Inhibition of hepatocarcinogenesis by the deletion of the p50 subunit of NF-κB in mice administered the peroxisome proliferator Wy-14,643

Toxicological Sciences

Volumn 90, Issue 2, 2006, Pages 331-336

  Glauert, Howard P ^a   Eyigor, Aysegul ^b   Tharappel, Job C ^a   Cooper, Simon ^b   Lee, Eun Y ^c   Spear, Brett T ^a,b  

^a UNIVERSITY OF KENTUCKY   (United States)

^b UNIVERSITY OF KENTUCKY   (United States)

^c ULUDAG UNIVERSITY   (Turkey)

Author keywords

Apoptosis; B; Carcinogenesis; Cell proliferation; NF ; Peroxisome

Indexed keywords

BROXURIDINE; DIETHYLNITROSAMINE; IMMUNOGLOBULIN ENHANCER BINDING PROTEIN; PIRINIXIC ACID; PROTEIN P50;

ANIMAL CELL; ANIMAL EXPERIMENT; ANIMAL MODEL; ANIMAL TISSUE; APOPTOSIS; ARTICLE; CANCER INCIDENCE; CELL LABELING; CELL PROLIFERATION; CHEMICAL CARCINOGENESIS; CONTROLLED STUDY; KNOCKOUT MOUSE; LIVER CANCER; LIVER CARCINOGENESIS; LIVER CELL; MOUSE; NICK END LABELING; NONHUMAN; PROTEIN FUNCTION; WILD TYPE;

ACYL-COA OXIDASE; ADENOMA, LIVER CELL; ANIMALS; APOPTOSIS; CARCINOGENS; CELL PROLIFERATION; DIETHYLNITROSAMINE; LIVER; LIVER NEOPLASMS, EXPERIMENTAL; MICE; MICE, INBRED STRAINS; MICE, KNOCKOUT; NF-KAPPA B P50 SUBUNIT; PEROXISOME PROLIFERATORS; PYRIMIDINES;

ANIMALIA; RODENTIA;

EID: 33645131526     PISSN: 10966080     EISSN: 10960929     Source Type: Journal    
DOI: 10.1093/toxsci/kfj116     Document Type: Article

References (49)

1. Barkett, M., and Gilmore, T. D. (1999). Control of apoptosis by Rel/ NF-kappaB transcription factors. Oncogene 18, 6910-6924.
2. Bayly, A. C., French, N. J., Dive, C., and Roberts, R. A. (1993). Non-genotoxic hepatocarcinogenesis in vitro-the fao hepatoma line responds to peroxisome proliferators and retains the ability to undergo apoptosis. J. Cell. Sci. 104, 307-315.
3. Bayly, A. C., Roberts, R. A., and Dive, C. (1994). Suppression of liver cell apoptosis in vitro by the non-genotoxic hepatocarcinogen and peroxisome proliferator nafenopin. J. Cell Biol. 125, 197-203.
4. Beg, A. A., and Baltimore, D. (1996). An essential role for NF-kappa B in preventing TNF-alpha-induced cell death. Science 274, 782-784.
5. Beg, A. A., Sha, W. C., Bronson, R. T., Ghosh, S., and Baltimore, D. (1995). Embryonic lethality and liver degeneration in mice lacking the RelA component of NF-kappa B. Nature 376, 167-170.
6. Borges, T., Peterson, R. E., Pitot, H. C., Robertson, L. W., and Glauert, H. P. (1993). Effect of the peroxisome proliferator perfluorodecanoic acid on the promotion of two-stage hepatocarcinogenesis in rats. Cancer Lett. 72, 111-120.
7. Calfee-Mason, K. G., Spear, B. T., and Glauert, H. P. (2004). Effects of vitamin E on the NF-kB pathway in rats treated with the peroxisome proliferator, ciprofibrate. Toxicol. Appl. Pharmacol. 199, 1-9.
8. Cattley, R. C., DeLuca, J., Elcombe, C., FennerCrisp, P., Lake, B. G., Marsman, D. S., Pastoor, T. A., Popp, J. A., Robinson, D. E., Schwetz, B., et al. (1998). Do peroxisome proliferating compounds pose a hepatocarcinogenic hazard to humans? Regul. Toxicol. Pharmacol. 27, 47-60.
9. Cattley, R. C., and Popp, J. A. (1989). Differences between the promoting activities of the peroxisome proliferator Wy-14,643 and phenobarbital in rat liver. Cancer Res. 49, 3246-3251.
10. Chaisson, M. L., Brooling, J. T., Ladiges, W., Tsai, S., and Fausto, N. (2002). Hepatocyte-specific inhibition of NF-kappa B leads to apoptosis after TNF treatment, but not after partial hepatectomy. J. Clin. Invest. 110, 193-202.
11. Chen, H., Huang, C. Y., Wilson, M. W., Lay, L. T., Robertson, L. W., Chow, C. K., and Glauert, H. P. (1994). Effect of the peroxisome proliferators ciprofibrate and perfluorodecanoic acid on hepatic cell proliferation and toxicity in Sprague-Dawley rats. Carcinogenesis 15, 2847-2850.
12. Deangelis, R. A., Kovalovich, K., Cressman, D. E., and Taub, R. (2001). Normal liver regeneration in p50/nuclear factor kappa B1 knockout mice. Hepatology 33, 915-924.
13. Demartin, R., Schmid, J. A., and Hoferwarbinek, R. (1999). The NF-kappa B/Rel family of transcription factors in oncogenic transformation and apoptosis. Mutat. Res. Rev. Mutat. Res. 437, 231-243.
14. Durnford, J. M., Hejtmancik, M. R., Kurtz, P. J., Renne, R. A., Gideon, K. M., Marsman, D. S., Vallant, M., Chhabra, R., and Cunningham, M. L. (1998). Peroxisomal enzyme activity and cell proliferation in rats, mice and hamsters exposed for 13-weeks to Wy-14,643 and gemfibrozil. Toxicol. Sci. 42, 11.
15. Eacho, P. I., and Feller, D. R. (1991). Hepatic peroxisome proliferation induced by hypolipidemic drugs and other chemicals. In Antilipidemic Drugs, Medicinal, Chemical and Biochemical Aspects (D. T. Witiak, H. A. I. Newman, and D. R. Feller, Eds.), pp. 375-426. Elsevier Science, Amsterdam.
16. Eacho, P. I., Lanier, T. L., and Brodhecker, C. A. (1991). Hepatocellular DNA synthesis in rats given peroxisome proliferating agents: Comparison of WY-14,643 to clofibric acid, nafenopin and LY171883. Carcinogenesis 12, 1557-1561.
17. Gabbita, S. P., Robinson, K. A., Stewart, C. A., Floyd, R. A., and Hensley, K. (2000). Redox regulatory mechanisms of cellular signal transduction. Arch. Biochem. Biophys. 376, 1-13.
18. Glauert, H. P., Beer, D., Rao, M. S., Schwarz, M., Xu, Y. D., Goldsworthy, T. L., Coloma, J., and Pitot, H. C. (1986). Induction of altered hepatic foci in rats by the administration of hypolipidemic peroxisome proliferators alone or following a single dose of diethylnitrosamine. Cancer Res. 46, 4601-4606.
19. Horwitz, B. H., Zelazowski, P., Shen, Y., Wolcott, K. M., Scott, M. L., Baltimore, D., and Snapper, C. M. (1999). The p65 subunit of NF-kappa B is redundant with p50 during B cell proliferative responses, and is required for germline C-H transcription and class switching to IgG3. J. Immunol. 162, 1941-1946.
20. Kato, A., Edwards, M. J., and Lentsch, A. B. (2002). Gene deletion of NF-kappa B p50 does not alter the hepatic inflammatory response to ischemia/reperfusion. J. Hepatol. 37, 48-55.
21. Kontgen, F., Grumont, R. J., Strasser, A., Metcalf, D., Li, R., Tarlinton, D., and Gerondakis, S. (1995). Mice lacking the c-rel proto-oncogene exhibit defects in lymphocyte proliferation, humoral immunity, and interleukin-2 expression. Genes Dev. 9, 1965-1977.
22. Ledda-Columbano, G. M., Curto, M., Piga, R., Zedda, A. I., Menegazzi, M., Sartori, C., Shinozuka, H., Bluethmann, H., Poli, V., Ciliberto, G., et al. (1998). In vivo hepatocyte proliferation is inducible through a TNF and IL-6-independent pathway. Oncogene 17, 1039-1044.
23. Li, Y., Leung, L. K., Glauert, H. P., and Spear, B. T. (1996). Treatment of rats with the peroxisome proliferator ciprofibrate results in increased liver NF-kappa B activity. Carcinogenesis 17, 2305-2309.
24. Li, Y. X., Glauert, H. P., and Spear, B. T. (2000a). Activation of nuclear factor-kappa B by the peroxisome proliferator ciprofibrate in H4IIEC3 rat hepatoma cells and its inhibition by the antioxidants N-acetylcysteine and vitamin E. Biochem. Pharmacol. 59, 427-434.
25. Li, Y. X., Tharappel, J. C., Cooper, S., Glenn, M., Glauert, H. P., and Spear, B. T. (2000b). Expression of the hydrogen peroxide-generating enzyme fatty acyl CoA oxidase activates NF-kappa B. DNA Cell Biol. 19, 113-120.
26. Lu, Z., Lee, E. Y., Robertson, L. W., Glauert, H. P., and Spear, B. T. (2004). Effect of 2,2′,4,4′,5,5′-hexachlorobiphenyl (PCB-153) on hepatocyte proliferation and apoptosis in mice deficient in the p50 subunit of the transcription factor NF-kB. Toxicol. Sci. 81, 35-42.
27. Maronpot, R. R., Montgomery, C. A. J., Boorman, G. A., and McConnell, E. E. (1986). National toxicology program nomenclature for hepatoproliferative lesions of rats. Toxicol. Pathol. 14, 263-273.
28. Marsman, D. S., Cattley, R. C., Conway, J. G., and Popp, J. A. (1988). 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, 6739-6744.
29. Meyer, M., Pahl, H. L., and Baeuerle, P. A. (1994). Regulation of the transcription factors NF-kappa B and AP-1 by redox changes. Chem. Biol. Interact. 91, 91-100.
30. Nilakantan, V., Spear, B. T., and Glauert, H. P. (1998). Liver-specific catalase expression in transgenic mice inhibits NF-kappa B activation and DNA synthesis induced by the peroxisome proliferator ciprofibrate. Carcinogenesis 19, 631-637.
31. O'Brien, M. L., Spear, B. T., and Glauert, H. P. (2005). Role of oxidative stress in peroxisome proliferator-mediated carcinogenesis. Crit. Rev. Toxicol. 35, 61-88.
32. Poosch, M. S., and Yamazaki, R. K. (1986). Determination of peroxisomal fatty acyl-CoA oxidase activity using a lauroyl-CoA-based fluorometric assay. Biochimica et Biophysica Acta 884, 585-593.
33. Rao, M. S., and Reddy, J. K. (1987). Peroxisome proliferation and hepatocarcinogenesis. Carcinogenesis 8, 631-636.
34. Reddy, J. K., and Lalwani, N. D. (1983). Carcinogenesis by hepatic peroxisome proliferators: Evaluation of the risk of hypolipidemic drugs and industrial plasticizers to humans. CRC Crit. Rev. Toxicol. 12, 1-58.
35. Reddy, J. K., and Rao, M. S. (1978). Enhancement by Wy-14,643, a hepatic peroxisome proliferator, of diethylnitrosamine-initiated hepatic tumorigenesis in the rat. Br. J. Cancer 38, 537-543.
36. Roberts, R. A., Soames, A. R., Gill, J. H., James, N. H., and Wheeldon, E. B. (1995). Non-genotoxic hepatocarcinogens stimulate DNA synthesis and their withdrawal induces apoptosis, but in different hepatocyte populations. Carcinogenesis 16, 1693-1698.
37. Schoemaker, M. H., Ros, J. E., Homan, M., Trautwein, C., Liston, P., Poelstra, K., vanGoor, H., Jansen, P. L. M., and Moshage, H. (2002). Cytokine regulation of pro- and anti-apoptotic genes in rat hepatocytes: NF-kappa B-regulated inhibitor of apoptosis protein 2 (CIAP2) prevents apoptosis. J. Hepatol. 36, 742-750.
38. Schoonjans, K., Staels, B., and Auwerx, J. (1996). Role of the peroxisome proliferator-activated receptor (PPAR) in mediating the effects of fibrates and fatty acids on gene expression. J. Lipid Res. 37, 907-925.
39. Schulte-Hermann, R., Bursch, W., and Grasl-Kraupp, B. (1995). Active cell death (apoptosis) in liver biology and disease. In Progress in Liver Disease (J. L. Boyer and R. K. Ockner, Eds.), pp. 1-35. Saunders, Philadelphia.
40. Sha, W. C., Liou, H. C., Tuomanen, E. I., and Baltimore, D. (1995). Targeted disruption of the p50 subunit of NF-kB leads to multifocal defects in immune responses. Cell 80, 321-330.
41. Snapper, C. M., Rosas, F. R., Zelazowski, P., Moorman, M. A., Kehry, M. R., Bravo, R., and Weih, F. (1996a). B cells lacking RelB are defective in proliferative responses, but undergo normal B cell maturation to Ig secretion and Ig class switching. J. Exp. Med. 184, 1537-1541.
42. Snapper, C. M., Zelazowski, P., Rosas, F. R., Kehry M. R., Tian, M., Baltimore, D., and Sha, W. C. (1996b). B cells from p50/NF-kappa B knockout mice have selective defects in proliferation, differentiation, germ-line CH transcription, and Ig class switching. J. Immunol. 156, 183-191.
43. Tharappel, J. C., Cunningham, M. L., Spear, B. T., and Glauert, H. P. (2001). Differential activation of hepatic NF-kappa B in rats and hamsters by the peroxisome proliferators Wy-14,643, gemfibrozil, and dibutyl phthalate. Toxicol. Sci. 62, 20-27.
44. Tharappel, J. C., Nalca, A., Owens, A. B., Ghabrial, L., Konz, E. C., Glauert, H. P., and Spear, B. T. (2003). Cell proliferation and apoptosis are altered in mice deficient in the NF-κB p50 subunit after treatment with the peroxisome proliferator ciprofibrate. Toxicol. Sci. 75, 300-308.
45. Vanantwerp, D. J., Martin, S. J., Kafri, T., Green, D. R., and Verma, I. M. (1996). Suppression of TNF-alpha-induced apoptosis by NF-kappa B. Science 274, 787-789.
46. Verma, I. M., Stevenson, J. K., Schwarz, E. M., Van Antwerp, D., and Miyamoto, S. (1995). Rel/NF-kB/IkB family: Intimate tales of association and dissociation. Genes Dev. 9, 2723-2735.
47. Wang, C. Y., Mayo, M. W., and Baldwin, A. S. (1996). TNF- and cancer therapy-induced apoptosis: Potentiation by inhibition of NF-kappa B. Science 274, 784-787.
48. Xu, Y., Bialik, S., Jones, B. E., Iumuro, Y., Kitsis, R. N., Srinivasan, A., Brenner, D. A., and Czaja, M. J. (1998). NF-kappa B inactivation converts a hepatocyte cell line TNF-alpha response from proliferation to apoptosis. Amer. J. Physiol. Cell. Physiol. 44, C1058-C1066.
49. Yeldandi, A. V., Milano, M., Subbarao, V., Reddy, J. K., and Rao, M. S. (1989). Evaluation of liver cell proliferation during ciprofibrate-induced hepatocarcinogenesis. Cancer Lett. 47, 21-27.