Comparison of the effects of various peroxisome proliferators on peroxisomal enzyme activities, DNA synthesis, and apoptosis in rat and human hepatocyte cultures

Toxicology and Applied Pharmacology

Volumn 160, Issue 1, 1999, Pages 21-32

  Goll, Valérie ^a   Alexandre, Eliane ^b   Viollon Abadie, Catherine ^a   Nicod, Laurence ^a   Jaeck, Daniel ^b,c   Richert, Lysiane ^a  

^a UNIVERSITÉ DE FRANCHE COMTÉ   (France)

^b Fondation Transplantation   (France)

^c HÔPITAL DE HAUTEPIERRE   (France)

Author keywords

Apoptosis; DNA synthesis; Enzyme activities; Hepatocyte culture; Human; Peroxisome proliferators; Rat

Indexed keywords

ACYL COENZYME A OXIDASE; AMANITIN; ANTILIPEMIC AGENT; BEZAFIBRATE; CARNITINE ACETYLTRANSFERASE; CIPROFIBRATE; CLOFIBRIC ACID; DNA; NAFENOPIN; PEROXISOME PROLIFERATOR; PHTHALIC ACID BIS(2 ETHYLHEXYL) ESTER; TRANSFORMING GROWTH FACTOR BETA; TUMOR NECROSIS FACTOR ALPHA;

ANIMAL CELL; APOPTOSIS; ARTICLE; DNA SYNTHESIS; ENZYME ACTIVITY; HUMAN; HUMAN CELL; IN VITRO STUDY; LIVER CARCINOGENESIS; LIVER CELL CULTURE; MALE; NONHUMAN; OXIDATIVE STRESS; RAT;

ANIMALIA; FELIS CATUS; RODENTIA;

EID: 0033214326     PISSN: 0041008X     EISSN: None     Source Type: Journal    
DOI: 10.1006/taap.1999.8737     Document Type: Article

References (64)

1. Ames B. N., Gold L. S. Too many rodent carcinogens: Mitogenesis increases mutagenesis. Science. 249:1990;970-971.
2. Bayly A. C., Roberts R. A., Dive C. Suppression of liver cell apoptosis in vitro by the non-genotoxic hepatocarcinogen and peroxisome proliferator nafenopin. J. Cell Biol. 125:1994;197-203.
3. Bentley P., Calder I., Elcombe C., Grasso P., Stringer D., Wiegand H. J. Hepatic peroxisome proliferation in rodents and its significance for humans. Food Chem. Toxicol. 31:1993;857-907.
4. Beyer H. S., Theologides A. Tumor necrosis factor-α is a direct hepatocyte mitogen in the rat. Biochem. Mol. Biol. Int. 29:1993;1-4.
5. Bichet N., Cahard D., Fabre G., Remandet B., Gouy D., Cano J.-P. Comparison of peroxisome proliferation in rat and human hepatocytes in primary cultures. Toxicol. Appl. Pharmacol. 106:1990;509-517.
6. Blaauboer B. J., van Holsteijn C. W. M., Bleumink R., Mennes W. C., van Pelt F. N. A. M., Yap S. H., van Pelt J. F., van Iersel A. A. J., Timmerman A., Schmid B. P. The effect of beclobric acid and clofibric acid on peroxisomal β-oxidation and peroxisome proliferation in primary cultures of rat, monkey and human hepatocytes. Biochem. Pharmacol. 40:1990;521-528.
7. Blanc P. B., Etienne H., Daujat M., Fabre I., Zindy F., Domergue J., Astre C., Saint Aubert B., Michel H., Maurel P. Mitotic responsiveness of cultured adult human hepatocytes to epidermal growth factor, transforming growth factor α, and human serum. Gastroenterology. 102:1992;1340-1350.
8. Bojes H. K., Germolec D. R., Simeonova P., Bruccoleri A., Schoonhoven R., Luster M. I., Thurman R. G. Antibodies to tumor necrosis factor α prevent increases in cell replication in liver due to the potent peroxisome proliferator Wy-14-643. Carcinogenesis. 18:1997;669-674.
9. Bojes H. K., Thurman R. G. Peroxisome proliferators activate Kupffer cells in vivo. Cancer Res. 56:1996;1.
10. Brocard C., Es-Souni M., Ramirez L., Latruffe N., Bournot P. Stimulation of peroxisomal palmitoyl-CoA oxidase activity by ciprofibrate in hepatic cell lines: Comparative studies in FaO, MH1C1 and HepG2 cells. Biol. Cell. 77:1993;37-41.
11. Christensen J. G., Gonzales A. J., Cattley R. C., Goldsworthy T. L. Regulation of apoptosis in mouse hepatocytes and alteration of apoptosis by nongenotoxic carcinogens. Cell Growth Differ. 9:1998;815-825.
12. David P., Viollon-Abadie C., Alexandre E., Nicod L., Wolf P., Jaeck D., Boudjema K., Richert L. Metabolic capacities in cultured human hepatocytes obtained by a new isolating procedure from non-wedge small liver biopsies. Hum. Exp. Toxicol. 17:1998;544-553.
13. Donato M. T., Gomez-Lechon M. J., Castell J. V. Effect of xenobiotics on monooxygenase activities in cultured human hepatocytes. Biochem. Pharmacol. 39:1990;1321-1326.
14. Elcock F. J., Chipman J. K., Roberts R. The rodent nongenotoxic hepatocarcinogen and peroxisome proliferator nafenopin inhibits intercellular communication in rat but not guinea-pig hepatocytes, perturbating S-phase but not apoptosis. Arch. Toxicol. 72:1998;439-444.
15. Elcombe C. R., Bell D. R., Elias E., Hasmall S. C., Plant N. J. Peroxisome proliferators: Species differences in response of primary hepatocyte cultures. Ann. NY Acad. Sci. 804:1996;628-635.
16. Foxworthy P. S., Eacho P. I. Conditions influencing the induction of peroxisomal β-oxidation in cultured rat hepatocytes. Toxicol. Lett. 30:1986;189-196.
17. Foxworthy P. S., Perry D. N., Eacho P. I. Induction of peroxisomal beta-oxidation by nonsteroidal anti-inflammatory drugs. Toxicol. Appl. Pharmacol. 118:1993;271-274.
18. Foxworthy P. S., White S. L., Hoover D. M., Eacho P. I. Effect of ciprofibrate, bezafibrate, and LY171883 on peroxisomal β-oxidation in cultured rat, dog, and rhesus monkey hepatocytes. Toxicol. Appl. Pharmacol. 104:1990;386-394.
19. Gibson G. G. Peroxisome proliferators: Paradigms and prospects. Toxicol. Lett. 68:1993;193-201.
20. Gill J. H., James N. H., Roberts R. A., Dive C. The non-genotoxic hepatocarcinogen nafenopin suppresses rodent hepatocyte apoptosis induced by TGFβ, DNA damage and FAS. Carcinogenesis. 19:1998;299-304.
21. Gomez-Lechon M. J., Castelli J., Guillen I., O'Connor E., Nakamura T., Fabra R., Trullenque R. Effects of hepatocyte growth factor on the growth and metabolism of human hepatocytes in primary cultures. Hepatology. 21:1995;1248-1254.
22. Grasl-Kraupp B., Ruttkay-Nedecky B., Mullauer L., Taper H., Huber W., Bursch W., Schulte-Hermann R. Inherent increase of apoptosis in liver tumors: Implications for carcinogenesis and tumor regression. Hepatology. 25:1997;906-912.
23. Gray T. J. B., Lake B. G., Beamand J. A., Foster J. R., Gangolli S. D. Peroxisome proliferation in primary cultures of rat hepatocytes. Toxicol. Appl. Pharmacol. 67:1983;15-25.
24. Green S., Issemann I., Tugwood J. D., Prince R. A., Aldridge T. C. Delineating peroxisome proliferation action to improve human risk assessment. Receptor-Mediated Biological Processes: Implications for Evaluating Carcinogenesis. 1994;Wiley-Liss, New York. p. 311-333.
25. Hong J. T., Glauert H. P. Comitogenicity of eicosanoids and the peroxisome proliferator ciprofibrate in cultured rat hepatocytes. J. Cell. Physiol. 169:1996;309-319.
26. Huber W. W., Grasl-Kraupp B., Schulte-Hermann R. Hepatocarcinogenic potential of di(2-ethylhexyl)phthalate in rodents and its implications of human risk. Crit. Rev. Toxicol. 26:1996;365-481.
27. Issemann I., Prince R. A., Tugwood J. D., Green S. The peroxisome proliferator-activated receptor: Retinoid X receptor heterodimer is activated by fatty acids and fibrate hypolipidaemic drugs. J. Mol. Endocrinol. 11:1993;37-47.
28. James N. H., Roberts R. A. Species differences in the clonal expansion of hepatocytes in response to the coaction of epidermal growth factor and nafenopin, a rodent hepatocarcinogenic peroxisome proliferator. Fundam. Appl. Toxicol. 26:1995;143-149.
29. James N. H., Roberts R. A. Species differences in response to peroxisome proliferators correlate in vitro with induction of DNA synthesis rather than suppression of apoptosis. Carcinogenesis. 17:1996;1623-1632.
30. Karam W. G., Ghanayem B. I. Induction of replicative DNA synthesis and PPARα-dependent gene transcription by Wy-14,643 in primary rat hepatocyte and non-parenchymal cell co-cultures. Carcinogenesis. 18:1997;2077-2083.
31. Kasai H., Okada Y., Nishimura S., Rao M. S., Reddy J. K. Formation of 8-hydroxydeoxyguanosine in liver DNA of rats following long-term exposure to a peroxisome proliferator. Cancer Res. 49:1989;2603-2605.
32. Lake B. G. Mechanisms of hepatocarcinogenicity of peroxisome-proliferating drugs and chemicals. Annu. Rev. Pharmacol. Toxicol. 35:1995a;483-507.
33. Lake B. G. Peroxisome proliferation: Current mechanisms relating to non-genotoxic carcinogenesis. Toxicol. Lett. 82/83:1995b;673-681.
34. Lazarow P. B. Three hypolipidemic drugs increase hepatic palmitoyl CoA oxidation in the rat. Science. 197:1977;580-581.
35. Lee S. S. T., Pineau T., Drago J., Lee E. J., Owens J. W., Kroetz D. L., Fernandez-Salguero P. M., Westphal H., Gonzalez F. J. Targeted disruption of the α isoform of the peroxisome proliferator-activated receptor gene in mice results in abolishment of the pleitropic effects of peroxisome proliferators. Mol. Cell. Biol. 15:1995;3012-3022.
36. Leist M., Gantner F., Naumann H., Bluethmann H., Vogt K., Brigelius-Flohe R., Nicotera P., Volk H.-D., Wendel A. Tumor necrosis factor-induced apoptosis during poisoning of mice with hepatotoxins. Gastroenterology. 112:1997;923-934.
37. Marsman D. S., Cattley R. C., Conway J. G., Popp J. A. Relationship of hepatic peroxisome proliferation and replicative DNA synthesis to the hepatocarcinogenicity of the peroxisome proliferators di(2-ethylhexyl)phthalate and [4-Chloro-6-(2,3-xylidino)-2-pyrimidinylthio]acetic acid (Wy-14,643) in rats. Cancer Res. 48:1988;6739-6744.
38. Marsman D. S., Swanson-Pfeiffer C. L., Popp J. A. Lack of comitogenicity by the peroxisome proliferator hepatocarcinogens, Wy-14,643 and clofibric acid. Toxicol. Appl. Pharmacol. 122:1993;1-6.
39. Mitchell A. M., Bridges J. W., Elcombe C. R. Factors influencing peroxisome proliferation in cultured rat hepatocytes. Arch. Toxicol. 55:1984;239-246.
40. Motojima K. Peroxisome proliferator-activated receptor (PPAR): Structure, mechanisms of action and diverse functions. Cell. Struct. Funct. 18:1993;267-277.
41. Muerhoff A. S., Griffin K. J., Johnson E. F. The peroxisome proliferator-activated receptor mediates the induction of CYP4A6, a cytochrome P450 fatty omega-hydroxylase, by clofibric acid. J. Biol. Chem. 267:1992;19051-19053.
42. Oliver M. F., Heady J. A., Morris J. N., Cooper J. WHO cooperative trial on primary prevention of ischemic hearth disease with clofibrate to lower serum cholesterol: Final mortality follow-up. Lancet. 8403:1984;600-605.
43. Parzefall W., Erber E., Sedivy R., Schulte-Hermann R. Testing for induction of DNA synthesis in human hepatocyte primary cultures by rat liver tumor promoters. Cancer Res. 51:1991;1143-1147.
44. Perrone C. E., Shao L., Williams G. M. Effect of rodent hepatocarcinogenic peroxisome proliferators on fatty acyl-CoA oxidase, DNA synthesis, and apoptosis in cultured human and rat hepatocytes. Toxicol. Appl. Pharmacol. 150:1998;277-286.
45. Peters J. M., Cattley R. S., Gonzalez F. J. Role of PPARα in the mechanism of action of the nongenotoxic carcinogen and peroxisome proliferator Wy-14,643. Carcinogenesis. 18:1997;2029-2033.
46. Plant N. J., Horley N. J., Dickins M., Hasmall S., Elcombe C. R., Bell D. R. The coordinate regulation of DNA synthesis and suppression of apoptosis is differentially regulated by the liver growth agents, phenobarbital and methylclofenapate. Carcinogenesis. 19:1998;1521-1527.
47. Randerath E., Randerath K., Reddy R., Danna T. F., Rao M. S., Reddy J. K. Induction of rat liver DNA alterations by chronic administration of peroxisome proliferators as detected by 32P-postlabeling. Mutat. Res. 247:1991;65-76.
48. Reddy J. K., Lalwani N. D. Carcinogenesis by hepatic peroxisome proliferators: Evaluation of the risk of hypolipidemic drugs and industrial plasticizers to humans. CRC Crit. Rev. Toxicol. 12:1983;1-59.
49. Reddy J. K., Reddy M. K., Usman M. I., Lalwani N. D., Rao M. S. Comparison of hepatic peroxisome proliferative effect and its implication for hepatocarcinogenicity of phthalate esters, di (2-ethylhexyl) adipate with a hypolipidemic drug. Environ. Health Perspect. 65:1986;317-327.
50. Richert L., Price S., Chesne C., Maita K., Carmichael N. Comparison of the induction of hepatic peroxisome proliferation by the herbicide oxadiazon in vivo in rats, mice, and dogs and in vitro in rat and human hepatocytes. Toxicol. Appl. Pharmacol. 141:1996;35-43.
51. Roberts R. A., James N. H., Woodyatt N. J., Macdonald N., Tugwood J. D. Evidence for the suppression of apoptosis by the peroxisome proliferator activated receptor alpha (PPARα). Carcinogenesis. 19:1998;43-48.
52. Roberts R. A., Soames A. R., Gill J. H., James N. H., Wheeldon E. B. Non-genotoxic hepatocarcinogens stimulate DNA synthesis and their withdrawal induces apoptosis, but in different hepatocyte populations. Carcinogenesis. 16:1995;1693-1698.
53. Rolfe M., James N. H., Roberts R. A. Tumour necrosis factor α (TNFα) suppresses apoptosis and induces DNA synthesis in rodent hepatocytes: A mediator of the hepatocarcinogenicity of peroxisome proliferators. Carcinogenesis. 18:1997;2277-2280.
54. Rose M. L., Germolec D., Arteel G. E., Schoonhoven R., Thurman R. G. Dietary glycine prevents increases in hepatocyte proliferation caused by peroxisome proliferator WY-14,643. Chem. Res. Toxicol. 10:1997a;1198-1204.
55. Rose M. L., Germolec D. R., Schoonhoven R., Thurman R. G. Kupffer cells are causally responsible for the mitogenic effect of peroxisome proliferators. Carcinogenesis. 18:1997b;1453-1456.
56. Seglen P. O. Preparation of rat liver cells. III. Enzymatic requirements for tissue dispersion. Exp. Cell Res. 82:1973;391-398.
57. Sharma R., Lake B. G., Gibson G. G. Co-induction of microsomal cytochrome P-452 and the peroxisomal fatty acid β-oxidation pathway in the rat by clofibrate and di-(2-ethylhexyl)phthalate. Biochem. Pharmacol. 37:1988;1203-1206.
58. Sher T., Yi H. F., McBride O. W., Gonzalez F. J. cDNA cloning, chromosomal mapping, and functional characterisation of the human peroxisome proliferator activated receptor. Biochemistry. 32:1993;5598-5604.
59. Takagi A., Sai K., Umemura T., Hasegawa R., Kurokawa Y. Hepatomegaly is an early biomarker for hepatocarcinogenesis induced by peroxisome proliferators. JEPTO. 11:1992;145-149.
60. Tanaka K., Smith P. F., Stromberg P. C., Liydelloth R. S., Herold E. G., Grossman S. J., Frank J. D., Hertzog P. R., Soper K. A., Keenan K. P. Studies of early hepatocellular proliferation and peroxisomal proliferation in Sprague-Dawley rats treated with tumorigenic doses of clofibrate. Toxicol. Appl. Pharmacol. 116:1992;71-77.
61. Tomaszewski K. E., Heindel S. W., Jenkins W. L., Melnick R. L. Induction of peroxisomal acyl CoA oxidase activity and lipid peroxidation in primary rat hepatocyte cultures. Toxicology. 65:1990;49-60.
62. Tugwood J. D., Aldridge T. C., Lambe K. G., MacDonald N., Woodyatt N. J. Peroxisome proliferator-activated receptors: Structure and function. Ann. NY Acad. Sci. 804:1996;252-265.
63. Wada N., Marsman D. S., Popp J. A. Dose related effects of hepatocarcinogen, Wy-14,643, on peroxisomes and cell proliferation. Fundam. Appl. Toxicol. 16:1992;149-154.
64. Zhang B., Marcus S., Miyata K. S., Subramani S., Capone J., Rachunbinski A. Characterization of protein-DNA interactions within peroxisome proliferation-responsive element of the rat hydratase-dehydrogenase gene. J. Biol. Chem. 268:1993;12939-12945.