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Published in: Endocrine 3/2014

01-12-2014 | Original Article

The cholinergic system of the preoptic-anterior hypothalamic areas regulates the ovarian follicular population in an asymmetric way

Authors: María Esther Cruz, Angélica Flores, Roberto Domínguez

Published in: Endocrine | Issue 3/2014

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Abstract

Atropine implants in the preoptic-anterior hypothalamic areas (POA-AHA) block ovulation. The blocking effects depend on the side of POA-AHA and the day of the estrous cycle in which the implants are inserted. Since ovulation is the result of the growth and differentiation of ovarian follicles, the purpose of this study was to analyze the changes in follicular and atresia population in the ovaries of non-ovulating rats resulting from the unilateral atropine implants in the POA-AHA. Groups of cyclic rats were implanted with atropine or cholesterol (sham treatment group) in the left (diestrus-1, diestrus-2) or the right side (estrus, diestrus-1) of the POA-AHA. The animals were sacrificed on the expected proestrus or estrus day, and the follicular population was counted and the follicles measured in both ovaries. Atropine implants inserted in the left POA-AHA on diestrus-2 resulted in lower follicular growth and atresia in the ipsilateral ovary (left one). No apparent effects were observed in the right ovary. Atropine implants inserted in the right POA-AHA on estrus day resulted in fewer numbers of small follicles in the ipsilateral ovary (right) and a greater number of pre-ovulatory ones. Present results suggest that acetylcholine, via muscarinic receptors of the POA-AHA, regulates ovarian follicular fate in an asymmetric way, and that its actions fluctuate during the estrous cycle. In addition, each ovary seems to respond differently to the POA-AHA’s muscarinic signal surge on estrus and diestrus-2 days.
Literature
1.
go back to reference A. Rajkovic, S.A. Pangas, M.M. Matzuk, Follicular development: mouse, sheep, and human models, in Knobil and Neill´s Physiology of Reproduction, ed. by J.D. Neill (Elsevier Press, St. Louis, 2006), pp. 383–424CrossRef A. Rajkovic, S.A. Pangas, M.M. Matzuk, Follicular development: mouse, sheep, and human models, in Knobil and Neill´s Physiology of Reproduction, ed. by J.D. Neill (Elsevier Press, St. Louis, 2006), pp. 383–424CrossRef
2.
go back to reference A.E. Herbison, Physiology of the gonadotropin-releasing hormone neuronal network, in Knobil and Neill´s Physiology of Reproduction, ed. by J.D. Neill (Elsevier Press, St. Louis, 2006), pp. 1415–1482CrossRef A.E. Herbison, Physiology of the gonadotropin-releasing hormone neuronal network, in Knobil and Neill´s Physiology of Reproduction, ed. by J.D. Neill (Elsevier Press, St. Louis, 2006), pp. 1415–1482CrossRef
3.
go back to reference G.F. Turi, Z. Liposits, E. Hrabovszky, Cholinergic afferents to gonadotropin-releasing hormone neurons of the rat. Neurochem. Int. 52, 723–728 (2008)PubMedCrossRef G.F. Turi, Z. Liposits, E. Hrabovszky, Cholinergic afferents to gonadotropin-releasing hormone neurons of the rat. Neurochem. Int. 52, 723–728 (2008)PubMedCrossRef
4.
go back to reference A.H. Lauber, R.E. Whalen, Muscarinic cholinergic modulation of hypothalamic estrogen binding sites. Brain Res. 443, 21–26 (1988)PubMedCrossRef A.H. Lauber, R.E. Whalen, Muscarinic cholinergic modulation of hypothalamic estrogen binding sites. Brain Res. 443, 21–26 (1988)PubMedCrossRef
5.
go back to reference M.E. Cruz, L.P. Jaramillo, R. Domínguez, Asymmetric ovulatory response induced by a unilateral implant of atropine in the anterior hypothalamus of the cyclic rat. J. Endocrinol. 123, 437–439 (1989)PubMedCrossRef M.E. Cruz, L.P. Jaramillo, R. Domínguez, Asymmetric ovulatory response induced by a unilateral implant of atropine in the anterior hypothalamus of the cyclic rat. J. Endocrinol. 123, 437–439 (1989)PubMedCrossRef
6.
go back to reference D. Koren, Y. Egozi, M. Sokolovsky, Muscarinic involvement in the regulation of gonadotropin-releasing hormone in the cyclic rat. Mol. Cell. Endocrinol. 90, 87–93 (1992)PubMedCrossRef D. Koren, Y. Egozi, M. Sokolovsky, Muscarinic involvement in the regulation of gonadotropin-releasing hormone in the cyclic rat. Mol. Cell. Endocrinol. 90, 87–93 (1992)PubMedCrossRef
7.
go back to reference J.M. Monti, M.A. Sala, J.T. Otegui, W.L. Benedetti, E. Grino, Inhibition of ovarian compensatory hypertrophy by implant of atropine in the hypothalamus. Experientia 26, 1244–1263 (1970)CrossRef J.M. Monti, M.A. Sala, J.T. Otegui, W.L. Benedetti, E. Grino, Inhibition of ovarian compensatory hypertrophy by implant of atropine in the hypothalamus. Experientia 26, 1244–1263 (1970)CrossRef
8.
go back to reference M.A. Sala, J.T. Otegui, W.L. Benedetti, J.M. Monti, E. Grino, Blockade of ovarian compensatory hypertrophy and ovulation in the rat by hypothalamic implant of an anticholinergic drug. J. Neurovisc. Relat. 32, 241–248 (1971)PubMedCrossRef M.A. Sala, J.T. Otegui, W.L. Benedetti, J.M. Monti, E. Grino, Blockade of ovarian compensatory hypertrophy and ovulation in the rat by hypothalamic implant of an anticholinergic drug. J. Neurovisc. Relat. 32, 241–248 (1971)PubMedCrossRef
9.
go back to reference C. Libertun, S.M. McCann, Further evidence for cholinergic control of gonadotropin and prolactin secretion. Proc. Soc. Exp. Biol. Med. 147, 498–504 (1974)PubMedCrossRef C. Libertun, S.M. McCann, Further evidence for cholinergic control of gonadotropin and prolactin secretion. Proc. Soc. Exp. Biol. Med. 147, 498–504 (1974)PubMedCrossRef
10.
go back to reference I. Simonovic, M. Motta, L. Martini, Acetylcholine and the release of the follicle-stimulating hormone-releasing factor. Endocrinology 95, 1373–1379 (1974)PubMedCrossRef I. Simonovic, M. Motta, L. Martini, Acetylcholine and the release of the follicle-stimulating hormone-releasing factor. Endocrinology 95, 1373–1379 (1974)PubMedCrossRef
11.
go back to reference R.P. Fiorindo, L. Martini, Evidence for a cholinergic component in the neuroendocrine control of luteinizing hormone (LH) secretion. Neuroendocrinology 18, 322–332 (1975)CrossRef R.P. Fiorindo, L. Martini, Evidence for a cholinergic component in the neuroendocrine control of luteinizing hormone (LH) secretion. Neuroendocrinology 18, 322–332 (1975)CrossRef
12.
go back to reference R. Domínguez, L. Riboni, D. Zipitría, R. Revilla, Is there a cholinergic circadian rhythm throughout the oestrous cycle related to ovulation in the rat? J. Endocrinol. 95, 175–180 (1982)PubMedCrossRef R. Domínguez, L. Riboni, D. Zipitría, R. Revilla, Is there a cholinergic circadian rhythm throughout the oestrous cycle related to ovulation in the rat? J. Endocrinol. 95, 175–180 (1982)PubMedCrossRef
13.
go back to reference M.E. Cruz, A. Domínguez-González, A. Flores, M. Cárdenas, R. Chavira, R. Domínguez, The cholinergic blockade during the rat estrous cycle results in opposite effects on gonadotropins and estradiol surge at proestrus. Proceeding of the 40th Meeting of Society for Neuroscience, San Diego, California, Poster Session 185.10, 13–17 Nov 2010 M.E. Cruz, A. Domínguez-González, A. Flores, M. Cárdenas, R. Chavira, R. Domínguez, The cholinergic blockade during the rat estrous cycle results in opposite effects on gonadotropins and estradiol surge at proestrus. Proceeding of the 40th Meeting of Society for Neuroscience, San Diego, California, Poster Session 185.10, 13–17 Nov 2010
14.
go back to reference T.M. Mattioli, S. da Silva, A.M. Grégio, M.A. Machado, A.A. de Lima, L.R. Azevedo-Alanis, The effects of antidepressants and pilocarpine on rat parotid glands: an immunohistochemical study. Clinics 66, 1605–1610 (2011)PubMedCentralPubMedCrossRef T.M. Mattioli, S. da Silva, A.M. Grégio, M.A. Machado, A.A. de Lima, L.R. Azevedo-Alanis, The effects of antidepressants and pilocarpine on rat parotid glands: an immunohistochemical study. Clinics 66, 1605–1610 (2011)PubMedCentralPubMedCrossRef
15.
go back to reference E. López, M.E. Cruz, R. Domínguez, Asymmetrical effects of the unilateral implant of pilocarpine on the preoptic-anterior hypothalamic area on spontaneous ovulation of the adult rat. Arch. Med. Res. 28, 343–348 (1997)PubMed E. López, M.E. Cruz, R. Domínguez, Asymmetrical effects of the unilateral implant of pilocarpine on the preoptic-anterior hypothalamic area on spontaneous ovulation of the adult rat. Arch. Med. Res. 28, 343–348 (1997)PubMed
16.
go back to reference M.E. Cruz, J. Castro, R. Domínguez, A comparative analysis of the neuroendocrine mechanisms regulating ovulation, affected by a unilateral implant of atropine in the preoptic-anterior hypothalamic area, in intact and hemiovariectomized adults rats. J. Endocrinol. 133, 205–210 (1992)PubMedCrossRef M.E. Cruz, J. Castro, R. Domínguez, A comparative analysis of the neuroendocrine mechanisms regulating ovulation, affected by a unilateral implant of atropine in the preoptic-anterior hypothalamic area, in intact and hemiovariectomized adults rats. J. Endocrinol. 133, 205–210 (1992)PubMedCrossRef
17.
go back to reference M. Fukuda, K. Yamanouchi, Y. Nakano, H. Furuya, Y. Arai, Hypothalamic laterality in regulating gonadotropic function: unilateral hypothalamic lesion and ovarian compensatory hypertrophy. Neurosci. Lett. 51, 365–370 (1984)PubMedCrossRef M. Fukuda, K. Yamanouchi, Y. Nakano, H. Furuya, Y. Arai, Hypothalamic laterality in regulating gonadotropic function: unilateral hypothalamic lesion and ovarian compensatory hypertrophy. Neurosci. Lett. 51, 365–370 (1984)PubMedCrossRef
18.
go back to reference D.M. Nance, W.H. Morger, Ipsilateral hypothalamic deafferentation blocks the increase in serum FSH following hemi-castration. Brain Res. Bull. 8, 299–302 (1982)PubMedCrossRef D.M. Nance, W.H. Morger, Ipsilateral hypothalamic deafferentation blocks the increase in serum FSH following hemi-castration. Brain Res. Bull. 8, 299–302 (1982)PubMedCrossRef
19.
go back to reference D.M. Nance, J.P. White, W.H. Moger, Neural regulation of the ovary: evidence for hypothalamic asymmetry in endocrine control. Brain Res. Bull. 10, 353–355 (1983)PubMedCrossRef D.M. Nance, J.P. White, W.H. Moger, Neural regulation of the ovary: evidence for hypothalamic asymmetry in endocrine control. Brain Res. Bull. 10, 353–355 (1983)PubMedCrossRef
20.
go back to reference B. Marchetti, M. Cioni, U. Scapagnini, Ovarian LHRH receptors increase following lesions of the major LHRH structures in the rat brain: involvement of a direct neural pathway. Neuroendocrinology 41, 321–331 (1985)PubMedCrossRef B. Marchetti, M. Cioni, U. Scapagnini, Ovarian LHRH receptors increase following lesions of the major LHRH structures in the rat brain: involvement of a direct neural pathway. Neuroendocrinology 41, 321–331 (1985)PubMedCrossRef
21.
go back to reference J.F.R. Köning, R.A. Klippel, The rat brain. A stereotaxic atlas of the Forebrain and lower parts of the brain stem (Williams and Wilkins, Co, Baltimore, 1963) J.F.R. Köning, R.A. Klippel, The rat brain. A stereotaxic atlas of the Forebrain and lower parts of the brain stem (Williams and Wilkins, Co, Baltimore, 1963)
22.
go back to reference J.M. Daniel, A.J. Fader, A.L. Spencer, G.P. Dohanich, Estrogen enhances performance of female rats during acquisition of a radial arm maze. Horm. Behav. 32, 217–225 (1997)PubMedCrossRef J.M. Daniel, A.J. Fader, A.L. Spencer, G.P. Dohanich, Estrogen enhances performance of female rats during acquisition of a radial arm maze. Horm. Behav. 32, 217–225 (1997)PubMedCrossRef
23.
go back to reference E. Jönsson, H. Kaiya, B.T. Björnsson, Ghrelin decreases food intake in juvenile rainbow trout (Oncorhynchus mykiss) through the central anorexigenic corticotropin-releasing factor system. Gen. Comp. Endocrinol. 166, 39–46 (2010)PubMedCrossRef E. Jönsson, H. Kaiya, B.T. Björnsson, Ghrelin decreases food intake in juvenile rainbow trout (Oncorhynchus mykiss) through the central anorexigenic corticotropin-releasing factor system. Gen. Comp. Endocrinol. 166, 39–46 (2010)PubMedCrossRef
24.
go back to reference K. Venkova, A.C. Johnson, B. Myers, M.B. Greenwood-Van, Exposure of the amygdala to elevated levels of corticosterone alters colonic motility in response to acute psychological stress. Neuropharmacology 58, 1161–1167 (2010)PubMedCrossRef K. Venkova, A.C. Johnson, B. Myers, M.B. Greenwood-Van, Exposure of the amygdala to elevated levels of corticosterone alters colonic motility in response to acute psychological stress. Neuropharmacology 58, 1161–1167 (2010)PubMedCrossRef
25.
go back to reference M.E. Cruz, R. Domínguez, Modifications in follicular compartment of the ovaries of adult rats with a unilateral lesion of the hypothalamus. Med. Sci. Res. 20, 939–941 (1992) M.E. Cruz, R. Domínguez, Modifications in follicular compartment of the ovaries of adult rats with a unilateral lesion of the hypothalamus. Med. Sci. Res. 20, 939–941 (1992)
26.
go back to reference A.N. Hirshfield, A.R. Midqley Jr, Morphometric analysis of follicular development in the rat. Biol. Reprod. 9, 597–605 (1978)CrossRef A.N. Hirshfield, A.R. Midqley Jr, Morphometric analysis of follicular development in the rat. Biol. Reprod. 9, 597–605 (1978)CrossRef
27.
go back to reference S.G. Hillier, G.T. Ross, Effects of exogenous testosterone on ovarian weight, follicular morphology and intraovarian progesterone concentration in estrogen-primed hypophysectomized immature female rats. Biol. Reprod. 20, 261–268 (1979)PubMedCrossRef S.G. Hillier, G.T. Ross, Effects of exogenous testosterone on ovarian weight, follicular morphology and intraovarian progesterone concentration in estrogen-primed hypophysectomized immature female rats. Biol. Reprod. 20, 261–268 (1979)PubMedCrossRef
28.
go back to reference R. Domínguez, M.E. Cruz, R. Chávez, Differences in the ovulatory ability between the right and left ovary are related to ovarian innervation, in Growth Factors and the Ovary, ed. by A.M. Hirshfiel (Plenum Press, New York, 1989), pp. 321–325CrossRef R. Domínguez, M.E. Cruz, R. Chávez, Differences in the ovulatory ability between the right and left ovary are related to ovarian innervation, in Growth Factors and the Ovary, ed. by A.M. Hirshfiel (Plenum Press, New York, 1989), pp. 321–325CrossRef
29.
go back to reference C. Morán, L. Morales, R.S. Razo, J. Apolonio, U. Quiroz, R. Chavira, R. Domínguez, Effects of sensorial denervation induced by capsaicin injection at birth or on day three of life, on puberty, induced ovulation and pregnancy. Life Sci. 73, 2113–2125 (2003)PubMedCrossRef C. Morán, L. Morales, R.S. Razo, J. Apolonio, U. Quiroz, R. Chavira, R. Domínguez, Effects of sensorial denervation induced by capsaicin injection at birth or on day three of life, on puberty, induced ovulation and pregnancy. Life Sci. 73, 2113–2125 (2003)PubMedCrossRef
30.
go back to reference R. Domínguez, L. Morales, M.E. Cruz, Ovarian asymmetry. Ann. Rev. Biomed. Sci. 5, 95–104 (2003) R. Domínguez, L. Morales, M.E. Cruz, Ovarian asymmetry. Ann. Rev. Biomed. Sci. 5, 95–104 (2003)
31.
go back to reference C. C. Ortega, R. Chavira, L. M. Santiago, P. Rosas, S. Cruz-Morales, R. Domínguez, R, The in vitro ability of the right and left ovary of cyclic rats to spontaneous or LH or FSH stimulated estradiol release varies during the estrous cycle and the time of the day. Proceeding of the 46th Meeting of the Society for the Study of Reproduction, Montreal, Canada, Poster Abstract 337, 22–26 July 2013 C. C. Ortega, R. Chavira, L. M. Santiago, P. Rosas, S. Cruz-Morales, R. Domínguez, R, The in vitro ability of the right and left ovary of cyclic rats to spontaneous or LH or FSH stimulated estradiol release varies during the estrous cycle and the time of the day. Proceeding of the 46th Meeting of the Society for the Study of Reproduction, Montreal, Canada, Poster Abstract 337, 22–26 July 2013
32.
go back to reference R. Domínguez, N. L. Rosas, M. L. Santiago, A. Zárate, A. Flores, The transcription of 3β HSD, 17β HSD and P450 aromatase in the ovaries varies during the estrous cycle and is asymmetric. Proceeding of the 95th Meeting of the Endocrine Society, San Francisco, USA, Poster Abstract 519, 15–18 June 2013 R. Domínguez, N. L. Rosas, M. L. Santiago, A. Zárate, A. Flores, The transcription of 3β HSD, 17β HSD and P450 aromatase in the ovaries varies during the estrous cycle and is asymmetric. Proceeding of the 95th Meeting of the Endocrine Society, San Francisco, USA, Poster Abstract 519, 15–18 June 2013
33.
go back to reference I. Gerendai, I.E. Tóth, Z. Boldogkoi, B. Halász, Recent findings on the organization of central nervous system structures involved in the innervation of endocrine glands and other organs; observations obtained by the transneuronal viral double-labeling technique. Endocrine 36, 179–188 (2009)PubMedCrossRef I. Gerendai, I.E. Tóth, Z. Boldogkoi, B. Halász, Recent findings on the organization of central nervous system structures involved in the innervation of endocrine glands and other organs; observations obtained by the transneuronal viral double-labeling technique. Endocrine 36, 179–188 (2009)PubMedCrossRef
34.
go back to reference I.E. Tóth, P. Banczerowski, Z. Boldogkoi, J.S. Tóth, A. Szabó, B. Halász, I. Gerendai, Cerebral neurons involved in the innervation of both the adrenal gland and the ovary: a double viral tracing study. Brain Res. Bull. 77, 306–311 (2008)PubMedCrossRef I.E. Tóth, P. Banczerowski, Z. Boldogkoi, J.S. Tóth, A. Szabó, B. Halász, I. Gerendai, Cerebral neurons involved in the innervation of both the adrenal gland and the ovary: a double viral tracing study. Brain Res. Bull. 77, 306–311 (2008)PubMedCrossRef
35.
go back to reference I.E. Tóth, O. Wiesel, Z. Boldogkoi, K. Bálint, Z. Tapaszti, I. Gerendai, Predominance of supraspinal innervation of the left ovary. Microsc. Res. Tech. 70, 710–718 (2007)PubMedCrossRef I.E. Tóth, O. Wiesel, Z. Boldogkoi, K. Bálint, Z. Tapaszti, I. Gerendai, Predominance of supraspinal innervation of the left ovary. Microsc. Res. Tech. 70, 710–718 (2007)PubMedCrossRef
36.
go back to reference M.E. Cruz, R. Chávez, R. Domínguez, Ovulation, follicular growth and ovarian reactivity to exogenous gonadotropins in adult rats with unilateral or bilateral section of the vagi nerves. Rev. Invest. Clin. 38, 167–171 (1986)PubMed M.E. Cruz, R. Chávez, R. Domínguez, Ovulation, follicular growth and ovarian reactivity to exogenous gonadotropins in adult rats with unilateral or bilateral section of the vagi nerves. Rev. Invest. Clin. 38, 167–171 (1986)PubMed
37.
go back to reference R. Domínguez, S.E. Cruz-Morales, The Ovarian innervation participates in the regulation of ovarian functions. Endocrinol. Metab. Syndr. S4, 001 (2011). doi:10.4172/2161-1017.S4-001 R. Domínguez, S.E. Cruz-Morales, The Ovarian innervation participates in the regulation of ovarian functions. Endocrinol. Metab. Syndr. S4, 001 (2011). doi:10.​4172/​2161-1017.​S4-001
38.
go back to reference K.A. Walters, C.M. Allan, D.J. Handelsman, Androgen actions and the ovary. Biol. Reprod. 78, 380–389 (2008)PubMedCrossRef K.A. Walters, C.M. Allan, D.J. Handelsman, Androgen actions and the ovary. Biol. Reprod. 78, 380–389 (2008)PubMedCrossRef
39.
go back to reference J.S. Richards, Hormonal control of follicular growth and maturation in mammals, in The Vertebrate Ovary. Comparative Biology, ed. by R.E. Jones (Plenum Press, New York, 1978), pp. 331–360 J.S. Richards, Hormonal control of follicular growth and maturation in mammals, in The Vertebrate Ovary. Comparative Biology, ed. by R.E. Jones (Plenum Press, New York, 1978), pp. 331–360
40.
go back to reference M.E. Cruz, G. Villegas, A. Domínguez-González, R. Chavira, Ovulation delay induced by blockade of the cholinergic system on dioestrus-1, is related to changes in dopaminergic activity of the preoptic anterior-hypothalamic area of the rat. Brain Res. Bull. 54, 339–344 (2001)PubMedCrossRef M.E. Cruz, G. Villegas, A. Domínguez-González, R. Chavira, Ovulation delay induced by blockade of the cholinergic system on dioestrus-1, is related to changes in dopaminergic activity of the preoptic anterior-hypothalamic area of the rat. Brain Res. Bull. 54, 339–344 (2001)PubMedCrossRef
41.
go back to reference J.W. Everett, Pituitary and hypothalamus: perspectives and overview, in Knobil and Neill´s Physiology of Reproduction, ed. by J.D. Neill (Elsevier Press, St. Louis, 2006), pp. 1289–1309CrossRef J.W. Everett, Pituitary and hypothalamus: perspectives and overview, in Knobil and Neill´s Physiology of Reproduction, ed. by J.D. Neill (Elsevier Press, St. Louis, 2006), pp. 1289–1309CrossRef
42.
go back to reference R.F. Weick, E.R. Smith, R. Dominguez, A.P.S. Dhariwal, J.M. Davidson, Mechanism of stimulatory feedback effect of estradiol benzoate on the pituitary. Endocrinology 88, 293–301 (1971)PubMedCrossRef R.F. Weick, E.R. Smith, R. Dominguez, A.P.S. Dhariwal, J.M. Davidson, Mechanism of stimulatory feedback effect of estradiol benzoate on the pituitary. Endocrinology 88, 293–301 (1971)PubMedCrossRef
Metadata
Title
The cholinergic system of the preoptic-anterior hypothalamic areas regulates the ovarian follicular population in an asymmetric way
Authors
María Esther Cruz
Angélica Flores
Roberto Domínguez
Publication date
01-12-2014
Publisher
Springer US
Published in
Endocrine / Issue 3/2014
Print ISSN: 1355-008X
Electronic ISSN: 1559-0100
DOI
https://doi.org/10.1007/s12020-014-0266-2

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