Effect of eicosapentaenoic acid on the proliferation and incidence of apoptosis in the colorectal cell line HT29

Lipids

Volumn 34, Issue 12, 1999, Pages 1287-1295

  Clarke, Rosemary G ^a   Lund, Elizabeth K ^a   Latham, Peter ^a   Pinder, Andrew C ^a   Johnson, Ian T ^a  

^a NORWICH RESEARCH PARK   (United Kingdom)

Author keywords

[No Author keywords available]

Indexed keywords

ANTINEOPLASTIC AGENT; FISH OIL; ICOSAPENTAENOIC ACID;

ANTINEOPLASTIC ACTIVITY; APOPTOSIS; ARTICLE; CELL CULTURE; COLORECTAL CANCER; DNA CLEAVAGE; DRUG MECHANISM; FLOW CYTOMETRY; GEL ELECTROPHORESIS; HUMAN; HUMAN CELL; MITOSIS INHIBITION;

ANIMALIA;

EID: 0033392868     PISSN: 00244201     EISSN: None     Source Type: Journal    
DOI: 10.1007/s11745-999-0480-7     Document Type: Article

References (64)

1. Office of Population Censuses and Surveys (1990) Mortality Statistics, Cause, Review of the Registrar General on Deaths by Cause, Sex and Age in England and Wales, Her Majesty's Stationer's Office, London.
2. Muto, T., Bussey, H.J.R., and Morson, B.C. (1975) The Evolution of Cancer of the Colon and Rectum, Cancer 36, 2251-2279.
3. Potten, C.S. (1995) Structure, Function and Proliferative Organisation of Mammalian Gut, in Radiation and Gut (Potten, C.S., and Hendry, J.H., eds.), pp. 1-31, Elsevier Science, B.V., Amsterdam.
4. Ponz de Leon, M., Roncucci, L., and Donanto, P.D. (1988) Pattern of Epithelial Cell Proliferation in Colorectal Mucosa of Normal Subjects and of Patients with Adenomatous Polyps or Cancer of the Large Bowel, Cancer Res. 48, 4121-4126.
5. Gibson, P., Rossela, O., and Nov, R. (1995) Colonic Epithelium is Diffusely Abnormal in Ulcerative Colitis and Colorectal Cancer, Gut 36:857-863.
6. Eastwood, G.L. (1995) A Review of Gastrointestinal Epithelial Cell Renewal and Its Relevance to the Development of Adenocarcinoma of the Gastrointestinal Tract, J. Clin. Gastroenterol. 21, 1-11.
7. Scott, N., and Quirke, P. (1993) Molecular Biology of Colorectal Neoplasia, Gut 34, 289-292.
8. Blot, W.J., Lanier, A., Fraumeni, J.F.J., and Bender, T.R. (1975) Cancer Mortality Among Alaskan Natives, 1960-1969, J. Natl. Cancer Inst. 55, 546-554.
9. Nielsen, N.H., and Hansen, J.P. (1980) Breast Cancer in Greenland: Selected Epidemiological, Clinical and Histological Features, J. Cancer Res. Clin. Oncol. 98, 287-299.
10. Schloss, I., Kidd, M.S., Tichelaar, H.Y., Young, G.O., and O'Keefe, S.J. (1997) Dietary Factors Associated with a Low Risk of Colon Cancer in Coloured West Coast Fishermen, S. Afr. Med. J. 87, 152-158.
11. Anti, M., Marra, G., Armelao, F., Bartoli, G.M., Ficarelli, R., Percesepe, A., De Vitis, I., Maria, G., Sofo, L., Rapaccini, G.L., Gentiloni, N., Piccioni, E., and Miggiano, G. (1992) Effect of Omega-3 Fatty Acids on Rectal Mucosal Cell Proliferation in Subjects at Risk for Colon Cancer [see comments], Gastroenterology 103, 883-891.
12. Anti, M., Marra, G., Percesepe, A., Armelao, F., and Gasbarrini, G. (1994) Reliability of Rectal Epithelial Kinetic Patterns as an Intermediate Biomarker of Colon Cancer, J. Cell Biochem. Suppl. 19, 68-75.
13. Huang, Y.-C., Jessup, J.M., Forse, R.A., Flickner, S., Pleskow, D., Anastopoulos, H.T., Ritter, V., and Blackburn, G.L. (1996) n-3 Fatty Acids Decrease Colonic Epithelial Cell Proliferation in High Risk Bowel Mucosa, Lipids 31, S313-S317.
14. Minoura, T., Takata, T., Sakaguchi, M., Takada, H., Yamamura, M., Hioki, K., and Yamamoto, M. (1988) Effect of Dietary Eicosapentaenoic Acid on Azoxymethane-Induced Colon Carcinogenesis in Rats, Cancer Res. 48, 4790-4794.
15. Deschner, E.E., Lytle, J.S., Wong, G., Ruperto, J.F., and Newmark, H.L. (1990) The Effect of Dietary Omega-3 Fatty Acids (fish oil) on Azoxymethanol-Induced Focal Areas of Dysplasia and Colon Tumor Incidence, Cancer 66, 2350-2356.
16. Lindner, M.A. (1991) A Fish Oil Diet Inhibits Colon Cancer in Mice, Nutr. Cancer 15, 1-11.
17. Latham, P., Lund, E.K., and Johnson, I.T. (1999) Dietary n-3 PUFA Increases the Apoptotic Response to 1,2-Dimethylhydrazine, Reduces Mitosis and Suppresses the Induction of Carcinogenesis in the Rat Colon, Carcinogenesis 20, 645-650.
18. Pell, J.D., Brown, J.C., and Johnson, I.T. (1994) Polyunsaturated Fatty Acids of the n-3 Series Influence Intestinal Crypt Cell Production in Rats, Carcinogenesis 15, 1115-1119.
19. Grammatikos, S.I., Subbaiah, P.V., Victor, T.A., and Miller, W.M. (1994) Diverse Effects of Essential (n-6 and n-3) Fatty Acids on Cultured Cells, Cytotechnology 15, 31-50.
20. Grammatikos, S.I., Subbaiah, P.V., Victor, T.A., and Miller, W.M. (1994) n-3 and n-6 Fatty Acid Processing and Growth Effects in Neoplastic and Non-cancerous Human Epithelial Cell Lines, Br. J. Cancer 70, 219-227.
21. Rose, D.P., and Connolly, J.M. (1991) Effects of Fatty Acids and Eicosanoid Synthesis Inhibitors on the Growth of Two Human Prostate Cancer Cell Lines, Prostate (NY) 18, 243-254.
22. Falconer, J.S., Ross, J.A., Fearon, K.C.H., Hawkins, R.A., O'Riordain, M.G., and Carter, D.C. (1994) Effect of Eicosapentaenoic Acid and Other Fatty Acids on the Growth in vitro of Human Pancreatic Cancer Cell Lines, Br. J. Cancer 69, 826-832.
23. Hawkins, R.A., Sangster, K., and Arends, M.J. (1998) Apoptotic Death of Pancreatic Cancer Cells Induced by Polyunsaturated Fatty Acids Caries with Double Bond Number and Involves an Oxidative Mechanism, J. Pathol. 185, 61-70.
24. Sagar, P.S., and Das, U.N. (1995) Cytotoxic Action of cis-Unsaturated Fatty Acids on Human Cervical Carcinoma (HeLa) Cells in vitro, Prostaglandins Leukotrienes Essential Fatty Acids 53, 287-299.
25. Mengeaud, V., Nanao, J.L., Fournel, S., and Rampal, P. (1992) Effects of Eicosapentaenoic Acid, γ-Linoleic Acid and Prostaglandin El on Three Human Colon Carcinoma Cell Lines, Prostaglandins Leukotrienes Essent. Fatty Acids 47, 313-319.
26. Noguchi, M., Rose, D.P., Earashi, M., and Miyazaki, I. (1995) The Role of Fatty Acids and Eicosanoid Synthesis Inhibitors in Breast Carcinoma, Oncology 52, 265-271.
27. Bégin, M.E., Ells, G., and Horrobin, D.F. (1987) Polyunsatu-Rated Fatty Acid-Induced Cytotoxicity Against Tumor Cells and Its Relationship to Lipid Peroxidation, J. Natl. Cancer Inst. 80, 188-194.
28. Das, U.N., Huang, Y.-S., Bégin, M.E., Ells, G., and Horrobin, D.F. (1987) Uptake and Distribution of cis-Unsaturated Fatty Acids and Their Effect on Free Radical Generation in Normal and Tumor Cells in vitro, Free Radical Biol. Med. 3, 9-14.
29. Das, U.N. (1990) Gamma-Linoleic Acid, Arachidonic Acid, and Eicosapentaenoic Acid as Potential Anticancer Drugs, Nutrition 6, 429-434.
30. Tomlinson, I.P., and Bodmer, W.F. (1996) Failure of Programmed Cell Death and Differentiation as Causes of Tumors: Some Simple Mathematical Models, Proc. Natl. Acad. Sci. USA 93, 14800-14803.
31. Pritchard, D.M., and Watson, A.J.M. (1996) Apoptosis and Gastrointestinal Pharmacology, Pharmacol. Ther. 72, 149-169.
32. Koike, M. (1996) Significance of Spontaneous Apoptosis During Colorectal Tumorigenesis, J. Surg. Oncol. 62, 97-108.
33. Marangoni, F., Angeli, M.T., Colli, S., Tremoli, S.E.E., Sirtori, C.R., and Galli, C. (1993) Changes of n-3 and n-6 Fatty Acids in Plasma and Circulating Cells of Normal Subjects, After Prolonged Administration of 20:5 (EPA) and 22:6 (DHA) Ethyl Esters and Prolonged Washout, Biochim. Biophys. Acta 1210, 55-62.
34. Gregory, C.D., Dive, C., Henderson, S., Smith, C.A., Williams, G.T., Gordon, J., and Rickinson, A.B. (1991) Activation of Epstein-Barr-Virus Latent Genes Protects Human B-cells from Death by Apoptosis, Nature 349, 612-614.
35. Wyllie, A.H. (1980) Glucocorticoid-Induced Thymocyte Apoptosis is Associated with Endogenous Endonuclease Activity, Nature 284, 555-556.
36. Van Engeland, M., Ramaekers, F.C.S., Schutte, B., and Reutelingsperger, C.P.M. (1996) A Novel Assay to Measure Loss of Plasma Membrane Asymmetry During Apoptosis of Adherent Cells in Culture, Cytometry 24, 131-139.
37. Nicoletti, I., Migliorati, G., Pagliucci, M.C., Grignani, F., and Riccardi, C. (1991) A Rapid and Simple Method for Measuring Thymocyte Apoptosis by Propidium Iodide Staining and Flow Cytometry, J. Immunol. Meth. 139, 271-279.
38. McClelland, R.G., and Pinder, A.C. (1994) Detection of Salmonella typhimurium in Dairy Products with Flow Cytometry and Monoclonal Antibodies, Appl. Environ. Microbiol. 60, 4255-4262.
39. Van Engeland, M., Nieland, L.J.W., Ramarkers, F.C.S., Schutte, B., and Reutelingsperger, C.P.M. (1998) Annexin V-Affinity Assay: A Review on an Apoptosis Detection System Based on Phosphatidylserine Exposure, Cytometry 31, 1-9.
40. Shiff, S.J., Qiao, L., Tsai, L.-L., and Rigas, B. (1995) Sulindac Sulfide, an Asprin-Like Compound. Inhibits Proliferation, Causes Cell Quiescence, and Induces Apoptosis in HT-29 Colon Adenocarcinoma Cells, J. Clin. Invest. 96, 491-503.
41. Shiff, S.J., Koutsos, M.I., Qiao, L., and Rigas, B. (1996) Nonsteroidal Antiinflammatory Drugs Inhibit Proliferation of Colon Adenocarcinoma Cells: Effects on Cell Cycle and Apoptosis, Exp. Cell. Res. 222, 179-188.
42. Fyfe, D.J. (1996) Studies of the Cytotoxic and Cytostatic Effects of Eicosapentaenoic Acid Towards Human Colon Cancer Cells in vitro, Ph.D. Thesis, University of East Anglia, Norwich, UK, pp. 69-74.
43. Finstad, H.S., Kolset. S.O., Holme, J.A., Wiger, R., Östlund Farrants, A.-K., Blomhoff, R., and Drevon, C.A. (1994) Effect of n-3 and n-6 Fatty Acids on Proliferation and Differentiation of Promyolocytic Leukemic HL-60 cells, Blood 84, 3799-3809.
44. Lai, P.B.S., Ross, J.A., Fearon, K.C.H., Anderson, J.D., and Carter, D.C. (1996) Cell Cycle Arrest and Induction of Apoptosis in Pancreatic Cancer Exposed to Eicosapentaenoic Acid in vitro, Br. J. Cancer 74, 1375-1383.
45. Shaw, P.H. (1996) The Role of p53 in Cell Cycle Regulation, Pathol. Res. Pract. 192, 669-675.
46. Merchant, A.K., Loney, T.L., and Maybaum, J. (1996) Expression of Wild-Type p53 Stimulates an Increase in Both Bax and Bcl-xL Protein Content in HT29 Cells, Oncogene 13, 2631-2637.
47. Hagve, T.A., Woldseth, B., Brox, J., Narce, M., and Poisson, J.P. (1998) Membrane Fluidity and Fatty Acid Metabolism in Kidney Cells from Rats Fed Purified Eicosapentaenoic Acid or Purified Docosahexaenoic Acid, Scand. J. Clin. Lab. Invest. 58, 187-194.
48. Heerdt, B.C., Houston, M.A., and Augenlicht, L.H. (1994) Potentiation of Specific Short-Chain Fatty Acids of Differentiation and Apoptosis in Human Colonic Carcinoma Cell Lines. Cancer Res. 54, 3288-3293.
49. Bracey, T.S., Miller, J.C., Preece, A., and Pareskeva, C. (1995) γ-Radiation-Induced Apoptosis in Human Colorectal Adenoma and Carcinoma Cell Lines Can Occur in the Absence of Wild Type p53, Oncogene 10, 2391-2396.
50. Gesmundo, N., Casali, E., Farruggia, G., Spisni, A., and Masotti, L. (1994) In vitro Effects of Hydroxystearic Acid on the Proliferation of HT29 and 1407 Cells, Biochem. Mol. Biol. Int. 33, 705-712.
51. Sweeney, E.A., Sakakura, C., Shirahama, T., Masamune, A., Ohta, H., Hakomori, S.-I., and Igarashi, Y. (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.
52. Heerdt, B.G., Houston, M.A., Rediske, J.J., and Augenlicht, L.H. (1996) Steady-State Levels of Mitochondrial Messenger RNA Species Characterize a Predominant Pathway Culminating in Apoptosis and Shedding of HT29 Human Colonic Carcinoma Cells, Cell Growth Differ. 7, 101-106.
53. Solary, E., Bertrand, R., and Pommier, Y. (1994) Apoptosis of Human Leukemic HL-60 Cells Induced to Differentiate by Phorhol Ester Treatment, Leukemia 8, 792-797.
54. Frisch, S.M., and Francis, H. (1994) Disruption of Epithelial Cell-Matrix Interactions Induces Apoptosis, J. Cell Biol. 124, 619-626.
55. Sträter, J., Wedding, U., Barth, T.F.E., Koretz, K., Elsing, C., and Möller, P. (1996) Rapid Onset of Apoptosis in vitro Follows Disruption of bl-Integrin/Matrix Interactions in Human Colonic Crypt Cells, Gastroenterology 110, 1776-1784.
56. Chang, W.C., Chapkin, R.S., and Lupton, J.R. (1997) Predictive Value of Proliferation, Differentiation and Apoptosis as Intermediate Markers for Colon Tumorigenesis, Carcinogenesis 18, 721-730.
57. Hughes, D.A., Pinder, A.C., Piper, Z., Johnson, I.T., and Lund, E.K. (1996) Fish Oil Supplementation Inhibits the Expression of Major Histocompatihility Complex Class II Molecules and Adhesion Molecules on Human Monocyte, Am. J. Clin. Nutr. 63, 267-272.
58. Lipkin, M., Uehara, K., Winawer, S., Sanchez, A., Bauer, C., Phillips, R., Lynch, H.T., Blattner, W.A., and Fraumeni, J.F. (1993) Seventh-Day Adventist Vegetarians Have a Quiescent Proliferative Activity in Colonic Mucosa, Cancer Lett. 26, 139-144.
59. Nicholson, D.W., Ali, A., Thornberry, N.A., Vaillancourt, J.P., Ding, C.K., Gallant, M., Gareau, Y., Griffin, P.R., Labelle, M., and Lazebnik, Y.A. (1995) Identification and Inhibition of the ICE/CED-3 Protease Necessary for Mammalian Apoptosis, Nature 376, 37-43.
60. Wen, L.P., Fahrni, J.A., Troie, S., Guan, J.L., Orth, K., and Rosen, G.D. (1997) Cleavage of Focal Adhesion Kinase by Caspases During Apoptosis, J. Biol. Chem. 272, 26056-26061.
61. Fukuda, K. (1999) Apoptosis-Associated Cleavage of β-Catenin in Human Colon Cancer and Rat Hepatoma Cells, Int. J. Biochem. Cell. Biol. 31, 519-529.
62. Brancolini, C., Sgorbissa, A., and Schneider, C. (1998) Proteolytic Processing of the Adherens Junctions Components β-Catenin and γ-Catenin/Plakoglobin During Apoptosis, Cell Death Differ. 5, 1042-1050.
63. Van de Water, B., Nagelkerke, J.F., and Stevens, J.L. (1999) Dephosphorylation of Focal Adhesion Kinase (FAK) and Loss of Focal Contacts Precede Caspase-Mediated Cleavage of FAK During Apoptosis in Renal Epithelial Cells, J. Biol. Chem. 274, 13328-13337.
64. Hague, A., Manning, A.M., Hanlon, K.A., Huschtscha. L.I., Hart, D., and Pareskeva, C. (1993) Sodium Butyrate Induces Apoptosis in Human Colonic Tumor Cell Lines in a p53-Independent Pathway: Implications for the Possible Role of Dietary Fibre in the Prevention of Large Bowel Cancer, Int. J. Cancer 55, 498-505.