Skip to main content
Key Specialties
Cardiology Diabetology Endocrinology Gastroenterology Geriatrics and Gerontology Gynecology and Obstetrics Hematology Infectious Disease Internal Medicine Nephrology Neurology Oncology Pediatrics Respiratory Medicine Rheumatology Surgery
Congress Coverage
2024 ACC Congress 2023 ESMO Congress 2023 EASD Congress 2023 ERS Congress 2023 ESC Congress
Clinical Collections
Advances in Alzheimer’s

Keynote webinar | Spotlight on medication adherence

LIVE: Thursday 27th June 2024, 18:00-19:30 (CEST)
Join our expert panel to discover why you need to understand the drivers of non-adherence in your patients, and how you can optimize medication adherence in your clinics to drastically improve patient outcomes.
ADVANCED SEARCH
Log in
Top
Endocrine
Published in: Endocrine 2/2014

01-06-2014 | Original Article

Lack of sensorial innervation in the newborn female rats affects the activity of hypothalamic monoaminergic system and steroid hormone secretion during puberty

Authors: Ubaldo Quiróz, Leticia Morales-Ledesma, Carolina Morán, Angélica Trujillo, Roberto Domínguez

Published in: Endocrine | Issue 2/2014

Login to get access

Abstract

There is evidence that sensory innervation plays a role regulating ovarian functions, including fertility. Since sensory denervation by means of capsaicin in newborn female rats results in a lower response to gonadotropins, the present study analyzed the effects that sensory denervation by means of capsaicin in neonatal rats has on the concentration of monoamines in the anterior (AH) and medium (MH) hypothalamus, and on steroid hormone levels in serum. Groups of newborn female rats were injected subcutaneously with capsaicin and killed at 10, 20, and 30 days of age and on the first vaginal estrous. The concentrations of noradrenaline, dopamine, serotonin (5-HT), and their metabolites in the AH and MH were measured using HPLC, and the levels of estradiol (E), progesterone (P), testosterone (T), FSH, and luteinizing hormone using radioimmunoanalysis. The results show that at 20 days of age, capsaicin-treated rats have lower noradrenergic and serotonergic activities in the AH, and that the dopaminergic activity was lower in the MH. These results suggest that the sensorial system connections within the monoaminergic systems of the AH and MH are different. Capsaicin-treated animals had lower T, E, and P levels than in the control group, suggesting that the lower activity in the AH monoaminergic system and lower hormone secretion could be explained by the blockade of information mediated by the sensory innervation (probably substance P), mainly between the ovary and the AH.
Literature
1.
C. Morán, L. Morales, R.S. Razo, J. Apolonio, U. Quiróz, 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
2.
A. Trujillo, L. Morales, X. Vargas, L. Alba, R. Domínguez, Effects of capsaicin treatment on the regulation of ovarian compensatory hypertrophy and compensatory ovulation. Endocrine 25, 155–162 (2004)PubMedCrossRef
3.
W.H. Burden, Ovarian Innervation, in The Vertebrate Ovary, ed. by R. Jones (Plenum Press, New York, 1978), pp. 615–638
4.
S. Fritz, I. Wessler, R. Breitling, W. Rossmanith, S.R. Ojeda, G.A. Dissen, A. Amsterdam, A. Mayerhofer, Expression of muscarinic receptor types in the primate ovary and evidence for nonneuronal acetylcholine synthesis. J. Clin. Endocrinol. Metab. 86, 349–354 (2001)PubMed
5.
A. Mayerhofer, G.A. Dissen, W.L. Dees, M.E. Costa, S.R. Ojeda, A role for neurotransmitters in early follicular development: induction of functional follicle-stimulating hormone receptors in newly formed follicles of the rat ovary. Endocrinology 138, 3320–3329 (1997)PubMed
6.
C.A. Maggi, A. Meli, The sensory-efferent function of capsaicin-sensitive sensory neurons. Gen. Pharmacol. 19, 1–43 (1988)PubMedCrossRef
7.
W.L. Dees, C.E. Ahmed, S.R. Ojeda, Substance P and vasoactive intestinal peptide-containing fibers reach the ovary by independent routes. Endocrinology 119, 638–641 (1986)PubMedCrossRef
8.
S.R. Ojeda, M.E. Costa, K.H. Katz, L.B. Hersh, Evidence for the existence of substance P in the prepubertal rat ovary. I. Biochemical and physiologic studies. Biol. Reprod. 33, 286–295 (1985)PubMedCrossRef
9.
R.E. Papka, J.P. Cotton, H.H. Traurig, Comparative distribution of neuropeptide tyrosine-vasoactive intestinal polypeptide, substance P-immunoreactive, acetylcholinesterase-positive and noradrenergic nerves in the reproductive tract of the female rat. Cell Tissue Res. 242, 475–490 (1985)PubMedCrossRef
10.
J. Calka, J.K. McDonald, S.R. Ojeda, The innervation of the immature rat ovary by calcitonin gene-related peptide. Biol. Reprod. 39, 1215–1223 (1988)PubMedCrossRef
11.
C.M. Klein, H.W. Burden, Substance P- and vasoactive intestinal polypeptide (VIP)-immunoreactive nerve fibers in relation to ovarian postganglionic perikarya in para- and prevertebral ganglia: evidence from combined retrograde tracing and immunocytochemistry. Cell Tissue Res. 252, 403–410 (1988)PubMedCrossRef
12.
D.L. McNeill, H.W. Burden, Neuropeptides in sensory perikarya projecting to the rat ovary. Am. J. Anat. 179, 269–276 (1987)PubMedCrossRef
13.
P. Kannisto, E. Ekblad, G. Helm, C. Owman, N.O. Sjöberg, M. Stjernquist, F. Sundler, B. Walles, Existence and coexistence of peptides in nerves of the mammalian ovary and oviduct demonstrated by immunocytochemistry. Histochemistry 86, 25–34 (1986)PubMedCrossRef
14.
R. Amann, Desensitization of capsaicin-evoked neuropeptide release-influence of Ca2+ and temperature. Naunyn Schmiedebergs Arch. Pharmacol. 342, 671–676 (1990)PubMedCrossRef
15.
A. Szallasi, P. Blumberg, Vanilloid (capsaicin) receptors and mechanisms. Pharmacol. Rev. 51, 159–211 (1999)PubMed
16.
J. Donnerer, R. Amann, G. Skofitsch, F. Lembeck, Substance P afferents regulate ACTH-corticosterone release. Ann. N. Y. Acad. Sci. 632, 296–303 (1991)PubMedCrossRef
17.
K.A. Wardle, J. Ranson, G.J. Sanger, Pharmacological characterization of the vanilloid receptor in the rat dorsal spinal cord. Br. J. Pharmacol. 121, 1012–1016 (1997)PubMedCentralPubMedCrossRef
18.
I. Gerendai, I.E. Toth, Z. Boldogkoi, I. Medveczky, B. Halasz, CNS structures presumably involved in vagal control of ovarian function. J. Auton. Nerv. Syst. 80, 40–45 (2000)PubMedCrossRef
19.
I. Gerendai, K. Kocsis, B. Halász, Supraespinal connections of the ovary: structural and functional aspects. Microsc. Res. Tech. 59, 474–483 (2002)PubMedCrossRef
20.
I. Gerendai, P. Banczerowski, B. Halász, Functional significance of the innervation of the gonads. Endocrine 28, 309–318 (2005)PubMedCrossRef
21.
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
22.
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
23.
D.P. Li, S.R. Chen, H.L. Pan, VR1 receptor activation induces glutamate release and postsynaptic firing in the paraventricular nucleus. J. Neurophysiol. 92, 1807–1816 (2004)PubMedCrossRef
24.
U. Karlsson, A.K. Sundgren-Andersson, S. Johansson, J.J. Krupp, Capsaicin augments synaptic transmission in the rat medial preoptic nucleus. Brain Res. 1043, 1–11 (2005)PubMedCrossRef
25.
V. Ralevic, P. Karoon, G. Burnstock, Long-term sensory denervation by neonatal capsaicin treatment augments sympathetic neurotransmission in rat mesenteric arteries by increasing levels of norepinephrine and selectively enhancing postjunctional actions. J. Pharmacol. Exp. Ther. 274, 64–71 (1995)PubMed
26.
G. Terenghi, S.Q. Zhang, W.G. Unger, J.M. Polak, Morphological changes of sensory CGRP-immunoreactive and sympathetic nerves in peripheral tissues following chronic denervation. Histochemistry 86, 89–95 (1986)PubMedCrossRef
27.
H. Sann, G. Jancsó, A. Ambrus, F.K. Pierau, Capsaicin treatment induces selective sensory degeneration and increased sympathetic innervation in the rat ureter. Neuroscience 67, 953–966 (1995)PubMedCrossRef
28.
R. Schicho, Y. Kanai, T. Ishikawa, G. Skofitsch, J. Donnerer, Involvement of NGF in the induction of increased noradrenergic innervation of the ureter in neonatally capsaicin-treated rats. J. Auton. Nerv. Syst. 73, 46–53 (1998)PubMedCrossRef
29.
J. Luthman, I. Strömberg, E. Broding, G. Jonsson, Capsaicin treatment to developing rats induces increase of noradrenaline levels in the iris without affecting the adrenergic terminal density. Int. J. Dev. Neurosci. 7, 613–622 (1989)PubMedCrossRef
30.
M.E. Castro, M.E. Ayala, J. Monroy, R. Chavira, P. Damian-Matsumura, R. Domínguez, Changes in monoaminergic activity in the anterior, medium and posterior hypothalamus, gonadotropins levels and ovarian hormones during puberty of the female rat. Brain Res. Bull. 54, 345–352 (2001)PubMedCrossRef
31.
S.M. Luza, L. Lizama, R.A. Burgos, H.E. Lara, Hypothalamic changes in norepinephrine release in rats with estradiol valerate-induced polycystic ovaries. Biol. Reprod. 52, 398–404 (1995)PubMedCrossRef
32.
M.E. Ayala, J. Monroy, L. Morales, M.E. Castro, R. Domínguez, Effects of a lesion in the dorsal raphe nuclei performed during the juvenile period of the female rat, on puberty. Brain Res. Bull. 47, 211–218 (1998)PubMedCrossRef
33.
J. Monroy, M.E. Ayala, R. Chavira, P. Damián-Matsumura, R. Domínguez, Comparative effects of injecting 5,6-dihydroxytryptamine in the dorsal or medial raphe nuclei on rat puberty. Brain Res. Bull. 60, 307–315 (2003)PubMedCrossRef
34.
N.J. Shannon, J.W. Gunnet, K.E. Moore, A comparison of biochemical indices of 5-hydroxytryptaminergic neuronal activity following electrical stimulation of the dorsal raphe nucleus. J. Neurochem. 47, 958–965 (1986)PubMedCrossRef
35.
B. Kerdelhué, F. Bojda, P. Lesieur, C. Pasqualini, A. el Abed, V. Lenoir, P. Douillet, M.C. Chiueh, M. Palkovits, Median eminence dopamine and serotonin neuronal activity. Temporal relationship to preovulatory prolactin and luteinizing hormone surges. Neuroendocrinology 49, 176–180 (1989)PubMedCrossRef
36.
S.C. Pingle, J.A. Matta, G.P. Ahern, Capsaicin receptor: TRPV1 a promiscuous TRP channel. Handb. Exp. Pharmacol. 179, 155–171 (2007)PubMedCrossRef
37.
K. Zavitsanou, V.S. Dalton, H. Wang, P. Newson, L.A. Chahl, Receptor changes in brain tissue of rats treated as neonates with capsaicin. J. Chem. Neuroanat. 39, 248–255 (2010)PubMedCrossRef
38.
T. Sasamura, M. Sasaki, C. Tohda, Y. Kuraishi, Existence of capsaicin-sensitive glutamatergic terminals in rat hypothalamus. Neuroreport 9, 2045–2048 (1998)PubMedCrossRef
39.
J. Xing, J. Li, TRPV1 receptor mediates glutamatergic synaptic input to dorsolateral periaqueductal gray (dl-PAG) neurons. J. Neurophysiol. 97, 503–511 (2007)PubMedCrossRef
40.
J.H. Peters, S.J. McDougall, J.A. Fawley, S.M. Smith, M.C. Andresen, Primary afferent activation of thermosensitive TRPV1 triggers asynchronous glutamate release at central neurons. Neuron 65, 657–669 (2010)PubMedCentralPubMedCrossRef
41.
M. Hajós, K. Svensson, H. Nissbrandt, F. Obál Jr, A. Carlsson, Effects of capsaicin on central monoaminergic mechanisms in the rat. J. Neural Transm. 66, 221–242 (1986)PubMedCrossRef
42.
R.M. Virus, D.Q. McManus, G.F. Gebhart, Capsaicin treatment in adult Wistar-Kyoto and spontaneously hypertensive rats: neurochemical effects in the spinal cord. Eur. J. Pharmacol. 92, 1–8 (1983)PubMedCrossRef
43.
R. Domínguez, S.E. Cruz-Morales, The ovarian innervation participates in the regulation of ovarian functions. Endocrinol. Metabol. Syndr. S4–001, 1–10 (2011)
44.
J.L. Barker, Physiological Role of Peptides in the Nervous System, in Peptides in Neurobiology, ed. by H. Gainer (Plenum Press, New York, 1977), pp. 295–343CrossRef
45.
L. Riboni, E. Chávez, R. Domínguez, Peripheral sympathetic denervation provoked by guanethidine injection results in the advancement of ovulation, induced by sequential gonadotrophin treatment, in prepubertal female guinea pigs. Med. Sci. Res. 25, 453–454 (1997)
46.
L. Riboni, C. Escamilla, R. Chavira, R. Domínguez, Effects of peripheral sympathetic denervation induced by guanethidine administration on the mechanisms regulating puberty in the female guinea pig. J. Endocrinol. 156, 91–98 (1998)PubMedCrossRef
47.
M.E. Ayala, J. Monroy, L. Morales, M.E. Castro, R. Domínguez, Effects of a lesion in the dorsal raphe nuclei performed during the juvenile period of the female rat, on puberty. Brain Res. Bull. 47, 211–218 (1998)PubMedCrossRef
48.
A. Trujillo, L. Riboni, Effects of functional peripheral sympathetic denervation induced by guanethidine on follicular development and ovulation of the adult female guinea pig. Gen. Comp. Endocrinol. 127, 273–278 (2002)PubMedCrossRef
49.
E. Vijayan, W.K. Samson, S.M. McCann, In vivo and in vitro effects of cholecystokinin on gonadotropin, prolactin, growth hormone and thyrotropin release in the rat. Brain Res. 172, 295–302 (1979)PubMedCrossRef
50.
M. Arisawa, L. De Palatis, R. Ho, G.D. Snyder, W.H. Yu, G. Pan, S.M. McCann, Stimulatory role of substance P on gonadotropin release in ovariectomized rats. Neuroendocrinology 51, 523–529 (1990)PubMedCrossRef
51.
G.E. Hoffman, Organization of LHRH cells: differential apposition of neurotensin, substance P and catecholamine axons. Peptides 6, 439–461 (1985)PubMedCrossRef
52.
T. Battmann, Mĕlik Parsadaniantz, S., Jeanjean, B., Kerdelhué, B.: In-vivo inhibition of the preovulatory LH surge by substance P and in vitro modulation of gonadotrophin-releasing hormone-induced LH release by substance P, oestradiol and progesterone in the female rat. J. Endocrinol. 130, 169–175 (1991)PubMedCrossRef
53.
L.C. Russell, K.J. Burchiel, Neurophysiological effects of capsaicin. Brain Res. 320, 165–176 (1984)PubMedCrossRef
54.
55.
S.R. Ojeda, M.E. Costa, K.H. Katz, Hersh LB Evidence for the existence of substance P in the prepubertal rat ovary. I. Biochemical and physiologic studies. Biol. Reprod. 33, 286–295 (1985)PubMedCrossRef
56.
H. Traurig, A. Saria, F. Lembeck, The effects of neonatal capsaicin treatment on growth and subsequent reproductive function in the rat. Naunyn-Schmiedeberg′s Arch. Pharmacol. 327, 254–259 (1984)CrossRef
57.
H. Traurig, R. Papka, M. Rush, Effects of capsaicin on reproductive function in the female rat: role of peptide-containing primary afferent nerves innervating the uterine cervix in the neuroendocrine copulatory response. Cell Tissue Res. 253, 573–581 (1988)PubMedCrossRef
58.
D.M. Nance, T.R. King, P.W. Nance, Neuroendocrine and behavioral effects of intrathecal capsaicin in adult female rats. Brain Res. Bull. 18, 109–114 (1987)PubMedCrossRef
59.
C.O. Pintado, F.M. Pinto, J.N. Pennefather, A. Hidalgo, A. Baamonde, T. Sanchez, M.L. Candenas, A role for tachykinins in female mouse and rat reproductive function. Biol. Reprod. 69, 6–940 (2003)CrossRef
60.
V. Tsatsaris, A. Tarrade, P. Merviel, J.M. Garel, N. Segond, A. Jullienne, D. Evain-Brion, Calcitonin gene-related peptide (CGRP) and CGRP receptor expression at the human implantation site. J. Clin. Endocrinol. Metab. 87, 4383–4390 (2002)PubMedCrossRef
61.
L. Debeljuk, M. Lasaga, Tachykinins and the control of prolactin secretion. Peptides 27, 3007–3019 (2006)PubMedCrossRef
62.
J. Donnerer, F. Lembeck, Different control of the adrenocorticotropin-corticosterone response and of prolactin secretion during cold stress, anesthesia, surgery, and nicotine injection in the rat: involvement of capsaicin-sensitive sensory neurons. Endocrinology 126, 921–926 (1990)PubMedCrossRef
63.
A. Bachelot, J. Beaufaron, N. Servel, C. Kedzia, P. Monget, P.A. Kelly, G. Gibori, N. Binart, Prolactin independent rescue of mouse corpus luteum life span: identification of prolactin and luteinizing hormone target genes. Am. J. Physiol. Endocrinol. Metab. 297, E676–E684 (2009)PubMedCentralPubMedCrossRef
Metadata
Title
Lack of sensorial innervation in the newborn female rats affects the activity of hypothalamic monoaminergic system and steroid hormone secretion during puberty
Authors
Ubaldo Quiróz
Leticia Morales-Ledesma
Carolina Morán
Angélica Trujillo
Roberto Domínguez
Publication date
01-06-2014
Publisher
Springer US
Published in
Endocrine / Issue 2/2014
Print ISSN: 1355-008X
Electronic ISSN: 1559-0100
DOI
https://doi.org/10.1007/s12020-013-0055-3

Other articles of this Issue 2/2014

Endocrine 2/2014 Go to the issue

Original Article

The calcium–phosphate balance, modulation of thyroid autoimmune processes and other adverse effects connected with thyroid arterial embolization

Endocrine Methods and Techniques

Establishment of robust controls for the normalization of miRNA expression in neuroendocrine tumors of the ileum and pancreas

Original Article

Midkine expression is associated with clinicopathological features and BRAF mutation in papillary thyroid cancer

Endocrine Imaging

Lingual thyroid

Original Article

Decrease in TSH levels after lactose restriction in Hashimoto’s thyroiditis patients with lactose intolerance

Original Article

Glycemic variability in normal glucose regulation subjects with elevated 1-h postload plasma glucose levels
Live Webinar | 27-06-2024 | 18:00 (CEST)

Keynote webinar | Spotlight on medication adherence

Reserve your place

Live: Thursday 27th June 2024, 18:00-19:30 (CEST)

WHO estimates that half of all patients worldwide are non-adherent to their prescribed medication. The consequences of poor adherence can be catastrophic, on both the individual and population level.

Join our expert panel to discover why you need to understand the drivers of non-adherence in your patients, and how you can optimize medication adherence in your clinics to drastically improve patient outcomes.

Prof. Kevin Dolgin
Prof. Florian Limbourg
Prof. Anoop Chauhan
Developed by: Springer Medicine
Obesity Clinical Trial Summary

At a glance: The STEP trials

Read more

A round-up of the STEP phase 3 clinical trials evaluating semaglutide for weight loss in people with overweight or obesity.

Developed by: Springer Medicine
Image Credits