The effect of LPS on LH release and gene expression of LH-beta, GnRH-R and TLR4 in the anterior pituitary of follicular phase ewes - an in vitro study

• Autorzy: Haziak K. , Herman A. P. , Tomaszewska-Zaremba D.
• Języki publikacji: EN

Abstrakty

EN

The study was designed to determine the in vitro effect of bacterial endotoxin – lipopolysaccharide (LPS) – on luteinizing hormone (LH) secretion from anterior pituitary (AP) explants collected from saline-treated ‘healthy’ and LPS-treated ewes in the follicular phase. In the AP explants, the expression of LH-β, gonadotropin-releasing hormone receptor (GnRH-R) and Toll-like receptor 4 (TLR4) genes was also assayed. It was found that explants incubated alone with LPS, as well as together with LPS-binding protein (LBP), abolished the stimulatory effect of GnRH on LH release. LPS added without LBP did not suppress LH-β gene expression in ‘healthy’ APs, however. Moreover, LBP intensified the inhibitory effect of LPS on gene expression in ‘healthy’ APs. These results show that LPS is a potent negative modulator of LH secretion and suggest that its direct action on the pituitary gland could be one of the mechanisms via which an immune/inflammatory challenge inhibits the reproductive process.

• Wydawca: -
• Czasopismo: Journal of Animal and Feed Sciences
• Rocznik: 2013
• Tom: 22
• Numer: 2
• Opis fizyczny: p.97-105,fig.,ref.

Twórcy

autor

Haziak K.

• The Kielanowski Institute of Animal Physiology and Nutrition, Polish Academy of Sciences, 05-110 Jablonna, Poland

autor

Herman A. P.

• The Kielanowski Institute of Animal Physiology and Nutrition, Polish Academy of Sciences, 05-110 Jablonna, Poland

autor

Tomaszewska-Zaremba D.

• The Kielanowski Institute of Animal Physiology and Nutrition, Polish Academy of Sciences, 05-110 Jablonna, Poland

Bibliografia

• Battaglia D.F., Beaver A.B., Harris T.G., Tanhehco E., Viguié C., Karsch F.J., 1999. Endotoxin disrupts the estradiol-induced luteinizing hormone surge: interference with estradiol signal reading, not surge release. Endocrinology 140, 2471−2479
• Battaglia D.F., Bowen J.M., Krasa H.B., Thrun L.A., Viguié C., Karsch F.J., 1997. Endotoxin inhibits the reproductive neuroendocrine axis while stimulating adrenal steroids: a simultaneous view from hypophyseal portal and peripheral blood. Endocrinology 138, 4273−4281
• Breen K.M., Stackpole C.A., Clarke I.J., Pytiak A.V., Tilbrook A.J., Wagenmaker E.R., Young E.A., Karsch F.J., 2004. Does the type II glucocorticoid receptor mediate cortisol-induced suppression in pituitary responsiveness to gonadotropin-releasing hormone? Neuroendocrinology 145, 2739−2746
• Breuel K.F., Kougias P., Rice P.J., Wei D., De Ponti K., Wang J., Laffan J.J., Li C., Kalbfleisch J., Williams D.L., 2004. Anterior pituitary cells express pattern recognition receptors for fungal glucans: implications for neuroendocrine immune involvement in response to fungal infections. Neuroimmunomodulation 11, 1−9
• Bilezikjian L.M., Leal A.M., Blount A.L., Corrigan A.Z., Turnbull A.V., Vale W.W., 2003. Rat anterior pituitary folliculostellate cells are targets of interleukin-1beta and a major source of intrapituitary follistatin. Endocrinology 144, 732−740
• Coleman E.S., Elsasser T.H., Kemppainen R.J., Coleman D.A., Sartin J.L., 1993. Effect of endotoxin on pituitary hormone secretion in sheep. Neuroendocrinology 58, 111−122
• Daniel J.A., Abrams M.S., deSouza L., Wagner C.G., Whitlock B.K., Sartin J.L., 2003. Endotoxin inhibition of luteinizing hormone in sheep. Domest. Anim. Endocrinol. 25, 13−19
• Dentener M.A., Vreugdenhil A.C., Hoet P.H., Vernooy J.H., Nieman F.H., Heumann D., Janssen Y.M., Buurman W.A., Wouters E.F., 2000. Production of the acute-phase protein lipopolysaccharide-binding protein by respiratory type II epithelial cells: implications for local defense to bacterial endotoxins. Amer. J. Respir. Cell Mol. Biol. 23, 146−153
• Dobson H., Ghuman S., Prabhakar S., Smith R., 2003. A conceptual model of the influence of stress on female reproduction. Reproduction 125, 15−163
• Fergani C., Saifullizam A.K., Routly J.E., Smith R.F., Dobson H., 2012. Estrous behavior, luteinizing hormone and estradiol profiles of intact ewes treated with insulin or endotoxin. Physiol. Behav. 105, 757-765
• Fox S.R., Hoefer M.T., Bartke A., Smith M.S., 1987. Suppression of pulsatile LH secretion, pituitary GnRH receptor content and pituitary responsiveness to GnRH by hyperprolactinemia in the male rat. Neuroendocrinology 46, 350-359
• Fry C.L., Gunter D.R., McMahon C.D., Steele B., Sartin J.L., 1998. Cytokine-mediated growth hormone release from cultured ovine pituitary cells. Neuroendocrinology 68, 192−200
• Gow R.M., O’Bryan M.K., Canny B.J., Ooi G.T., Hedger M.P., 2001. Differential effects of dexamethasone treatment on lipopolysaccharide-induced testicular inflammation and reproductive hormone inhibition in adult rats. J. Endocrinol. 168, 193−201
• Herman A.P., Misztal T., Romanowicz K., Tomaszewska-Zaremba D.2012. Central injection of exogenous IL-1b in the control activities of hypothalamic–pituitary–gonadal axis in anestrous ewes. Reprod. Domest. Anim. 47, 44−52
• Herman A.P., Romanowicz K., Tomaszewska-Zaremba D., 2010. Effect of LPS on the reproductive system at the level of the pituitary of anestrous ewes. Reprod. Domest. Anim. 45, 351−359
• Herman A.P., Tomaszewska-Zaremba D., 2010. Effect of endotoxin on the expression of GnRH and GnRHR genes in the hypothalamus and anterior pituitary gland of anestrous ewes. Anim. Reprod. Sci. 120, 105−111
• Igaz P., Salvi R., Rey J.-P., Glauser M., Pralong F.P., Gaillard R.C.,, 2006. Effects of cytokines on gonadotropin-releasing hormone (GnRH) gene expression in primary hypothalamic neurons and in GnRH neurons immortalized conditionally. Neuroendocrinology 147, 1037−1043
• Karsch F.J., Battaglia D.F., 2002. Mechanisms for endotoxin-induced disruption of ovarian cyclicity observations in sheep. Reproduction 59, Suppl., 101−113
• Kitchens R.L., Thompson P.A., 2005. Modulatory effects of sCD14 and LBP on LPS-host cell interactions. J. Endotoxin Res. 11, 225−229
• Knapp S., Florquin S., Golenbock D.T., van der Poll T., 2006. Pulmo- nary lipopolysaccharide (LPS)-binding protein inhibits the LPS-induced lung inflammation in vivo. J. Immunol. 176, 3189−3195
• Leon C.G., Tory R., Jia J., Sivak O., Wasan K.M., 2008. Discovery and development of Toll-like Receptor 4 (TLR4) antagonists: a new paradigm for treating sepsis and other diseases. Pharm. Res. 25, 1751−1761
• Lohrer P., Gloddek J., Nagashima A.C., Korali Z., Hopfner U., Pereda M.P., Arzt E., Stalla G.K., Renner U., 2000. Lipopolysaccharide directly stimulates the intrapituitary interleukin-6 production by folliculostellate cells via specific receptors and the p38alpha mitogen-activated protein kinase/nuclear factorkappaB pathway. Endocrinology 141, 4457−4465
• Maeda K., Tsukamura H., 2006. The impact of stress on reproduction: are glucocorticoids inhibitory or protective to gonadotropin secretion? Endocrinology 147, 1085−1086
• Mainardi G.L., Saleri R., Tomanini C., Baratta M., 2002. Effects of interleukin-1-beta, interleukin-6 and tumor necrosis factoralpha, alone or in association with hexarelin or galanin, on growth hormone gene expression and growth hormone release from pig pituitary cells. Horm. Res. 58, 180−186
• Martin T.R., Mathison J.C., Tobias P.S, Leturcq D.J., Moriarty A.M., Maunder R.J., Ulevitch R.J., 1992. Lipopolysaccharide bind- ing protein enhances the responsiveness of alveolar mac- rophages to bacterial lipopolysaccharide: implications for cytokine production in normal and injured lungs. J. Clin. Invest. 90, 2209−2219
• Meilleur M.A., Akpovi C.D., Pelletier R.M., Vitale M.L., 2007. Tumor necrosis factor-alpha-induced anterior pituitary folliculostellate TtT/GF cell uncoupling is mediated by connexin 43 dephosphorylation. Endocrinology 148, 5913−5924
• Miyake K., 2007. Innate immune sensing of pathogens and danger signals by cell surface Toll-like receptors. Semin. Immunol. 19, 3−10
• Muzio M., Bosisio D., Polentarutti N., D’amico G., Stoppacciaro A., Mancinelli R., van’t Veer C., Penton-Rol G., Ruco L.P., Allavena P., Mantovani A., 2000. Differential expression and regulation of Toll-like receptors (TLR) in human leukocytes: selective expression of TLR3 in dendritic cells. J.Immunol. 164, 5998−6004
• Nett T.M., Turzillo A.M., Baratta M., Rispoli L.A., 2002. Pituitary effects of steroid hormones on secretion of follicle-stimulating hormone and luteinizing hormone. Domest. Anim. Endocrinol. 23, 33−42
• Parnet P., Pousset F., Laye S., 2003. NFκB activation in mouse pituitary: comparison of response to interleukin-1β and lipopolysaccharide. J. Neuroendocrinol. 15, 304−314
• Pfaffl M.W., 2001. A new mathematical model for relative quantification in real-time RT–PCR. Nucl. Acids Res. 29, E45
• Pfaffl M.W., Horgan G.W., Dempfle L., 2002. Relative Expression Software Tool (REST) for group-wise comparison and statistical analysis of relative expression results in Real-Time PCR. Nucl. Acids Res. 30, E36
• Pfaffl M.W., Tichopad A., Prgomet C., Neuvians T.P., 2004. Determination of stable housekeeping genes, differentially regulated target genes and sample integrity: BestKeeperexcel-based tool using pair-wise correlations. Biotechnol. Lett. 26, 509−515
• Poltorak A., He X., Smirnova I., Liu M.Y., Van Huffel C., Du X., Birdwell D., Alejos E., Silva M., Galanos C., Freudenberg M., Ricciardi-Castagnoli P., Layton B., Beutler B., 1998. Defective LPS signaling in C3H/HeJ and C57BL/10ScCr mice: mutations in TLR4 gene. Science 282, 2085−2088
• Priego T., Granado M., Ibáñez de Cáceres I., Martín A.I., Villanúa M.A., López-Calderón A., 2003. Endotoxin at low doses stimulates pituitary GH whereas it decreases IGF-I and IGF-binding protein-3 in rats. J. Endocrinol. 179, 107−117
• Refojo D., Arias P., Moguilevsky J.A., Feleder C., 1998. Effect of bacterial endotoxin on in vivo pulsatile gonadotropin secretion in adult male rats. Neuroendocrinology 67, 275−281
• Rietschel E.T., Kirikae T., Schade F.U., Mamat U., Schmidt G., Loppnow H., Ulmer A.J., Zähringer U., Seydel U., Di Padova F., 1994. Bacterial endotoxin: molecular relationships of structure to activity and function. FASEB J. 8, 217−225
• Rispoli L.A., Nett T.M., 2005. Pituitary gonadotropin-releasing hormone (GnRH) receptor: structure, distribution and regulation of expression. Anim. Reprod. Sci. 88, 57−74
• Rivest S., Rivier C., 1995. The role of corticotropin-releasing factor and interleukin- 1 in the regulation of neurons controlling reproductive functions. Endocrine Rev.16, 177−196
• Rivier C., 2002. Inhibitory effect of neurogenic and immune stressors on testosterone secretion in rats. Neuroimmunomodulation 10, 17−29
• Stupnicki R., Madej A., 1976. Radioimmunoassay of LH in blood plasma of farm animals. Endokrinologie 68, 6−13
• Takahashi K., Sugi Y., Hosono A., Kaminogawa S., 2009. Epigenetic regulation of TLR4 gene expression in intestinal epithelial cells for the maintenance of intestinal homeostasis. J. Immunol. 183, 6522−6529
• Van Langevelde P., Kwappenberg K.M.C., Groeneveld P.H.P., Mattie H., van Dissel J.T., 1998. Antibiotic-induced lipopolysaccharide (LPS) release from Salmonella typhi: delay between killing by Ceftazidime and Imipenem and release of LPS. Antimicrob. Agents Chemother. 42, 739−743
• Wang S.C., Klein R.D, Wahl W.L., Alarcon W.H., Garg R.J., Daniel G. Remick D.G., Su G.L., 1998. Tissue coexpression of LBP and CD14 mRNA in a mouse model of sepsis. J. Surg. Res. 76, 67−73
• Watanobe H., Hayakawa Y., 2003. Hypothalamic interleukin-1β and tumor necrosis factor-α, but not interleukin-6, mediate the endotoxin-induced suppression of the reproductive axis in rats hypothalamic interleukin. Endocrinology 144, 4868−4875
• Wurfel M.M., Monks B.G., Ingalls R.R, Dedrick R.L., Delude R., Zhou D., Lamping N., Schumann R.R., Thieringer R, Fenton M.J., Wright S.D., Golenbock D., 1997. Targeted deletion of the lipopolysaccharide (LPS)-binding protein gene leads to profound suppression of LPS responses ex vivo, whereas in vivo responses remain intact. J. Exp. Med. 186, 2051−2056
• Yoo M.J., Nishihara M., Takahashi M., 1997. Tumor necrosis factor α mediates endotoxin induced suppression of gonadotropinreleasing hormone pulse generator activity in the rat. Endocr. J. 44, 141–148
• Zhang G., Ghosh S., 2002. Negative regulation of Toll-like receptormediated signaling by Tollip. J. Biol. Chem. 277, 7059−7065