Projections to the Preoptic Area from the Paraventricular Nucleus, Arcuate Nucleus and the Bed Nucleus of the Stria Terminalis Are Unlikely to Be Involved in Stress-Induced Suppression of GnRH Secretion in SheepRivalland E.T.A. · Tilbrook A.J. · Turner A.I. · Iqbal J. · Pompolo S. · Clarke I.J.
Department of Physiology, Monash University, Melbourne, Vic., Australia
Do you have an account?
- Rent for 48h to view
- Buy Cloud Access for unlimited viewing via different devices
- Synchronizing in the ReadCube Cloud
- Printing and saving restrictions apply
Rental: USD 8.50
Cloud: USD 20.00
Stress compromises reproductive function and the major physiological system activated during stress is the hypothalamo-pituitary-adrenal axis. Corticotrophin-releasing hormone and arginine vasopressin (AVP), which are produced in neurones of the paraventricular nucleus (PVN), drive the hypothalamo-pituitary-adrenal axis and are also implicated in the suppression of the reproductive axis. We used retrograde tracing and Fos labelling to map the projections from the PVN to the preoptic area (POA) where most gonadotrophin releasing hormone (GnRH) neurones are found. Fluorogold (FG) injections were made into the POA of gonadectomised male and female sheep (n = 5/sex), the animals were stressed and the brains recovered for histochemistry. All animals responded to stress with an increase in the number of Fos-labelled nuclei in the PVN. Few retrogradely labelled cells of the PVN were activated by stress. Dual labelling showed that very few FG-labelled cells also stained for corticotrophin-releasing hormone, none for AVP or enkephalin. Dual labelling for FG and Fos in the bed nucleus of the stria terminalis (BNST) and the arcuate nucleus showed that no FG-labelled cells in the BNST and only few in the ARC were activated by stress. No sex differences were observed in the activation of FG-labelled cells in any of the nuclei examined. We conclude that, although cells of the PVN, BNST and/or arcuate nucleus may affect reproduction via the GnRH cells of the POA, this is unlikely to involve direct input to the POA. If cells of these regions are involved in GnRH suppression during stress, this may occur via interneuronal pathways.
© 2006 S. Karger AG, Basel
- Battaglia DF, Bowen J, Krasa H, Thrun L, Viguie C, Karsch FJ: Endotoxin inhibits the reproductive neuroendocrine axis while stimulating adrenal steroids: a simultaneous view from the hypophyseal portal and peripheral blood. Endocrinology 1997;138:4273–4281.
- Rivest S, Rivier C: The role of corticotropin-releasing factor and interleukin-1 in the regulation of neurons controlling reproductive functions. Endocr Rev 1995;16:177–199.
- Tilbrook AJ, Turner AI, Clarke IJ: Effects of stress on reproduction in non-rodent mammals: the role of glucocorticoids and sex differences. Rev Reprod 2000;5:105–113.
- Itoi K, Helmreich DL, Lopez-Figueroa M, Watson S: Differential regulation of corticotropin-releasing hormone and vasopressin gene transcription in the hypothalamus by norepinephrine. J Neurosci 1999;19:5464–5472.
- Whitnall MH: Regulation of the hypothalamic corticotropin-releasing hormone neurosecretory system. Prog Neurobiol 1993;40:573–629.
- Paull WK, Scholer J, Arimura A, Meyers CA, Chang JK, Chang D, Shimizu M: Immunocytochemical localization of CRF in the ovine hypothalamus. Peptides 1982;3:183–191.
- Hallbeck M, Hermanson O, Blomqvist A: Distribution of preprovasopressin mRNA in the rat central nervous system. J Comp Neurol 1999;411:181–200.
- Mathews S, Parrott RF, Sirinathsinghji D: Distribution and cellular localization of vasopressin mRNA in the ovine brain, pituitary and pineal glands. Neuropeptides 1993;25:11–17.
- Rivier C, Vale W: Influence of corticotropin-releasing factor on reproductive functions in the rat. Endocrinology 1984;114:914–921.
- Petraglia F, Sutton S, Vale W, Plotsky P: Corticotropin-releasing factor decreases plasma luteinising hormone levels in female rats by inhibiting gonadotropin-releasing hormone release into hypophysial-portal circulation. Endocrinology 1987;120:1083–1088.
- Heisler LE, Tumber AJ, Reid RL, Van Vugt DA: Vasopressin mediates hypoglycemia-induced inhibition of luteinizing hormone secretion in the ovariectomized rhesus monkey. Neuroendocrinology 1994;60:297–304.
- MacLusky NJ, Naftolin F, Leranth C: Immunocytochemical evidence for direct synaptic connections between corticotropin-releasing factor (CRF) and gonadotrophin-releasing hormone (GnRH)-containing neurons is the preoptic area of the rat. Brain Res 1988;439:391–395.
- Thind KK, Boggan JE, Goldsmith PC: Interactions between vasopressin- and gonadotropin-releasing-hormone-containing neuroendocrine neurons in the monkey supraoptic nucleus. Neuroendocrinology 1991;53:287–297.
- Merchenthaler I: Enkephalin-immunoreactive neurons in the parvicellular subdivisions of the paraventricular nucleus project to the external zone of the median eminence. J Comp Neurol 1992;326:112–120.
- Harlan R, Shivers B, Romano G, Howells R, Pfaff D: Localization of preproenkephalin mRNA in the rat brain and spinal cord by in situhybridization. J Comp Neurol 1987;258:159–184.
- Mathews S, Heavens R, Sirinathsinghji D: Distribution and cellular localization of preproenkephalin mRNA in the ovine brain and the pituitary. Brain Res Mol Brain Res 1992;12:349–353.
- Drouva S, Epelbaum J, Tapia-Arancibia L, Laplante E, Kordon C: Opiate receptors modulate LHRH and SIRF release from mediobasal hypothalamic neurons. Neuroendocrinology 1981;32:163–167.
- Slama A, Burg-Poveda D, Tramu G: Colocalized peptides in gonadotrophs: LeuEnkephalin and ACTH interact differently on GnRH-induced LH and FSH release. Neuropeptides 1990;16:135–140.
- Ferris CF, Pan JX, Singer EA, Boyd ND, Carraway RE, Leeman SE: Stimulation of luteinizing hormone release after stereotaxic microinjection of neurotensin into the medial preoptic area of rats. Neuroendocrinology 1984;38:145–151.
- Bruni JF, Van Vugt D, Marshall S, Meites J: Effects of naloxone, morphine and methionine enkephalin on serum prolactin, luteinizing hormone, follicle-stimulating hormone, thyroid-stimulating hormone and growth hormone. Life Sci 1977;21:461–466.
- Tilbrook AJ, Canny BJ, Serapiglia MD, Ambrose TJ, Clarke IJ: Suppression of the secretion of luteinizing hormone due to isolation/restraint stress in gonadectomized rams and ewes is influenced by sex steroids. J Endocrinol 1999;160:469–481.
- Clarke IJ, Cummins JT: The temporal relationship between gonadotropin-releasing hormone (GnRH) and luteinizing hormone (LH) in ovariectomized ewes. Endocrinology 1982;111:1737–1739.
- Debus N, Breen KM, Barrell GK, Billings HJ, Brown M, Young EA, Karsch FJ: Does cortisol mediate endotoxin-induced inhibition of pulsatile luteinizing hormone and gonadotropin-releasing hormone secretion? Endocrinology 2002;143:3748–3758.
- Breen KM, Karsch FJ: Does cortisol inhibit pulsatile luteinizing hormone secretion at the hypothalamic or pituitary level? Endocrinology 2004;145:692–698.
- Rivest S, Rivier C: Influence of the paraventricular nucleus of the hypothalamus in the alteration of neuroendocrine functions induced by intermittent footshock or interleukin. Endocrinology 1991;129:2049–2057.
- Makino S, Smith M, Gold P: Increased expression of corticotropin-releasing hormone and vasopressin messenger ribonucleic acid (mRNA) in the hypothalamic paraventricular nucleus during repeated stress: association with reduction in glucocorticoid receptor mRNA levels. Endocrinology 1995;136:3299–3309.
- Forray MI, Gysling K: Role of noradrenergic projections to the bed nucleus of the stria terminalis in the regulation of the hypothalamic-pituitary-adrenal axis. Brain Res Brain Res Rev 2004;47:145–160.
- Burow A, Day HEW, Campeau S: A detailed characterization of loud noise stress: intensity analysis of hypothalamo-pituitary-adrenocortical axis and brain activation. Brain Res 2005;1062:63–73.
- Spencer SJ, Buller KM, Day TA: Medial prefrontal cortex control of the paraventricular hypothalamic nucleus response to psychological stress: possible role of the bed nucleus of the stria terminalis. J Comp Neurol 2005;481:363–376.
- Reyes TM, Walker JR, DeCino C, Hogenesch JB, Sawchenko PE: Categorically distinct acute stressors elicit dissimilar transcriptional profiles in the paraventricular nucleus of the hypothalamus. J Neurosci 2003;23:5607–5616.
- McDougall SJ, Widdop RE, Lawrence AJ: Differential gene expression in WKY and SHR brain following acute and chronic air-puff stress. Brain Res Mol Brain Res 2005;133:329–336.
- Sergeyev V, Fetissov S, Mathe AA, Jimenez PA, Bartfai T, Mortas P, Gaudet L, Moreau JL, Hokfelt T: Neuropeptide expression in rats exposed to chronic mild stresses. Psychopharmacology 2005;178:115–124.
- Pompolo S, Rawson JA, Clarke I: Projections from the arcuate/ventromedial region of the hypothalamus to the preoptic area and bed nucleus of the stria terminalis in the brain of the ewe; lack of direct input to gonadotropin-releasing hormone neurons. Brain Res 2001;904:1–2.
- Scott CJ, Clarke LJ, Tilbrook AJ: Neuronal inputs from the hypothalamus and brain stem to the medial preoptic area of the ram: neurochemical correlates and comparison to the ewe. Biol Reprod 2003;68:1119–1133.
- Pompolo S, Ischenko O, Pereira A, Iqbal J, Clarke IJ: Evidence that projections from the bed nucleus of the stria terminalis and from the lateral and medial regions of the preoptic area provide input to gonadotropin-releasing hormone (GNRH) neurons in the female sheep brain. Neuroscience 2005;132:421–436.
- Sawchenko PE, Swanson LW: The organization of forebrain afferents to the paraventricular and supraoptic nuclei of the rat. J Comp Neurol 1983;218:121–144.
- Cullinan WE, Herman JP, Watson SJ: Ventral subicular interaction with the hypothalamic paraventricular nucleus: evidence for a relay in the bed nucleus of the stria terminalis. J Comp Neurol 1993;332:1–20.
- Maejima Y, Aoyama M, Abe A, Sugita S: Induced expression of c-fos in the diencephalon and pituitary gland of goats following transportation. J Anim Sci 2005;83:1845–1853.
- Tilbrook AJ, Turner AI, Clarke IJ: Stress and Reproduction: central mechanisms and sex differences in non-rodent species. Stress 2002;5:83–100.
- Broadbear JH, Pierce BN, Clarke IJ, Canny BJ: Role of sex and sex steroids in mediating pituitary-adrenal responses to acute buspirone treatment in sheep. J Neuroendocrinol 2005;17:804–810.
- Rivalland ET, Iqbal J, Clarke IJ, Turner AI, Tilbrook AJ: Co-localization and distribution of corticotrophin-releasing hormone, arginine vasopressin and enkephalin in the paraventricular nucleus of sheep: a sex comparison. Neuroscience 2005;132:755–766.
Bremner WJ, Cumming IA, Winfield CG, de Kretser DM, Galloway DB: A study of the reproductive performance of mature Romney and Merino rams throughout the year; in Lindsay DR, Pearce DT (eds): Reproduction in Sheep. Canberra, Australian Academy of Science and Australian Wool Corporation, 1984, pp 16–17.
- Scott CJ, Cummins JT, Clarke IJ: Effects on plasma luteinising hormone levels of microinjection of noradenaline and adrenaline into the septo-preoptic area of the brain of the ovariectomized ewe: changes with season and chronic oestrogen treatment. J Neuroendocrinol 1992;4:131–141.
- Scott CJ, Kuehl DE, Ferreira SA, Jackson GL: Hypothalamic sites of action for testosterone, dihydrotestosterone, and estrogen in the regulation of luteinizing hormone secretion in male sheep. Endocrinology 1997;138:3686–3694.
- Walsh JP, Rao A, Simmons DM, Clarke IJ: Proopiomelanocortin mRNA levels in ovine hypothalamus are not reduced at the time of the preovulatory luteinising hormone surge. J Neuroendocrinol 1998;10:803–808.
- Iqbal J, Pompolo S, Considine RV, Clarke IJ: Localization of leptin receptor-like immunoreactivity in the corticotropes, somatotropes, and gonadotropes in the ovine anterior pituitary. Endocrinology 2000;141:1515–1520.
- De Martino C, Zamboni L: Silver methenamine stain for electron microscopy. J Ultrastruct Res 1967;19:273–282.
- Iqbal J, Pompolo S, Sakurai T, Clarke IJ: Evidence that orexin-containing neurones provide direct input to gonadotropin-releasing hormone neurones in the ovine hypothalamus. J Neuroendocrinol 2001;13:1033–1041.
- Simmons D, Ariza J, Swanson LW: A complete protocol for in situ hybridisation of messenger RNAa in brain and other tissues with radio-labeled single-stranded RNA probes. J Histotechnol 1989;12:169–181.
- Clarke IJ, Pompolo S, Scott CJ, Rawson JA, Caddy D, Jakubowska AE, Pereira AM: Cells of the arcuate nucleus and ventromedial nucleus of the ovariectomized ewe that respond to oestrogen: a study using fos immunohistochemistry. J Neuroendocrinol 2001;13:934–941.
- Scott CJ, Rawson JA, Pereira AM, Clarke IJ: Oestrogen receptors in the brainstem of the female sheep: relationship to noradrenergic cells and cells projecting to the medial preoptic area. J Neuroendocrinol 1999;11:745–755.
- Romijn HJ, van Uum JF, Breedijk I, Emmering J, Radu I, Pool CW: Double immunolabeling of neuropeptides in the human hypothalamus as analyzed by confocal laser scanning fluorescence microscopy. J Histochem Cytochem 1999;47:229–236.
Bocking AD, McMillen IC, Harding R, Thorbun GD: Effect of reduced uterine blood flow on fetal and maternal cortisol. J Develop Physiol 1986;8:237–245.
- Swanson LW, Sawchenko PE: Hypothalamic integration: organization of the paraventricular and supraoptic nuclei. Annu Rev Neurosci 1983;6:269–324.
- Dudas B, Merchenthaler I: Close juxtapositions between luteinizing hormone-releasing-hormone-immunoreactive neurons and corticotropin-releasing-factor-immunoreactive axons in the human diencephalon. J Clin Endocrinol Metab 2002;87:5778–5784.
- Gambacciani M, Yen SSC, Rasmussen DD: GnRH release from the mediobasal hypothalamus:in vitro inhibition by corticotropin-releasing factor. Neuroendocrinology 1986;43:533–536.
- Nikolarakis KE, Almeida OFX, Herz A: Corticotropin-releasing factor (CRF) inhibits gonadotropin-releasing hormone (GnRH) release from superfused rat hypothalami in vitro. Brain Res 1986;377:388–390.
- Rivest S, Plotsky PM, Rivier C: CRF alters the infundibular LHRH secretory system from the medial preoptic area of female rats: possible involvement of opioid receptors. Neuroendocrinology 1993;57:236–246.
- Mathews S, Heavens R, Sirinathsinghji D: Cellular localisation of corticotropin-releasing factor mRNA in the ovine brain. Brain Res Mol Brain Res 1991;11:171–176.
- Broad K, Keverne E, Kendrick K: Corticotropin-releasing factor mRNA in the sheep brain during pregnancy, parturition and lactation and following exogneous progesterone and estrogen treatment. Brain Res Mol Brain Res 1995;29:310–316.
- Handa RJ, Burgess LH, Kerr JE, O’Keefe JA: Gonadal steroid hormone receptors and sex differences in the hypothalamo-pituitary-adrenal axis. Horm Behav 1994;28:464–476.
- Handa RJ, Nunley K, Lorens S, Louie J, McGivern R: Androgen regulation of adrenocorticotropin and corticosterone secretion in the male rat following novelty and footshock stressors. Physiol Behav 1994;55:117–124.
- Turner AI, Canny BJ, Hobbs RJ, Bond J, Clarke I: Influence of sex and gonadal status of sheep on cortisol secretion in response to ACTH and on cortisol and LH secretion in response to stress: importance of different stressors. J Endocrinol 2002;173:113–122.
Article / Publication Details
Copyright / Drug Dosage / DisclaimerCopyright: All rights reserved. No part of this publication may be translated into other languages, reproduced or utilized in any form or by any means, electronic or mechanical, including photocopying, recording, microcopying, or by any information storage and retrieval system, without permission in writing from the publisher.
Drug Dosage: The authors and the publisher have exerted every effort to ensure that drug selection and dosage set forth in this text are in accord with current recommendations and practice at the time of publication. However, in view of ongoing research, changes in government regulations, and the constant flow of information relating to drug therapy and drug reactions, the reader is urged to check the package insert for each drug for any changes in indications and dosage and for added warnings and precautions. This is particularly important when the recommended agent is a new and/or infrequently employed drug.
Disclaimer: The statements, opinions and data contained in this publication are solely those of the individual authors and contributors and not of the publishers and the editor(s). The appearance of advertisements or/and product references in the publication is not a warranty, endorsement, or approval of the products or services advertised or of their effectiveness, quality or safety. The publisher and the editor(s) disclaim responsibility for any injury to persons or property resulting from any ideas, methods, instructions or products referred to in the content or advertisements.