Publications by authors named "Raphael Escorsim Szawka"

13 Publications

  • Page 1 of 1

GATA-1 mutation alters the spermatogonial phase and steroidogenesis in adult mouse testis.

Mol Cell Endocrinol 2022 Feb 26;542:111519. Epub 2021 Nov 26.

Laboratory of Cellular Biology, Department of Morphology, Institute of Biological Sciences, Federal University of Minas Gerais, Belo Horizonte, MG, Brazil. Electronic address:

GATA-1 is a transcription factor from the GATA family, which features zinc fingers for DNA binding. This protein was initially identified as a crucial regulator of blood cell differentiation, but it is currently known that the Gata-1 gene expression is not limited to this system. Although the testis is also a site of significant GATA-1 expression, its role in testicular cells remains considerably unexplored. In the present study, we evaluated the testicular morphophysiology of adult ΔdblGATA mice with a mutation in the GATA-1 protein. Regarding testicular histology, GATA-1 mutant mice exhibited few changes in the seminiferous tubules, particularly in germ cells. A high proportion of differentiated spermatogonia, an increased number of apoptotic pre-leptotene spermatocytes (Caspase-3-positive), and a high frequency of sperm head defects were observed in ΔdblGATA mice. The main differences were observed in the intertubular compartment, as ΔdblGATA mice showed several morphofunctional changes in Leydig cells. Reduced volume, increased number and down-regulation of steroidogenic enzymes were observed in ΔdblGATA Leydig cells. Moreover, the mutant animal showed lower serum testosterone concentration and high LH levels. These results are consistent with the phenotypic and biometric data of mutant mice, i.e., shorter anogenital index and reduced accessory sexual gland weight. In conclusion, our findings suggest that GATA-1 protein is an important factor for germ cell differentiation as well as for the steroidogenic activity in the testis.
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http://dx.doi.org/10.1016/j.mce.2021.111519DOI Listing
February 2022

Social interaction masking contributes to changes in the activity of the suprachiasmatic nucleus and impacts on circadian rhythms.

Physiol Behav 2021 08 18;237:113420. Epub 2021 Apr 18.

Departamento de Fisiologia e Biofísica, Instituto de Ciências Biológicas, Universidade Federal de Minas Gerais, Belo Horizonte, Brazil. Electronic address:

Light is the most powerful temporal cue that entrains physiology and behavior through modulation of the suprachiasmatic nucleus (SCN) of the hypothalamus. However, on a daily basis, individuals face a combination of light and several non-photic cues, such as social interaction. In order to investigate whether SCN activity and SCN-driven rhythms are altered by social interaction, adult male C57BLJ/6 mice were maintained in groups of 3-4 animals per cage or 1 animal per cage (socially isolated) under 12:12 h / light:dark (LD) cycles or constant darkness (DD). Analysis of the two anatomical subdivisions (ventral, v and dorsal, d) of the medial SCN revealed an effect of housing conditions on the d-SCN but not on the v-SCN on the number of c-Fos immunoreactive (ir) neurons. As such, 2 h after the light-phase onset d-SCN c-Fos-ir number was lower in single-housed mice under LD. Importantly, under DD there were no effect of housing conditions in the number of c-Fos-ir SCN neurons. Social isolation increased the amplitude and strength of SCN-driven rhythm of body temperature (Tc) entrained to LD and it advanced its onset, uncoupling with spontaneous locomotor activity (SLA) rhythm, without altering endogenous Tc and SLA rhythms expressed under DD. Associated with reduced Tc in the light phase, single-housed mice showed reduced body weight. However, these phenotypes were not accompanied by changes in the number of c-Fos-ir neurons in the preoptic area (POA), which are known to regulate energy metabolism and Tc. Altogether, these results imply that the social interaction masking effect on the d-SCN is added to that of light stimulus, in order to achieve full c-Fos expression in the SCN, which, in turn seems to be required to maintain daily-phase coherence between the photo-entrained rhythms of Tc and SLA. There might be an inter-relationship between masking (social interaction) and entrainment stimulus (light) that impacts the circadian parameters of the photo-entrained Tc rhythm. As such, in the absence of social interactions a more robust Tc rhythm is shown. This inter-relationship seems to occur in the dorsal subdivision of the SCN but not in the POA.
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http://dx.doi.org/10.1016/j.physbeh.2021.113420DOI Listing
August 2021

Impaired thermoregulation in spontaneously hypertensive rats during physical exercise is related to reduced hypothalamic neuronal activation.

Pflugers Arch 2020 12 10;472(12):1757-1768. Epub 2020 Oct 10.

Laboratório de Endocrinologia e Metabolismo, Departamento de Fisiologia e Biofísica, Universidade Federal de Minas Gerais, Av. Antônio Carlos, 6627., Belo Horizonte, MG, 31270-901, Brazil.

This study aimed to evaluate the physical exercise-induced neuronal activation in brain nuclei controlling thermoregulatory responses in hypertensive and normotensive rats. Sixteen-week-old male normotensive Wistar rats (NWRs) and spontaneously hypertensive rats (SHRs) were implanted with an abdominal temperature sensor. After recovery, the animals were subjected to a constant-speed treadmill running (at 60% of the maximum aerobic speed) for 30 min at 25 °C. Core (T) and tail-skin (T) temperatures were measured every minute during exercise. Ninety minutes after the exercise, the rats were euthanized, and their brains were collected to determine the c-Fos protein expression in the following areas that modulate thermoregulatory responses: medial preoptic area (mPOA), paraventricular hypothalamic nucleus (PVN), and supraoptic nucleus (SON). During treadmill running, the SHR group exhibited a greater increase in T and an augmented threshold for cutaneous heat loss relative to the NWR group. In addition, the SHRs showed reduced neuronal activation in the mPOA (< 49.7%) and PVN (< 44.2%), but not in the SON. The lower exercise-induced activation in the mPOA and PVN in hypertensive rats was strongly related to the delayed onset of cutaneous heat loss. We conclude that the enhanced exercise-induced hyperthermia in hypertensive rats can be partially explained by a delayed cutaneous heat loss, which is, in turn, associated with reduced activation of brain areas modulating thermoregulatory responses.
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http://dx.doi.org/10.1007/s00424-020-02474-2DOI Listing
December 2020

Selective post-training time window for memory consolidation interference of cannabidiol into the prefrontal cortex: Reduced dopaminergic modulation and immediate gene expression in limbic circuits.

Neuroscience 2017 05 24;350:85-93. Epub 2017 Mar 24.

Brain Institute, Federal University of Rio Grande do Norte, Natal - RN, Brazil. Electronic address:

The prefrontal cortex (PFC), amygdala and hippocampus display a coordinated activity during acquisition of associative fear memories. Evidence indicates that PFC engagement in aversive memory formation does not progress linearly as previously thought. Instead, it seems to be recruited at specific time windows after memory acquisition, which has implications for the treatment of post-traumatic stress disorders. Cannabidiol (CBD), the major non-psychotomimetic phytocannabinoid of the Cannabis sativa plant, is known to modulate contextual fear memory acquisition in rodents. However, it is still not clear how CBD interferes with PFC-dependent processes during post-training memory consolidation. Here, we tested whether intra-PFC infusions of CBD immediately after or 5h following contextual fear conditioning was able to interfere with memory consolidation. Neurochemical and cellular correlates of the CBD treatment were evaluated by the quantification of extracellular levels of dopamine (DA), serotonin, and their metabolites in the PFC and by measuring the cellular expression of activity-dependent transcription factors in cortical and limbic regions. Our results indicate that bilateral intra-PFC CBD infusion impaired contextual fear memory consolidation when applied 5h after conditioning, but had no effect when applied immediately after it. This effect was associated with a reduction in DA turnover in the PFC following retrieval 5days after training. We also observed that post-conditioning infusion of CBD reduced c-fos and zif-268 protein expression in the hippocampus, PFC, and thalamus. Our findings support that CBD interferes with contextual fear memory consolidation by reducing PFC influence on cortico-limbic circuits.
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http://dx.doi.org/10.1016/j.neuroscience.2017.03.019DOI Listing
May 2017

Counteraction by nitric oxide synthase inhibitor of neurochemical alterations of dopaminergic system in 6-OHDA-lesioned rats under L-DOPA treatment.

Neurotox Res 2014 Jan 27;25(1):33-44. Epub 2013 Jun 27.

Department of Morphology, Physiology and Pathology, School of Odontology, University of São Paulo, Campus Ribeirão Preto, Av. Café S/N, Ribeirão Preto, SP, 14040-904, Brazil,

Nitric oxide synthase inhibitors reduce L-3, (Del-Bel et al., Cell Mol Neurobiol 25(2):371-392, 2005) 4-dihydroxyphenylalanine (L-DOPA)-induced abnormal motor effects subsequent to depletion of dopaminergic neurons in rodents and non-human primates. The present study used quantitative high-performance liquid chromatography to analyze, for the first time, dopamine metabolism in striatum of rats in order to elucidate the mechanism of action of the nitric oxide synthase inhibitors. Adult male Wistar rats received unilateral microinjection of saline (sham) or 6-hydroxydopamine (6-OHDA-lesioned) in the medial forebrain bundle. Past 3 weeks, rats were treated during 21 days with L-DOPA/benserazide (30 mg/kg/7.5 mg/kg, respectively, daily). On the 22nd day rats received an intraperitoneal (i.p.) injection of either vehicle or 7-nitroindazole, a preferential neuronal nitric oxide synthase inhibitor before L-DOPA. Abnormal involuntary movements and rotarod test were assessed as behavioral correlate of motor responses. Lesion intensity was evaluated through tyrosine hydroxylase immunohystochemical reaction. Dopamine, 3,4-dihydroxyphenylacetic acid (DOPAC), and an extent of dopamine striatal tissue levels/dopamine metabolism were measured in the striatum. Lesion with 6-OHDA decreased dopamine, DOPAC, and DOPAC/dopamine ratio in the lesioned striatum. L-DOPA treatment induced abnormal involuntary movements and increased DOPAC/dopamine ratio (nearly five times) in the lesioned striatum. L-DOPA-induced dyskinesia was mitigated by 7-nitroindazole, which also decreased dopamine turnover, dopamine and DOPAC levels. Our results revealed an almost two times increase in dopamine content in the non-lesioned striatum of 6-OHDA-lesioned rats. Reduction of striatal DOPAC/dopamine ratio in dyskinetic rats may suggest an increase in the dopamine availability. Our data confirm contribution of nitrergic transmission in the pathogenesis of L-DOPA-induced dyskinesia with potential utilization of nitric oxide synthase inhibitors for treatment.
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http://dx.doi.org/10.1007/s12640-013-9406-3DOI Listing
January 2014

Prenatal stress produces sex differences in nest odor preference.

Physiol Behav 2012 Feb 20;105(3):850-5. Epub 2011 Oct 20.

Departamento de Fisiologia, Instituto de Ciências Básicas da Saúde, Universidade Federal do Rio Grande do Sul, Sarmento Leite, 500, Porto Alegre, RS, CEP 90050-170, Brazil.

Prenatal stress (PS) and early postnatal environment may alter maternal care. Infant rats learn to identify their mother through the association between maternal care and familiar odors. Female Wistar rats were exposed to restraint stress for 30 min, 4 sessions per day, in the last 7 days of pregnancy. At birth, pups were cross-fostered and assigned to the following groups: prenatal non-stressed mothers raising non-stressed pups (NS:NS), prenatal stressed mothers raising non-stressed pups (S:NS), prenatal non-stressed mothers raising stressed pups (NS:S), prenatal stressed mothers raising stressed pups (S:S). Maternal behaviors were assessed during 6 postpartum days. On postnatal day (PND) 7, the behavior of male and female pups was analyzed in the odor preference test; and noradrenaline (NA) activity in olfactory bulb (OB) was measured. The results showed that restraint stress increased plasma levels of corticosterone on gestational day 15. After parturition, PS reduced maternal care, decreasing licking the pups and increasing frequency outside the nest. Female pups from the NS:S, S:NS, S:S groups and male pups from the S:S group showed no nest odor preference. Thus, at day 7, female pups that were submitted to perinatal interventions showed more impairment in the nest odor preference test than male pups. No changes were detected in the NA activity in the OB. In conclusion, repeated restraint stress during the last week of gestation reduces maternal care and reduces preference for a familiar odor in rat pups in a sex-specific manner.
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http://dx.doi.org/10.1016/j.physbeh.2011.10.012DOI Listing
February 2012

Effect of different doses of estrogen on the nigrostriatal dopaminergic system in two 6-hydroxydopamine-induced lesion models of Parkinson's disease.

Neurochem Res 2011 Jun 24;36(6):955-61. Epub 2011 Feb 24.

Laboratório de Neurofisiologia, Departamento de Fisiologia, Universidade Federal do Paraná, Curitiba, PR 81.531-990, Brazil.

Parkinson's disease results from a degeneration of dopaminergic neurons of the substantia nigra pars compacta (SNpc) and it is more prevalent in men than in women. Estrogen has neuroprotective action of the nigrostriatal dopaminergic (NSDA) neurons. It was investigated whether differences in plasma 17β-estradiol (E2) levels alter the degree of neuroprotection in NSDA neurons. Ovariectomized rats, implanted with subcutaneous capsules containing 400, 800 or 1,600 μg of E2 or corn oil, were injected with 1 μg of 6-OHDA in the SNpc or the medial forebrain bundle (MFB). Striatal dopamine (DA), 3,4-dihydroxyphenylacetic acid (DOPAC) and plasma E2 levels were measured. Only at 400 μg, E2 protected striatal DA against lesion of the MFB. In the SNpc, E2 failed to prevent DA depletion, but increased DOPAC/DA ratio in the striatum. In an NSDA moderate lesion, E2 has a neuroprotective action. In a severe lesion, E2 could stimulate DA activity in remaining neurons.
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http://dx.doi.org/10.1007/s11064-011-0428-zDOI Listing
June 2011

Evaluation of estrogen neuroprotective effect on nigrostriatal dopaminergic neurons following 6-hydroxydopamine injection into the substantia nigra pars compacta or the medial forebrain bundle.

Neurochem Res 2008 Jul 9;33(7):1238-46. Epub 2008 Feb 9.

Laboratório de Neurofisiologia, Departamento de Fisiologia, Universidade Federal do Paraná, C.P. 19 031, 81 531-990, Curitiba, PR, Brazil.

Studies involving estrogen treatment of ovariectomized rats or mice have attributed to this hormone a neuroprotective effect on the substantia nigra pars compacta (SNpc) neurons. We investigated the effect of estradiol replacement in ovariectomized rats on the survival of dopaminergic mesencephalic cell and the integrity of their projections to the striatum after microinjections of 1 microg of 6-hydroxydopamine (6-OHDA) into the right SNpc or medial forebrain bundle (MFB). Estradiol replacement did not prevent the reduction either in the striatal concentrations of DA and metabolites or in the number of nigrostriatal dopaminergic neurons following lesion with 1 microg of 6-OHDA into the SNpc. Nevertheless, estradiol treatment reduced the decrease in striatal DA following injection of 1 microg of 6-OHDA into the MFB. Results suggest therefore that estrogen protect nigrostriatal dopaminergic neurons against a 6-OHDA injury to the MFB but not the SNpc. This may be due to the distinct degree of lesions promoted in these different rat models of Parkinson's disease.
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http://dx.doi.org/10.1007/s11064-007-9575-7DOI Listing
July 2008

Effects of neonatal handling on central noradrenergic and nitric oxidergic systems and reproductive parameters in female rats.

Neuroendocrinology 2008 6;87(3):151-9. Epub 2007 Dec 6.

Laboratório de Neuroendocrinologia do Comportamento, Departamento de Fisiologia, Instituto de Ciências Básicas da Saúde, Universidade Federal do Rio Grande do Sul, Porto Alegre, RS, Brazil.

Early-life environmental events that disrupt the mother-pup relationship may induce profound long-lasting changes on several behavioral and neuroendocrine systems. The neonatal handling procedure, which involves repeated brief maternal separations followed by experimental manipulations, reduces sexual behavior and induces anovulatory estrous cycles in female rats. On the afternoon of proestrus, neonatally handled females show a reduced surge of luteinizing hormone (LH) and an increased content of gonadotropin-releasing hormone in the medial preoptic area (MPOA). In order to detect the possible causes for the reduced ovulation and sexual behavior, the present study aimed to analyze the effects of neonatal handling on noradrenaline (NA) and nitric oxide (NO) levels in the MPOA on the afternoon of proestrus. Neonatal handling reduced MHPG (NA metabolite) levels and MHPG/NA ratio in the MPOA, indicating decreased NAergic activity. Additionally, neonatal handling decreased NO levels, as measured by the metabolites (NO(x)), nitrite and nitrate in the same period. We may conclude that the neonatal handling procedure decreased activity of the NAergic and NOergic systems in the MPOA during proestrus, which is involved in the control of LH and FSH secretion, and this may possibly explain the anovulatory estrous cycles and reduced sexual behavior of the neonatally handled female rats.
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http://dx.doi.org/10.1159/000112230DOI Listing
June 2008

Pargyline effect on luteinizing hormone secretion throughout the rat estrous cycle: correlation with serotonin, catecholamines and nitric oxide in the medial preoptic area.

Brain Res 2007 Apr 20;1142:37-45. Epub 2007 Jan 20.

Departamento de Fisiologia, Faculdade de Medicina de Ribeirão Preto, Universidade de São Paulo, Ribeirão, Preto, SP, Brazil.

The neurons that produce gonadotrophin-releasing hormone (GnRH) are mainly found in the medial preoptic area (MPOA) and constitute a common final pathway to the control of luteinizing hormone (LH) surge on proestrus. The control of GnRH secretion depends on several neurotransmitters, such as serotonin (5-HT), noradrenaline (NA), dopamine (DA) and nitric oxide (NO). The aim of this work was to study the profile of 5-HT, catecholamines and their main metabolites in the MPOA throughout the estrous cycle and their interactions with NO system in this area to control LH surge. For this purpose, the following were evaluated: (I) the effect of pargyline (a monoamine oxidase inhibitor) acute treatment on plasma LH secretion throughout the estrous cycle, correlated with changes of 5-HT, DA and NA content as well as activity and expression of neuronal NO synthase (nNOS) within MPOA; (II) the effect of 5,7-dihydroxitriptamine (a drug that depletes 5-HT) microinjection into MPOA on plasma LH in ovariectomized rats treated with oil, estradiol (E(2)) or E(2) plus progesterone (P(4)). Pargyline prevented LH surge on proestrus without altering its basal secretion. Throughout the estrous cycle, pargyline augmented both 5-HT and DA contents in approximately 300% and NA content in 50% in the MPOA. During proestrus, pargyline stimulated nNOS activity at 9 h and inhibited it at 11 h. nNOS expression was inhibited by pargyline at 15 h. Depletion of 5-HT content in the MPOA increased LH secretion in ovariectomized rats treated with E(2) plus P(4), but it did not modify in rats treated with either oil or E(2). Therefore, the present data show that pargyline treatment can inhibit proestrus LH surge through a mechanism that may involve 5-HT and NO systems in the MPOA. Moreover, the effect of 5-HT in the MPOA for limiting LH surge seems to depend on plasma levels of E(2) and P(4).
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http://dx.doi.org/10.1016/j.brainres.2007.01.045DOI Listing
April 2007

Role of the locus coeruleus in the prolactin secretion of female rats.

Brain Res Bull 2004 May;63(4):331-8

Departamento de Fisiologia, Faculdade de Medicina de Ribeirão Preto, Universidade de São Paulo, Av. Bandeirantes 3900, CEP 14049-900 Ribeirão Preto, SP, Brazil.

Since locus coeruleus (LC) lesion blocks preovulatory prolactin surge, the aim of this study was to determine if this lesion would also block prolactin surges induced by steroids in ovariectomized rats and would modify basal prolactin secretion. To determine the time of the steroid-induced prolactin surges, ovariectomized rats treated with estradiol (OVE) or estradiol and progesterone (OVEP) were cannulated at 08:00 h and blood samples were collected hourly between 14:00 and 18:00 h. Ovariectomized rats treated with oil (OV-Oil) were used as control. Prolactin peaked at 16:00 h in OVE rats and at 15:00 h in OVEP. In a second experiment, male rats, cycling rats, OVE, OVEP, and OV-Oil groups were cannulated at 08:00 h, followed by LC lesion or sham-surgery. Blood samples were withdrawn at times of basal and peak prolactin levels. LC lesion blocked afternoon prolactin surges of OVE, OVEP and proestrus rats. However, the low levels observed at 16:00 h in OV-Oil, diestrus and male rats as well as at 11:00 h in OVE, OVEP, estrus, and proestrus rats were not modified by LC lesion. The high prolactin levels observed on estrus afternoon were dramatically reduced by LC lesion. Data suggest that LC neurons are important for steroid-induced prolactin surge genesis, but not for prolactin basal secretion.
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http://dx.doi.org/10.1016/j.brainresbull.2004.04.003DOI Listing
May 2004

A secondary surge of prolactin on the estrus afternoon.

Life Sci 2004 Jul;75(8):911-22

Faculdade de Medicina de Ribeirão Preto, Departamento de Fisiologia, Universidade de São Paulo, Ribeirão Preto, SP, Brazil.

It has been described that throughout the estrous cycle of the rat, plasma prolactin (PRL) is basal except on proestrus afternoon when a preovulatory surge occurs. However, there have been controversies about PRL levels on the estrus day. Thus, the aim of this study was to evaluate the existence of a secondary surge of PRL on estrus afternoon and correlate it with plasma estradiol levels. The jugular vein of cycling rats was cannulated at 14:00 h on proestrus and a blood sample was withdrawn at 17:00 h for plasma LH measurement and determination of the preovulatory LH surge occurrence. In order to exclude the regular cycling rats that do not present the gonadotropins preovulatory surge and do not ovulate, only rats showing the LH surge on proestrus were considered in this study. Blood samples were collected hourly during estrus from midnight to 9:00 h (group 1) and from 10:00 to 18:00 h (group 2). In group 1, PRL showed a descending profile from midnight to 9:00 h, whereas the estradiol concentrations were constant. In group 2, a secondary surge of PRL was observed in 20 of 25 (80%) rats and plasma estradiol remained constant, but was higher in animals with the PRL surge. Thus the present data suggest the occurrence of a secondary surge of PRL in the afternoon of estrus that seems to be related to plasma estradiol levels of estrus day, which might exert only a permissive role in this surge generation.
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http://dx.doi.org/10.1016/j.lfs.2004.01.027DOI Listing
July 2004

A method to study preovulatory surges of gonadotropins.

Brain Res Brain Res Protoc 2003 Aug;12(1):41-8

Departamento de Fisiologia, Faculdade de Medicina de Ribeirão Preto, Universidade de São Paulo, Ribeirão Preto, São Paulo, Brazil.

The aim of this study was to describe and validate a method to evaluate the preovulatory surges of gonadotropins in rats submitted to anesthesia and implantation of a jugular vein cannula in the morning of proestrus and to withdrawal of serial blood samples in the afternoon of the same day. In experiment I, to choose an adequate anesthetic, cycling female rats were anesthetized in the morning of proestrus (10:00-11:00 h) with tribromoethanol, ketamine/xylazine or tiletamine/zolazepam and a Silastic cannula was implanted into the jugular vein. Blood samples (0.6 ml) were withdrawn hourly between 12:00 and 18:00 h of the same day and, on estrus morning, the rats were decapitated and the number of ova was counted. The preovulatory gonadotropin surges as well as ovulation occurred in rats anesthetized with tribromoethanol, while they were prevented by ketamine/xylazine or tiletamine/zolazepam. To investigate if the jugular cannulation under tribromoethanol anesthesia and serial blood sampling performed in experiment I altered the magnitude of the gonadotropin surges and the number of ova, intact rats (control) or rats anesthetized with tribromoethanol followed or not by jugular vein cannulation were decapitated at 16:00 h of proestrus and in the morning of estrus. The magnitude of preovulatory gonadotropin surges and the number of ova were not different among groups. Thus, since neither tribromoethanol nor surgical procedures or serial blood sampling altered the preovulatory gonadotropin surges or the ovulation process, this method seems to be suitable for this sort of study in rats.
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http://dx.doi.org/10.1016/s1385-299x(03)00070-9DOI Listing
August 2003
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