26S proteasome inhibitors inhibit dexamethasone-dependent increase of tyrosine aminotransferase and tryptophan 2,3-dioxygenase mRNA levels in primary cultured rat hepatocytes — Oak Academic Publishing
Research ArticleOpen AccessGoogle Scholar indexed
26S proteasome inhibitors inhibit dexamethasone-dependent increase of tyrosine aminotransferase and tryptophan 2,3-dioxygenase mRNA levels in primary cultured rat hepatocytes
Department of Nutrition and Physiology, Nihon University College of Bioresource Sciences, Fujisawa, Japan
,
Division of Biological Chemistry and Biologicals, National Institute of Health Sciences, Tokyo, Japan
,
Department of Nutrition and Physiology, Nihon University College of Bioresource Sciences, Fujisawa, Japan
,
Department of Nutrition and Physiology, Nihon University College of Bioresource Sciences, Fujisawa, Japan
,
Department of Nutrition and Physiology, Nihon University College of Bioresource Sciences, Fujisawa, Japan
,
Department of Nutrition and Physiology, Nihon University College of Bioresource Sciences, Fujisawa, Japan
,
Department of Nutrition and Physiology, Nihon University College of Bioresource Sciences, Fujisawa, Japan
,
Division of Biological Chemistry and Biologicals, National Institute of Health Sciences, Tokyo, Japan
,
Division of Biological Chemistry and Biologicals, National Institute of Health Sciences, Tokyo, Japan
1 Department of Nutrition and Physiology, Nihon University College of Bioresource Sciences, Fujisawa, Japan
2 Division of Biological Chemistry and Biologicals, National Institute of Health Sciences, Tokyo, Japan
3 Department of Nutrition and Physiology, Nihon University College of Bioresource Sciences, Fujisawa, Japan
4 Department of Nutrition and Physiology, Nihon University College of Bioresource Sciences, Fujisawa, Japan
5 Department of Nutrition and Physiology, Nihon University College of Bioresource Sciences, Fujisawa, Japan
6 Department of Nutrition and Physiology, Nihon University College of Bioresource Sciences, Fujisawa, Japan
7 Department of Nutrition and Physiology, Nihon University College of Bioresource Sciences, Fujisawa, Japan
8 Division of Biological Chemistry and Biologicals, National Institute of Health Sciences, Tokyo, Japan
9 Division of Biological Chemistry and Biologicals, National Institute of Health Sciences, Tokyo, Japan
Dexamethasone (Dex), a ligand for transcriptional enhancement of tyrosine aminotransferase (TAT) and tryptophan 2,3-dioxygenase (TO) genes, (100 nM) maximally increased these mRNA levels at 12 h and 7 h in primary cultured rat hepatocytes and the nuclear fraction, respectively. Lactacystin (5 μM) and epoxomicin (0.5 μM), 26S proteasome inhibitors, significantly suppressed the Dex-dependent maximum increase of TAT and TO mRNA levels in the cells and the nuclear fraction. Electrophoretic mobility shift assay demonstrated that lactacystin did not affect binding of glucocorticoid receptor to glucocorticoid responsive element. Furthermore, lactacystin did not affect the activation of GRE luciferase reporter by Dex transfected to the cells. The results demonstrate that 26S proteasome is positively involved in the Dex-dependent increase of TAT and TO mRNA levels in the cells and suggest that the mechanism of action of 26S proteasome may be degradation of some RNase(s), which breaks down TAT and TO mRNAs.
Beato, M., Truss, M. and Chavez, S. (1996) Control of transcription by steroid hormones. Annals of the New York Academy of Sciences, 784, 93-123. doi:10.1111/j.1749-6632.1996.tb16231.x
Schmid, E., Schmid, W., Jantzen, M., Mayer, D., Jastorff, B. and Schutz, G. (1987) Transcription activation of the tyrosine aminotransferase gene by glucocorticoids and cAMP in primary hepatocytes. European Journal of Biochemistry, 165, 499-506. doi:10.1111/j.1432-1033.1987.tb11467.x
Cake, M.H., Ho, K.K., Shelly, L., Milward, E. and Yeoh, G.C. (1989) Insulin antagonism of dexamethasone induction of tyrosine aminotransferase in cultured fetal hepatocytes. A correlation between enzyme activity, synthesis, level of messenger RNA and transcription. European Journal of Biochemistry, 182, 429-435. doi:10.1111/j.1432-1033.1989.tb14849.x
Danesch, U., Hashimoto, S., Renkawitz, R., Schutz, G. (1983) Transcriptional regulation of the tryptophan oxygenase gene in rat liver by glucocorticoids. The Journal of Biological Chemistry, 258, 4750-4753.
Nakamura, T., Niimi, S., Nawa, K., Noda, C., Ichihara, A., Takagi, Y., Anai, M. and Sakaki, Y. (1987) Multihormonal regulation of transcription of the tryptophan 2,3-dioxygenase gene in primary cultures of adult rat hepatocytes with special reference to the presence of a transcriptional protein mediating the action of glucocorticoids. Journal of Biological Chemistry, 262, 727-733.
Zilliacus, J., Wright, A.P., Carlstedt-Duke, J. and Gustafsson, J.A. (1995) Structural determinants of DNA-binding specificity by steroid receptors. Molecular Endocrinology, 9, 389-400. doi:10.1210/me.9.4.389
Newton, R. (2000) Molecular mechanisms of glucocorticoid action: What is important? Thorax, 55, 603-613. doi:10.1136/thorax.55.7.603
Deroo, B.J., Rentsch, C., Sampath, S., Young, J., De-Franco, D.B. and Archer, T.K. (2002) Proteasomal inhibition enhances glucocorticoid receptor transactivation and alters its subnuclear trafficking. Molecular and Cellular Biology, 22, 4113-4123. doi:10.1128/MCB.22.12.4113-4123.2002
Wallace, A.D. and Cidlowski, J.A. (2001) Proteasome-mediated glucocorticoid receptor degradation restricts transcriptional signaling by glucocorticoids. The Journal of Biological Chemistry, 276, 42714-42721.
Kinyamu, H.K. and Archer, T.K. (2007) Proteasome activity modulates chromatin modifications and RNA polymerase II phosphorylation to enhance glucocorticoid receptor-mediated transcription. Molecular and Cellular Biology, 27, 4891-4904. doi:10.1128/MCB.02162-06
Stavreva, D.A., Muller, W.G., Hager, G.L., Smith, C.L. and McNally, J.G. (2004) Rapid glucocorticoid receptor exchange at a promoter is coupled to transcription and regulated by chaperones and proteasomes. Molecular and Cellular Biology, 24, 2682-2697. doi:10.1128/MCB.24.7.2682-2697.2004
Daino, H., Matsumura, I., Takada, K., Odajima, J., Tanaka, H., Ueda, S., Shibayama, H., Ikeda, H., Hibi, M., Machii, T., Hirano, T. and Kanakura, Y. (2000) Induction of apoptosis by extracellular ubiquitin in human hematopoietic cells: Possible involvement of STAT3 degradation by proteasome pathway in interleukin 6-dependent hematopoietic cells. Blood, 95, 2577-2585.
Malek, R.L. and Halvorsen, S.W. (1999) Ciliary neurotrophic factor and phorbol ester each decrease selected STAT3 pools in neuroblastoma cells by proteasome-dependent mechanisms. Cytokine, 11, 192-199. doi:10.1006/cyto.1998.0421
Baumann, C.T., Ma, H., Wolford, R., Reyes, J.C., Maruvada, P., Lim, C., Yen, P.M., Stallcup, M.R., Hager, G.L. (2001) The glucocorticoid receptor interacting protein 1 (GRIP1) localizes in discrete nuclear foci that associate with ND10 bodies and are enriched in components of the 26S proteasome. Molecular Endocrinology, 15, 485-500. doi:10.1210/me.15.4.485
Zhang, Z., Jones, S., Hagood, J.S., Fuentes, N.L. and Fuller, G.M. (1997) STAT3 acts as a co-activator of glucocorticoid receptor signaling. The Journal of Biological Chemistry, 272, 30607-30610. doi:10.1074/jbc.272.49.30607
Hong, H., Kohli, K., Trivedi, A., Johnson, D.L. and Stallcup, M.R. (1996) GRIP1, a novel mouse protein that serves as a transcriptional co-activator in yeast for the hormone binding domains of steroid receptors. Proceedings of the National Academy of Sciences of the USA, 93, 4948-4952. doi:10.1073/pnas.93.10.4948
Hermida-Matsumoto, M.L., Chock, P.B., Curran, T. and Yang, D.C. (1996) Ubiquitinylation of transcription factors c-Jun and c-Fos using reconstituted ubiquitinylating enzymes. The Journal of Biological Chemistry, 271, 4930- 4936. doi:10.1074/jbc.271.9.4930
Stancovski, I., Gonen, H., Orian, A., Schwartz, A.L., Ciechanover, A. (1995) Degradation of the protooncogene product c-Fos by the ubiquitin proteolytic system in vivo and in vitro: Identification and characterization of the conjugating enzymes. Molecular and Cellular Biology, 15, 7106-7116.
Tsurumi, C., Ishida, N., Tamura, T., Kakizuka, A., Nishida, E., Okumura, E., Kishimoto, T., Inagaki, M., Okazaki, K., Sagata, N., Ichihara, A. and Tanaka, K. (1995) Degradation of c-Fos by the 26S proteasome is accelerated by c-Jun and multiple protein kinases. Molecular and Cellular Biology, 15, 5682-5687.
Jonat, C., Rahmsdorf, H.J., Park, K.K., Cato, A.C., Gebel, S., Ponta, H. and Herrlich, P. (1990) Antitumor promotion and antiinflammation: Down-modulation of AP-1 (Fos/Jun) activity by glucocorticoid hormone. Cell, 62, 1189-1204. doi:10.1016/0092-8674(90)90395-U
Yang-Yen, H.F., Chambard, J.C., Sun, Y.L., Smeal, T., Schmidt, T.J., Drouin, J. and Karin, M. (1990) Transcriptional interference between c-Jun and the glucocorticoid receptor: Mutual inhibition of DNA binding due to direct protein-protein interaction, Cell, 62, 1205-1215. doi:10.1016/0092-8674(90)90396-V
Schule, R., Rangarajan, P., Kliewer, S., Ransone, L.J., Bolado, J., Yang, N., Verma, I.M. and Evans, R.M. (1990) Functional antagonism between oncoprotein c-Jun and the glucocorticoid receptor, Cell, 62, 1217-1226. doi:10.1016/0092-8674(90)90397-W
Chase, B.I., Zhou Y.X., Xiang Y., Silverman R. and Zhou A. (2003) Proteasome-mediated degradation of RNase L in response to phorbol-12-myristate-13-acetate (PMA) treatment of mouse L929 cells. Journal of Interferon & Cytokine Research, 23, 565-573. doi:10.1089/107999003322485062
Badawy, A.A. (1977) The functions and regulation of tryptophan pyrrolase. Life sciences, 21, 755-768. doi:10.1016/0024-3205(77)90402-7
Dunn, A., Chenoweth, M. and Hemington, J.G. (1971) The relationship of adrenal glucocorticoids to transaminase activity and gluconeogenesis in the intact rat. Biochimica et Biophysica Acta (BBA)—General Subjects, 237, 192-202. doi:10.1016/0304-4165(71)90311-4
Uwiler, A., Wetterberg, L. and Geller, E. (1970) Alterations in induction of tyrosine aminotransferase and tryptophan oxygenase by glucose pretreatment. Biochimica et Biophysica Acta (BBA)—General Subjects, 208, 428-433. doi:10.1016/0304-4165(70)90215-1
Acharya, P., Engel, J.C. and Correia, M.A. (2009) Hepatic CYP3A suppression by high concentrations of proteasomal inhibitors: A consequence of endoplasmic reticulum (ER) stress induction, activation of RNA-dependent protein kinase-like ER-bound eukaryotic initiation factor 2alpha (eIF2alpha)-kinase (PERK) and general control nonderep-ressible-2 eIF2alpha kinase (GCN2), and global transla-tional shutoff. Molecular Pharmacology, 76, 503-515. doi:10.1124/mol.109.056002
Acharya, P., Liao, M., Engel, J.C. and Correia, M.A. (2011) Liver cytochrome P450 3A endoplasmic reticulum-associated degradation: A major role for the p97 AAA ATPase in cytochrome P450 3A extraction into the cytosol. The Journal of Biological Chemistry, 286, 3815-3828. doi:10.1074/jbc.M110.186981
Dominy Jr., J.E., Hirschberger, L.L., Coloso, R.M. and Sti-panuk, M.H. (2006) Regulation of cysteine dioxygenase degradation is mediated by intracellular cysteine levels and the ubiquitin-26S proteasome system in the living rat. Biochemical Journal, 394, 267-273. doi:10.1042/BJ20051510
Faouzi, S., Medzihradszky, K.F., Hefner, C., Maher, J.J. and Correia, M.A. (2007) Characterization of the physiological turnover of native and inactivated cytochromes P450 3A in cultured rat hepatocytes: A role for the cytosolic AAA ATPase p97? Biochemistry, 46, 7793-7803. doi:10.1021/bi700340n
Stipanuk, M.H., Hirschberger, L.L., Londono, M.P., Cresenzi, C.L. and Yu, A.F. (2004) The ubiquitin-proteasome system is responsible for cysteine-responsive regulation of cysteine dioxygenase concentration in liver. American Journal of Physiology—Endocrinology and Metabolism, 286, E439-E448. doi:10.1152/ajpendo.00336.2003
Tanaka, K., Sato, M., Tomita, Y. and Ichihara, A. (1978) Biochemical studies on liver functions in primary cultured hepatocytes of adult rats. I. Hormonal effects on cell viability and protein synthesis. The Journal of Biological Chemistry, 84, 937-946.
Gordon, G.J., Coleman, W.B. and Grisham, J.W. (2000) Temporal analysis of hepatocyte differentiation by small hepatocyte-like progenitor cells during liver regeneration in retrorsine-exposed rats. American Journal of Pathology, 157, 771-786. doi:10.1016/S0002-9440(10)64591-9
Harashima, M., Harada, K., Ito, Y., Hyuga, M., Seki, T., Ariga, T., Yamaguchi, T. and Niimi, S. (2008) Annexin A3 expression increases in hepatocytes and is regulated by hepatocyte growth factor in rat liver regeneration. The Journal of Biological Chemistry, 143, 537-545. doi:10.1093/jb/mvm248
Patrone, G., Puppo, F., Cusano, R., Scaranari, M., Cec- cherini, I., Puliti, A. and Ravazzolo, R. (2000) Nuclear run-on assay using biotin labeling, magnetic bead capture and analysis by fluorescence-based RT-PCR. Biotechniques, 29, 1012-1014, 1016-1017.
Kren, B.T. and Steer, C.J. (1996) Posttranscriptional regulation of gene expression in liver regeneration: Role of mRNA stability. The FASEB Journal, 10, 559-573.