The Participation of the Cholinergic System in Regulating Progesterone Secretion Through the Ovarian-adrenal Crosstalk Varies Along the Estrous Cycle

Overview

Journal Endocrine

Specialty Endocrinology

Date 2006 Jan 3

PMID 16388086

Citations 12

Authors

Angelica Flores

Griselda Melendez

Maria T Palafox

Jorge O Rodriguez

Ana I Barco

Roberto Chavira

Roberto Dominguez

M Esther Cruz

Affiliations

Soon will be listed here.

Abstract

This study was designed to analyze the acute effects of unilateral or bilateral ovariectomy or adrenalectomy, performed on different days of the estrous cycle, on progesterone (P4) serum levels 1 h after surgery. The effects of blocking the cholinergic system by injecting atropine sulfate were also analyzed. Ether anesthesia treatment on diestrus 1 (D1) increased P4 serum levels. Compared to right sham-operated animals, right ovariectomy (left ovary in situ) performed on diestrus 2 (D2) or proestrus (P), resulted in P4 serum levels increase. Compared to animals with left sham surgery, left adrenalectomy (right adrenal in situ) performed on P day resulted in significantly lower P4 concentrations. Bilateral adrenalectomy resulted in a significant drop of P4 serum levels; the most remarkable drop was observed in animals treated on D2. Bilateral ovariectomy performed on D1 resulted in lower P4 serum levels, and the same treatment performed on P resulted in a significant rise of P4 serum levels. Injecting atropine sulfate to untouched (control group) rats resulted in significantly higher P4 concentrations. Blocking the cholinergic sys-tem on D1 or P to rats with the right adrenal removed resulted in lower P4 serum levels; while, in contrast, atropine sulfate treatment performed on D2 resulted in P4 serum levels increase. The results support the hypothesis of asymmetry in the ovaries' and adrenals' capacities to secrete P4; that this capacity varies along the estrous cycle; and that P4 secretion by the ovaries and adrenals is regulated by the cholinergic system.

Citing Articles

Participation of the Cholinergic System in the Development of Polycystic Ovary Syndrome.

Linares R, Acuna X, Rosas G, Vieyra E, Ramirez D, Chaparro A Molecules. 2021; 26(18).

PMID: 34576975 PMC: 8471679. DOI: 10.3390/molecules26185506.

The Neural Signals of the Superior Ovarian Nerve Modulate in an Asymmetric Way the Ovarian Steroidogenic Response to the Vasoactive Intestinal Peptide.

Rosas G, Linares R, Ramirez D, Vieyra E, Trujillo A, Dominguez R Front Physiol. 2018; 9:1142.

PMID: 30177887 PMC: 6110177. DOI: 10.3389/fphys.2018.01142.

Unilaterally blocking the muscarinic receptors in the suprachiasmatic nucleus in proestrus rats prevents pre-ovulatory LH secretion and ovulation.

Vieyra E, Ramirez D, Lagunas N, Cardenas M, Chavira R, Damian-Matsumura P Reprod Biol Endocrinol. 2016; 14(1):34.

PMID: 27306649 PMC: 4910191. DOI: 10.1186/s12958-016-0168-7.

Ovulation requires the activation on proestrus of M₁ muscarinic receptors in the left ovary.

Cruz M, Flores A, Alvarado B, Hernandez C, Zarate A, Chavira R Endocrine. 2015; 49(3):809-19.

PMID: 25586874 DOI: 10.1007/s12020-014-0524-3.

Asymmetric steroidogenic response by the ovaries to the vasoactive intestinal peptide.

Rosas G, Ramirez M, Linares R, Trujillo A, Dominguez R, Morales-Ledesma L Endocrine. 2014; 48(3):968-77.

PMID: 25331816 DOI: 10.1007/s12020-014-0449-x.

References

Smith M, Freeman M, Neill J . The control of progesterone secretion during the estrous cycle and early pseudopregnancy in the rat: prolactin, gonadotropin and steroid levels associated with rescue of the corpus luteum of pseudopregnancy. Endocrinology. 1975; 96(1):219-26. DOI: 10.1210/endo-96-1-219. View

Gerendai I, Toth I, Boldogkoi Z, Medveczky I, Halasz B . CNS structures presumably involved in vagal control of ovarian function. J Auton Nerv Syst. 2000; 80(1-2):40-5. DOI: 10.1016/s0165-1838(00)00071-0. View

Moran C, Morales L, Quiroz U, Dominguez R . Effects of unilateral or bilateral superior ovarian nerve section in infantile rats on follicular growth. J Endocrinol. 2000; 166(1):205-11. DOI: 10.1677/joe.0.1660205. View

De Geyter C, De Geyter M, Huber P, Nieschlag E, Holzgreve W . Progesterone serum levels during the follicular phase of the menstrual cycle originate from the crosstalk between the ovaries and the adrenal cortex. Hum Reprod. 2002; 17(4):933-9. DOI: 10.1093/humrep/17.4.933. View

Matzuk M, Finegold M, Mather J, Krummen L, Lu H, Bradley A . Development of cancer cachexia-like syndrome and adrenal tumors in inhibin-deficient mice. Proc Natl Acad Sci U S A. 1994; 91(19):8817-21. PMC: 44697. DOI: 10.1073/pnas.91.19.8817. View

Wu X, Zhou S, Sallinen K, Pollanen P, Erkkola R . Ovarian-adrenal cross-talk in polycystic ovary syndrome: evidence from wedge resection. Eur J Endocrinol. 2000; 143(3):383-8. DOI: 10.1530/eje.0.1430383. View

Kalantaridou S, Makrigiannakis A, Zoumakis E, Chrousos G . Stress and the female reproductive system. J Reprod Immunol. 2004; 62(1-2):61-8. DOI: 10.1016/j.jri.2003.09.004. View

Galvez A, Paredes A, Fiedler J, Venegas M, Lara H . Effects of adrenalectomy on the stress-induced changes in ovarian sympathetic tone in the rat. Endocrine. 1999; 10(2):131-5. DOI: 10.1385/endo:10:2:131. View

Adashi E, Hsueh A . Stimulation of beta 2-adrenergic responsiveness by follicle-stimulating hormone in rat granulosa cells in vitro and in vivo. Endocrinology. 1981; 108(6):2170-8. DOI: 10.1210/endo-108-6-2170. View

10.

Lobo R, Goebelsmann U, Brenner P, Mishell Jr D . The effects of estrogen on adrenal androgens in oophorectomized women. Am J Obstet Gynecol. 1982; 142(4):471-8. DOI: 10.1016/s0002-9378(16)32393-6. View

11.

Aguado L . Role of the central and peripheral nervous system in the ovarian function. Microsc Res Tech. 2002; 59(6):462-73. DOI: 10.1002/jemt.10232. View

12.

De Bortoli M, Garraza M, Aguado L . Adrenergic intracerebroventricular stimulation affects progesterone concentration in the ovarian vein of the rat: participation of the superior ovarian nerve. J Endocrinol. 1998; 159(1):61-8. DOI: 10.1677/joe.0.1590061. View

13.

Baljet B, DRUKKER J . The extrinsic innervation of the pelvic organs in the female rat. Acta Anat (Basel). 1980; 107(3):241-67. DOI: 10.1159/000145249. View

14.

Ahmed C, Dees W, Ojeda S . The immature rat ovary is innervated by vasoactive intestinal peptide (VIP)-containing fibers and responds to VIP with steroid secretion. Endocrinology. 1986; 118(4):1682-9. DOI: 10.1210/endo-118-4-1682. View

15.

Bateman A, Singh A, Kral T, Solomon S . The immune-hypothalamic-pituitary-adrenal axis. Endocr Rev. 1989; 10(1):92-112. DOI: 10.1210/edrv-10-1-92. View

16.

Dominguez R, Riboni L, Zipitria D, Revilla R . Is there a cholinergic circadian rhythm throughout the oestrous cycle related to ovulation in the rat?. J Endocrinol. 1982; 95(2):175-80. DOI: 10.1677/joe.0.0950175. View

17.

Moran C, Franco A, Moran J, Handal A, Morales L, Dominguez R . Neural activity between ovaries and the prevertebral celiac-superior mesenteric ganglia varies during the estrous cycle of the rat. Endocrine. 2005; 26(2):147-52. DOI: 10.1385/ENDO:26:2:147. View

18.

Judd S, Terry A, Petrucco M, White G . The source of pulsatile secretion of progesterone during the human follicular phase. J Clin Endocrinol Metab. 1992; 74(2):299-305. DOI: 10.1210/jcem.74.2.1730808. View

19.

Frankel A, Chapman J, Cook B . Testes are asymmetric in the testicular hemicastration response of the male rat. J Endocrinol. 1989; 122(2):485-8. DOI: 10.1677/joe.0.1220485. View

20.

Saper C, Loewy A, Swanson L, Cowan W . Direct hypothalamo-autonomic connections. Brain Res. 1976; 117(2):305-12. DOI: 10.1016/0006-8993(76)90738-1. View