sauer, D.E. Blask, R.T. Dauchy, Dietary factors and growth and metabolism in experimental tumors. J. Nutr. Biochem. (2007), in press.
6. Chin S.F., Liu W., Storkson J.M., Ha Y.L., and Pariza M.W. Dietary sources of conjugated dienoic isomers of linoleic acid, a newly recognized class of anticarcinogens. J. Food Compos. Anal. 5 (1992) 185-197
7. Ip C., Singh M., Thompson H.J., and Scimeca J.A. Conjugated linoleic acid suppresses mammary carcinogenesis and proliferation activity of the mammary gland. Cancer Res. 54 (1994) 1212-1215
8. Visonneau S., Cesano A., Tepper S.A., Scimeca J.A., Santoli D., and Kritchevsky D. Conjugated linoleic acid suppresses the growth of human breast adenocarcinoma cells in SCID mice. Anticancer Res. 17 (1997) 969-974
9. Belury M.A., Nickel K.P., Bird C.E., and Wu Y. Dietary conjugated linoleic acid modulation of phorbol ester skin tumor promotion. Nutr. Cancer 26 (1996) 149-157
10. Parodi P.W. Conjugated linoleic acid and other anticarcinogenic agents of bovine milk fat. J. Dairy Sci. 82 (1999) 1339-1349
11. Park H.S., Ryu J.H., Ha Y.L., and Park J.H. Dietary conjugated linoleic acid (CLA) induces apoptosis of colonic mucosa in 1,2-dimethylhydrazine-treated rats: a possible mechanism of the anticarcinogenic effect by CLA. Br. J. Nutr. 86 (2001) 549-555
12. Cho H.J., Kim E.J., Lim S.S., Kim M.K., Sung M.K., Kim J.S., and Park J.H. Trans-10, cis-12, not cis-9, trans-11, conjugated linoleic acid inhibits G1-S progression in HT-29 human colon cancer cells. J. Nutr. 136 (2006) 893-898
13. Maggiora M., Bologna M., Ceru M.P., Possati L., Angelucci A., Cimini A., Miglietta A., Bozzo F., Margiotta C., Muzio G., and Canuto R.A. An overview of the effect of linoleic and conjugated-linoleic acids on the growth of several human tumor cell lines. Int. J. Cancer 112 (2004) 909-919
14. Ochoa J.J., Farquaharson A.J., Grant I., Moffat L.E., Heys S.D., and Wahle K.W.J. Conjugated linoleic acid (CLA's) decrease prostate cancer cell proliferation: different molecular mechanisms for cis-9, trans-11 and trans-10, cis-12 isomers. Carcinogenesis 25 (2004) 1185-1191
15. Miglietta A., Bozzo F., Gabriel L., Bocca C., and Canuto R.A. Extracellular signal-regulated kinase 1/2 and protein phosphatase 2A are involved in the antiproliferative activity of conjugated linoleic acid in MCF-7 cells. Br. J. Nutr. 96 (2006) 22-27
16. Degner S.C., Kemp M.Q., Bowden G.T., and Romagnolo D.F. Conjugated linoleic acid attenuates cyclooxygenase-2 transcriptional activity via an anti-AP-1 mechanism in MCF-7 breast cancer cells. J. Nutr. 136 (2006) 421-427
17. Lampen A., Leifheit M., Voss J., and Nau H. Molecular and cellular effects of cis-9, trans-11-conjugated linoleic acid in enterocytes: effects on proliferation, differentiation, and gene expression. Biochim. Biophys. Acta 1735 (2005) 30-40
18. Escher P., and Wahli W. Peroxisome proliferator-activated receptors: insight into multiple cellular functions. Mutat. Res. 448 (2000) 121-138
19. Saez E., Tontonoz P., Nelson M.C., Alvarez J.G., Ming U.T., Baird S.M., Thomazy V.A., and Evans R.M. Activators of the nuclear receptor PPARgamma enhance colon polyp formation. Nat. Med. 4 (1998) 1058-1061
20. Jackson L., Wahli W., Michalik L., Watson S.A., Morris T., Anderton K., Bell D.R., Smith J.A., Hawkey C.J., and Bennett A.J. Potential role for peroxisome proliferator activated receptor (PPAR) in preventing colon cancer. Gut 52 (2003) 1317-1322
21. Girnun G.D., Smith W.M., Drori S., Sarraf P., Mueller E., Eng C., Nambiar P., Rosenberg D.W., Bronson R.T., Edelmann W., Kucherlapati R., Gonzalez F.J., and Spiegelman B.M. APC-dependent suppression of colon carcinogenesis by PPARgamma. Proc. Natl. Acad. Sci. U.S.A. 99 (2002) 13771-13776
22. Iida K.T., Kawakami Y., Suzuki H., Sone H., Shimano H., Toyoshima H., Okuda Y., and Yamada N. PPAR gamma ligands, troglitazone and pioglitazone, up-regulate expression of HMG-CoA synthase and HMG-CoA reductase gene in THP-1 macrophages. FEBS Lett. 520 (2002) 177-181
23. 1 arrest and differentiation marker expression in vascular smooth muscle cells. Mol. Pharmacol. 58 (2000) 837-844
24. cip1 by modulating the protein kinase C delta pathway in vascular smooth muscle cells. J. Biol. Chem. 276 (2001) 47650-47657
25. Jansson E.A., Are A., Greicius G., Kuo I.C., Kelly D., Arulampalam V., and Pettersson S. The Wnt/beta-catenin signaling pathway targets PPARgamma activity in colon cancer cells. Proc. Natl. Acad. Sci. USA 102 (2005) 1460-1465
26. Jin Z., Tamura G., Tsuchiya T., Sakata K., Kashiwaba M., Osakabe M., and Motoyama T. Adenomatous polyposis coli (APC) gene promoter hypermethylation in primary breast cancers. Br. J. Cancer 85 (2001) 69-73
27. Kolligs F.T., Kolligs B., Hajra K.M., Hu G., Tani M., Cho K.R., and Fearon E.R. gamma-catenin is regulated by the APC tumor suppressor and its oncogenic activity is distinct from that of beta-catenin. Genes Dev. 14 (2000) 1319-1331
28. Simcha I., Geiger B., Yehuda-Levenberg S., Salomon D., and Ben-Ze'ev A. Suppression of tumorigenicity by plakoglobin: an augmenting effect of N-cadherin. J. Cell Biol. 133 (1996) 199-209
29. Kemler R. From cadherins to catenins: cytoplasmic protein interactions and regulation of cell adhesion. Trends Genet. 9 (1993) 317-321
30. Conacci-Sorrell M., Zhurinsky J., and Ben-Ze'ev A. The cadherin-catenin adhesion system in signaling and cancer. J. Clin. Invest. 109 (2002) 987-991
31. Nelson W.J., and Nusse R. Convergence of Wnt, beta-catenin, and cadherin pathways. Science 303 (2004) 1483-1487
32. Willert K., and Nusse R. Beta-catenin: a key mediator of Wnt signalling. Curr. Opin. Genet. Dev. 8 (1998) 95-102
33. Giles R.H., van Es J.H., and Clevers H. Caught up in a Wnt storm: Wnt signaling in cancer. Biochim. Biophys. Acta 1653 (2003) 1-24
34. Fearnhead N.S., Britton M.P., and Bodmer W.F. The ABC of APC. Hum. Mol. Genet. 10 (2001) 721-733
35. Sparks A.B., Morin P.J., Vogelstein B., and Kinzler K.W. Mutational analysis of the APC/β-catenin/Tcf pathway in colorectal cancer. Cancer Res. 58 (1998) 1130-1134
36. Cimini A., Cristiano L., Colafarina S., Benedetti E., Di Loreto S., Festuccia C., Amicarelli F., Canuto R.A., and Ceru M.P. PPARgamma-dependent effects of conjugated linoleic acid on the human glioblastoma cell line (ADF). Int. J. Cancer 117 (2005) 923-933
37. Sarraf P., Mueller E., Smith W.M., Wright H.M., Kum J.B., Aaltonen L.A., de la Chapelle A., Spiegelman B.M., and Eng C. Loss-of-function mutations in PPAR gamma associated with human colon cancer. Mol. Cell 3 (1999) 799-804
38. Liu J., Wang H., Zuo Y., and Farmer S.R. Functional interaction between peroxisome proliferator-activated receptor gamma and beta-catenin. Mol. Cell Biol. 26 (2006) 5827-5837
39. Lampen A., Leifheit M., Voss J., and Nau H. Molecular and cellular effects of cis-9, trans-11-conjugated linoleic acid in enterocytes: effects on proliferation, differentiation, and gene expression. Biochim. Biophys. Acta 1735 (2005) 530-540
40. Bocca C., Bozzo F., Gabriel L., and Miglietta A. Conjugated linoleic acid inhibits Caco-2 cell growth via ERK-MAPK signalling pathway. J. Nutr. Biochem. 18 (2007) 332-340
41. Larsson S.C., Bergkvist L., and Wolk A. High-fat dairy food and conjugated linoleic acid intakes in relation to colorectal cancer incidence in the Swedish Mammography Cohort. Am. J. Clin. Nutr. 82 (2005) 894-900
42. Beppu F., Hosokawa M., Tanaka L., Kohno H., Tanaka T., and Miyashita K. Potent inhibitory effect of trans9, trans11 isomer of conjugated linoleic acid on the growth of human colon cancer cells. J. Nutr. Biochem. 17 (2006) 830-836
43. Moya-Camarena S.Y., Vanden Heuvel J.P., Blanchard S.G., Leesnitzer L.A., and Belury M.A. Conjugated linoleic acid is a potent naturally occurring ligand and activator of PPARalpha. J. Lipid Res. 40 (1999) 1426-1433
44. Belury M., Moya-Camarena S.Y., Lu M., Shi L., Leesnitzer L., and Blanchard S.G. Conjugated linoleic acid is an activator and ligand for peroxisome proliferator-activated receptor-gamma (PPARg). Nutr. Res. 22 (2002) 817-824
45. Eynard A.R., and Lopez C.B. Conjugated linoleic acid (CLA) versus saturated fats/cholesterol: their proportion in fatty and lean meats may affect the risk of developing colon cancer. Lipids Health Dis. 2 (2003) 6
46. Sarraf P., Mueller E., Jones D., King F.J., DeAngelo D.J., Partridge J.B., Holden S.A., Chen L.B., Singer S., Fletcher C., and Spiegelman B.M. Differentiation and reversal of malignant changes in colon cancer through PPARγ. Nat. Med. 4 (1998) 1046-1052
47. Yoshizumi T., Ohta T., Ninomiya I., Terada I., Fushida S., Fujimura T., Nishimura G., Shimizu K., Yi S., and Miwa K. Thiazolidinedione, a peroxisome proliferator-activated receptor-gamma ligand, inhibits growth and metastasis of HT-29 human colon cancer cells through differentiation-promoting effects. Int. J. Oncol. 25 (2004) 631-639
48. Gelman L., Michalik L., Desvergne B., and Wahli W. Kinase signaling cascades that modulate peroxisome proliferator-activated receptors. Curr. Opin. Cell Biol. 17 (2005) 216-222
49. Camp H.S., and Tafuri S.R. Regulation of peroxisome proliferator activated receptor γ activity by mitogen activated protein kinase. J. Biol. Chem. 272 (1997) 10811-10816
50. Kuniyasu H., Yoshida K., Sasaki T., Sasahira T., Fujii K., and Ohmori H. Conjugated linoleic acid inhibits peritoneal metastasis in human gastrointestinal cancer cells. Int. J. Cancer 118 (2006) 571-576
51. Lustig B., and Behrens J. The Wnt signalling pathway and its role in tumor development. J. Cancer Res. Clin. Oncol. 129 (2003) 199-221
52. He T.C., Chan T.A., Vogelstein B., and Kinzler K.W. PPARdelta is an APC-regulated target of nonsteroidal anti-inflammatory drugs. Cell 99 (1999) 335-345
53. Mariadason J.M., Bordonaro M., Aslam F., Shi L., Kuraguchi M., Velcich A., and Augenlicht L.H. Down-regulation of beta-catenin TCF signaling is linked to colonic epithelial cell differentiation. Cancer Res. 61 (2001) 3465-3471
54. Liu J.R., Chen B.Q., Yang Y.M., Wang X.L., Xue Y.B., Zheng Y.M., and Liu R.H. Effect of apoptosis on gastric adenocarcinoma cell line SGC-7901 induced by cis-9, trans-11-conjugated linoleic acid. World J. Gastroenterol. 8 (2002) 999-1004
55. Kim E.J., Holthuizen P.E., Park H.S., Ha Y.L., Jung K.C., and Park J.H. Trans-10, cis-12-conjugated linoleic acid inhibits Caco-2 colon cancer cell growth. Am. J. Physiol. Gasterointest. Liver Physiol. 283 (2002) G357-G367
56. Langford K.J., Askham J.M., Lee T., Adams M., and Morrison E.E. Examination of actin and microtubule dependent APC localisations in living mammalian cells. BMC Cell Biol. 7 (2006) 3-21
57. Reilein A., and Nelson W.J. APC is a component of an organizing template for cortical microtubule networks. Nat. Cell Biol. 7 (2005) 463-473
58. Etienne-Manneville S., and Hall A. Cdc42 regulates GSK-3beta and adenomatous polyposis coli to control cell polarity. Nature 421 (2003) 753-756
59. Zumbrunn J., Kinoshita K., Human A.A., and Näthke I.S. Binding of the adenomatous polyposis coli protein to microtubules increases microtubule stability and is regulated by GSK3β phosphorylation. Curr. Biol. 11 (2001) 44-49
60. Xiao D., Deguchi A., Gundersen G.G., Oehlen B., Arnold L., and Weinstein I.B. The sulindac derivatives OSI-461, OSIP486823, and OSIP487703 arrest colon cancer cells in mitosis by causing microtubule depolymerization. Mol. Cancer Ther. 5 (2006) 60-67