Artículo

La versión final de este artículo es de uso interno. El editor solo permite incluir en el repositorio el artículo en su versión post-print. Por favor, si usted la posee enviela a
Consulte el artículo en la página del editor
Consulte la política de Acceso Abierto del editor

Abstract:

The aryl hydrocarbon receptor (AHR) mediates toxic responses to environmental contaminants and plays pivotal physiological roles in various biological processes as well, particularly in ovarian function. It is well documented that expression and function of the AHR is negatively regulated by transforming growth factor-β (TGF-β) in many cell types. In addition, several studies indicate that AHR activity inhibits TGF-β expression and function in some systems. However, the interplay between these two signals is highly dependent upon the cell type being studied, precluding a generalization about the outcome of such interaction. Therefore, the goal of the present study was to determine the effect of TGF-β on AHR expression and activation in granulosa cells, an ovarian cell type where the growth factor is mitogenic and AHR activation has been associated with promotion of proliferation as well. In addition, we conducted experiments aimed at evaluating the effect of AHR ligands on TGF-β action in our system. Results presented herein demonstrate that AHR expression is not regulated by TGF-β in rat granulosa cells, neither at the mRNA level nor at the protein level. Moreover, we find that the growth factor does not alter the transcriptional function of the AHR. Conversely, we show that activation of AHR by an agonist deregulates TGF-β function in granulosa cells, inhibiting its transcriptional activity and its mitogenic action. The described one-sided interplay between TGF-β and AHR signaling pathway may help provide a mechanistic explanation to some of the physiological outcomes of AHR or TGF-β activation in granulosa cells. © 2008 Elsevier Inc. All rights reserved.

Registro:

Documento: Artículo
Título:Interaction between the aryl hydrocarbon receptor and transforming growth factor-β signaling pathways: Evidence of an asymmetrical relationship in rat granulosa cells
Autor:Bussmann, U.A.; Barañao, J.L.
Filiación:Instituto de Biología y Medicina Experimental-CONICET, Argentina
Facultad de Ciencias Exactas y Naturales, Universidad de Buenos Aires, Argentina
Palabras clave:β-Naphthoflavone; Aryl hydrocarbon receptor; Granulosa cells; Proliferation; Transforming growth factor-β; aromatic hydrocarbon; aromatic hydrocarbon receptor; ligand; transforming growth factor beta; animal cell; animal experiment; article; cell proliferation; female; gene expression; granulosa cell; mitogenesis; nonhuman; priority journal; protein expression; protein function; protein interaction; rat; signal transduction; transcription regulation; Animals; Cells, Cultured; Female; Granulosa Cells; Rats; Rats, Sprague-Dawley; Receptors, Aryl Hydrocarbon; Sheep; Signal Transduction; Swine; Transforming Growth Factor beta
Año:2008
Volumen:76
Número:9
Página de inicio:1165
Página de fin:1174
DOI: http://dx.doi.org/10.1016/j.bcp.2008.08.019
Título revista:Biochemical Pharmacology
Título revista abreviado:Biochem. Pharmacol.
ISSN:00062952
CODEN:BCPCA
CAS:Receptors, Aryl Hydrocarbon; Transforming Growth Factor beta
Registro:https://bibliotecadigital.exactas.uba.ar/collection/paper/document/paper_00062952_v76_n9_p1165_Bussmann

Referencias:

  • Okey, A.B., An aryl hydrocarbon receptor odyssey to the shores of toxicology: the Deichmann Lecture, International Congress of Toxicology-XI (2007) Toxicol Sci, 98 (1), pp. 5-38
  • Mandal, P.K., Dioxin: a review of its environmental effects and its aryl hydrocarbon receptor biology (2005) J Comp Physiol [B], 175, pp. 221-230
  • Puga, A., Tomlinson, C.R., Xia, Y., Ah receptor signals cross-talk with multiple developmental pathways (2005) Biochem Pharmacol, 69, pp. 199-207
  • Baba, T., Mimura, J., Nakamura, N., Harada, N., Yamamoto, M., Morohashi, K., Intrinsic function of the aryl hydrocarbon (dioxin) receptor as a key factor in female reproduction (2005) Mol Cell Biol, 25, pp. 10040-10051
  • Mimura, J., Fujii-Kuriyama, Y., Functional role of AhR in the expression of toxic effects by TCDD (2003) Biochim Biophys Acta, 1619, pp. 263-268
  • Davis, B.J., Mccurdy, E.A., Miller, B.D., Lucier, G.W., Tritscher, A.M., Ovarian tumors in rats induced by chronic 2,3,7,8-tetrachlorodibenzo-p-dioxin treatment (2000) Cancer Res, 60, pp. 5414-5419
  • Pocar, P., Fischer, B., Klonisch, T., Hombach-Klonisch, S., Molecular interactions of the aryl hydrocarbon receptor and its biological and toxicological relevance for reproduction (2005) Reproduction, 129, pp. 379-389
  • Bussmann, U.A., Bussmann, L.E., Baranao, J.L., An aryl hydrocarbon receptor agonist amplifies the mitogenic actions of estradiol in granulosa cells: evidence of involvement of the cognate receptors (2006) Biol Reprod, 74, pp. 417-426
  • Ohtake, F., Takeyama, K., Matsumoto, T., Kitagawa, H., Yamamoto, Y., Nohara, K., Modulation of estrogen receptor signalling by association with the activated dioxin receptor (2003) Nature, 423, pp. 545-550
  • Harper, P.A., Riddick, D.S., Okey, A.B., Regulating the regulator: factors that control levels and activity of the aryl hydrocarbon receptor (2006) Biochem Pharmacol, 72, pp. 267-279
  • Bussmann, U.A., Barañao, J.L., Regulation of aryl hydrocarbon receptor expression in rat granulosa cells (2006) Biol Reprod, 75 (3), pp. 360-369
  • Bielefeld, K.A., Lee, C., Riddick, D.S., Regulation of aryl hydrocarbon receptor expression and function by glucocorticoids in mouse hepatoma cells (2008) Drug Metab Dispos, 36 (3), pp. 543-551
  • Chaffin, C.L., Stouffer, R.L., Duffy, D.M., Gonadotropin and steroid regulation of steroid receptor and aryl hydrocarbon receptor messenger ribonucleic acid in macaque granulosa cells during the periovulatory interval (1999) Endocrinology, 140, pp. 4753-4760
  • Chaffin, C.L., Trewin, A.L., Hutz, R.J., Estrous cycle-dependent changes in the expression of aromatic hydrocarbon receptor (AHR) and AHR-nuclear translocator (ARNT) mRNAs in the rat ovary and liver (2000) Chem Biol Interact, 124, pp. 205-216
  • Lin, S.J., Lerch, T.F., Cook, R.W., Jardetzky, T.S., Woodruff, T.K., The structural basis of TGF-β, bone morphogenetic protein, and activin ligand binding (2006) Reproduction, 132, pp. 179-190
  • Knight, P.G., Glister, C., Local roles of TGF superfamily members in the control of ovarian follicle development (2003) Anim Reprod Sci, 78, pp. 165-183
  • Knight, P.G., Glister, C., TGF-b superfamily members and ovarian follicle development (2006) Reproduction, 132, pp. 191-206
  • Kaivo-oja, N., Jeffery, L.A., Ritvos, O., Mottershead, D.G., Smad signalling in the ovary (2006) Reprod Biol Endocrinol, 4, p. 21
  • Saragüeta, P.E., Lanuza, G.M., Barañao, J.L., Autocrine role of transforming growth factor beta1 on rat granulosa cell proliferation (2002) Biol Reprod, 66 (6), pp. 1862-1868
  • Chang, X., Fan, Y., Karyala, S., Schwemberger, S., Tomlinson, C.R., Sartor, M.A., Ligand-Independent regulation of transforming growth factor-β1 expression and cell cycle progression by the aryl hydrocarbon receptor (2007) Mol Cell Biol, 27 (17), pp. 6127-6139
  • Dohr, O., Abel, J., Transforming growth-β1 coregulates mRNA expression of aryl hydrocarbon receptor and cell-cycle-regulating genes in human cancer cell lines (1997) Biochem Biophys Res Commun, 241, pp. 86-91
  • Dohr, O., Sinning, R., Vogel, C., Munzel, P., Abel, J., Effect of transforming growth factor-beta1 on expression of aryl hydrocarbon receptor and genes of Ah gene battery: clues for independent down-regulation in A549 cells (1997) Mol Pharmacol, 51, pp. 703-710
  • Bley, M.A., Saragüeta, P.E., Barañao, J.L., Concerted stimulation of rat granulosa cell deoxyribonucleic acid synthesis by sex steroids and follicle stimulating hormone (1997) J Steroid Biochem Mol Biol, 62, pp. 11-19
  • Bley, M.A., Simón, J.C., Saragüeta, P.E., Barañao, J.L., Hormonal regulation of rat granulosa cell deoxyribonucleic acid synthesis: effects of estrogens (1991) Biol Reprod, 44, pp. 880-888
  • Bley, M.A., Simón, J.C., Estévez, A.G., Jiménez de Asúa, L., Barañao, J.L., Effect of follicle-stimulating hormone on insulin-like growth factor-I-stimulated rat granulosa cell deoxyribonucleic acid synthesis (1992) Endocrinology, 131, pp. 1223-1229
  • Dasmahapatra, A.K., Wimpee, B.A., Trewin, A.L., Hutz, R.J., 2,3,7,8-Tetrachlorodibenzo-p-dioxin increases steady-state estrogen receptor-beta mRNA levels after CYP1A1 and CYP1B1 induction in rat granulosa cells in vitro (2001) Mol Cell Endocrinol, 182, pp. 39-48
  • Timsit, Y.E., Chia, F.S., Bhathena, A., Riddick, D.S., Aromatic hydrocarbon receptor expression and function in liver of hypophysectomized male rats (2002) Toxicol Appl Pharmacol, 185, pp. 136-145
  • Wrana, J.L., Attisano, L., Carcamo, J., Zentella, A., Doody, J., Laiho, M., TGF beta signals through a heteromeric protein kinase receptor complex (1992) Cell, 71, pp. 1003-1014
  • Sokal, R.R., Rohlf, F.J., (1995) Biometry, , WH Freeman and Co., New York
  • Juenguel, J.L., Bibby, A.H., Reader, K.L., Lun, S., Quirke, L.D., Haydon, L.J., The role of transforming growth factor-beta (TGF-beta) during ovarian follicular development in sheep (2004) Reprod Biol Endocrinol, 25, pp. 2-78
  • Müller, G.F., Döhr, O., El-Bahay, C., Kahl, R., Abel, J., Effect of transforming growth factor-beta1 on cytochrome P450 expression: inhibition of CYP1 mRNA and protein expression in primary rat hepatocytes (2000) Arch Toxicol, 74 (3), pp. 145-152
  • Wolff, S., Harper, P.A., Wong, J.M., Mostert, V., Wang, Y., Abel, J., Cell-specific regulation of human aryl hydrocarbon receptor expression by transforming growth factor-beta(1) (2001) Mol Pharmacol, 59 (4), pp. 716-724
  • Fujii-Kuriyama, Y., Mimura, J., Molecular mechanisms of AhR functions in the regulation of cytochrome P450 genes (2005) Biochem Biophys Res Commun, 338, pp. 311-317
  • Bernet, K.R., Domic, D., Gupta, R.K., Miller, K.P., Meachum, S., Paulose, T., The aryl hydrocarbon receptor affects mouse ovarian follicle growth via mechanisms involving estradiol regulation and responsiveness (2007) Biol Reprod, 76, pp. 1062-1070
  • McMillan, B.J., Bradfield, C.A., The Aryl hydrocarbon receptor is activated by modified low-density lipoprotein (2007) Proc Natl Acad Sci USA, 104, pp. 1412-1417
  • Song, J., Celeste, A.J., Kong, F.M., Jirtle, R.L., Rosen, V., Thies, R.S., Bone morphogenetic protein-9 binds to liver cells and stimulates proliferation (1995) Endocrinology, 136, pp. 4293-4297
  • Vaziri, C., Schneider, A., Sherr, D.H., Faller, D.V., Expression of the aryl hydrocarbon receptor is regulated by serum and mitogenic growth factors in murine 3T3 fibroblasts (1996) J Biol Chem, 271, pp. 25921-25927
  • Abdel-Razzak, Z., Corcos, L., Fautrel, A., Campion, J.P., Guillouzo, A., Transforming growth factor-β1 down-regulates basal and polycyclic aromatic hydrocarbon-induced cytochrome P450 1A1 and 1A2 in adult human hepatocytes in primary culture (1994) Mol Pharmacol, 46, pp. 1100-1110
  • Guo, J., Sartor, M., Karyala, S., Medvedovic, M., Kann, S., Puga, A., Expression of genes in the TGFbeta signaling pathway is significantly deregulated in smooth muscle cells from aorta of aryl hydrocarbon receptor knockout mice (2004) Toxicol Appl Pharmacol, 194, pp. 79-89
  • Leighton, J.K., Canning, S., Guthrie, H.D., Hammond, J.M., Expression of cytochrome P450 1A1, an estrogen hydroxylase, in ovarian granulosa cells is developmentally regulated (1995) J Steroid Biochem Mol Biol, 52, pp. 351-356
  • Dasmahapatra, A.K., Trewin, A.L., Hutz, R.J., Estrous cycle-regulated expression of CYP1B1 mRNA in the rat ovary (2002) Comp Biochem Physiol B: Biochem Mol Biol, 133, pp. 127-134
  • Deok-Soo, S., Rozman, K., 2,3,7,8-Tetrachlorodibenzo-p-dioxin (TCDD) induces plasminogen activator inhibitor-1 through an aryl hydrocarbon receptor-mediated pathway in mouse hepatoma cell lines (2002) Arch Toxicol, 76, pp. 404-413
  • Tan, Z., Huang, M., Puga, A., Xia, Y., A critical role for MAP kinases in the control of Ah receptor complex activity (2004) Toxicol Sci, 82, pp. 80-87
  • Weiss, C., Faust, D., Durk, H., Kumar Kolluri, S., Pelzer, A., Schneider, S., TCDD induces c-jun expression via a novel Ah (dioxin) receptor-mediated p38-MAPK-dependent pathway (2005) Oncogene, 24, pp. 4975-4983
  • Wenner, C.E., Yan, S., Biphasic role of TGF-β1 in signal transduction and crosstalk (2003) J Cell Physiol, 196, pp. 42-50
  • Bock, K.W., Köhle, C., Ah receptor: dioxin-mediated toxic responses as hints to deregulated physiologic functions (2006) Biochem Pharmacol, 72 (4), pp. 393-404
  • Voronov, I., Li, K., Tenenbaum, H.C., Manolson, M.F., Benzo[a]pyrene inhibits osteoclastogenesis by affecting RANKL-induced activation of NF-kappaB (2008) Biochem Pharmacol, 75 (10), pp. 2034-2044

Citas:

---------- APA ----------
Bussmann, U.A. & Barañao, J.L. (2008) . Interaction between the aryl hydrocarbon receptor and transforming growth factor-β signaling pathways: Evidence of an asymmetrical relationship in rat granulosa cells. Biochemical Pharmacology, 76(9), 1165-1174.
http://dx.doi.org/10.1016/j.bcp.2008.08.019
---------- CHICAGO ----------
Bussmann, U.A., Barañao, J.L. "Interaction between the aryl hydrocarbon receptor and transforming growth factor-β signaling pathways: Evidence of an asymmetrical relationship in rat granulosa cells" . Biochemical Pharmacology 76, no. 9 (2008) : 1165-1174.
http://dx.doi.org/10.1016/j.bcp.2008.08.019
---------- MLA ----------
Bussmann, U.A., Barañao, J.L. "Interaction between the aryl hydrocarbon receptor and transforming growth factor-β signaling pathways: Evidence of an asymmetrical relationship in rat granulosa cells" . Biochemical Pharmacology, vol. 76, no. 9, 2008, pp. 1165-1174.
http://dx.doi.org/10.1016/j.bcp.2008.08.019
---------- VANCOUVER ----------
Bussmann, U.A., Barañao, J.L. Interaction between the aryl hydrocarbon receptor and transforming growth factor-β signaling pathways: Evidence of an asymmetrical relationship in rat granulosa cells. Biochem. Pharmacol. 2008;76(9):1165-1174.
http://dx.doi.org/10.1016/j.bcp.2008.08.019