Induction of an altered lipid phenotype by two cancer promoting treatments in rat liver

Food and Chemical Toxicology

Volumn 78, Issue , 2015, Pages 96-104

  Riedel, S ^a   Abel, S ^b   Swanevelder, S ^a   Gelderblom, W C A ^b,c  

^a SOUTH AFRICAN MEDICAL RESEARCH COUNCIL   (South Africa)

^b CAPE PENINSULA UNIVERSITY OF TECHNOLOGY   (South Africa)

^c STELLENBOSCH UNIVERSITY   (South Africa)

Author keywords

2 Acetylaminofluorene; Cancer promotion; Fatty acids; Fumonisins; Hepatocyte nodules; Rats

Indexed keywords

CHOLESTEROL; FUMONISIN B1; LIPID; MONOUNSATURATED FATTY ACID; N (2 FLUORENYL)ACETAMIDE; OMEGA 3 FATTY ACID; OMEGA 6 FATTY ACID; PHOSPHATIDYLCHOLINE; PHOSPHATIDYLETHANOLAMINE; POLYUNSATURATED FATTY ACID; FATTY ACID; FUMONISIN; UNSATURATED FATTY ACID;

ANIMAL EXPERIMENT; ANIMAL MODEL; ANIMAL TISSUE; ARTICLE; CANCER GROWTH; CONTROLLED STUDY; FATTY ACID METABOLISM; LIVER CANCER; LIVER CARCINOGENESIS; MALE; MEMBRANE FLUIDITY; MEMBRANE STRUCTURE; NONHUMAN; PARTIAL HEPATECTOMY; PHENOTYPE; RAT; TUMOR PROMOTION; ANIMAL; CHEMICALLY INDUCED; DRUG EFFECTS; EXPERIMENTAL LIVER NEOPLASM; FISCHER 344 RAT; LIPID METABOLISM; LIVER; LIVER CELL; METABOLISM;

RATTUS;

2-ACETYLAMINOFLUORENE; ANIMALS; CHOLESTEROL; FATTY ACIDS; FATTY ACIDS, MONOUNSATURATED; FATTY ACIDS, UNSATURATED; FUMONISINS; HEPATOCYTES; LIPID METABOLISM; LIVER; LIVER NEOPLASMS, EXPERIMENTAL; MALE; PHENOTYPE; PHOSPHATIDYLCHOLINES; PHOSPHATIDYLETHANOLAMINES; RATS; RATS, INBRED F344;

EID: 84923200286     PISSN: 02786915     EISSN: 18736351     Source Type: Journal    
DOI: 10.1016/j.fct.2015.01.023     Document Type: Article

References (81)

1. Abel S., Gelderblom W.C. Oxidative damage and fumonisin B1-induced toxicity in primary rat hepatocytes and rat liver in vivo. Toxicology 1998, 131:121-131.
2. Abel S., Smuts C.M., de Villiers C., Gelderblom W.C. Changes in essential fatty acid patterns associated with normal liver regeneration and the progression of hepatocyte nodules in rat hepatocarcinogenesis. Carcinogenesis 2001, 22:795-804.
3. Abel S., De Kock M., Smuts C.M., de Villiers C., Swanevelder S., Gelderblom W.C.A. Dietary modulation of fatty acid profiles and oxidative status of rat hepatocyte nodules: effect of different n-6/n-3 fatty acid ratios. Lipids 2004, 39:963-976.
4. Abel S., De Kock M., Van Schalkwyk D.J., Swanevelder S., Kew M.C., Gelderblom W.C.A. Altered lipid profile, oxidative status and hepatitis B virus interactions in human hepatocellular carcinoma. Prostaglandins Leukot. Essent. Fatty Acids 2009, 81:391-399. 10.1016/j.plefa.2009.08.003.
5. AIN Report of the American Institute of Nutrition Ad Hoc Committee on standards for nutritional studies. J. Nutr 1977, 107:1340-1348.
6. Bieri J.G. Second report of the ad hoc committee on standards for nutritional studies. J. Nutr 1980, 110:1726.
7. Bougnoux P., Chajes V., Lanson M., Hacene K., Body G., Couet C., et al. Prognostic significance of tumor phosphatidylcholine stearic acid level in breast carcinoma. Breast Cancer Res. Treat 1992, 20:185-194.
8. Burger H.-M., Abel S., Snijman P.W., Swanevelder S., Gelderblom W.C.A. Altered lipid parameters in hepatic subcellular membrane fractions induced by fumonisin B1. Lipids 2007, 42:249-261. 10.1007/s11745-007-3025-9.
9. Calviello G., Palozza P., Piccioni E., Maggiano N., Frattucci A., Franceschelli P., et al. Dietary supplementation with eicosapentaenoic and docosahexaenoic acid inhibits growth of Morris hepatocarcinoma 3924A in rats: effects on proliferation and apoptosis. Int. J. Cancer 1998, 75:699-705.
10. Canuto R.A., Biocca M.E., Muzio G., Dianzani M.U. Fatty acid composition of phospholipids in mitochondria and microsomes during diethylnitrosamine carcinogenesis in rat liver. Cell Biochem. Funct 1989, 7:11-19. 10.1002/cbf.290070104.
11. Cawood M.E., Gelderblom W.C.A., Vleggaar R., Behrend Y., Thiel P.G., Marasas W.F.O. Isolation of the fumonisin mycotoxins: a quantitative approach. J. Agric. Food Chem 1991, 39:1958-1962.
12. Chajès V., Joulin V., Clavel-Chapelon F. The fatty acid desaturation index of blood lipids, as a biomarker of hepatic stearoyl-CoA desaturase expression, is a predictive factor of breast cancer risk. Curr. Opin. Lipidol 2011, 22:6-10. 10.1097/MOL.0b013e3283404552.
13. Cheeseman K.H., Burton G.W., Ingold K.U., Slater T.F. Lipid peroxidation and lipid antioxidants in normal and tumor cells. Toxicol. Pathol 1984, 12:235-239.
14. Cuendet M., Pezzuto J.M. The role of cyclooxygenase and lipoxygenase in cancer chemoprevention. Drug Metabol. Drug Interact 2000, 17:109-157.
15. Cuvillier O. Downregulating sphingosine kinase-1 for cancer therapy. Expert Opin. Ther. Targets 2008, 12:1009-1020. 10.1517/14728222.12.8.1009.
16. Denda A., Ura H., Tsujiuchi T., Tsutsumi M., Eimoto H., Takashima Y., et al. Possible involvement of arachidonic acid metabolism in phenobarbital promotion of hepatocarcinogenesis. Carcinogenesis 1989, 10:1929-1935.
17. Diplock A.T., Balasubramanian K.A., Manohar M., Mathan V.I., Ashton D. Purification and chemical characterisation of the inhibitor of lipid peroxidation from intestinal mucosa. Biochim. Biophys. Acta 1988, 962:42-50.
18. Emoto K., Umeda M. An essential role for a membrane lipid in cytokinesis. Regulation of contractile ring disassembly by redistribution of phosphatidylethanolamine. J. Cell Biol 2000, 149:1215-1224.
19. Farber E. Clonal adaptation as an important phase of hepatocarcinogenesis. Cancer Biochem. Biophys 1991, 12:157-165.
20. Farombi E.O., Tahnteng J.G., Agboola A.O., Nwankwo J.O., Emerole G.O. Chemoprevention of 2-acetylaminofluorene-induced hepatotoxicity and lipid peroxidation in rats by kolaviron - a Garcinia kola seed extract. Food Chem. Toxicol 2000, 38:535-541.
21. Folch J., Lees M., Sloane Stanley G.H. A simple method for the isolation and purification of total lipids from animal tissues. J. Biol. Chem 1957, 226:497-509.
22. Gelderblom W.C., Snyman S.D., van der Westhuizen L., Marasas W.F. Mitoinhibitory effect of fumonisin B1 on rat hepatocytes in primary culture. Carcinogenesis 1995, 16:625-631.
23. Gelderblom W.C., Snyman S.D., Abel S., Lebepe-Mazur S., Smuts C.M., van der Westhuizen L., et al. Hepatotoxicity and -carcinogenicity of the fumonisins in rats: a review regarding mechanistic implications for establishing risk in humans. Adv. Exp. Med. Biol 1996, 392:279-296.
24. Gelderblom W.C., Snyman S.D., Lebepe-Mazur S., van der Westhuizen L., Kriek N.P., Marasas W.F. The cancer-promoting potential of fumonisin B1 in rat liver using diethylnitrosamine as a cancer initiator. Cancer Lett 1996, 109:101-108.
25. Gelderblom W.C., Abel S., Smuts C.M., Marnewick J., Marasas W.F., Lemmer E.R., et al. Fumonisin-induced hepatocarcinogenesis: mechanisms related to cancer initiation and promotion. Environ. Health Perspect 2001, 109(Suppl. 2):291-300.
26. Gelderblom W.C.A., Marasas W.F.O. Controversies in fumonisin mycotoxicology and risk assessment. Hum. Exp. Toxicol 2012, 31:215-235. 10.1177/0960327110395338.
27. Gelderblom W.C.A., Moritz W., Swanevelder S., Smuts C.M., Abel S. Lipids and delta6-desaturase activity alterations in rat liver microsomal membranes induced by fumonisin B1. Lipids 2002, 37:869-877.
28. Gilfillan A.M., Chu A.J., Smart D.A., Rooney S.A. Single plate separation of lung phospholipids including disaturated phosphatidylcholine. J. Lipid Res 1983, 24:1651-1656.
29. Grant K.I. LOWRY - a simple BASIC program for the analysis of protein assays over a wide range of concentrations. Comput. Methods Programs Biomed 1990, 31:237-242.
30. Gruner S.M. Intrinsic curvature hypothesis for biomembrane lipid composition: a role for nonbilayer lipids. Proc. Natl. Acad. Sci. U.S.A. 1985, 82:3665-3669.
31. Horrobin D.F. Unsaturated lipids and cancer. New Approaches to Cancer Treatment - Unsaturated Lipids and Photodynamic Therapy 1994, 3-29. Churchill Communications Europe, London. D.F. Horrobin (Ed.).
32. Howard P.C., Eppley R.M., Stack M.E., Warbritton A., Voss K.A., Lorentzen R.J., et al. Fumonisin b1 carcinogenicity in a two-year feeding study using F344 rats and B6C3F1 mice. Environ. Health Perspect 2001, 109(Suppl. 2):277-282.
33. Igal R.A. Stearoyl-CoA desaturase-1: a novel key player in the mechanisms of cell proliferation, programmed cell death and transformation to cancer. Carcinogenesis 2010, 31:1509-1515. 10.1093/carcin/bgq131.
34. Itaya K., Ui M. A new micromethod for the colorimetric determination of inorganic phosphate. Clin. Chim. Acta 1966, 14:361-366.
35. Jayadev S., Linardic C.M., Hannun Y.A. Identification of arachidonic acid as a mediator of sphingomyelin hydrolysis in response to tumor necrosis factor alpha. J. Biol. Chem 1994, 269:5757-5763.
36. Kolesnick R.N., Krönke M. Regulation of ceramide production and apoptosis. Annu. Rev. Physiol 1998, 60:643-665. 10.1146/annurev.physiol.60.1.643.
37. Kuhajda F.P. Fatty-acid synthase and human cancer: new perspectives on its role in tumor biology. Nutrition 2000, 16:202-208.
38. Laconi E., Pani P., Farber E. The resistance phenotype in the development and treatment of cancer. Lancet Oncol 2000, 1:235-241.
39. Lemmer E.R., de la Motte Hall P., Omori N., Omori M., Shephard E.G., Gelderblom W.C., et al. Histopathology and gene expression changes in rat liver during feeding of fumonisin B1, a carcinogenic mycotoxin produced by Fusarium moniliforme. Carcinogenesis 1999, 20:817-824.
40. Li Z., Agellon L.B., Allen T.M., Umeda M., Jewell L., Mason A., et al. The ratio of phosphatidylcholine to phosphatidylethanolamine influences membrane integrity and steatohepatitis. Cell Metab 2006, 3:321-331. 10.1016/j.cmet.2006.03.007.
41. Li Z.Z., Berk M., McIntyre T.M., Feldstein A.E. Hepatic lipid partitioning and liver damage in nonalcoholic fatty liver disease: role of stearoyl-CoA desaturase. J. Biol. Chem 2009, 284:5637-5644. 10.1074/jbc.M807616200.
42. Lii C.K., Ko J.J., Chen H.W. No inhibition of gamma-glutamyl transpeptidase-positive foci by vitamin E with or without phenobarbital. Nutr. Cancer 1997, 27:200-205. 10.1080/01635589709514525.
43. Listenberger L.L., Ory D.S., Schaffer J.E. Palmitate-induced apoptosis can occur through a ceramide-independent pathway. J. Biol. Chem 2001, 276:14890-14895. 10.1074/jbc.M010286200.
44. Mahler S.M., Wilce P.A., Shanley B.C. Studies on regenerating liver and hepatoma plasma membranes - I. Lipid and protein composition. Int. J. Biochem 1988, 20:605-611.
45. Markwell M.A., Haas S.M., Bieber L.L., Tolbert N.E. A modification of the Lowry procedure to simplify protein determination in membrane and lipoprotein samples. Anal. Biochem 1978, 87:206-210.
46. Marnewick J.L., van der Westhuizen F.H., Joubert E., Swanevelder S., Swart P., Gelderblom W.C.A. Chemoprotective properties of rooibos (Aspalathus linearis), honeybush (Cyclopia intermedia) herbal and green and black (Camellia sinensis) teas against cancer promotion induced by fumonisin B1 in rat liver. Food Chem. Toxicol 2009, 47:220-229. 10.1016/j.fct.2008.11.004.
47. Menendez J.A., Lupu R. Fatty acid synthase and the lipogenic phenotype in cancer pathogenesis. Nat. Rev. Cancer 2007, 7:763-777. 10.1038/nrc2222.
48. Merritt W.D., Morré D.J., Keenan T.W. Gangliosides of liver tumors induced by N-2-fluorenylacetamide. II. Alterations in biosynthetic enzymes. J. Natl Cancer Inst 1978, 60:1329-1337.
49. Merritt W.D., Richardson C.L., Keenan T.W., Morré D.J. Gangliosides of liver tumors induced by N-2-fluorenylacetamide. I. Ganglioside alterations in liver tumorigenesis and normal development. J. Natl Cancer Inst 1978, 60:1313-1327.
50. Minville-Walz M., Pierre A.-S., Pichon L., Bellenger S., Fèvre C., Bellenger J., et al. Inhibition of stearoyl-CoA desaturase 1 expression induces CHOP-dependent cell death in human cancer cells. PLoS ONE 2010, 5. e14363. 10.1371/journal.pone.0014363.
51. Miyazaki M., Ntambi J.M. Role of stearoyl-coenzyme A desaturase in lipid metabolism. Prostaglandins Leukot. Essent. Fatty Acids 2003, 68:113-121.
52. Mu Y.M., Yanase T., Nishi Y., Tanaka A., Saito M., Jin C.H., et al. Saturated FFAs, palmitic acid and stearic acid, induce apoptosis in human granulosa cells. Endocrinology 2001, 142:3590-3597.
53. Navarro J., Obrador E., Carretero J., Petschen I., Aviñó J., Perez P., et al. Changes in glutathione status and the antioxidant system in blood and in cancer cells associate with tumour growth in vivo. Free Radic. Biol. Med 1999, 26:410-418.
54. Neumann H.G., Bitsch A., Klöhn P.C. The dual role of 2-acetylaminofluorene in hepatocarcinogenesis: specific targets for initiation and promotion. Mutat. Res 1997, 376:169-176.
55. Ohlson L.C., Koroxenidou L., Hällström I.P. Inhibition of in vivo rat liver regeneration by 2-acetylaminofluorene affects the regulation of cell cycle-related proteins. Hepatology 1998, 27:691-696. 10.1002/hep.510270309.
56. Olsson J.M., Eriksson L.C., Dallner G. Lipid compositions of intracellular membranes isolated from rat liver nodules in Wistar rats. Cancer Res 1991, 51:3774-3780.
57. Pinelli E., Poux N., Garren L., Pipy B., Castegnaro M., Miller D.J., et al. Activation of mitogen-activated protein kinase by fumonisin B(1) stimulates cPLA(2) phosphorylation, the arachidonic acid cascade and cAMP production. Carcinogenesis 1999, 20:1683-1688.
58. Pitot H.C., Sirica A.E. The stages of initiation and promotion in hepatocarcinogenesis. Biochim. Biophys. Acta 1980, 605:191-215.
59. Ramakrishnan G., Elinos-Báez C.M., Jagan S., Augustine T.A., Kamaraj S., Anandakumar P., et al. Silymarin downregulates COX-2 expression and attenuates hyperlipidemia during NDEA-induced rat hepatocellular carcinoma. Mol. Cell. Biochem 2008, 313:53-61. 10.1007/s11010-008-9741-5.
60. Ramesh G., Das U.N. Effect of dietary fat on diethylnitrosamine induced hepatocarcinogenesis in Wistar rats. Cancer Lett 1995, 95:237-245.
61. Ramljak D., Calvert R.J., Wiesenfeld P.W., Diwan B.A., Catipovic B., Marasas W.F., et al. A potential mechanism for fumonisin B(1)-mediated hepatocarcinogenesis: cyclin D1 stabilization associated with activation of Akt and inhibition of GSK-3beta activity. Carcinogenesis 2000, 21:1537-1546.
62. Richmond W. Preparation and properties of a cholesterol oxidase from Nocardia sp. and its application to the enzymatic assay of total cholesterol in serum. Clin. Chem 1973, 19:1350-1356.
63. Riley R.T., Hinton D.M., Chamberlain W.J., Bacon C.W., Wang E., Merrill A.H., et al. Dietary fumonisin B1 induces disruption of sphingolipid metabolism in Sprague-Dawley rats: a new mechanism of nephrotoxicity. J. Nutr 1994, 124:594-603.
64. Riley R.T., Enongene E., Voss K.A., Norred W.P., Meredith F.I., Sharma R.P., et al. Sphingolipid perturbations as mechanisms for fumonisin carcinogenesis. Environ. Health Perspect 2001, 109(Suppl. 2):301-308.
65. Rothman J.E., Lenard J. Membrane asymmetry. Science 1977, 195:743-753.
66. Schulte-Hermann R., Ohde G., Schuppler J., Timmermann-Trosiener I. Enhanced proliferation of putative preneoplastic cells in rat liver following treatment with the tumor promoters phenobarbital, hexachlorocyclohexane, steroid compounds, and nafenopin. Cancer Res 1981, 41:2556-2562.
67. Seeds M.C., Bass D.A. Regulation and metabolism of arachidonic acid. Clin. Rev. Allergy Immunol 1999, 17:5-26. 10.1007/BF02737594.
68. Seegers J.C., Joubert A.M., Panzer A., Lottering M.L., Jordan C.A., Joubert F., et al. Fumonisin B1 influenced the effects of arachidonic acid, prostaglandins E2 and A2 on cell cycle progression, apoptosis induction, tyrosine- and CDC2-kinase activity in oesophageal cancer cells. Prostaglandins Leukot. Essent. Fatty Acids 2000, 62:75-84. 10.1054/plef.1999.0129.
69. Semple-Roberts E., Hayes M.A., Armstrong D., Becker R.A., Racz W.J., Farber E. Alternative methods of selecting rat hepatocellular nodules resistant to 2-acetylaminofluorene. Int. J. Cancer 1987, 40:643-645.
70. Serhan C.N. Mediator lipidomics. Prostaglandins Other Lipid Mediat 2005, 77:4-14. 10.1016/j.prostaglandins.2004.09.016.
71. Smuts C.M., Kruger M., van Jaarsveld P.J., Fincham J.E., Schall R., van der Merwe K.J., et al. The influence of fish oil supplementation on plasma lipoproteins and arterial lipids in vervet monkeys with established atherosclerosis. Prostaglandins Leukot. Essent. Fatty Acids 1992, 47:129-138.
72. Smuts C.M., Weich H.F., Weight M.J., Faber M., Kruger M., Lombard C.J., et al. Free cholesterol concentrations in the high-density lipoprotein subfraction-3 as a risk indicator in patients with angiographically documented coronary artery disease. Coron. Artery Dis 1994, 5:331-338.
73. Solt D., Farber E. New principle for the analysis of chemical carcinogenesis. Nature 1976, 263:701-703. 10.1038/263701a0.
74. Sparfel L., Loewert M., Huc L., Payen L., Guillouzo A., Lagadic-Gossmann D., et al. Acute cytotoxicity of the chemical carcinogen 2-acetylaminofluorene in cultured rat liver epithelial cells. Toxicol. Lett 2002, 129:245-254.
75. Tamiya-Koizumi K., Koizumi K., Ishihara H., Kojima K. Lipid composition of the plasma membrane isolated from hyperplastic nodules of rat liver. J. Biochem 1985, 97:773-779.
76. Tang Q., Denda A., Tsujiuchi T., Tsutsumi M., Amanuma T., Murata Y., et al. Inhibitory effects of inhibitors of arachidonic acid metabolism on the evolution of rat liver preneoplastic foci into nodules and hepatocellular carcinomas with or without phenobarbital exposure. Jpn. J. Cancer Res 1993, 84:120-127.
77. Trachootham D., Alexandre J., Huang P. Targeting cancer cells by ROS-mediated mechanisms: a radical therapeutic approach?. Nat. Rev. Drug Discov 2009, 8:579-591. 10.1038/nrd2803.
78. van der Westhuizen L., Gelderblom W.C.A., Shephard G.S., Swanevelder S. Disruption of sphingolipid biosynthesis in hepatocyte nodules: selective proliferative stimulus induced by fumonisin B1. Toxicology 2004, 200:69-75. 10.1016/j.tox.2004.03.011.
79. Wang E., Norred W.P., Bacon C.W., Riley R.T., Merrill A.H. Inhibition of sphingolipid biosynthesis by fumonisins: implications for diseases associated with Fusarium moniliforme. J. Biol. Chem 1991, 266:14486-14490.
80. Yamashita T., Honda M., Takatori H., Nishino R., Minato H., Takamura H., et al. Activation of lipogenic pathway correlates with cell proliferation and poor prognosis in hepatocellular carcinoma. J. Hepatol 2009, 50:100-110. 10.1016/j.jhep.2008.07.036.
81. Zaidi N., Lupien L., Kuemmerle N.B., Kinlaw W.B., Swinnen J.V., Smans K. Lipogenesis and lipolysis: the pathways exploited by the cancer cells to acquire fatty acids. Prog. Lipid Res 2013, 52:585-589. 10.1016/j.plipres.2013.08.005.