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Biology of Reproduction 62, 1818-1822 (2000)
© 2000 Society for the Study of Reproduction, Inc.

Regular Article

Region-Specific Regulation of Cytochrome P450 Aromatase Messenger Ribonucleic Acid by Androgen in Brains of Male Rhesus Monkeys1

J.A. Resko2,a, A.C. Pereyra-Martineza, H.L. Stadelmana, and C.E. Rosellia

a Department of Physiology and Pharmacology, School of Medicine, Oregon Health Sciences University, Portland, Oregon 97201-3098

ABSTRACT

We demonstrated previously that testosterone regulates aromatase activity in the anterior/dorsolateral hypothalamus of male rhesus macaques. To determine the level of the androgen effect, we developed a ribonuclease protection assay to study the effects of testosterone or dihydrotestosterone (DHT) on aromatase (P450AROM) mRNA in selected brain areas. Adult male rhesus monkeys were treated with testosterone or DHT. Steroids in serum were quantified by RIA. Fourteen brain regions were analyzed for P450AROM mRNA. Significant elevations of its message over controls (P < 0.05) were found in the medial preoptic area/anterior hypothalamus of both androgen treatment groups and the medial basal hypothalamus of the testosterone-treated males. Other brain areas were not affected by androgen treatment. We conclude that testosterone and DHT regulate P450AROM mRNA in brain regions that mediate reproductive behaviors and gonadotropin release. The P450AROM mRNA of other brain areas is not androgen dependent. Brain-derived estrogens may also be important for maintaining neural circuitry in brain areas not related to reproduction. The control of P450AROM mRNA in these areas may differ from what we report here, but it is equally important to understand the function of in situ estrogen formation in these areas.

INTRODUCTION

In nonhuman primates, testosterone affects reproductive [1, 2] and aggressive behaviors [3–5] as well as gonadotropin secretion [6, 7]. In castrated (Cx) males, the repertoire of sexual behaviors decreases with time after castration and can be restored by treatment with exogenous testosterone [2] or dihydrotestosterone (DHT) [8]. The area of the brain that mediates reproductive behaviors seems to be located in the preoptic/anterior hypothalamic continuum as ablation of this region results in behavioral deficits [9], and electrical stimulation of this region evokes penile erections [10] and ejaculations [11]. In addition to behavior, testicular androgens regulate gonadotropin secretion through a negative feedback loop that seems to function at the level of the central nervous system [12, 13] and, at least for FSH, at the level of the anterior pituitary gland [14]. In Cx males, LH concentrations in the systemic circulation are greatly elevated over those found in intact males [7, 15] and can be reduced to intact concentrations by exogenous testosterone [7, 16]. The area of the brain that controls gonadotropin secretion in the male monkey may be the arcuate nucleus because radiofrequency lesions of this area abolish pulsatile LH secretion that can be reinstated by pulsatile GnRH replacement [17].

Although the effects of testosterone, mentioned above, have been known for many years, it is still debated whether testosterone or one of its metabolites, DHT or estradiol-17ß (E2) is the effective hormone. Evidence that both metabolites can have effects on the central nervous system both in regulating behaviors [2, 8, 18, 19] and gonadotropin secretion [7, 15, 20, 21] can be found in the literature. The basic question revolves around the physiological effects of these hormones. There can be little doubt, however, that large doses of exogenous testosterone or DHT (a nonaromatizable androgen) can exert negative feedback effects on LH secretion in Cx rhesus macaques [16, 21].

We demonstrated previously the presence of aromatase (P450AROM) activity in the medial preoptic/anterior hypothalamus (MPAH) of adult rhesus macaques and showed that this activity was regulated by testosterone [22]. Because these brain areas have been shown to be important for the mediation of sexual behaviors and, perhaps, the control of gonadotropin secretion, the presence of the cellular machinery for aromatization in the same regions suggests some function for its presence. Because testosterone can not only serve as a substrate for aromatization but also stimulate the amount of P450AROM activity in the MPAH of the male monkey [22], we wondered whether testosterone as well as its nonaromatizable metabolite, DHT, affects P450AROM mRNA in brains of male monkeys. The purpose of this work was to answer this question.

MATERIALS AND METHODS

Animals

Thirteen adult male rhesus monkeys (Macaca mulatta, 5–10 yr of age) were used in this study. The housing and care of the animals have been described previously [22]. Experiments and animal care were conducted in accordance with the principles and procedures outlined by the National Institute of Health Guide for the Care and Use of Laboratory Animals. Blood samples (3 ml) were obtained from each animal through a cardiac catheter at 0900 and 2100 h, each day for 28 days (7 days before and 21 days after Cx) before they were killed. The placement of the catheter to obtain blood remotely has been described previously [23]. Testosterone and DHT were administered at the time of castration by placing four (4 cm in length) silastic capsules (0.330 cm internal diameter; 0.465 cm outer diameter) filled with crystalline steroid s.c. between the scapulae under aseptic conditions. Empty capsules placed in the same location in Cx males, were used as a control for implant placement.

The tissues that were used for P450AROM mRNA measurements by the ribonuclease protection assays were obtained from four Cx males, four Cx males treated with testosterone, and four Cx males treated with DHT. Tissues from one gonad-intact male were used in Figure 1 to compare with the other treatment groups. On the day of autopsy, each animal was anesthetized with ketamine hydrochloride (15 mg/kg, i.m.) for transport from its cage to the autopsy room and then killed by injecting a lethal dose of pentobarbital (85 mg/kg body weight, i.m., Terminol-III; Anthony Products Co., Arcadia, CA).



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  		FIG. 1. A representative ribonuclease protection assay autoradiogram showing the distribution of P450AROM mRNA in the MPAH of adult male rhesus macaques with and without exposure to androgen (10 µg total RNA/lane). Lanes are: (1) incubated undigested probe; (2) incubated, ribonuclease-digested probe; (3) MPAH from Cx male; (4) MPAH from T-treated male; (5) MPAH from DHT-treated male; (6) MPAH from intact male; (7–13) P450AROM sense RNA standard curve (31.2, 62.4, 125, 250, 500, 1000, 2000 fg, respectively). Exposure time was 40 h

The brain was rapidly removed from the cranium and rinsed in ice-cold 0.9% saline. It was placed in a chilled ASI monkey brain matrix (Ted Pella, Inc., Redding, CA) and cut into 4-mm coronal sections through the length of the preoptic area, hypothalamus, and adjacent amygdala. Individual regions were dissected from either these coronal slices or the remaining brain using diagrams of the monkey brain from the atlas of Snider and Lee [24] and Martin and Bowden [25]. The dissected tissue was frozen immediately on dry ice and stored at -80°C until they were assayed. The regional dissections used in the current study were somewhat larger than those used in our previous punch dissection studies [26] and in many cases encompassed more than one discrete brain nucleus or subregion. Specifically, the MPAH included: medial preoptic nucleus (n.), preoptic periventricular n., suprachiasmatic n., rostral part of the supraoptic n., paraventricular n., anterior hypothalamic region, and anterior n. of the hypothalamus. The LPAH included: lateral preoptic area, substantia inominata, and the lateral part of the supraoptic n. The MBH included: arcuate n., ventromedial hypothalamic n., medial-caudal part of the supraoptic n., median eminence, intermediate hypothalamic region, ventral part of the hypothalamic periventricular n., and tuber cinereum. The DMH included the dorso-medial hypothalamic n., caudal part of the paraventricular n., and dorsal part of the hypothalamic periventricular n. The LH included: lateral hypothalamic n. and medial part of the substantia innominata.

RNA Isolation

Total RNA was isolated by homogenizing tissues in 4 M guanidium isothiocyanate, 10 mM EDTA, 2% sodium N-lauryl sarcosine, 1% (v/v) ß-mercaptoethanol, 50 mM Tris, pH 7.6, in the presence of 10 mM vanadyl ribonucleoside complexes. The guanidium isothiocyanate homogenate was centrifuged through 5.7 M cesium chloride [27], and the RNA was extracted once with phenol, once with chloroform/isoamyl alcohol (49/1, v/v), and concentrated by ethanol precipitation.

Ribonuclease Protection Assay

Tissue concentrations of P450AROM mRNA were measured by a RNase protection assay using the 455-nt [32P]cRNA probe transcribed from the 5' coding region of the rhesus monkey P450AROM cDNA as described previously [26]. Cyclophilin mRNA that was used as a control for RNA loading on the gels was measured using a 185-nt [32P]cRNA probe that was transcribed from a rhesus monkey p1B15 cyclophilin cDNA cloned into pGEM-3Z vector (provided by Dr. Sergio Ojeda at the Oregon Regional Primate Research Center). The protected cyclophilin mRNA fragment in the ribonuclease protection assay was 158 nt long.

Protected areas on the polyacrylamide gels were quantified using a Molecular Imaging System (Bio-Rad GS-525, Hercules, CA). Exposure time was 40 h. The phosphoimage signal for each sample was compared to the signals obtained from a standard curve of known amounts of P450AROM sense RNA (31.25–2000 fg) that were run with each gel.The results were expressed as P450AROM mRNA/µg total RNA analyzed.

Steroid Assays

Testosterone, DHT, and E2 were quantified in systemic serum by RIA after chromatography on Sephadex LH-20 as described previously [28]. The intra- and interassay coefficients for testosterone were 8.6 and 10.4% respectively; for DHT they were 8.3 and 16.4% and for E2 they were 5.3 and 16.5%. The lower limits of detectability, i.e., the first point on the standard curve lying outside 2 standard deviations of cpm in tubes containing unlabeled hormone, were 11.1 fmol/tube for testosterone, 10.2 fmol/tube for DHT, and 10.3 fmol/tube for E2.

Statistical Analysis

The within- and among-treatment steroid concentrations in serum and differences in P450AROM mRNA concentrations in the same brain areas among treatments were analyzed by an ANOVA. If a significant F value was obtained by the ANOVA, differences between treatment groups were determined by the Newman-Keul's multiple range test. The data in the various treatment groups were tested for homogeneity of variances before the ANOVA, and if the variances differed, the data were log transformed for the analysis. Probability values of P < 0.05 were considered statistically significant.

RESULTS

A representative autoradiogram of a ribonuclease protection assay is shown in Figure 1. In this figure, the amounts of P450AROM mRNA in the MPAH from males in various treatment groups (Cx lane 3; testosterone treatment for 21 days, lane 4; DHT-treatment for 21 days, lane 5; and an untreated intact male, lane 6) were compared in the same protection assay. The intensity of the P450AROM mRNA band on the gel of the protection assay in the MPAH from the Cx male was lower than that observed in males treated with either testosterone, DHT, or from the male in which the testes were not removed.

The composite data from all 14 brain areas in which P450AROM mRNA from Cx males (n = 4) was compared with testosterone- and DHT-treated males (n = 4 each) are shown in Figure 2. The abbreviations for the brain areas are identified in the legend to Figure 2. Of the 14 brain areas that we studied, only one area, the MPAH, contained statistically significant elevations of P450AROM mRNA in both testosterone- and DHT-treated subjects compared to Cx controls (P < 0.05). Statistically significant elevations of P450AROM mRNA in testosterone-treated subjects, compared to Cx controls, were also found in the MBH (P < 0.05). Because two samples of MBH were lost in the DHT-treated males, statistical comparisons were not performed between controls and DHT-treated males in this brain area. Even though, we found larger quantities of P450AROM mRNA in the LPAH, cortical amygdala (CA), medial amygdala (MA), and bed nucleus stria terminalis (BNST) compared to the MPAH and MBH, these areas did not change significantly in response to androgen treatment (P > 0.05).



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  		FIG. 2. The effects of testosterone and DHT treatment on P450AROM mRNA in brain tissues of adult rhesus monkeys analyzed by a ribonuclease protection assay (10 µg total RNA/brain area was used in each assay). Messenger RNA was quantified using a phosphoimager. Exposure time was 40 h. Three groups of male monkeys were compared: those that were Cx (n = 4), those Cx and treated with testosterone for 21 days (n = 4), and those Cx and treated with DHT for 21 days (n = 4). Data are presented as means (bars) ± SEM (vertical lines). Data were log transformed when necessary because of heterogeneity of variances and comparisons between treatment groups within tissues were made by an ANOVA. If a significant F value was obtained, differences between treatment groups were determined by the Newman-Keul's multiple range test. The exception to this analysis was the MBH and the basal lateral amygdala (BLA). Because two samples from the DHT-treated group were lost in each of these tissues, statistical tests were not performed. However, individual data points (circles) from the two males for which data were obtained for MBH and BLA are presented along with the means. Bars marked with different letters differ significantly (P < 0.05) from Cx controls. Abbreviations: septum (Sept), frontal cortex (F. Ctx), parietal cortex (P. Ctx), hippocampus (Hipp), cerebellum (Cerb)

In Table 1, we present sex steroid concentrations (testosterone, DHT, and E2) in serum among treatment groups before and after Cx. Before Cx, testosterone and DHT, but not E2 concentrations in serum vary diurnally. After Cx, the concentrations of testosterone, DHT, and E2 were below the limits of detectability of our RIA when 100 µl of serum were assayed. After testosterone treatment, all three steroid hormones were elevated in serum of Cx males, whereas only DHT was elevated in serum of DHT-treated males. These and other statistical comparisons are presented in Table 1.


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  		TABLE 1. Sex steroid concentrations in serum of male rhesus macaques before and after castration and treatment with testosterone or DHT

DISCUSSION

The results of the present study complement our previous work by showing that testosterone not only serves as a substrate for aromatization within the central nervous system of nonhuman primates but also regulates the transcription and/or stability of P450AROM mRNA. In addition to the above, our results show that the nonaromatizable androgen, DHT, can produce the same effects as testosterone in the MPAH and possibly in the MBH as well. Because of the actions of testosterone and DHT, the potential for greater amounts of estrogen formation from androgen precursors in situ exists in the MPAH and MBH. Because DHT cannot be aromatized, it appears that the effects of androgen on P450AROM mRNA are independent of estrogen formation. The in situ synthesis of estrogen, however, presumably serves some other biological function(s) such as the control of both gonadotropin secretion and sexual behaviors in macaques.

Previously, we described the distribution of P450AROM mRNA in many of the same brain areas of male monkeys that we used in the present work [26]. Aromatase activity was highly correlated with the amounts of mRNA that we found. We also showed the distribution of P450AROM mRNA in the brains of Cynomolgus macaques by in situ hybridization techniques [29]. The results in the many distribution studies were basically the same [26, 29, 30]. The highest amounts of aromatase activity and its mRNA are found in the BNST, the CA and MA, and the anterior hypothalamic area. Intermediate amounts can be found in the medial preoptic area and the ventromedial nucleus of the hypothalamus. Low amounts are found in the lateral septum, lateral hypothalamus, the cerebral cortex, hippocampus, and cerebellum.

In this study, the pattern of distribution of P450AROM mRNA among the various brain areas is similar to those previously reported [26], but the quantities in each tissue are lower. This difference between the two studies may be due to the fact that the males used in the previous study were older (between 10 and 15 yr of age), whereas those used in this study were between 5 and 10 yr of age. In general, however, we were unable to identify conditions that affect P450AROM mRNA between experiments that were performed alike. The quantities of testosterone that we measured in the systemic circulation of the testosterone-treated Cx males was approximately 11 ng/ml serum. These quantities of testosterone are significantly higher than the amounts measured in the same male over a 1-wk period before Cx. However, they fall within the range of endogenous testosterone concentrations that have been reported for male rhesus monkeys by other investigators [31–33].

The present observation regarding the effects of exogenous testosterone on P450AROM mRNA is similar to those reported for male rats [34], quail [35], and developing mice [36]. Because of the diversity between these species, one is tempted to speculate that this control mechanism is highly conserved in the animal kingdom. Some discrepancies can be found among the brain areas in which P450AROM activity is stimulated by testosterone and those in which the P450AROM mRNA is stimulated by testosterone. For example, in a previous study [30], we demonstrated that aromatase activity in the MPAH of the male monkey did not change significantly after Cx and treatment with testosterone. These discrepancies appear to be due to differences in dissection. The rationale for using different dissection techniques between experiments was to obtain enough tissue from a brain area to measure P450AROM mRNA. The dissections in the present study were larger than in previously used punch dissections [30]. Thus, the MPAH dissection includes several brain nuclei and their subregions, i.e., the periventricular area, medial preoptic nucleus, suprachiasmatic nucleus, and supraoptic nucleus. The P450AROM mRNA was previously shown to be regulated in at least in one of the nuclei contained in the present dissection, which may account for the regulation that we observed in the present study. Likewise other differences between the two reports can be explained in this way.

In contrast to the MPAH and the MBH, the P450AROM mRNA from other parts of the brain were not testosterone dependent. This observation is similar to that reported previously from our laboratory for the male rat in which the P450AROM mRNA extracted from the MPAH and MBH was higher in males treated with exogenous testosterone compared to untreated controls, whereas the P450AROM mRNA in the amygdala did not change after hormone treatment [34]. In the male monkey, these two parts of the brain, i.e., the MPAH and the MBH, also contained the largest amounts of androgen receptor mRNA [37], which may explain the differences in responsiveness to androgen.

Our results suggest that one of the cellular mechanisms for controlling in situ estrogen formation in the male monkey brain is the ability of androgens such as testosterone and/or DHT to regulate P450AROM mRNA. This regulation is region specific and confines itself to the MPAH and the MBH, regions known to mediate gonadotropin secretion and sexual behaviors in nonhuman primates.

ACKNOWLEDGMENTS

The authors acknowledge Salah E. Abdelgadir, Ph.D., who developed the P450AROM cDNA probe that was used in these experiments.

FOOTNOTES

First decision: 23 November 1999.

1 Supported by NIH grant HD-18196 and D43 TW HD00669. Back

2 Correspondence. FAX: 505 494 4352; reskoj{at}ohsu.edu Back

Accepted: January 24, 2000.

Received: November 2, 1999.

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