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Biology of Reproduction 60, 65-71 (1999)
©Copyright 1999 Society for the Study of Reproduction, Inc.

Concurrent Pulsatile Secretion of Luteinizing Hormone and Follicle-Stimulating Hormone during Different Phases of the Estrous Cycle and Anestrus in Beagle Bitches

Hans S. Kooistra1,a, Auke C. Okkensa, Mart M. Beversb, Corrie Popp-Snijdersc, Bas van Haaftena, Steph J. Dielemanb, and Joop Schoemakerc

a Department of Clinical Sciences of Companion Animals and b Department of Herd Health and Reproduction,Faculty of Veterinary Medicine, Utrecht University, NL-3508 TD Utrecht, The Netherlands c Research Institute for Endocrinology, Reproduction and Metabolism, University Hospital, Vrije Universiteit,Amsterdam, The Netherlands


   ABSTRACT
TOP
 ABSTRACT
INTRODUCTION
 MATERIALS AND METHODS
 RESULTS
 DISCUSSION
 REFERENCES
 
The 6-h secretory profiles of LH and FSH and the possible concordance between the episodic release of LH and FSH were studied in 6 beagle bitches during early, mid-, and late anestrus and during the follicular and luteal phases of the estrous cycle. Plasma samples were obtained at 10-min intervals via jugular venipuncture. In all stages of anestrus and in the luteal phase, FSH and LH secretion was pulsatile. All FSH pulses coincided with LH pulses. However, the mean duration of the FSH pulse (115 min) was significantly longer than that of the LH pulse (72 min). The basal plasma LH concentration was low compared with the maximum peak levels, whereas FSH pulses were characterized by relatively low peaks compared with the basal levels. In contrast to the basal plasma LH levels and the area under the curve (AUC) for LH, the basal plasma FSH levels and the AUC for FSH increased significantly as anestrus progressed. During the follicular phase, the secretory pattern of LH was characterized by frequent increases of short duration. During this phase, the basal plasma FSH concentration was relatively low, whereas the basal plasma LH level was high in comparison with that in the other phases of the estrous cycle. The luteal phase was characterized by an increased frequency of LH pulses, a shorter duration of the LH peaks, and a tendency to a lower amplitude of both LH and FSH peaks compared with values observed during anestrus. It is concluded that in the bitch, FSH and LH pulses are released in concordance and that progression from early to late anestrus is associated with an increase in basal plasma FSH concentration without a concomitant rise in basal plasma LH concentrations. The latter suggests that in the bitch an increase in circulating FSH should be considered to be a critical event required for the initiation of ovarian folliculogenesis and consequently for the termination of anestrus.


   INTRODUCTION
TOP
 ABSTRACT
 INTRODUCTION
MATERIALS AND METHODS
 RESULTS
 DISCUSSION
 REFERENCES
 
The gonadotropins LH and FSH are heterodimers consisting of two noncovalently bound subunits: a common {alpha} subunit and a hormone-specific ß subunit. Unlike the other hormones of the pituitary anterior lobe, each secreted by a unique cell type, LH and FSH are secreted by the same pituitary cell type, the gonadotrophs. The primary stimulator of the synthesis and pulsatile secretion of both LH and FSH is the decapeptide GnRH. GnRH is released from the median eminence of the hypothalamus in a pulsatile manner and reaches the gonadotrophs via capillaries of the pituitary portal system [1]. Consequently, it might be expected that FSH and LH molecules are discharged concomitantly by the gonadotrophs, as has indeed been demonstrated in humans [2–5], rats [6], horses [7, 8], deer [9], and cattle [10].

However, in most of these, species differential secretion of LH and FSH has also been demonstrated, indicating the presence of regulatory mechanisms that allow independent secretion of LH and FSH. One mechanism for differential control of LH and FSH is gonadal feedback. Both estradiol and inhibin can specifically suppress FSH synthesis and secretion [11, 12]. Other important factors in gonadotropin control are the frequency and amplitude of GnRH pulses, which have been shown to differentially alter LH and FSH gene expression as well as the secretion of these hormones [13, 14]. In addition, a specific hypothalamic FSH-releasing decapeptide has recently been demonstrated in the rat [15].

Gonadotropins act on the ovary to stimulate ovarian hormone secretion. Granulosa, theca, interstitial, and luteal cells are capable of secreting hormones in response to LH and FSH. The type and amount of hormone released will vary according to the morphological status of the follicle and corpus luteum. The secretory pattern of LH and FSH, together with the morphologic and secretory changes in the ovaries, will determine the species-specific configuration of the estrous cycle. The estrous cycle of the domestic bitch is characterized by extended periods of proestrus and estrus, both with an average duration of 9 days, and a metestrus with an average duration of about 2 mo, irrespective of pregnancy [16]. A nonseasonal anestrus of variable duration (2–10 mo) follows each estrous cycle [17, 18]. Endocrine changes leading to a new follicular phase in the bitch are poorly understood. An increasing pituitary secretion of LH and FSH has been reported to occur during the progression of anestrus [19, 20]. This may be due to an increasing release of GnRH by the hypothalamus [21] together with an increase in the sensitivity of the pituitary to GnRH from early to late anestrus [22]. In addition, an increase in ovarian responsiveness to gonadotropins [23], increased circulating basal LH concentrations [19], and a brief period of increased LH pulsatility [24] have been reported as important determinants in the start of a new follicular phase. Through characterization of the endocrine events occurring during anestrus, a better understanding of the factors that initiate a new follicular phase in the bitch may be obtained.

In contrast to the situation for other mammals, little is known about the characteristics of gonadotropin secretion in the bitch. There is evidence that LH is secreted in a pulsatile manner in the bitch [18, 24, 25]. Mainly due to technical limitations with regard to the specific identification of canine FSH, there is very little information on the pattern of secretion of FSH in this species; but Concannon [18] presented data indicating that it is also pulsatile. So far there is no information on the possible concurrent or differential secretion of LH and FSH in the dog.

The present study was designed to investigate the patterns of secretion of LH and FSH, as well as the possible concordance between the episodic release of FSH and that of LH, during different phases of the estrous cycle and anestrus in the bitch.


   MATERIALS AND METHODS
TOP
 ABSTRACT
 INTRODUCTION
 MATERIALS AND METHODS
RESULTS
 DISCUSSION
 REFERENCES
 
Animals and Collection of Blood Samples

Six healthy beagle bitches, 3–5 yr of age, were used in this study, which was approved by the Ethical Committee of the Faculty of Veterinary Medicine, Utrecht University. All had been born and raised in the Department of Clinical Sciences of Companion Animals and were accustomed to the laboratory environment and handling procedures such as collection of blood samples. The dogs were housed singly or in pairs in indoor-outdoor runs, fed a standard commercial dog food once daily, and given water ad libitum. Investigations were conducted in accordance with the Guiding Principles for the Care and Use of Research Animals promulgated by the Society for the Study of Reproduction.

All dogs were examined three times per week for the presence of vulvar swelling and a serosanguinous vaginal discharge, which were considered to signify the onset of proestrus. Plasma concentrations of progesterone were determined three times per week from the start of proestrus until the end of the luteal phase. Day 1 was defined as the day on which the plasma progesterone concentration exceeded 16 nM, which is when ovulation was assumed to occur [26–28]. The duration of the interval between Day 1 of the preceding cycle and Day 1 of the cycle in which experiments were carried out was 221 ± 25 (mean ± SD) days. Anestrus was defined as the period from the first day following the luteal phase on which the plasma concentration of progesterone fell below 3 nM until the onset of the proestrus of the next estrous cycle.

Blood samples for determination of the secretory profiles of LH and FSH were collected from each dog between 0800 h and 1400 h, at 10-min intervals, during late anestrus (Day -33 ± 8, mean ± SD), the follicular phase (Day -8 ± 2), the luteal phase (Day +42 ± 2), early anestrus (Day +91 ± 2), and mid-anestrus (Day +140 ± 2). On the day on which the secretory profiles of LH and FSH during the follicular phase were determined, blood was also collected for measurement of the plasma concentration of estradiol. Blood samples were collected from the jugular vein, immediately placed in chilled, heparin-coated tubes, and centrifuged. Plasma was stored at -20°C until assayed.

Hormone Determinations

Plasma LH concentrations were determined by a heterologous RIA as described previously by Nett et al. [29]. A rabbit antiserum raised against ovine LH (CSU-204, kindly supplied by G.D. Niswender, Colorado State University, Fort Collins, CO), radioiodinated bLH-4 (a gift from the National Institute of Arthritis, Metabolism, and Digestive Diseases), and canine pituitary standard LER 1685-1 (a gift from Dr. L.E. Reichert, Albany Medical College, NY) were used in this assay. The intraassay and interassay coefficients of variation for values above 0.5 µg/L were 2.3% and 10.5%, respectively. The lowest detectable amount of LH was 0.3 µg/L.

Plasma FSH concentrations were determined applying a human immunometric sandwich assay (Amerlite; Amersham, Buckinghamshire, UK). Results are expressed in units of a human FSH standard (2nd International Reference Preparation 78/549). Values of FSH measured with the Amerlite assay in serum, EDTA plasma, or heparin plasma from dogs were similar. Values of FSH measured with the Amerlite assay after serial dilution of various dog samples showed good linearity down to a concentration of 0.5 U/L, indicating that in this assay, dog FSH behaves immunochemically similar to the human FSH standards. The sensitivity, i.e., the concentration of FSH that can be distinguished (p < 0.01) from a sample containing no FSH, was 0.5 U/L. The intraassay coefficient of variation was < 5%. The interassay coefficients of variation were 5% at a level of 35 U/L and 9% at a level of 3 U/L. Recovery of human FSH (assay standard preparation) added to dog samples was 103%. Possible cross-reactivity of dog LH in the FSH assay was tested by analyzing the canine pituitary standard LER 1685-1, purified by Dr. L.E. Reichert, in the FSH assay. The purified canine pituitary LH standard showed an apparent cross-reactivity in the FSH assay. However, this apparent cross-reactivity was probably due to a contamination of the LH preparation with dog FSH, as judged from the perfect parallelism of the LH preparation in the FSH assay. Even if we consider the cross-reactivity a real one, the contribution of an LH peak to a concomitant FSH peak was less than 10% of the FSH value. Plasma from hypophysectomized dogs showed FSH concentrations below 0.5 U/L.

Plasma concentrations of progesterone were determined by a previously validated RIA [28, 30]. The intraassay and interassay coefficients of variation were 11% and 14%, respectively. The lowest detectable amount was 0.13 nM.

Plasma concentrations of estradiol were determined by a solid-phase RIA using 125I (Count-A-Count TKE; Diagnostic Products Corporation, Los Angeles, CA) according to the manufacturer's instructions with slight modifications as described by Dieleman and Bevers [31] and validated for the dog by Van Haaften et al. [22]. The intraassay and interassay coefficients of variation were 14% and 11.8%, respectively. The sensitivity was 7 pM.

Data Analysis

Plasma concentrations of estradiol were determined only in samples collected during the follicular phase. Plasma concentrations of LH were determined in all samples, whereas plasma concentrations of FSH were determined in plasma samples at 10-min intervals in 2 bitches and at 20-min intervals in the other 4 bitches.

The pattern of pulses in the 6-h profiles of FSH and LH was analyzed by means of the Pulsar program developed by Merriam and Wachter [32]. The program identifies secretory peaks by height and duration from a smoothed baseline, using the assay SD as a scale factor. The cut-off parameters G1-G5 of the Pulsar program were set at 3.98, 2.40, 1.68, 1.24, and 0.93 times the assay SD as criteria for accepting peaks 1, 2, 3, 4, and 5 points wide, respectively. The smoothing time, a window used to calculate a running mean value omitting peaks, was set at 4 h. The splitting cut-off parameter was set at 2.7, and the weight assigned to peaks was 0.05. The A, B, and C values of the Pulsar program, used to calculate the variance of the assay, were set at A = 0, B = 10.5, and C = 0 for the LH assay and A = 0, B = 5, and C = 0 for the FSH assay. The values extracted from the Pulsar analyses included the mean of the smoothed baseline, the mean peak amplitude, the pulse frequency, the mean peak duration, and the area under the curve (AUC). The AUC was estimated above the zero level.

Changes in the parameters of the secretory patterns were evaluated by repeated-measures ANOVA for main effect of phase of the estrous cycle. Subsequently, multiple comparisons were performed for data with significant (p <= 0.05) main effect using the Student-Newman-Keuls test. Since the data were not assumed to be normally distributed, differences in pulse frequency were determined by nonparametric analysis, using the Friedman test, and multiple comparisons were performed using Dunnett's test. Differences in the duration of LH and FSH peaks were evaluated by paired two-tailed Student's t-tests. Values are expressed as mean ± SEM or as mean and range; p <= 0.05 was considered significant.


   RESULTS
TOP
 ABSTRACT
 INTRODUCTION
 MATERIALS AND METHODS
 RESULTS
DISCUSSION
 REFERENCES
 
During the luteal phase and anestrus, all dogs had relatively constant plasma LH and FSH levels with occasional distinct elevations, indicating pulsatile secretion of LH and FSH. Most peaks were characterized by very abrupt and rapid increases in both LH and FSH, and a slow decrease in plasma LH and, even slower, in plasma FSH concentrations. A representative example of the pulsatile secretion of LH and FSH during the various phases of the estrous cycle and anestrus is shown in Figure 1.



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  		FIG. 1. The secretory profiles of FSH (triangles) and LH (circles) in a 4-yr-old beagle bitch. Blood samples were collected at 10-min intervals for 6 h during the follicular phase, the luteal phase, and early, mid-, and late anestrus.

The duration of the FSH peaks (mean 115 min, range 70–160 min) was significantly (p < 0.01) longer than that of the LH peaks (mean 72 min, range 50–100 min). The duration of the LH peaks was significantly shorter during the luteal phase than during early and late anestrus. The duration of the FSH peaks did not differ significantly when the various stages of anestrus and the luteal phase were compared. Although the mean LH and FSH peak amplitudes during the luteal phase tended to be lower than those during the various phases of anestrus, these differences were not significant (Table 1).


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  		TABLE 1. Pulse characteristics of the 6-hour secretory profiles of LH and FSH (mean and range or mean ± SEM).

During early, mid-, and late anestrus, each of the 22 LH peaks, identified by the Pulsar program in the 6-h profiles of the 6 bitches, coincided with an FSH peak. Twelve LH peaks were identified during the luteal phase, and although each coincided with a definite increase in plasma FSH concentration, only 9 of the latter were recognized as significant FSH peaks by the Pulsar program. There were no FSH peaks without LH peaks during anestrus and the luteal phase. The frequency of LH pulses was significantly higher during the luteal phase than during the various stages of anestrus.

The mean plasma LH concentration of the smoothed baseline and the mean AUC for LH did not differ significantly when the various phases of anestrus and the luteal phase were compared. In contrast, the mean plasma FSH concentration of the smoothed baseline and the AUC for FSH during late anestrus were significantly higher than those during mid-anestrus, early anestrus, and the luteal phase (Table 1, Fig. 2).



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  		FIG. 2. The mean (± SEM) plasma FSH and LH concentrations of the smoothed baseline in six beagle bitches during the follicular phase, the luteal phase, and early, mid-, and late anestrus. *Indicates significant difference.

During the follicular phase, the mean plasma estradiol concentration was 125 ± 26 pM (range 40–202 pM). During this phase, the secretory pattern of LH in most dogs was characterized by frequent increases of short duration (Fig. 1). However, these increases were often too small to be recognized as significant peaks by the Pulsar program. The mean plasma LH concentration of the smoothed baseline was significantly higher during the follicular phase than during the luteal phase, early anestrus, mid-anestrus, and late anestrus (Fig. 2). However, the mean AUC for LH during the follicular phase did not differ significantly from that during the luteal phase and the various phases of the anestrus. The mean plasma FSH concentration of the smoothed baseline was significantly lower during the follicular phase than during late anestrus (Fig. 2). In concordance, the mean AUC for FSH was significantly lower during the follicular phase than during the luteal phase and the various phases of anestrus (Table 1).


   DISCUSSION
TOP
 ABSTRACT
 INTRODUCTION
 MATERIALS AND METHODS
 RESULTS
 DISCUSSION
REFERENCES
 
The results of this study demonstrate the pulsatile secretion of FSH and its temporal coupling to the pulsatile secretion of LH during anestrus and the luteal phase in the bitch. The fact that FSH pulses were always concomitant with LH pulses suggests that GnRH is the sole hypothalamic releasing hormone for both LH and FSH in the bitch. Despite the coincidence of pulses of LH and FSH, there are differences in basal levels and pulse characteristics in the bitch that indicate a differential regulation of the secretion of these hormones. The basal plasma FSH concentration increased significantly as anestrus progressed, whereas the basal LH concentration did not change. The differential regulation of the two gonadotropic hormones was even more obvious during the follicular phase. In agreement with the findings of Olson et al. [19], basal plasma FSH concentrations were relatively low during this phase. As has been observed in other species, this is probably attributable to negative feedback effects of estradiol and the gonadal peptides inhibin and follistatin [12]. In contrast to the low basal plasma FSH level, we found, in agreement with the results of Hegsted et al. [33], that the basal plasma LH level during the follicular phase was high as compared with that in the other phases of the estrous cycle. LH enhances synthesis of aromatase substrates in thecal cells and is regarded as the primary regulatory factor in controlling estrogen secretion in all but the most immature of follicles [1, 34]. Consequently, especially during the follicular phase, LH levels must be adequate to stimulate the last stages of follicular development. The relatively high basal plasma LH level may be the result of the positive feedback control that estradiol exerts over pituitary LH release during this phase [35].

Although all FSH pulses coincided with LH pulses, there were some remarkable differences in pulse characteristics. First, plasma FSH concentrations declined more slowly than plasma LH concentrations, due to a longer half-life of FSH in comparison to LH. This indicates that, as in other mammals [36], the pattern of glycosylation of canine FSH differs from that of canine LH with the result that clearance of canine LH from circulation is faster [37, 38]. Secondly, the basal plasma LH concentration was low compared with the maximum peak levels, whereas FSH pulses were characterized by a relatively small magnitude of increase in circulating concentrations above the basal level. This may be explained by a different regulation of basal and pulsatile secretion of FSH and LH. Indeed, it has been reported in other mammalian species that FSH secretion is regulated by a dual mechanism, one controlling the basal and the other controlling the pulsatile component of FSH secretion [39, 40]. Another explanation may be that intracellular mechanisms for storage and release are different for FSH and LH. This view is supported by in vitro studies showing that although LH and FSH are made in the same cell type they are stored in different secretory granules [1], that newly synthesized FSH is secreted at a greater rate than LH [41], and that the magnitude of FSH secretion in response to secretagogues is smaller than that of LH [41, 42].

In agreement with the findings of Shille et al. [20, 25], we found that the basal plasma FSH level, and in addition the AUC for FSH, increased significantly during the progression of anestrus. In contrast, the basal plasma LH and the AUC for LH did not change as anestrus progressed. This indicates that an increase in FSH levels is a key event in ovarian folliculogenesis. Indeed, in most mammals studied, FSH is regarded as the most important factor in the early stages of follicular development, whereas LH is regarded as the primary regulatory factor in the more mature follicles [1, 34]. The relative importance of FSH for the early stages of follicular development is supported by two more observations. First, FSH has been identified as the major survival factor protecting early antral follicles against apoptosis [43]. Secondly, in cows, as in humans, mRNA encoding for the FSH receptor is expressed in granulosa cells of all growing follicles, whereas mRNA encoding for the LH receptor is expressed only in granulosa cells of the larger follicles and in thecal cells [44, 45]. Although the latter has not yet been demonstrated in the bitch, there are no reasons to assume a different pattern in the expression of FSH and LH receptors in this species. Consequently, it may be hypothesized that at a certain moment during anestrus, the rising plasma FSH concentrations will exceed the threshold value of the most sensitive follicles of the canine ovarian antral follicle pool, leading to an enhancement of the development of these follicles. One of the main effects of FSH is the acquisition of LH receptors in the granulosa cells. Beyond this stage, LH is progressively able to replace FSH in supporting follicular maturation [34]. This may also explain why administration of pharmacological doses of LH alone during anestrus can cause follicle growth and induce proestrus in the bitch [18, 46].

The most obvious difference between the luteal phase and the other phases of the estrous cycle is the high plasma progesterone concentration in the luteal phase. Consequently, differences in the secretory pattern of LH between the luteal phase and the various phases of anestrus are most likely due to effects of this steroid. However, in agreement with the findings of Fernandes et al. [47] and Hegsted et al. [33], the basal plasma LH concentration during the luteal phase did not differ significantly from that during the various phases of anestrus. Administration of contraceptive doses of progestins to ovariohysterectomized bitches also does not reduce basal plasma LH levels [48]. Therefore it has been suggested that in the bitch, endogenous progesterone and exogenous progestins may exert an effect on the pulsatile secretion of LH rather than on the basal LH secretion [49]. This may also explain the observed increase in LH pulse frequency, the shorter duration of the LH peaks, and the tendency to a lower amplitude of the LH peaks in the luteal phase compared with anestrus. However, pulse frequency, pulse amplitude, and pulse duration cannot be considered totally independent variables. Lambalk et al. [50] have demonstrated that LH pulse frequency correlates negatively with LH pulse amplitude. The tendency for LH peaks to have a lower amplitude in the luteal phase may therefore be a direct result of the increased LH pulse frequency during this phase. The LH pulse duration not only is the result of the half-life of LH but also depends on the pulse amplitude. The shorter duration of the LH pulses in the luteal phase may therefore also be ascribed to the lower LH pulse amplitude during this phase.

In conclusion, we have demonstrated that in the bitch, FSH and LH pulses are concordant, and that progression from early to late anestrus is associated with an increase in basal plasma FSH concentrations without a concomitant rise in basal plasma LH concentrations. The latter suggests that in the bitch, an increase in circulating FSH should be considered to be a critical event required for the initiation of ovarian folliculogenesis and consequently for the termination of anestrus.


   ACKNOWLEDGMENTS
 
The authors are grateful for the technical assistance of Mrs. D.M. Blankenstein, Mr. A.V.P. van de Poll, and Mrs. Y.W.E.A. Pollak. The authors thank Dr. W.E. van den Brom for his valuable assistance with the statistical analysis. The critical reading of the manuscript by Prof. Dr. A. Rijnberk and Dr. B.E. Belshaw is highly appreciated.


   FOOTNOTES
 
1 Correspondence: H.S. Kooistra, Department of Clinical Sciences of Companion Animals, Faculty of Veterinary Medicine, Utrecht University, PO Box 80.154, NL-3508 TD Utrecht, The Netherlands. FAX: 31 30 2518126; h.s.kooistra{at}vet.uu.nl Back

Accepted: August 25, 1998.

Received: June 4, 1998.


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 ABSTRACT
 INTRODUCTION
 MATERIALS AND METHODS
 RESULTS
 DISCUSSION
 REFERENCES
 

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