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Poult Sci 2006. 85:1769-1774
© 2006 Poultry Science Association
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PHYSIOLOGY, ENDOCRINOLOGY, AND REPRODUCTION

Activity of Three-ß-Hydroxysteroid Dehydrogenase in Granulosa Cells Treated in Vitro with Luteinizing Hormone, Follicle-Stimulating Hormone, Prolactin, or a Combination1

H. Taira and M. M. Beck2

Department of Animal Science, University of Nebraska, Lincoln 68583-0908

2 Corresponding author: mbeck1{at}unl.edu


   ABSTRACT
TOP
 ABSTRACT
INTRODUCTION
 MATERIALS AND METHODS
 RESULTS
 DISCUSSION
 REFERENCES
 
Three-ß-hydroxysteroid dehydrogenase (3ß-HSD) is a key enzyme in the pathway that produces progesterone. Hy-Line hens (W36, W98, and Brown) were subjected to mild heat stress [36°C for 24 h (acute heat stress, AHS) or 2 wk (chronic heat stress, CHS)] or maintained at 22°C (thermoneutral, TN). Granulosa cells (GC) from the 3 largest follicles were isolated, dispersed, and incubated with luteinizing hormone (LH), follicle-stimulating hormone (FSH), prolactin (PRL), a combination, or no hormone (control), and then with pregnenolone nitro blue tetrazolium to determine 3ß-HSD activity. Treatment by LH (TN, P = 0.04; AHS, CHS, P < 0.0001) and by LH+FSH (TN, AHS, CHS, P < 0.0001) resulted in increased enzyme activity compared with the respective controls. In TN and CHS, LH+FSH increased the activity to a greater extent than LH alone (TN, P = 0.02; CHS, P = 0.0004); in AHS the increase was not significant (P = 0.29). Treatment with FSH, PRL, or LH+PRL decreased (TN, AHS) or had no effect (CHS) on 3ß-HSD activity. In TN and AHS cells, FSH and PRL reduced enzyme activity (P = 0.006 and 0.0580, respectively). When LH was added to PRL, suppression by PRL was mitigated somewhat. When LH and FSH were added to PRL, 3ß-HSD activity in AHS and CHS cells actually increased compared with the respective controls (P = 0.052 and 0.003) but remained below the activity of cells incubated with LH+FSH or LH alone. This suggests that gonadotropic actions of LH and LH+FSH are countered by the antigonadotropic action of PRL and, conversely, that PRL reduces the stimulatory action of LH and FSH. Strain differences in GC response to hormones were observed primarily in the CHS-treated birds; generally, W98 was highest; Browns showed the weakest response, and W36 was intermediate. In earlier studies, HS reduced circulating LH and GC progesterone and 3ß-HSD activity in vitro and increased circulating PRL. The results suggest a mechanism by which reduced activity of 3ß-HSD and progesterone by GC during HS might be explained, particularly with the differences in strains observed.

Key Words: 3ß-hydroxysteroid dehydrogenase • granulosa cell • heat stress


   INTRODUCTION
TOP
 ABSTRACT
 INTRODUCTION
MATERIALS AND METHODS
 RESULTS
 DISCUSSION
 REFERENCES
 
The enzyme 3ß-hydroxysteroid dehydrogenase (3ß-HSD) is one of the key enzymes in the steroidogenic pathway responsible for producing progesterone (P4) in the female and testosterone in the male. Three-ß-HSD converts pregnenolone to P4 and dehydroepiandrosterone to androstenedione. Three-ß-HSD is first localized in the theca cells when follicles are small, and localization of the enzyme shifts to granulosa cells (GC) as follicle grows (Nitta et al., 1993). Because P4 is one of the main ovarian ovulatory/oviposition hormones in the female bird, it is important to have normal 3ß-HSD activity. The 3ß-HSD activity appears to be regulated by gonadotropins and prolactin (PRL). Shaw et al. (1979) demonstrated that administration of luteinizing hormone (LH) to hypophysectomized male rats increased 3ß-HSD activity to intact control levels and that treating with LH and follicle-stimulating hormone (FSH) in combination caused a more dramatic increase. Hafiez et al. (1971) demonstrated that 3ß-HSD activity was reduced to normal levels when hypophysectomized rats were treated with LH and PRL in combination.

Heat stress (HS) is known to disrupt egg production in hens and to suppress circulating P4, LH, and estrogen. In laying hens, HS reduces circulating LH levels (Donoghue et al., 1989; Novero et al., 1991) and increases circulating PRL in female birds (Elnager, 2000; Rozenboim et al., 2004). Heat stress also decreases activity of 3ß-HSD in GC of laying hens (Alodan, 2001, Taira and Beck, 2004) and in testes of Japanese quail (Taira et al., 2003). It has been shown that laying hens of different strains respond differentially to HS exposure with regard to effect on egg production and certain acid-base parameters (Franco, 2004). This study was conducted to investigate the function of gonadotropins (LH and FSH) and PRL on the activity of 3ß-HSD in GC of the same 3 strains of Hy-Line laying hens (W36, W98, and Brown) and to determine whether the enzyme response would be different by strain, heat stress regimen, or both.


   MATERIALS AND METHODS
TOP
 ABSTRACT
 INTRODUCTION
 MATERIALS AND METHODS
RESULTS
 DISCUSSION
 REFERENCES
 
Experimental Animals

Three strains of 65- to 70-wk-old Hy-Line hens (W36, W98, and Brown) were used. All birds were housed in individual laying cages at 22°C until subjected to thermal challenge. Water and feed were provided for ad libitum consumption. The photoperiod consisted of 16 h of light and 8 h of darkness (16L:8D).

Thermal Treatments

Each strain was divided into 3 groups (5 hens/group), and assigned to acute (24 h, AHS) or chronic (2 wk, CHS) heat stress (36°C, 50% RH), or maintained at the thermoneutral (22°C, TN) temperature.

Preparation of Granulosa Cells

At 24 h and 2 wk of HS, hens were euthanized by CO2 gas, and the 3 largest follicles (F1 to F3) were removed. The GC layers of F1, F2, and F3 follicles were pooled because P4 production occurs mainly in GC of these 3 largest follicles (Robinson and Etches, 1986) and 3ß-HSD is also localized extensively in these cells (Nitta et al., 1993). The follicles were immediately placed in ice-cold 1% physiological saline. Granulosa cells were isolated and dispersed as previously described (Gilbert et al., 1977; Zakar and Hertelendy, 1980; Tilly and Johnson, 1987; Tilly and Johnson, 1989; Novero et al., 1991; Alodan, 2001) with minor modifications. Briefly, each follicle was held by fingers with the stigma facing up, and an incision was made with a surgical blade in the follicular wall along the stigma. The follicles were then inverted over a Petri dish containing 1% saline, and the GC layer surrounding the yolk mass was peeled off with fine forceps. After yolk residual was washed off in 1% saline, GC layers were transferred to a Petri dish containing 0.5 mL of incubation medium [RPMI with L-glutamine, 0.2% D-(+)glucose, 0.2% bovine serum albumin, 0.2% sodium bicarbonate, 0.01% trypsin inhibitor (lima bean, type II-L), and 1% penicillin-streptomysin; pH 7.4.] The layers were minced by microdissection scissors into pieces approximately 2 mm2 that were transferred to 50 mL tubes containing 5 mL of 0.3% collagenase (type II) diluted in incubation medium (dispersion media). The minced tissue was aspirated approximately 20 times with a 1-mL micropipette, and the dispersion process was continued in a shaking water bath (70 cycle/min) for 30 min at 39°C. The manual dispersion with the micropipette was repeated after 15 min and again at the end of incubation (30 min). Granulosa cells were collected by centrifugation at 250 x g for 10 min at room temperature. The cell pellet was resuspended and washed twice with 8 mL of incubation medium. The number of viable cells was estimated by the trypan blue-exclusion technique (Tilly and Johnson, 1987). The GC suspension was then diluted with an appropriate volume of incubation medium to give a final concentration of approximately 500,000 viable cells/mL of incubation medium.

Hormone Incubations

Aliquots (1.2 mL) of the GC suspensions were placed into 12 x 75 mm borosilicate culture tubes and incubated in 60 ng of ovine LH, 120 ng of ovine FSH, 600 ng of ovine PRL (NIDDK-oLH-26; NIDDK-oFSH-20; NIDDK-oPRL-21; Torrance, CA), a combination of these hormones (LH+FSH, LH+PRL, or LH+FSH+PRL), or the absence of any hormone (control). Appropriate amounts of fresh incubation media were added to the tubes to give a final incubation volume of 1.8 mL. The cells were incubated for 4 h at 39°C. After incubation, 100 µL was removed for 3ß-HSD staining.

Staining GC for 3ß-HSD Activity

After incubation with hormones, 100 µL aliquots were placed in 12-well flat bottom plates that contained 1.5 mL of staining medium (PBS, pregnenolone, ß-nicotinamide adenine dinucleotide, and nitroblue tetrazolium) per well. The plates were incubated for 90 min at 39°C. After incubation, a total of 100 cells per well were counted with an inverted microscope, and the percentage of 3ß-HSD active cells, as indicated by dark blue formazan deposits, was calculated.

Statistical Analysis

The experiment was set as a completely randomized design. All data were analyzed by ANOVA using PROC MIXED, and least square means were separated using the t-test (DIFF option; SAS Institute, 1999–2001). Unless otherwise noted, the level of probability for significance was set at P ≤ 0.05.


   RESULTS
TOP
 ABSTRACT
 INTRODUCTION
 MATERIALS AND METHODS
 RESULTS
DISCUSSION
 REFERENCES
 
In all strains, with LH alone or LH+FSH, 3ß-HSD activity in GC from all thermal treatments was significantly increased compared with their respective controls (no hormones; TN-LH, P = 0.04; P < 0.0001 for both other hormone incubations and all other thermal treatments; Figure 1Go); with TN and CHS, the increase in response to LH+FSH was greater than with LH alone (TN, P = 0.002; AHS, P = 0.28; CHS, P = 0.0004; Figure 1Go). In GC incubated with FSH alone, 3ß-HSD activity was significantly decreased (TN, P = 0.006; AHS, P = 0.0580) or not affected (CHS, P = 0.54; Figure 1Go). Similar results were observed with GC incubated with PRL (TN, P = 0.006; AHS, P = 0.0580; CHS, P = 0.35; Figure 1Go) and with LH+PRL (TN, P = 0.085; AHS, P = 0.48); CHS, P = 0.23; Figure 1Go). In contrast, LH+FSH+PRL resulted in 3ß-HSD activity in AHS and CHS cells that was intermediate between the responses to PRL, FSH, and LH+PRL and the responses to LH and LH+FSH (P = 0.052 and 0.0023, respectively); this was not observed in TN cells (P = 1.000; Figure 1Go).


Figure 1
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  		Figure 1. Activity of 3ß-hydroxysteroid dehydrogenase (3ß-HSD), expressed as percentage of positive cells, in granulosa cells under different thermal conditions among 7 hormone treatments. HS = heat stress; LH = luteinizing hormone; FSH = follicle-stimulating hormone; PRL = prolactin. a–eLetters indicate differences within each treatment (P < 0.05 unless otherwise noted in text).

 
During CHS, LH and LH+FSH increased the 3ß-HSD activity to be equal to (P = 0.56) or greater than (P = 0.003) that of AHS-control cells (no hormone added), but it was less than TN-control cells (Figure 2Go; P < 0.0001). Similarly, during AHS, a significant increase in enzyme activity in response to LH and LH+FSH compared with AHS-control was observed in all strains, but it remained below the activity seen in TN-control cells (Figure 2Go; P < 0.0001).


Figure 2
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  		Figure 2. Activity of 3ß-hydroxysteroid dehydrogenase (3ß-HSD), expressed as percentage of positive cells, in granulosa cells under each hormone treatment among 3 thermal treatments. All granulosa cells from thermoneutral birds showed the highest enzyme activity; the lowest was in granulosa cells from chronic heat stress (HS), and enzyme activity from acute HS was intermediate (P < 0.1). LH = luteinizing hormone; FSH = follicle-stimulating hormone; PRL = prolactin.

 
No strain differences were observed in enzyme activity in GC from hens housed in TN conditions, but the enzyme did react differently to hormone treatments when GC from AHS and CHS hens were examined (Figure 3Go). When GC from AHS hens were treated with PRL, the suppressive effect on 3ß-HSD was least in Browns and greatest in W98 (P < 0.1); the effect in W36 was intermediate and not different (P > 0.1) from the other two. When GC from AHS hens were treated with LH+FSH+PRL, the highest percentage of 3ß-HSD-active cells was in W98, the lowest from Browns (P < 0.1), and intermediate activity was found in GC from W36 hens (Figure 4Go). Under CHS, the greatest response to all hormone treatments in terms of enzyme activity was in GC from W98 hens, the lowest response was in GC from Browns (P < 0.1); enzyme activity in GC from W36 hens was always intermediate—sometimes different from both and sometimes equal to one or the other (Figure 5Go).


Figure 3
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  		Figure 3. Activity of 3ß-hydroxysteroid dehydrogenase (3ß-HSD), expressed as percentage of positive cells, in granulosa cells under thermoneutral condition among 3 strains. No strain differences were observed in enzyme activity from each hormone treatment (P > 0.05). LH = luteinizing hormone; FSH = follicle-stimulating hormone; PRL = prolactin.

 

Figure 4
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  		Figure 4. Activity of 3ß-hydroxysteroid dehydrogenase (3ß-HSD), expressed as percentage of positive cells, in granulosa cells under acute heat stress among 3 strains. a,bLetters indicate differences within each hormone treatment (P < 0.05 unless otherwise noted in text). LH = luteinizing hormone; FSH = follicle-stimulating hormone; PRL = prolactin.

 

Figure 5
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  		Figure 5. Activity of 3ß-hydroxysteroid dehydrogenase (3ß-HSD), expressed as percentage of positive cells, in granulosa cells under chronic heat stress among 3 strains. a–cLetters indicate differences within each hormone treatment (P < 0.05 unless otherwise noted in text). LH = luteinizing hormone; FSH = follicle-stimulating hormone; PRL = prolactin.

 

   DISCUSSION
TOP
 ABSTRACT
 INTRODUCTION
 MATERIALS AND METHODS
 RESULTS
 DISCUSSION
REFERENCES
 
The results demonstrate that, in the laying hen, gonadotropins and PRL function to regulate the activity of 3ß-HSD in GC, which is in agreement with previous studies in the male rat (Hafiez et al., 1971; Shaw et al., 1979). The consistency of GC response from hens housed under all 3 thermal conditions to LH alone, LH+FSH, and FSH alone suggests that, to maintain 3ß-HSD activity, some level of LH is necessary. Although LH is generally thought to be the more active gonadotropin in stimulating large follicles to produce P4 and FSH is thought to be more effective on smaller follicles (Calvo and Bahr, 1983; Johnson, 1993), it appears that to achieve maximal 3ß-HSD activity, both LH and FSH are necessary. Further support for this suggestion is found in responses of GC to the series of PRL incubations, which resulted either in a decrease in activity or, when combined with LH or LH+FSH, in no effect. Because PRL is known as antigonadotropic (El Halawani et al., 1984), the effect of combining it with LH (gonadotropic) would likely be to cancel each other out. However, interestingly, adding FSH to the combination resulted in a significant increase in the percentage of active cells during AHS and CHS. This may be because the synergistic effect of LH and FSH on enzyme activity is greater than the inhibitory effect of PRL, even though the PRL obviously dampened the synergism.

It is well known that high environmental temperatures have an adverse effect on egg production in birds by disrupting reproductive hormone status at the hypothalamus (LH-releasing hormone, Donoghue et al., 1989), systemically (LH, Donoghue et al., 1989; LH, P4, Novero et al., 1991) and at the ovary (P4, even when stimulated by LH; Novero et al., 1991) and by increasing systemic PRL (Elnager, 2000). It seems certain that the effect of HS on these hormones has to be upstream, and it is likely that more than one mechanism is involved because the systemic effects of high environmental temperatures are so ubiquitous (Siegel and Drury, 1968a,b and many others) The results of the current study suggest a more specific mechanism—or at least a more specific hint about a focus of future studies.

From the data collected in this study, it appears that 3ß-HSD activity in GC is suppressed within the first 24 h after onset of HS, that it decreases further over 2 wk, and that all 3 strains respond in generally the same way. Granulosa cells from hens subjected to AHS retain some but not all of the normal ability to produce steroid hormones and lose more of this ability over subsequent days of HS. Shimizu et al. (2005) found that the expression of LH and FSH receptors in rats was adversely affected by HS. During the first 24 h, it is therefore likely that GC lose their ability to be affected by LH by, for example, LH receptor alteration or by a decrease in LH receptor populations. This may be true for FSH receptors in chicken GC. Although expression of FSH receptors is decreased as the follicle grows (You et al., 1996), it appears from this study that FSH receptors as well as LH receptors are important in maintaining 3ß-HSD activity.

A study with mouse MA-10 Leydig tumor cells (Murphy et al., 2001) showed that the expression of steroidogenic acute regulatory protein, cytochrome cholesterol side-chain cleavage enzyme, and 3ß-HSD were all reduced by heat shock, and another study showed that HS enhances susceptibility to apoptosis of GC (Shimizu et al., particularly in response to HS, but Mussche and D’Herde (2001) reported that FSH appears to enhance GC survival and P4 production in Japanese quail under thermoneutral conditions. Taken together, if HS reduces FSH in the chicken, it would not be available to prevent HS-induced apoptosis and associated decreases in enzyme activity, LH receptors (Erickson et al., 1979), and steroid hormone production. Although some of the elements in this model have already been shown (current study; Donoghue et al., 1989; Novero et al., 1991), other components have not yet been addressed.

Among the current leading commercial layer strains, Hy-Line W36 and W98 hens, although similar in many respects, differ in age of onset of sexual maturity and in persistence of hormone and acid base status and egg production during HS (Franco, 2004). In a series of studies with the White and the Brown strains, Franco (2004) showed that the W98 hens consistently outperformed the other 2 during HS, that the Browns (larger, heavier) did least well, and that W36 hens were always intermediate in performance during HS and that acid-base disruptions were least in the W98, most in the Browns, and intermediate in the W36. In this study, similar results were observed during chronic HS. In chronic HS, incubation of GC from W98 and W36 birds with LH+FSH boosted the enzyme activity much higher than the level of activity in AHS control cells, but this did not hold for Brown hens. This weak response to gonadotropins may help explain why Brown hens have been shown to recover more slowly from HS compared with the other 2 strains (Franco, 2004).

In conclusion, 3ß-HSD appears to be regulated by gonadotropins and PRL. It seems that some level of LH is necessary to maintain 3ß-HSD activity and that both LH and FSH are necessary to achieve maximal activity. It is interesting that the W98, W36, and Brown responses mimic the systemic responses to HS at the cellular level; it remains to be seen whether the molecular responses follow suit. The W98 hen, considered somewhat labile endocrinologically under typical commercial conditions (undergoing spontaneous mini-molts at ~35 wk of age; R. Dutton, Michael Foods, Wakefield, NE, personal communication), has a remarkably stable endocrine system under adverse high temperatures. In contrast, the W36 hen, very stable over its laying lifetime under normal conditions, does not respond as well during HS.


   FOOTNOTES
 
1 A contribution of the University of Nebraska Agricultural Research Division. Supported in part by funds provided through USDA Regional Research Project NE-1022. Back

Received for publication March 1, 2006. Accepted for publication April 28, 2006.


   REFERENCES
TOP
 ABSTRACT
 INTRODUCTION
 MATERIALS AND METHODS
 RESULTS
 DISCUSSION
 REFERENCES
 
Alodan, M. A. 2001. Cytokine IL-1ß modulation of reproductive function in heat stressed hens. PhD Dissertation. Univ. Nebraska, Lincoln, NE.

Calvo, F. O., and J. M. Bahr. 1983. Adenylyl cyclase system of the small preovulatory follicles of the domestic hen: Responsiveness to follicle-stimulating hormone and luteinizing hormone. Biol. Reprod. 29:542–547.[Abstract]

Donoghue, D. J., B. F. Kruger, B. M. Hargis, A. M. Miller, and M. E. El Halawani. 1989. Thermal stress reduces serum luteinizing hormone and bioassayable hypothalamic content of luteinizing hormone-releasing hormone in hens. Biol. Reprod. 41:419–424.[Abstract]

El Halawani, M. E., J. L. Silsby, E. J. Behnke, and S. C. Fehrer. 1984. Effect of ambient temperature on serum prolactin and luteinizing hormone levels during the reproductive life cycle of the female turkey (Meleagris gallopavo). Biol. Reprod. 30:809–815.[Abstract]

Elnager, S. A. 2000. Hypothyroid-mediated changes in reproductive function during heat stress in laying hens at different stages of production. Ph.D. Dissertation. Alexandria Univ., Egypt.

Erickson, G. F., C. Wang, and A. J. W. Hsueh. 1979. FSH induction of functional LH receptors in granulose cells cultured in a chemically defined medium. Nature 279:336–338.[Medline]

Franco, D. J. 2004. Effect of heat stress of production, physiological and metabolic parameters in three varieties of laying hens. PhD Dissertation, Univ. of Nebraska, Lincoln.

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