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Regular Article |
a Laboratory of Cellular Biology, Department of Morphology, Institute of Biological Sciences, Federal University of Minas Gerais, Belo Horizonte, MG, Brazil 31270-901
b Department of Zootechny, School of Veterinary Medicine at Federal University of Minas Gerais, Belo Horizonte, MG, Brazil 31270-901
c Departments of Physiology and Health Care Professions, Southern Illinois University, Carbondale, Illinois 62901
ABSTRACT
Histometrical evaluation of the testis was performed in 36 Piau pigs from birth to 16 mo of age to investigate Sertoli cell, Leydig cell, and germ cell proliferation. In addition, blood samples were taken in seven animals from 1 wk of age to adulthood to measure plasma levels of FSH and testosterone. Sertoli cell proliferation in pigs shows two distinct phases. The first occurs between birth and 1 mo of age, when the number of Sertoli cells per testis increases approximately sixfold. The second occurs between 3 and 4 mo of age, or just before puberty, which occurs between 4 to 5 mo of age, when Sertoli cells almost double their numbers per testis. The periods of Sertoli cell proliferation were concomitant with high FSH plasma levels and prominent elongation in the length of seminiferous cord/tubule per testis. Leydig cell volume increased markedly from birth to 1 mo of age and just before puberty. In general, during the first 5 mo after birth, Leydig cell volume growth showed a similar pattern as that observed for testosterone plasma levels. Also, the proliferation of Leydig cells per testis before puberty showed a pattern similar to that observed for Sertoli cells. However, Leydig cell number per testis increased up to 16 mo of age. Substantial changes in Leydig cell size were also observed after the pubertal period. From birth to 4 mo of age, germ cells proliferated continuously, increasing their number approximately two- to fourfold at each monthly interval. A dramatic increase in germ cells per cross-section of seminiferous tubule was observed from 4 to 5 mo of age; their number per tubule cross-section stabilized after 8 mo. To our knowledge, this is the first longitudinal study reporting the pattern of Sertoli cell, germ cell, and Leydig cell proliferative activity in pigs from birth to adulthood and the first study to correlate these events with plasma levels of FSH and testosterone.
FSH, Leydig cells, pituitary hormones, Sertoli cells, spermatogenesis, steroid hormones, testes, testosterone
INTRODUCTION
The FSH is considered to be the main mitogenic factor responsible for Sertoli cell divisions [1–3]. The Sertoli cell number established during the prepubertal period determines the final testicular size and the number of sperm produced in sexually mature animals [4–9]. This occurs because the Sertoli cell division stops before puberty, with the Sertoli cell population becoming stable thereafter, and also because Sertoli cells can support only a limited number of germ cells, with this support capacity cell being both variable and species-specific [10, 11]. The period of postnatal Sertoli cell proliferation is well established in rats and mice [1, 12, 13]. However, to our knowledge, no comprehensive morphometrical study has shown the period of Sertoli cell proliferation after birth in pigs or other large animals. Some reports in the literature suggest that Sertoli cell mitosis in pigs occurs mainly during the first month after birth [14–16]. Sertoli cell maturation in pigs, however, occurs only at approximately 3 mo of age [17, 18].
In contrast to most mammalian species, which exhibit a biphasic pattern of Leydig cell development [19], pigs exhibit three phases of Leydig cell development: two transient phases, one during the early fetal period [20] and the other during the perinatal period [20, 21]; and a final phase from 3 mo of age through pubertal development and adulthood [20–22]. Also, in pigs, the Leydig cell individual volume and number of LH receptors per Leydig cell change substantially during the different periods of testicular development [20, 22–24]. However, to our knowledge, no morphometrical study has shown the changes that occur in Leydig cell volume and number from birth to adulthood.
The Piau pig is a swine breed that has been improved during the past decades in Brazil. This pig is considerably smaller than the standard breeds and is a good model with which to develop longitudinal studies. In the present investigation, we describe the proliferation periods of Sertoli cells, Leydig cells, and germ cells from birth to adulthood in Piau pigs. We also report the correlation between the proliferative phase of these cells with the plasma levels of FSH and testosterone.
MATERIALS AND METHODS
Animals and Experimental Design
Forty-three Piau pigs from the Experimental Farm of the Veterinary School at the Federal University of Minas Gerais were randomly selected and utilized. Thirty-six animals were distributed in 12 groups composed of three animals each (Table 1), whereas seven animals were used to measure plasma FSH and testosterone levels from 1 wk of age to adulthood. All surgical procedures were performed by a veterinarian and followed approved guidelines for the ethical treatment of animals.
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Tissue Preparation
Immediately after orchidectomy, testes were cut longitudinally by hand with a razor blade to obtain cross-sections of the seminiferous cords/tubules. Tissue samples, measuring 3 mm in thickness, were obtained close to the tunica albuginea. These testicular samples were immersed immediately in Bouin fixative for 20 to 24 h and then dehydrated and embedded in paraffin. Sections of approximately 7 µm in thickness were obtained and stained with hematoxylin and eosin as well as with Gomori trichrome and subjected to testicular histological and histometrical analysis.
Testosterone and FSH Assay
Blood samples were obtained biweekly from the external jugular vein to determine plasma testosterone and FSH levels from 1 wk of age to adulthood. All samples were obtained between 0900 and 1000 h. Testosterone was measured by a solid-phase radioimmunoassay using a commercial kit (ICN Pharmaceuticals, Costa Mesa, CA). One 50-µl aliquot of plasma was dispensed in each assay tube, and then 1 ml of buffer containing the tracer (40 000 cpm/tube) was added. A standard curve was established with doses of testosterone ranging from 0.2 to 16 ng/ml. The mixture was incubated for 3 h at 37°C, the tubes were decanted, and the radioactivity bound to the tube was measured in a gamma counter with a built-in computer, which calculated the final values of testosterone (ng/ml) in plasma. A single assay was performed; the intra-assay coefficient of variation was 4%.
The FSH levels were determined with a double-antibody radioimmunoassay using reagents provided by the National Hormone and Pituitary Program, National Institutes of Health, and U.S. Department of Agriculture through the courtesy of Dr. J. Proudman. Porcine FSH was used as a standard preparation. Purified porcine FSH was labeled with 125I, and anti-pig FSH serum was used as the first antibody. The separation between antibody-bound and free tracer was achieved by use of an anti-rabbit gamma globulin obtained in goats, which was facilitated by the addition of 10% polyethylene glycol. A single assay was performed; the intra-assay coefficient of variation was 6.5%.
Morphometry of the Testis
Diameter of the seminiferous cords/tubules was measured at 160x and 400x magnification using an ocular micrometer calibrated with a stage micrometer. Twenty seminiferous cords/tubules profiles that were round or nearly round were measured, and a mean was determined for each animal. Basic morphometric data on testicular composition were obtained using point counting by systematic placement of a 25-point grid over sectioned material at 800x magnification. Approximately 1000 points and 40 fields randomly selected were utilized for each animal. The volume of each testicular component was determined as the product of the volume density and the testicular volume. For subsequent morphometric calculations, the specific gravity of testicular tissue was considered to be 1.0. To obtain a more precise measure of the testicular volume, the testicular capsule and the testicular mediastinum weight obtained for the same animals [25] were excluded from the total testicular weight. A correction for shrinkage was then performed [26]. The total length of seminiferous cord/tubule (m) was obtained by dividing the seminiferous tubule volume by the squared radius of the tubule [27].
Cell Counts and Cell Numbers
Sertoli cell nuclei were counted in 20 round seminiferous cord/tubule cross-sections per animal. Because the Sertoli cell nucleus from birth to 4 mo of age presented, in general, an ovoid shape, its nuclear diameter was obtained as the mean of its larger and smaller diameters. At these ages, the Sertoli cell nuclei obtained for each animal were corrected for section thickness and nucleus size according to the method described by Abercrombie [28] and modified by Amann and Almquist [29]. The mean number of Sertoli cells per testis and per gram of testis as well as the number of germ cells per testis were determined from the corrected counts of Sertoli cell and germ cell nuclei per cross-section of seminiferous tubule and the total length of seminiferous tubules according to the method described by Hochereau-de Reviers and Lincoln [30]. Because correcting nuclei that present irregular shapes is not possible with the formula mentioned earlier, Sertoli cell nuclei profiles were not counted in pigs after 4 mo of age. For animals 16 mo of age, the Sertoli cell population was obtained using the corrected number of Sertoli cell nucleoli according to the methodology described earlier.
The number of germ cells per seminiferous cord/tubule was obtained from cell counts in 10 to 20 cross-sections for each animal. These counts were also corrected for section thickness and nucleus size as mentioned earlier. After puberty, germ cell counts were performed at stage 1 of the cycle and classified according to the tubular morphology system described for Piau pigs [31]. The following germ cells were counted: type A spermatogonia, preleptotene/leptotene primary spermatocytes, pachytene primary spermatocytes, and round spermatids.
Leydig cell individual volume was obtained from the nucleus volume and the proportion between the nucleus and cytoplasm. Because the Leydig cell nucleus in pigs is spherical, its nucleus volume was obtained using the mean nuclear diameter. For this purpose, 30 nuclei showing evident nucleolus had their diameters measured for each animal. Individual nuclear volumes were expressed (µm3) using the formula 4/3
R3, where R = nuclear diameter/2. To calculate the proportion between nucleus and cytoplasm, a 441-point square lattice was placed over the sectioned material at 400x magnification. Three-thousand points over Leydig cells were counted for each animal. The number of Leydig cells per testis and per gram of testis was estimated from the Leydig cell individual volume and the volume occupied by Leydig cells in the testis.
Statistical Analysis
The results were transformed to logarithms for ANOVA. All values for volume densities were subjected to arcsine transformation before analyses. Analysis of correlation and variance (Newman-Keuls test) was made using the program STATISTICA for Windows (StatSoft, Inc., Tulsa, OK). The significance level was considered to be P < 0.05. All data are presented as the mean ± SEM.
RESULTS
Testicular Histometry
Basic biometric and histometric data are shown in Table 1. As can be observed, testicular weight increased dramatically in pigs from birth to 1 mo of age and from 4 to 5 mo of age and showed a lower rate of growth after 7 mo of age. During the period investigated, the testicular weight was highly and significantly correlated with the body weight (r = 0.96).
Diameter of the seminiferous cords/tubules increased slowly from birth to 4 mo of age and presented a marked growth from 4 to 5 mo of age. After 7 mo of age, the tubular diameter showed a tendency to stabilize. The seminiferous cord/tubule volume density occupied approximately 40% to 50% of the testicular parenchyma from birth to 2 mo of age. From 2 to 5 mo of age, its volume density increased continuously, reaching almost 90%. The volume density occupancy was approximately 80% thereafter. Table 1 also shows that the total length of the seminiferous cords/tubules per testis augmented more than sevenfold from birth to 1 mo of age. Another evident period of increase, by approximately 100%, was observed in animals at 3 to 4 mo of age. In general, after this period, the tubular length increased gradually, up to 16 mo of age. The total length of the seminiferous tubule correlated significantly with the testicular weight (r = 0.93) and tubular diameter (r = 0.79).
Germ Cell and Sertoli Cell Numbers
Table 2 shows that the number of germ cells per seminiferous cord/tubule cross-section was very low from birth to 4 mo of age. A very dramatic increase in germ cell population per cross-section of seminiferous tubule occurred from 4 to 5 mo of age. After 7 mo of age, the number of germ cells per tubule cross-section at stage 1 of the seminiferous epithelial cycle showed a tendency to stabilize. In general, the pattern observed for the number of germ cells per cross-section of seminiferous cord/tubule during testicular development was very similar to that observed for testicular growth. So, significant correlation (r = 0.82) was observed between the testicular weight and the number of germ cells per seminiferous cord/tubule cross-section. The number of germ cells per seminiferous cord/tubule was also significantly correlated with tubular diameter (r = 0.95) and with the total tubular length per testis (r = 0.77).
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The total number of germ cells per testis increased continuously, between two- to fourfold at each monthly interval, from birth to 4 mo of age (Table 2). During this period, germ cell numbers per testis correlated significantly with the testicular weight (r = 0.86) and the total tubular length (r = 0.91).
The crude number of Sertoli cell nuclei per cross-section of seminiferous cord/tubule was very similar from birth to 1 mo of age (Table 2), increasing by approximately 30% from 1 mo to 2 mo of age, and then being stable from 2 to 4 mo of age. After that, the number of Sertoli cells decreased continuously, showing a trend to stabilize in pigs between 7 and 16 mo of age. As can be observed in Table 2, the number of germ cell and Sertoli cell nuclei per tubule cross-section showed basically opposite growth patterns during testicular development. So, the significant and negative correlation observed between these two cell types (r = -0.89) was expected.
Table 2 indicates that although the magnitude was not very high, Sertoli cell nuclear diameter increased gradually and significantly (P < 0.05) from birth to 3 mo of age. Figure 1 shows the Sertoli cell nuclear morphology at birth, puberty, and sexual maturity. The pattern found for Sertoli cell number per testis before puberty was the same as that observed for the total length of seminiferous cords/tubules. So, Sertoli cell proliferation occurred mainly during two periods. During the first, between birth and 1 mo of age, the number of Sertoli cells per testis increased approximately sixfold. During the second evident proliferative phase, between 3 to 4 mo of age, an augmentation of approximately 80% was observed. After 4 mo of age, the number of Sertoli cells per testis was similar to that found for 16-mo-old animals (P > 0.05, Table 2) [32]. The number of Sertoli cells per gram of testis decreased drastically after 4 mo of age (Table 2). From birth to 4 mo of age, the number of Sertoli cells per testis correlated significantly with testicular weight (r = 0.98), total tubular length (r = 0.91), and number of germ cells per testis (r = 0.92).
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FSH Plasma Levels
Figure 2 shows that plasma FSH levels were high during the first weeks after birth, then decreased markedly up to 3 mo of age. The FSH levels increased around 3 mo of age, being elevated in pigs up to approximately 130 days of age. After this period, FSH levels decreased again, showing an irregular pattern at subsequent ages. From birth to approximately 4 mo of age, the highest levels of FSH coincided with the two periods of most prominent Sertoli cell proliferation.
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Leydig Cell Parameters and Testosterone Plasma Levels
The Leydig cell constitutes the main component of the intertubular space in pigs. Basically, all Leydig cell parameters showed a large variation during testicular development. Table 3 shows that from birth to 2 mo of age, Leydig cells occupied approximately 30% to 40% of the testicular parenchyma. After 2 mo of age, Leydig cell volume density gradually decreased, reaching its minimal value (
7%) at 5 mo of age. From 6 to 16 mo of age, Leydig cell volume density remained approximately 10% to 15%. The Leydig cell nuclear diameter and volume changed substantially during testicular development (Table 3). The minimum value found for nuclear volume (110 µm3) was observed in 4-mo-old pigs. The maximum value (210 µm3) was observed in 1-mo-old animals. The volume density of the Leydig cell nucleus ranged from 8% in 9-mo-old pigs to 21% in 4-mo-old animals (Table 3). Leydig cell individual volume also showed great variation during testicular development in pigs. Nevertheless, three phases of cell growth can be emphasized: between birth and 1 mo of age, between 4 and 5 mo of age, and between 6 to 7 mo of age, with these increases representing approximately 110%, 160% and 80%, respectively.
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Testosterone plasma levels are indicated in Figure 3. From birth to approximately 4 mo of age, the pattern of Leydig cell individual volume growth and testosterone levels were similar (Table 3 and Fig. 3). Also, from birth to 4 mo of age, FSH and testosterone levels were significantly correlated (r = 0.27).
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Leydig cell volume correlated significantly with testicular weight (r = 0.70), tubular diameter (r = 0.71), germ cell number per tubule cross-section (r = 0.73), and total tubular length (r = 0.62). In general, although numerically lower, significant correlations between the nuclear volume and the same parameters mentioned earlier were observed.
The total number of Leydig cells per testis in pigs increased rapidly. In fact, this number increased approximately 130-fold from birth to 16 mo of age (Table 3). During this period, two distinct phases of Leydig cell proliferation can be observed. From birth to 1 mo of age, Leydig cell number per testis increased by 700%, whereas approximately 115% of the Leydig cell number increase was observed in pigs from 5 to 6 mo of age. Other periods of evident cell proliferation were also observed during testicular development in Piau pigs. Although not shown in Table 3, the number of Leydig cells per testis in 16-mo-old pigs was significantly higher compared with that in 9-mo-old animals. On the other hand, in the intervals between 4 to 5 mo and 8 to 9 mo, Leydig cell proliferation apparently does not occur. From birth to 4 mo of age, the patterns of Leydig cell and Sertoli cell proliferation were similar. The number of Leydig cells per gram of testis was very high during the first 4 mo of age; after this age, Leydig cell numbers per gram of testis decreased considerably (Table 3).
From birth to adulthood, the number of Leydig cells per testis correlated significantly with testicular weight (r = 0.94), tubular diameter (r = 0.77), total tubular length (r = 0.89), and germ cell number per seminiferous tubule cross-section (r = 0.81). Also, from birth to 4 mo of age, Leydig cell population showed significant correlation with testicular weight (r = 0.85), seminiferous cord/tubule diameter (r = 0.64), total tubular length (r = 0.73), number of Sertoli cells per testis (r = 0.87), and number of germ cells per testis (r = 0.75).
DISCUSSION
To our knowledge, no comprehensive morphometric report has shown the proliferation activity of Sertoli cells and Leydig cells in pigs from birth to 16 mo of age. In the present investigation, Sertoli cell proliferation occurred up to 4 mo of age. The total number of germ cells per testis increased continuously, showing a drastic expansion in number per cross-section of seminiferous tubule from 4 to 5 mo of age and stabilizing its population after 7 mo of age. Except for some brief intervals (i.e., between 4 to 5 mo and 8 to 9 mo), Leydig cells also increased continuously in their population per testis, although at different growth rate. Based on the many parameters analyzed, such as testicular weight, tubular diameter, first spermatids released from the seminiferous epithelium, and plasma levels of testosterone, puberty in Piau pigs occurs between 4 and 5 mo of age. In these pigs, sexual maturity is attained from 7 to 8 mo of age. During this period, a trend occurs toward stabilizing the tubular diameter, the seminiferous tubule and Leydig cell volume density, and the number of germ cells and Sertoli cell nuclei per cross-section of seminiferous tubule. These findings are in agreement with the time period mentioned for the occurrence of puberty and sexual maturity in most pig breeds that have been investigated [33–36].
Based on the total number of Sertoli cells per testis found in Piau pigs, two proliferative phases were evident. The first, and the more prominent, occurred from birth to 1 mo of age, whereas another cell expansion occurred between 3 to 4 mo. This result does not support observations in the literature regarding pigs, in which Sertoli cell mitotic activity is considered not to last beyond 1 to 2 mo after birth [14–16].
The pattern of Sertoli cell proliferation found in Piau pigs also differs from that reported for rats and mice. In these well-studied rodents, Sertoli cell proliferation dropped steadily after birth, ceasing its mitosis completely at approximately 15 and 20 days after birth in mice [12, 13] and rats [1], respectively. Also, our results do not support the general conclusion that Sertoli cell proliferation is maximal at a very early age, as the situation is considered to be for most domestic mammals, including pigs [37]. The pattern of Sertoli cell proliferation in rabbits [37], as determined by the labeling index, is similar to that found in Piau pigs.
In rats and mice, Sertoli cell proliferation ends around the period of the development of the Sertoli cell barrier, tubular fluid secretion and flow, development of the actin cytoskeleton within the Sertoli cell, and extensive primary spermatocytes proliferation [37, 38]. Most of these events occur at approximately 3 to 4 mo of age in pigs [17], which is in agreement with the second phase of Sertoli cell proliferation as found in the present study. Because the germ cell proliferation rate is relatively low before the period preceding Sertoli cell maturation, the seminiferous cord/tubule elongation that occurs during this period probably results from Sertoli cell mitotic activity [18, 39]. The highly significant correlation between Sertoli cell number per testis and the total cord/tubule length found in our study supports this possibility.
The reason for the observed pattern of Sertoli cell mitotic activity in Piau pigs is unknown. The FSH curve found in Piau pigs is very similar to that reported for other pig breeds [40, 41]. Plasma levels of FSH in Piau pigs are higher around the two periods of increased Sertoli cell proliferation, and they parallel the marked increase in length of the seminiferous cord/tubule. The second Sertoli cell proliferative phase coincides with the period during which primary spermatocytes are proliferating actively in pigs. In addition to playing a key role in the mitotic activity of postnatal Sertoli cells, FSH is also important in the maturation of prepubertal Sertoli cells and initiation of the first wave of spermatogenesis [42]. The function of this hormone in the testis of adult mammals is not yet clearly defined. Results of recent studies suggest that FSH is important for the maintenance of quantitatively normal rat spermatogenesis, apparently in a stage-dependent manner [43–45].
The results found for germ cell proliferation in Piau pigs are similar to those reported for other pig breeds [35], and they show that germ cells proliferate continuously, although at a different growth rate, after birth. The apparent decrease in germ cell number observed from birth to 1 mo, as evidenced by the number of cells per cross-section of seminiferous cord, was also observed by Van Vorstenbosh et al. [46] and probably results from the decrease in germ cell numerical density. The growth rate of germ cells during the first month after birth is approximately half that observed for Sertoli cells and the tubular length. Also, during this period, gonocyte mitosis was a common finding, whereas gonocyte apoptosis was rarely seen in the present work. In humans, gonocytes also divide continuously, at a low rate, throughout testicular postnatal development [47]. The data obtained for pigs contrast with the situation as described for rats, mice, and rabbits. In these species, germ cells are quiescent or degenerate massively soon after birth [7, 39, 48, 49]. However, the time interval used in studies involving large animals such as pigs is usually longer, which could mask a possible quiescent period of germ cell proliferation. Because Sertoli cells apparently do not proliferate after puberty, germ cell proliferation is the main factor responsible for the seminiferous tubule growth, both in diameter and length, that occurs after this period.
The remarkably large Leydig cell volume density observed in the present work, particularly in prepubertal testes, is characteristic of boars [20–22, 35]. In accordance with the expanding volume occupied by seminiferous tubules, Leydig cell volume density decreases around the pubertal period [22]. Leydig cell volume density increases again at subsequent ages because of the extended Leydig cell proliferation and increase in cell size observed in our study.
In agreement with our results, data in the literature show that Leydig cell volume and Leydig cell nucleus volume change substantially in pigs during postnatal testicular development [20–24]. Also, as according to the literature for pigs [20, 21], we found two phases of Leydig cell development (i.e., perinatal and pubertal). However, concerning cell size, our data show that Leydig cell volume increases almost 100% at the subsequent ages investigated after the postpubertal period. In pigs, a possible explanation for this cell cycle could relate to LH binding to Leydig cells. In their report, Peyrat et al. [23] concluded that the number of LH receptors per Leydig cell correlated with cell size rather than with stage of sexual maturation.
Except for the period around 1 mo of age, the testosterone levels found in Piau pigs clearly show that the steroidogenic activity of Leydig cells in prepubertal testes is low. In general, this finding is similar to reports for other pig breeds [41, 50, 51]. The elevated testosterone levels observed during the first neonatal weeks coincide with the increased Leydig cell individual volume and correlate with the elevated LH serum levels [52] and higher LH-receptor numbers per cell [23, 41] observed around this period. These data show that as in other pig breeds, and different from the rat model, Leydig cells in Piau boars are fully differentiated at this age.
As observed in Piau pigs, the onset of puberty coincides with a substantial increase in testosterone level, Leydig cell size, and smooth endoplasmic reticulum volume per Leydig cell [24, 36, 40]. Results of studies relating Leydig cell structure to its function in several mammalian species showed that variation in testosterone secretion results from differences in Leydig cell capacity for testosterone secretion rather than from quantitative differences in the mass of the Leydig cells [53]. This capacity is highly correlated with the amount of Leydig cell smooth endoplasmic reticulum [54].
In Piau boars, similar to what has been found for other pig breeds [22], Leydig cell proliferation apparently does not occur during puberty and 2 to 3 mo after this period. However, in our study, the Leydig cell number per testis still increases approximately 60% after the second "resting" phase, showing that Leydig cells still proliferate actively in sexually mature animals. Because most investigations in pigs are not extended after the animals are older than 6 to 8 mo, changes in Leydig cell number per testis and in cell size are not recorded. Because the body weight, testicular weight, and sperm production per testis in Piau boars increases substantially after the postpubertal period [55], the demands for steroids and other substances secreted by Leydig cells are probably higher, requiring more Leydig cells per testis.
In the present work, Sertoli cells, Leydig cells, and germ cells proliferated actively during prepubertal development, with their total number per testis being significantly correlated. Significant correlation was also observed between FSH and testosterone levels during this period. However, in contrast to what has been shown in rats, Vandalen et al. [41] reported no correlation in pigs between evolution of testicular receptors and gonadotropin levels. Results of several studies have shown complex interactions between the seminiferous and interstitial compartments of the testis during development [7]. Sertoli cells can influence Leydig cell proliferation [56] as well as Leydig cell function [7, 57]. On the other hand, Leydig cells also can depress the proliferative response of perinatal Sertoli cells to FSH in vivo [7]. Therefore, the balance between Sertoli cells and Leydig cells as well as the cross-talk between different testicular cell types are critical to allowing the testis to fulfill both its endocrine and exocrine functions [7, 58, 59]. Because of its peculiar characteristics during early postnatal development, the pig testis is a very attractive model for studying cellular interactions and hormonal control of testicular function.
ACKNOWLEDGMENTS
We are grateful to the School of Veterinary Medicine at the Federal University of Minas Gerais for providing the animals utilized in this experiment.
FOOTNOTES
First decision: 30 March 2000.
1 The scholarship awarded to V.A.S. from the Brazilian Foundation (CAPES) is fully appreciated. Financial support from the Minas Gerais State Foundation (FAPEMIG) and FUNDEP/UFMG is gratefully acknowledged. 
2 Correspondence. FAX: 55 31 4992780; lrfranca{at}icb.ufmg.br
Accepted: July 12, 2000.
Received: February 21, 2000.
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T. M. Segatelli, L. R. Franca, P. F. F. Pinheiro, C. C. D. Alemida, M. Martinez, and F. E. Martinez Spermatogenic Cycle Length and Spermatogenic Efficiency in the Gerbil (Meriones unguiculatus) J Androl, November 1, 2004; 25(6): 872 - 880. [Abstract] [Full Text] [PDF]
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S. Walker, O. W. Robison, C. S. Whisnant, and J. P. Cassady Effect of divergent selection for testosterone production on testicular morphology and daily sperm production in boars J Anim Sci, August 1, 2004; 82(8): 2259 - 2263. [Abstract] [Full Text] [PDF]
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A Wagner and R Claus Involvement of glucocorticoids in testicular involution after active immunization of boars against GnRH Reproduction, February 1, 2004; 127(2): 275 - 283. [Abstract] [Full Text] [PDF]
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C.J. Corbin, F.M. Moran, J.D. Vidal, J.J. Ford, T. Wise, S.M. Mapes, V.C. Njar, A.M. Brodie, and A.J. Conley Biochemical Assessment of Limits to Estrogen Synthesis in Porcine Follicles Biol Reprod, August 1, 2003; 69(2): 390 - 397. [Abstract] [Full Text] [PDF]
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L. R. Franca and C. L. Godinho Testis Morphometry, Seminiferous Epithelium Cycle Length, and Daily Sperm Production in Domestic Cats (Felis catus) Biol Reprod, May 1, 2003; 68(5): 1554 - 1561. [Abstract] [Full Text] [PDF]
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D.D. Lunstra, T.H. Wise, and J.J. Ford Sertoli Cells in the Boar Testis: Changes During Development and Compensatory Hypertrophy after Hemicastration at Different Ages Biol Reprod, January 1, 2003; 68(1): 140 - 150. [Abstract] [Full Text] [PDF]
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J. M. Dufour, R. V. Rajotte, and G. S. Korbutt Development of an In Vivo Model to Study Testicular Morphogenesis J Androl, September 1, 2002; 23(5): 635 - 644. [Abstract] [Full Text] [PDF]
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E. S. Neves, H. Chiarini-Garcia, and L. R. Franca Comparative Testis Morphometry and Seminiferous Epithelium Cycle Length in Donkeys and Mules Biol Reprod, July 1, 2002; 67(1): 247 - 255. [Abstract] [Full Text] [PDF]
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L. Benbrahim-Tallaa, E. Tabone, G. Tosser-Klopp, F. Hatey, and M. Benahmed Glutathione S-Transferase Alpha Expressed in Porcine Sertoli Cells Is under the Control of Follicle-Stimulating Hormone and Testosterone Biol Reprod, June 1, 2002; 66(6): 1734 - 1742. [Abstract] [Full Text] [PDF]
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H. Roelants, F. Schneider, F. Goritz, J. Streich, and S. Blottner Seasonal Changes of Spermatogonial Proliferation in Roe Deer, Demonstrated by Flow Cytometric Analysis of c-kit Receptor, in Relation to Follicle-Stimulating Hormone, Luteinizing Hormone, and Testosterone Biol Reprod, February 1, 2002; 66(2): 305 - 312. [Abstract] [Full Text] [PDF]
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J.J. Ford, T.H. Wise, D.D. Lunstra, and G.A. Rohrer Interrelationships of Porcine X and Y Chromosomes with Pituitary Gonadotropins and Testicular Size Biol Reprod, September 1, 2001; 65(3): 906 - 912. [Abstract] [Full Text] [PDF]
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