High expression of bovine alpha glutathione S-transferase (GSTA1, GSTA2) subunits is mainly associated with steroidogenically active cells and regulated by gonadotropins in bovine ovarian follicles.
[en] We have previously shown that a major group of 28-30 kDa proteins decreases after the LH surge in bovine granulosa cells (GC). In the present study, we have characterized two proteins in this group in search of factors that may intervene in folliculogenesis and oocyte maturation. Polyclonal antibodies raised against 28 kDa or 29 kDa bovine GC proteins were used to screen a complementary DNA (cDNA) expression library. This resulted in the characterization of two isoenzyme subunits for alpha class glutathione S-transferase, named bGSTA1 and bGSTA2. Both bGSTA1 (25.4 kDa, pI 8.9; 791 bp cDNA; GenBank Accession No. BTU49179) and bGSTA2 (25.6 kDa, pI 7.2; 959 bp cDNA; GenBank Accession No. AF027386) have 222 amino acids. The deduced amino acid sequences were compared and showed 82% (bGSTA1) and 74% (bGSTA2) identity to human GSTA1, whereas bGSTA1 and bGSTA2 are 81% identical to each other. The bGSTA2 represents a novel GSTA subunit because it harbors a specific 16 amino acid sequence not found in any other species and GST classes. Northern blots showed that bGSTA1 and bGSTA2 are coexpressed and are tissue specific with single transcripts of 1.2 kb and 1.4 kb, respectively for bGSTA1 and bGSTA2. The messenger RNA (mRNA) were detected in GC, corpus luteum, adrenal gland, testis, liver, lung, thyroid, kidney and cotyledon, and the relative abundance of their mRNA varied. Ratios of bGSTA1/bGSTA2 mRNA vary between tisssues, indicating that expression of these genes is controlled differently. Immunohistochemistry observations revealed that expression of GSTA is cell specific, being associated with GC and theca cells, small luteal cells, Leydig cells, hepatocytes, adrenal cortex, specific chromaffin cells in the adrenal medulla, renal proximal convoluted tubular cells, and Clara cells in the bronchioles. Studies in vivo showed that levels of mRNA for bGSTA1 were elevated in follicular wall of preovulatory follicles before hCG treatment, but decreased by 77% 12 h after hCG injection. However, in FSH stimulated preovulatory follicles, the decrease in mRNA for both GSTAs was only 21% at 24 h following hCG injection. We concluded that bGSTA1 and bGSTA2 expression is tissue- and cell-specific, is associated with steroidogenically active cells, and is hormonally regulated by gonadotropins in the bovine ovarian follicle.
Disciplines :
Veterinary medicine & animal health
Author, co-author :
Rabahi, Flora; Centre de recherche en reproduction animale, Faculté de médecine vétérinaire, Université de Montréal, St-Hyacinthe, Québec, Canada
Brûlé, Sophie; Centre de Recherche en Reproduction Animale, Faculté de Médecine Vétérinaire, Université de Montréal, St-Hyacinthe, Que. J2S 7C6, Canada
Sirois, Jean; Centre de Recherche en Reproduction Animale, Faculté de Médecine Vétérinaire, Université de Montréal, St-Hyacinthe, Que. J2S 7C6, Canada
Beckers, Jean-François ; Université de Liège - ULiège > Département des sciences fonctionnelles (DSF) > Physiologie de la reproduction
Silversides, David W.; Centre de Recherche en Reproduction Animale, Faculté de Médecine Vétérinaire, Université de Montréal, St-Hyacinthe, Que. J2S 7C6, Canada
Lussier, Jacques G.; Centre de Recherche en Reproduction Animale, Faculté de Médecine Vétérinaire, Université de Montréal, St-Hyacinthe, Que. J2S 7C6, Canada ; Centre de Recherche en Reproduction Animale, Faculté de Médecine Vétérinaire, Université de Montréal, St-Hyacinthe, Que. J2S 7C6, Canada
Language :
English
Title :
High expression of bovine alpha glutathione S-transferase (GSTA1, GSTA2) subunits is mainly associated with steroidogenically active cells and regulated by gonadotropins in bovine ovarian follicles.
Salustri A., Hascall V.C., Camaioni A., Yanagishita M. (1993) Oocyte-granulosa cell interactions., Adashi EY, Leung PPK (eds) The Ovary. Raven Press, New York; 209-225.
Wassarman P.M., Albertini D.F. (1994) The mammalian ovum., Knobil E, Neill JD (eds) The Physiology of Reproduction. Raven Press, New York; 1:79-122.
Eppig J.J. (1996) Mammalian oocyte growth and development in vitro. Mol Reprod Dev 44:260-273.
Rabahi F., Monniaux D., Pisselet C., Chupin D., Durand P. (1991) Qualitative and quantitative changes in protein synthesis of bovine follicular cells during the preovulatory period. Mol Reprod Dev 30:265-274.
Mannervik B., Awasthi Y.C., Board P.G., Hayes J.D., Di Ilio C., Ketterer B., Listowsky I., Morgenstern R., Muramatsu M., Pearson W.R., Pickett C.B., Sato K., Widersten M., Wolf C.R. (1992) Nomenclature for human glutathione transferases. Biochem J 282:305-308.
Hayes J.D., Strange R.C. (1995) Potential contribution of the glutathione S-transferase supergene family to resistance to oxidative stress. Free Radic Res 22:193-207.
Board P.G., Johnston P.N., Ross V.L., Webb G.C., Coggan M., Suzki T. (1991) Molecular genetics of the human glutathione S-transferase., Ernster L (ed) Xenobiotics and Cancer. 21st Symposia Princess Takamatsu. Japan Sci Soc Press, Tokyo/Tatlor and Francis Ltd., London; 199-211.
Hayes J.D., Pulford D.J. (1995) The glutathione S-transferase supergene family: Regulation of GST and the contribution of the isoenzymes to cancer chemo-protection and drug resistance. Crit Rev Biochem Mol Biol 30:445-600.
Laemmli U.K. (1970) Cleavage of structural proteins during the assembly of the head of bacteriophage T4. Nature 227:680-685.
Towbin H., Staehelin T., Gordon J. (1979) Electrophoretic transfer of proteins from polyacrylamide gels to nitrocellulose sheets: Procedure and some applications. Proc Natl Acad Sci USA 76:4350-4354.
Knudsen K.A. (1985) Proteins transferred to nitrocellulose for use as immunogens. Anal Biochem 147:285-288.
Harlow E., Lane D., Antibodies. A Laboratory Manual. ColdSpring Harbor Laboratory Press, New York; 1988.
Houde A., Lambert A., Saumande J., Silversides D.W., Lussier J.G. (1994) Structure of the bovine follicle-stimulating hormone receptor complementary DNA and expression in bovine tissues. Mol Reprod Dev 39:127-135.
Bairoch A., Bucher P., Hofmann K. (1996) The PROSITE database, its status in 1995. Nucleic Acids Res 24:189-196.
Levine R.A., Serdy M., Guo L., Holzschu D. (1993) Elongation factor TU as a control gene for mKNA analysis of lung development and other differentiation and growth regulated systems. Nucleic Acids Res 21:4426.
Sirois J. (1994) Induction of prostaglandin endoperoxide synthetase-2 by human chorionic gonadotropin in bovine preovulatory follicles in vivo. Endocrinology 135:841-848.
Liu J., Sirois J. (1998) Follicle size-dependent induction of prostaglandin G/H synthase-2 during superovulation in cattle. Biol Reprod 58:1527-1532.
Sevigny J., Levesque F.P., Grondin G., Beaudoin A.R. (1997) Purification of the blood vessel ATP diphosphohydrolase, identification and localisation by immunological techniques. Biochim Biophys Acta 1334:73-78.
Tu C.P., Qian B. (1986) Human liver glutathione S-transferases: Complete primary sequence of an Ha subunit cDNA. Biochem Biophys Res Commun 141:229-237.
Tosser-Klopp G., Benne F., Bonnet A., Mulsant P., Gasser F., Hatey F. (1997) A first catalog of genes involved in pig ovarian follicular differentiation. Mamm Genome 8:250-254.
Stenberg G., Board P.G., Calberg I., Mannervik B. (1991) Effects of directed mutagenesis on conserved arginine residues in a human class alpha glutathione transferase. Biochem J 274:549-555.
Sinning I., Kleywegt G.J., Cowan S.W., Reinemer P., Dirr H.W., Huber R., Gilliland G.L., Armstrong R.N., Ji X., Board P.G., Olin B., Mannervik B., Jones T.A. (1993) Structure determination and refinement of human alpha class glutathione transferase A1-1, and a comparison with the Mu and Pi class enzymes. J Mol Biol 232:192-212.
Atkins W.M., Wang R.W., Bird A.W., Newton D.J., Lu A.Y. (1993) The catalytic mechanism of glutathione S-transferase (GST). Spectroscopic determination of the pKa of Tyr-9 in rat α 1-1 GST. J Biol Chem 268:19188-19191.
Cameron A.D., Sinning I., L'Hermite G., Olin B., Board P.G., Mannervik B., Jones T.A. (1995) Structural analysis of human α-class glutathione transferase A1-1 in the apo-form and in complexes with ethacrynic acid and its glutathione conjugate. Structure 3:717-727.
Bjornestedt R., Stenberg G., Widersten M., Board P.G., Sinning I., Jones T.A., Mannervik B. (1995) Functional significance of arginine 15 in the active site of human class a glutathione transferase A1-1. J Mol Biol 247:765-773.
Hayes J.D., Milner S.W., Walker S.W. (1989) Expression of glyoxalase, glutathione peroxidase and glutathione S-transferase isoenzymes in different bovine tissues. Biochim Biophys Acta 994:21-29.
Meikle I., Hayes J.D., Walker S.W. (1992) Expression of an abundant α-class glutathione S-transferase in bovine and human adrenal cortex tissues. J Endocrinol 132:83-92.
Bogaards J.J., Van Ommen B., Van Bladeren P.J. (1992) Purification and characterization of eight glutathione S-transferase isoenzymes of hamster. Comparison of subunit composition of enzymes from liver, kidney, testis, pancreas and trachea. Biochem J 286:383-388.
Alin P., Danielson U.H., Mannervik D. (1985) 4-Hydroxy-2-enals are substrates for glutathione transferase. FEBS Lett 179:267-270.
Poli G., Dianzani M.U., Cheeseman K.H., Slater T.F., Lang J., Esterbauer H. (1985) Separation and characterization of the aldehydic products of lipid peroxidation stimulated by carbon tetrachloride or ADP-iron isolated hepatocytes and rat liver microsomal suspensions. Biochem J 227:629-638.
Kaur K., Salomon R.G., O'Neil J., Hoff H.F. (1997) (Carboxyalkyl) pyrroles in human plasma and oxidized low-density lipoproteins. Chem Res Toxicol 10:1387-1396.
McNatty K.P., Heath D.A., Lundy T., Fidler A.E., Quirke L.D., Stent V.C., O'Connell A., Smith P.R., Groome N., Tisdall D.J. Control of early ovarian follicular development. J Reprod Fertil Suppl, in press; .
Keira M., Nishihira J., Ishibahi T., Tanaka T., Fujimoto S. (1994) Identification of a molecular species in porcine ovarian luteal glutathione S-transferase and its hormonal regulation by pituitary gonadotropins. Arch Biochem Biophys 308:126-132.
Rahilly M., Carder P.J., Al Nafussi A., Harrison D.J. (1991) Distribution of glutathione S-transferase isoenzymes in human ovary. J Reprod Fertil 93:303-311.
Fortune J.E., Hansel W. (1985) Concentrations of steroids and gonadotropins in follicular fluid from normal heifers and heifers primed for superovulation. Biol Reprod 32:1069-1079.
Toft E., Becedas L., Soderstrom M., Lundqvist A., Depierre J.W. (1997) Glutathione transferase isoenzyme patterns in the rat ovary. Chem-Biol Interact 108:79-93.
Alila H.W., Dowd J.P., Corradino R.A., Harris W.V., Hansel W. (1988) Control of progesterone production in small and large bovine luteal cells separated by flow cytometry. J Reprod Fertil 82:645-655.
Sundberg A.G.M., Nilsson R., Appelkvist E.-L., Dallner G. (1993) Immunohistochemical localization of α and p class glutathione transferases in normal human tissues. Pharmacol Toxicol 72:321-331.
Mankowitz L., DePierre J.W., Mannervik B., Hansson H.-A. (1991) Immunohistochemical distribution of isoenzymes of glutathione transferase in adult rat adrenal gland before and after hypophysectomy. Biochem J 280:399-405.
Aceto A., Sacchetta P., Dragani B., Bucciarelli T., Angelucci S., Longo V., Gervasi G.P., Martini F., Carmine D.I. (1993) Glutathione transferase isoenzymes in olfactory and respiratory epithelium of cattle. Biochem Pharmacol 46:2127-2133.
Anttila S., Hirvonen A., Vaino H., Husgafvel-Pursiainen K., Hayes J.D., Ketterer B. (1993) Immunohistochemical localization of glutathione S-transferase in human lung. Cancer Res 53:5643-5648.
Wilson J.D., Foster D.W., Kronengerg H.M., Larsen P.R., Williams Textbook of Endocrinology, ed 9. WB Saunders Co, Philadelphia; 1998.
Honkakoski P., Maenpaa J., Leikola J., Pasanen M., Juvonen R., Lang M.A., Pelkonen O., Raunio H. (1993) Cytochrome P450 2A-mediated coumarin 7-hydroxylation and testosterone hydroxylation in mouse and rat lung. Pharmacol Toxicol 72.
Waxman D.J., Lapenson D.P., Aoyama T., Gelboin H.V., Gonzalez F.J., Korzekwa K. (1991) Steroid hormone hydroxylase specificities of eleven cDNA-expressed human cytochrome P450s. Arch Biochem Biophys 290:160-166.
Ji C.M., Cardoso W.V., Gebremichael A., Philpot R.M., Buckpitt A.R., Plopper C.G., Pinkerton K.E. (1995) Pulmonary cytochrome P-450 monooxygenase system and Clara cell differentiation in rats. Am J Physiol 269.
Rapoport R., Sklan D., Hanukoglu I. (1995) Electron leakage from the adrenal cortex mitochondrial P450scc and P450c11 systems: NADPH and steroid dependence. Arch Biochem Biophys 317:412-416.
