Prolactin, Follicle-Stimulating Hormone, and Luteinizing Hormone

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h on Day 5. PRL levels in serum showed a distinct, biphasic, nocturnal surge pattern. Levels during the light phase were low, with variable PRL during Day 2, ...

BIOLOGY OF REPRODUCTION 50, 1328-1333 (1994)

Prolactin, Follicle-Stimulating Hormone, and Luteinizing Hormone Levels during Preimplantation in the Djungarian Hamster (Phodopus campbellf 1 GRACE E. ERB and KATHERINE E. WYNNE-EDWARDS 2 Department of Biology, Queen's University, Kingston, Ontario, CanadaK7L 3N6 ABSTRACT The reproductive physiology of female Djungarian hamsters (Phodopus campbelli) varies in several ways from that of more conventional laboratory models. In this study we investigated serum and pituitary levels of prolactin (PRL), LH, and FSH during preimplantation pregnancy. Data were collected from independent females every 2 h from 2200 h on proestrus through 0600 h on Day 5. PRL levels in serum showed a distinct, biphasic, nocturnal surge pattern. Levels during the light phase were low, with variable PRL during Day 2, when both estrogen and progesterone are at low levels in serum. FSH and LH levels in serum were determined twice daily. Elevated FSH and LH levels were found on Day 0 (proestrus). FSH then remained at a basal level while LH began to increase, with evidence for a daily rhythm in serum LH levels. Both FSH and LH accumulated in the pituitary over the first 4 days of pregnancy, although patterns were difficult to interpret. Data were consistent with a hypothesis that ovarian follicular development and preparation for a possible ovulation occur during preimplantation.


In species with early reproductive maturity, rapid reproductive cycles, and short life spans, adaptive modification of reproductive physiology to an ecological niche is expected [1]. Expansion of studies in comparative reproductive physiology to encompass less conventional animal models has provided ample evidence that this variability exists even within apparently homogeneous groups such as small rodents [2-5]. Djungarian hamsters (Phodopus campbelli), of the family Cricetidae, are small (20-40 g) nocturnal rodents, native to the desert plains and steppes of Siberia and Northern Mongolia [6]. They have a 4-day estrous cycle and an 18-day gestation period [7], experience a fertile postpartum estrus, and show a high incidence of pregnancy block following disruption of contact with the mate [7, 8]. Although they are spontaneous ovulators, female Djungarian hamsters appear to require signals garnered from the presence of a male to initiate and maintain spontaneous cycles [9]. In addition, ovariectomized Djungarian hamster females require only physiological levels of 17{3-estradiol to show behavioral receptivity [10]. Cyclic females [10] and mating females [11] do not show the proestrous progesterone surge characteristic of other spontaneous, short estrous cycles, although females mating after a pseudopregnancy do [12]. Throughout the first 14 days of the 18-day gestation period, serum progesterone remains at typical cycle levels, then doubles as ovarian CL sustain late pregnancy and pituitary prolactin (PRL) surges resume [13]. During pregnancy, the initial response of serum steroid levels to coital stimulation occurs on Day 2 (36-48 h earlier than in the rat [14]), as serum progesterone values decrease relaAccepted February 9, 1994. Received July 26, 1993. 'This study was supported by an NSERC research grant to Dr. K.Wynne-Edwards. 2Correspondence. FAX: (613) 545-6117.

tive to the estrous cycle and relative to the progesterone content of the CL [11]. This reproductive physiology may be seen as an adaptation to rapid reproduction [13]. If so, then the endocrinology of the preimplantation progestational response may also show similar adaptations. A previous study [11] documented ovarian steroid changes during preimplantation. The present study expands the previous report by adding serum and pituitary levels of LH and FSH to that study. MATERIALS AND METHODS

The results presented in this paper are from the same population of animals as that of Erb and Wynne-Edwards [11]. Detailed methods with respect to handling of animals and sample collection are presented in that study. Sample Collection Djungarian hamsters were from a colony most recently outbred against animals trapped in Tuva, Siberia, in 1990 [6]. Animals were maintained on a 14L:1OD schedule, (lightson 0130-1530 h), at 18 - 10C to mimic burrow temperatures in the wild [15]. Animals were housed in 27 x 21 x 14-cm cages with wood-chip bedding; food and water were given ad libitum. Females and males were paired in the early afternoon irrespective of the stage of the female's estrous cycle [10]; they remained housed together until the female was sampled. Direct observation of at least one behavioral ejaculation [9] during the 4-h period of behavioral receptivity surrounding lights-off was used to define proestrus (Day 0), with Day 1 of pregnancy beginning at midnight. Sampling was conducted between 4 October 1991 and 21 May 1992. After mating, females were sampled on a time series that eventually resulted in independent groups of at least five females representing a 2-h resolution from 2000 h on the evening of proestrus (Day 0), through 0600 h on the morn-




been validated for use in Djungarian hamsters [13]. Figure 1 shows the parallelism [21] for the FSH and LH assays. These heterologous assays were also useful in the closely related Siberian hamster (Phodopus sungorus) [22]. The mean slope of the standard curve for FSH was 1.47 + 0.11

a 0: -J

(n = 5) and for LH was 1.22 + 0.68 (n = 6). Anti-rat LH


Logdose(pg/tube) orLogvolume sampled(ml)


FIG. 1. Tests for parallelism in the ovine FSH and rat LH assays against Djungarian hamster pituitary and serum pools. Pituitary pools were derived from KRBG containing sonicated pituitaries at a concentration of 2 pituitaries/ml KRBG. Serum pools were derived from a group of reproductive females. LOGIT B/Bo = Ln [B/Bo]/[1-B/B]), where B is the cpm for 0% displacement (total binding-nonspecific binding) and B is the comparable binding for the standard or sample.

ing of Day 5 of pregnancy. Females were removed from their cages and bled from the orbit of the eye [10], then killed by cervical dislocation; total handling time was limited to 20 sec to minimize stress-induced PRL surges [16,17]. Blood was collected into an unheparinized Pasteur pipette, transferred into a 1.5-ml Eppendorf microfuge tube, and allowed to clot overnight at 4°C. Clots were then removed, blood was centrifuged at 6000 rpm, 4C, for 20 min, and serum was withdrawn and stored at -20°C until assayed. Pituitaries were excised within 5-20 min of death and incubated in 0.5 ml of Krebs-Ringer bicarbonate glucose (KRBG) [18] at room temperature for 45-60 min. Tissue was sonicated, and the homogenates were stored frozen (-20°C) until assayed.

Four persons were involved in the collection of blood and sampling of Djungarian hamster females for this experiment. There was no evidence of systematic variation in PRL levels resulting from collection of the sample by different persons (serum,p = 0.27; pituitary,p = 0.71) or the order in which sampling was handled (serum, p = 0.33; pituitary, p = 0.44).

RIA Protocols used for FSH, LH, and PRL radioiodinations and RIA were modified from those of both Dr. A.F. Parlow (Pituitary Hormones and Antisera Center, Harbor-UCLA Medical Center, Los Angeles, CA) and Dr. F. Talamantes [19], detailed in Edwards et al. [13]. Ovine FSH (NIDDK-oFSH-I1/AFP5679C), rat LH (NIDDK-rLH-I-9/AFP10250C), or hamster PRL (haPRL AFP-10302E) was iodinated with the use of chloramine-T in a gaseous phase reaction [20], diluted, and stored at 4C for a maximum of 3 wk. Primary antibody (100 l1)was NIDDK-anti-oFSH-1/AFP-C528 (rabbit) at a 1:16000 working dilution, NIDDK-anti-rLHS-10/AFP-C528 (rabbit) at 1:40000, or anti-haPRL-AFP-7472988 (rat) at 1:16 000. Reference preparations were NLAMDD-oFSH-RP1, NIDDK-rLH-RP3, and haPRL-AFP10302-E. The PRL assay has

CSU-120 (rabbit), anti-ovine LH GDN-15 (rabbit)-which was parallel but is no longer available, NIADDK-anti-oLH-1 (rabbit), and NIDDK-anti-rFSH-S-11 (rabbit) were also screened, but are not shown. All PRL samples (serum and pituitary) and FSH and LH pituitary samples were assayed in duplicate. Serum FSH and LH assays required large volumes and were assayed singly, and not in every sample. Volumes assayed were 0.1-5.0 l1 for PRL; 100 il for FSH; and 150 1 for LH in serum; and 0.1-5.0 Il for each hormone in pituitary homogenate. Volumes smaller than 5.0 1l were pipetted by serial dilution. All small-volume samples were initially assayed at 1.0 1. The sensitivity limits of the assays left some samples on the curve but out of range. Each was re-assayed in duplicate at one or more dilutions until agreement between determinations at different dilutions was reliable and the sample fell on the linear portion of the standard curve. Upper and lower limits of assay sensitivity were conservatively set at 20% and 85% of total binding [11]. Values outside these limits were entered into analyses as the limiting value. By these criteria PRL was sensitive between 20 and 1600 pg/tube, FSH between 94 and 950 pg/tube, and LH between 13 and 206 pg/tube. The intraassay coefficient of variation was 8.7 for PRL, 9.4 for FSH, and 10.8% for LH. The comparable interassay coefficients of variation were 13.7%, 16.2%, and 17.4%, respectively. Values were calculated from duplicate determinations in 24 PRL and 6 FSH assays, and from quadruplicate determinations in 6 LH assays. Screening for PregnantFemales After mating occurred, behavioral observations continued on a daily basis. Remating [7], the presence of atypical embryos (e.g., single cells on Day 4), degenerating ova or embryos [23], and the absence of CL were used to screen females for successful pregnancy initiation. Because Djungarian hamster CL degenerate within less than 24 h [10, 12], these criteria detect most nonpregnant females and were used to eliminate 8.6% of the females from the study. A further 3.8% of the females were eliminated from pituitary analyses when the pituitary was not successfully harvested. Data Analyses To identify peaks and troughs in serum PRL, the statistically independent means obtained every 2 h were compared to the global mean by use of a t-test against the mean. This test has no error estimate on the global mean (the sample size gives high confidence in the value) and iden-



FIG. 2. Mean + SE serum PRL, FSH, and LH levels as measured by RIA between 2200 h on Day 0 (proestrus) and 0600 h on Day 5 of pregnancy. For PRL measurements, N -5 females/point, whereas for FSH and LH measurements, N = 3-5 females/point. Dark bars and shaded areas denote the dark phase of the light:dark cycle. Horizontal dashed lines show the lower limit of assay sensitivity. Mating occurred between 1600 and 2000 h on Day 0.

tifies cases where double the sample standard deviation does not include that mean. One-factor ANOVA was used to detect trends over time with Tukey's multiple comparison test as the post hoc test for significant differences between times (p - 0.05 for all analyses). RESULTS Serum Levels of PRL, FSH, and LH Results of PRL determinations in serum are shown in Figure 2a (ANOVA,p < 0.001). Large error estimates (SEM) on each sample are a result of the serial dilutions and serum determinations from small volumes. However, the changes seen encompass several orders of magnitude and are statistically robust. The initial PRL value at 2200 h on Day 0 was over 350 ng/ml. Within 16 h, values decreased to nadir levels of about 1 ng/ml, and a few samples were below assay detection limits (Fig. 2a). By the later half of Day 1, a PRL surge was initiated followed by another surge early on Day 2. This general pattern of a peak in PRL prior to lights-on followed by decreased PRL values during the day and a second surge just prior to lights-off was repeated on

SE pituitary PRL, FSH, and LH levels as measured by FIG. 3. Mean RIA (N -3-5 females/sample point) between 2200 h on Day 0 (proestrus) and 0600 h on Day 5 of pregnancy. Dark bars and shaded areas denote the dark phase of the light:dark cycle. Horizontal dashed lines show the lower limit of assay sensitivity. Mating occurred between 1600 and 2000 h on Day 0.

both Days 3 and 4. Mean light phase values were similar + 29.1; 133.4 each day (142.3 + 35.1; 142.6 ± 29.8; 137.5 + 28.0; NS), but Day 2 was most variable, with both nadir and surge values during mid-day. Peaks, except for 1400 h on Day 2 and 1800 h on Day 1, were all significantly different from the global mean (181.2, N = 248), but not from each other. Samples near the lower limit of sensitivity were also significantly different from the mean, and may have been considerably lower than shown. Serum FSH levels are shown in Figure 2b (ANOVA, p < 0.001). Elevated serum FSH was found late on Day 0 (proestrus) and through the next day. By the next sample (2200 h on Day 1), the values were significantly lower and remained stable. Limits of assay sensitivity were not reached in these analyses. Both the two highest and the two lowest samples were significantly different from the mean (4.32, N = 34). Serum LH levels are shown in Figure 2c (ANOVA, p = 0.44). Mean serum LH concentration decreased from late on Day 0 to a minimum early on Day 1, with the assay not sensitive enough for accurate determinations. Actual values


may have been significantly lower than those shown. In subsequent samples, serum LH at dusk was consistently below the detection limits of the assay, whereas samples taken at dawn were assayable, but variable. Application of assay limits decreased the variance associated with low-concentration samples and precluded comparisons against the mean (136.6, N = 44). Pituitary Levels of PRL, FSH, and LH

Figure 3 shows the mean concentrations of PRL, FSH, and LH extracted from pituitary tissue. In each case, the ANOVA detected significant changes in pituitary hormone content over time (p < 0.005). All pituitary PRL values fell within the range of the assay. Only the maximum value (5.5 + 0.9 Ixg/pituitary on Day 3 at 1600 h) was significantly different from the two lowest samples (0.42 + 0.10 Ig/ pituitary on Day 2 at 0600 h and 0.06 ± 0.15 at 0200 h on Day 3) (Fig. 3a). The overall pattern was complex, with alternating periods of stable low levels and periods of sustained high levels of pituitary PRL. All mean values below 1.5 Lg, except three with a reduced sample size, were significantly different from the mean (2.54, N = 243). Only three of the highest values on Days 3 and 4 were significantly different from the mean, and each had a comparatively large sample size. There was no clear relationship between serum PRL and pituitary PRL. High and low levels were sometimes synchronous and sometimes opposite. The initial value of FSH in pituitary extract, at 2200 h on Day 0, was the minimum seen (9.2 ± 2.9 ng/pituitary); the maximum occurred on Day 3 at 0200 h (33.2 2.7 ng/ pituitary). After 1200 h on Day 3, pituitary FSH levels were stable. During previous days, both high and low levels of pituitary FSH were found, with no clear daily pattern. As a result of the poor resolution in the serum FSH data, no direct correlation with pituitary was detected. Four of the six highest FSH levels, and the minimum level, were significantly different from the mean (23.0, N = 129). Levels of LH found in pituitary tissue were stable and low for the first 42 h of pregnancy, after which values increased up to 6-fold (Fig. 3c). Both high and low pituitary LH concentrations were found on Days 3 and 4. Maximum LH concentrations in pituitary tissue were 123.7 ± 15.2 ng/ pituitary on Day 4 at 0200 h, while a minimum value of 26.7 2.6 ng/pituitary was obtained on Day 1 at 000 h. Samples with mean values near or above 100 ng/ml were significantly higher than all samples prior to lights-off on the evening of Day 2. Comparisons against the mean (63.5, N = 124) showed the same pattern. Although serum LH resolution was poor, the patterns in pituitary and serum were similar. For the first 2 days, pituitary LH levels were stable while pituitary FSH levels were variable. Over the subsequent 2 days the pattern was reversed, with pituitary FSH levels stable and pituitary LH levels variable.



The rise in estrogen that begins on diestrus and reaches a peak on proestrus is believed to be the primary stimulus for the proestrous surge of PRL and LH [14]. If vaginal stimulation occurs during the period of behavioral receptivity on proestrus, PRL surges are initiated [24]. While PRL surges persist, CL progesterone secretion is maintained for a length of time approaching that in species with longer estrous cycles [25]. A biphasic pattern of PRL release occurs after vaginal stimulation in the rat [14] and mouse [26], one nocturnal and one diurnal surge, while golden hamsters have only one daily surge of PRL, which is nocturnal [27]. The physiological significance of the two daily PRL surges during the first half of gestation is unknown [28], although it is clear that the most sensitive times for the induction of pregnancy-blocking responses are during PRL surges [29]. These data show that PRL secretion throughout preimplantation pregnancy in the Djungarian hamster is also biphasic, with one surge occurring just prior to lights-off and another just prior to lights-on, in a pattern similar to that in the mouse [26]. PRL, LH, and FSH are all required to some extent for optimal luteal function in the pregnant golden hamster, rat, and mouse [14, 30, 31]. PRL is the initial luteotropic stimulus, which converts the CL into functional CL of pregnancy or pseudopregnancy, whereas LH and FSH levels are not different from those during an estrous cycle [14,31,32]. The nocturnal PRL surge on Day 3 of pregnancy (where Day 0 equals the day of mating) precedes the divergence of serum progesterone levels from those of the estrous cycle [14]. Serum progesterone levels in Djungarian hamsters during pregnancy begin to diverge from those of the estrous cycle on the evening of Day 2 [11], 24 h earlier than in the rat. PRL secretion during the light phase on Day 2 in Djungarian hamsters differed from that on the other days studied by including high levels during mid-day, rather than in the early morning and late evening. The average level of PRL during the light phase was not affected, but the temporal pattern may be luteotropic. The light phase of Day 2 is also the time of unexpectedly low progesterone levels in serum [11], and high sensitivity to pregnancy block [7]. In the rat and golden hamster, serum concentrations of LH and FSH surge during the afternoon of proestrus [33,34]. LH levels return to baseline, but FSH levels remain elevated through noon of the next day and are responsible for recruiting the follicles that will ovulate 4 days later [14, 35]. Djungarian hamsters also have biphasic FSH in serum during preimplantation. After pregnancy block, Djungarian hamsters have a fertile ovulation as if estrous cyclicity had not been disrupted [7, 8]. For this to occur, a wave of follicular development within the ovary during preimplantation pregnancy is needed. Although there is no evidence of an ovulatory LH surge on Day 4 of pregnancy, several factors could reflect preparation for a second ovulation: the



accumulation of FSH and LH in serum, indications that serum LH varies with a daily pattern of increasing amplitude, and the transition between variable pituitary FSH levels for the first 2 days of pregnancy and variable pituitary LH levels during the next 2 days of pregnancy. The two daily PRL surges are sensitive to photoperiod and are under separate control [28]. In most rodents, estrogen is required for maintenance of the diurnal surge whereas progesterone is required for maintenance of the nocturnal surge [24, 28]. The mechanisms by which estrogens stimulate PRL release, however, may differ in other mammals [36]. Circulating levels of estrogen are low throughout preimplantation in the Djungarian hamster [11], but do not preclude involvement of estradiol or another estrogen in the regulation of PRL. Djungarian hamsters exhibit sensitive and widespread pregnancy-blocking responses to mate removal and lack of prior familiarity with the mate [8]. These pregnancy blocks are adaptive if a pregnancy has a low probability of success [37], which, in Djungarian hamsters, means a pregnancy with a low probability of paternal care during lactation [7, 38]. The most sensitive periods found for pregnancy-blocking responses in Djungarian hamsters are during mating [8] and within the first 24-48 h of pregnancy [7]. At each of these times, serum progesterone is low [10, 11], and, during the light phase of Day 2, the temporal pattern of PRL is also different from that on other days. In species with strong selection for rapid reproduction, accurate discrimination between a pregnancy and a pseudopregnancy, and early termination of pregnancies with a low probability of success, would be adaptive advantages. While not conclusive about the causal relationships, this study suggests that Day 2 may represent a sensitive window for pregnancy-blocking responses prior to endocrine commitment to the pregnancy. ACKNOWLEDGMENTS We would like to thank Heather Edwards, Kathy Jenkins, Laura Mucklow, and Charlotte Tweedie for their late (all) night help. NIDDK supplied the hormones for iodination, antiserum, and reference preparations for rat FSH, ovine FSH, rat LH, and rat PRL. LH antisera GDN-15 and CSU-120 were provided by G.D. Niswender, and A.F. Parlow supplied the hamster PRL kit. Some of the initial gonadotropin validations were undertaken while K.E. Wynne-Edwards was a Lalor Postdoctoral Fellow with P.F. Terranova at the University of Kansas Medical Center. We would also like to thank NJ. MacLusky for his assistance with statistical pulse analyses.

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PREIMPLANTATION PRL, FSH, AND LH IN PHODOPUS 33. Blake CA, Kelch RP. Administration of antiluteinizing hormone-releasing hormone serum to rats: effects on periovulatory secretion of luteinizing hormone and follicle-stimulating hormone. Endocrinology 1981; 109:2175-2179. 34. Rush ME, Ashiru OA, Blake CA Effects of complete hypothalamic deafferentation on the estrous phase of follicle-stimulating hormone release in the cyclic rat. Biol Reprod 1982; 26:399-403. 35. Greenwald GS, Siegel HI. Is the first or second periovulatory surge of FSH responsible for follicular recruitment in the hamster? Proc Soc Exp Biol Med 1982; 170:225-230.


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