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Testis |
Laboratory of Cellular Biology, Department of Morphology, Institute of Biological Sciences, Federal University of Minas Gerais, Belo Horizonte, MG, Brazil 31270-901
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ABSTRACT |
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 TOP ABSTRACT INTRODUCTIONMATERIALS AND METHODSRESULTSDISCUSSIONREFERENCES |
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Leydig cells, Sertoli cells, spermatogenesis, testis
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INTRODUCTION |
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TOPABSTRACTINTRODUCTIONMATERIALS AND METHODSRESULTSDISCUSSIONREFERENCES |
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Spermatogenesis is a cyclic and highly coordinated process in which spermatogonia differentiate into mature spermatozoa. This highly organized and complex process encompasses different cell associations called stages, which might be classified according to the changes in the shape of the spermatid nucleus, the occurrence of meiotic divisions, and the arrangement of spermatids within the germinal epithelium [7, 8]. Also, these stages can be identified based on the development of the acrosomic system and the morphology of developing spermatids [9, 10]. The sequence of events that occurs from the disappearance of a given cellular association to its reappearance in a given area of the seminiferous epithelium constitutes the cycle of seminiferous epithelium [9]. The time interval required for one complete series of cellular associations to appear at one point within the tubule is called duration of the cycle of the seminiferous epithelium [9]. The total duration of spermatogenesis, that takes approximately 4.5 cycles, lasts from 30 to 75 days in mammals [11]. Although strain or breed differences can be found in the literature among members of the same species [10, 11], the length of the spermatogenic cycle has been generally considered to be constant for a given species [12]. It is not established yet which genes regulate the duration of spermatogenesis; however, recent work has demonstrated that the spermatogenic cycle length is under the control of germ cell genotype [13].
Most quantitative investigations of spermatogenesis require identification of the stages of seminiferous epithelium cycle and the knowledge of the cycle length [8]. There are few reports in the literature concerning the testis structure, spermatogenic process, and testis morphometry in cats [14–19]. In these studies, the seminiferous epithelium cycle length and quantitative investigation of Sertoli and Leydig cells and daily sperm production were not investigated. In this regard, the objectives of the present study were to perform a more detailed and comprehensive histologic and morphometric investigation of the testis and to estimate the spermatogenic cycle length and daily sperm production in sexually mature cats.
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MATERIALS AND METHODS |
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TOPABSTRACTINTRODUCTIONMATERIALS AND METHODSRESULTSDISCUSSIONREFERENCES |
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Thirteen sexually mature domestic cats (Felis catus) were utilized in the present work. Additionally, 16 testes from sexually mature cats orchyectomized in veterinarian clinics were frozen at -20°C to estimate the tunica albuginea and testis mediastinum relative weights. As sperm production in domestic cats appears unaffected by season [20, 21], the testis samples were not collected at any specific period of the year. Testes were fixed by immersion (n = 6) or were perfused fixed (n = 7) by gravity-fed perfusion through the left ventricle with 0.9% saline and abdominal aorta with 4–5% buffered glutaraldehyde for 25–30 min. Before surgery, all animals received i.m. injection of 0.4 ml of Rompum (Bayer, Leverkusen, Germany) + 0.4 ml of Ketalar (Parke-Davis, Morris Plains, NJ) per kg of body weight. All surgical procedures were performed by a veterinarian and followed approved guidelines for the ethical treatment of animals.
Thymidine Injections and Tissue Preparation
To estimate the duration of seminiferous epithelium cycle, six animals received intratesticular injections of tritiated thymidine (thymidine [methyl-3H], specific activity 82.0 Ci/mmol; Amersham, Life Science, England). The injections of 150 µCi of tritiated thymidine were performed in three different regions (50 µCi in 0.5 ml) of each testis (near the epididymal head, body, and tail) using a hypodermic needle. Two animals were utilized for each time interval considered (1 h, 7 days, and 17 days) after thymidine injections. After fixation by immersion, testes were trimmed out from the epididymis and weighed and cut longitudinally by hand with a razor blade. Tissue samples, measuring 1–3 mm in thickness, were taken near the site of thymidine injections. Testis fragments were routinely processed and embedded in plastic (glycol methacrylate).
To perform autoradiographic analysis, unstained testis sections (3 µm) were dipped in autoradiography emulsion (Kodak NTB-2; Eastman Kodak Company, Rochester, NY) at 45°C. After drying for approximately 1 h at 25°C, sections were placed in sealed black boxes and stored in a refrigerator at 4°C for approximately 8 wk. Subsequently, testis sections were developed in Kodak D-19 solution at 15°C [22] and stained with toluidine blue. Analyses of these sections were performed by light microscopy to detect the most advanced germ cell type labeled at different periods postthymidine injections. Cells were considered labeled when 4–5 or more grains were present over the nucleus in the presence of low-to-moderate background.
Testis Morphometry
To perform light microscopic investigations, testis fragments were routinely processed and embedded in plastic (glycol methacrylate). Subsequently, sections of 3-µm thickness were obtained and stained with toluidine blue. The tubular diameter and the height of seminiferous tubule epithelium were measured at 160x magnification using an ocular micrometer calibrated with a stage micrometer. At least 30 tubular profiles that were round or nearly round were chosen randomly and measured for each animal. The epithelium height was obtained in the same tubules utilized to determine tubular diameter. The volume densities of various testicular tissue components were determined by light microscopy using a 441-intersection grid placed in the ocular of the light microscope. Fifteen fields chosen randomly (6615 points) were scored for each animal at 400x magnification. Artifacts were rarely seen and were not considered in the total number of points utilized to obtain volume densities. Points were classified as one of the following: seminiferous tubule, comprising tunica propria, epithelium, and lumen; Leydig cell; blood and lymphatic vessels; and connective tissue. The volume of each component of the testis was determined as the product of the volume density and testis volume. For subsequent morphometric calculations, the specific gravity of testis tissue was considered to be 1.0. To obtain a more precise measure of testis volume, the testis capsule plus mediastinum were excluded from the testis weight. The total length of seminiferous tubule (meters) was obtained by dividing seminiferous tubule volume by the squared radius of the tubule times the pi value [23].
Stages and the Length of the Seminiferous Epithelium Cycle
Stages of the cycle in cats were characterized based on the shape and location of spermatid nuclei, presence of meiotic divisions, and overall seminiferous epithelium composition [7, 8]. This method provides eight stages of the seminiferous epithelium cycle. The relative stage frequencies were determined from the analysis of 200 seminiferous tubule cross sections per animal at 400x magnification. Both testes were analyzed for each animal. The histological sections utilized were those that presented better quality and more tubular cross sections. The duration of the spermatogenic cycle was estimated based on the stage frequencies and the most advanced germ cell type labeled at different periods postthymidine injections. The total duration of spermatogenesis took into account that approximately 4.5 cycles are necessary for this process to be completed, from type A1 spermatogonia to spermiation [24].
Cell Counts and Cell Numbers
All germ cell nuclei and Sertoli cell nucleoli present at stage 1 of the cycle were counted in 10 round or nearly round seminiferous tubule cross sections, chosen at random, for each animal. These counts were corrected for section thickness and nucleus or nucleolus diameter according to Abercrombie [25], as modified by Amann [26]. For this purpose, 10 nuclei or nucleoli diameters were measured for each cell type analyzed per animal. Cell ratios were obtained from the corrected counts obtained at stage 1. The total number of Sertoli cells was determined from the corrected counts of Sertoli cell nucleoli per seminiferous tubule cross section and the total length of seminiferous tubules according to Hochereau-de Reviers and Lincoln [27]. The daily sperm production (DSP) per testis and per gram of testis (spermatogenic efficiency) were obtained according to the formula developed by França [28] as follow: DSP = total number of Sertoli cells per testis x the ratio of round spermatids to Sertoli cells at stage 1 x stage 1 relative frequency (%)/stage 1 duration (days).
Individual volume of a Leydig cell was obtained from nucleus volume and the proportion between nucleus and cytoplasm. Because the Leydig cell nucleus in cats is spherical, its nucleus volume was obtained from the knowledge of the mean nuclear diameter. For this purpose, 30 nuclei showing evident nucleolus had their diameters measured for each animal. Leydig cell nuclear volume was expressed in µm3 and obtained by 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. One thousand points over Leydig cells were counted for each animal. The number of Leydig cells per testis was estimated from the Leydig cell individual volume and the volume occupied by Leydig cells in the testis parenchyma.
Statistical Analysis
All data are presented as the mean ± SEM. Analysis of correlation was made using the program STATISTICA for Windows (StatSoft, Inc., Tulsa, OK). The significance level considered was P < 0.05.
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RESULTS |
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TOPABSTRACTINTRODUCTIONMATERIALS AND METHODSRESULTSDISCUSSIONREFERENCES |
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The mean testis weight found for the adult cat was approximately 1.2 g, providing a gonadosomatic index (testes mass divided by body weight) of approximately 0.08% (Table 1). The mean weights observed for the left and right testes were very similar (P > 0.05), and no significant correlation was observed between testis weight and body weight (r = 0.36). The mean percentage found for the tunica albuginea was approximately 19%. It was not possible to observe the testis mediastinum macroscopically; in this regard, its weight was not obtained. The volume density of seminiferous tubules and Leydig cells was approximately 90% and 6%, respectively (Table 1). This means that Leydig cells occupy 50% of the intertubular compartment. In this compartment, Leydig cells are organized in clusters and the lymphatic vessels, irregularly shaped, are randomly distributed. The mean tubular diameter and epithelium height were 223 and 81 µm, respectively (Table 1). Based on the volume of the testis parenchyma (testis weight minus tunica albuginea weight) and the volume occupied by seminiferous tubules in the testis and the tubular diameter, approximately 23 m of seminiferous tubules were found per testis and testis gram (Table 1). It should be mentioned that the testis parenchyma weight was almost 1.0 g in the animals investigated in the present work. In this regard, all values expressed per testis and per gram of testis were basically the same. The total length of seminiferous tubules per testis and the Leydig cell volume density showed significant correlation (P < 0.05) with testis weight (r = 0.99 and r = 0.80, respectively). However, no significant correlation (P > 0.05) was observed between tubular diameter and testis weight (r = 0.11).
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Stages of the Seminiferous Epithelium Cycle and Relative Stage Frequencies
The eight stages of the cycle in cats, characterized according to the tubular morphology system, are briefly described in the caption of Figure 1. The mean percentage of each stage of the seminiferous epithelium cycle was as follows: stage 1, 24.9 ± 1.9; stage 2, 12.9 ± 1.0; stage 3, 7.7 ± 1.1; stage 4, 17.6 ± 1.7; stage 5, 7.2 ± 1.4; stage 6, 11.9 ± 0.9; stage 7, 6.8 ± 1.3; and stage 8, 11.0 ± 0.9. As can be observed, stage 1 was the most frequent and stage 7 presented the lowest frequency. The frequencies of premeiotic (stages 1–3), meiotic (stage 4), and postmeiotic (stages 5–8) stages were 45.5%, 17.6%, and 36.9%, respectively.
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It was not uncommon to find abnormally shaped spermatids (data not shown) and missing generations of germ cells in the domestic cat, most noticeable of more advanced cell types (Fig. 2). Seminiferous tubules showing missing generations of germ cells were not utilized for stage frequencies and cell quantification.
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Seminiferous Epithelium Cycle Length
The most advanced labeled germ cell type observed at different time periods investigated after thymidine injections are shown in Table 2 and Figure 3. Approximately 1 h after injection, the most advanced labeled germ cells were identified as preleptotene spermatocytes or cells in transition from preleptotene to leptotene. These cells were present at the beginning of stage 1 and were located in the basal compartment (Fig. 3a). The most advanced germ cell type labeled 7 days after thymidine injection was pachytene spermatocyte at the end of stage 5 (Fig. 3b). At the end of this stage, the elongated spermatid bundles were less evident and were moving toward the seminiferous tubule lumen. Also, at stage 5, intermediate spermatogonia were not present yet. Labeled meiotic figures from both first and second meiotic divisions and secondary spermatocytes present at stage 4 were observed 17 days after thymidine injection (Fig. 3c). Labeled newly formed round spermatids were also eventually observed at late stage 4.
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Based on the most advanced labeled germ cell type observed at each time period investigated postthymidine injections (Figs. 3 and 4) and the stages frequencies, the mean duration of the seminiferous epithelium cycle was estimated to be 10.4 ± 0.3 days (Table 2). The duration of various stages of the cycle was determined taking into account the cycle length and the percentage of occurrence of each stage (Fig. 4). The shortest stage was stage 7 (0.71 days), while the longest stage was stage 1 (2.59 days). Considering that approximately 4.5 cycles are necessary for the spermatogenic process to be completed, the total length of spermatogenesis was estimated as being 46.8 days. The approximate duration of the spermatogonial phase was 16.4 days. While the life span of primary spermatocytes and spermatids was 16.2 and 14.2 days, respectively, the meiotic divisions, corresponding to the duration of stage 4, lasted 1.83 days.
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Testis Morphometry
Leydig cell nuclear volume and cell size were approximately 260 and 2050 µm3, respectively (Table 3). The number of Leydig and Sertoli cells per testis and per gram of testis were similar and around 30 million (Table 3). No significant correlation (P > 0.05) was observed between the Sertoli cell number per testis and testis weight and seminiferous tubule volume (r = 0.67 and r = 0.63, respectively). However, negative and significant correlation (P < 0.05) was found between Sertoli cell number per gram of testis and tubular diameter (r = -0.89). Leydig cell number per testis showed significant correlation (P < 0.05) with testis weight (r = 0.83). Although high (r = 0.71), the correlation between Leydig cell number and seminiferous tubule volume was not significant (P > 0.05).
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The meiotic index, measured as the number of round spermatids produced per pachytene primary spermatocytes, was 2.8 ± 0.3 (data not shown). This result shows that 30% of cell loss occurs during the two meiotic divisions. The Sertoli cell efficiency in cats, estimated from the total number of germ cells, and the number of round spermatids per Sertoli cell was 9.8 ± 0.8 and 5.1 ± 0.6, respectively (data not shown). Approximately eight primary spermatocytes at preleptotene/leptotene or pachytene phase were found per each type A spermatogonia present at stage 1 of the cycle.
The daily sperm production per testis and per gram of testis in domestic cats was approximately 16 million (Table 3). The DSP per testis showed significant correlation (P < 0.05) with the total number of germ cells (r = 0.84) and the number of round spermatids (r = 0.84) per seminiferous tubule cross section at stage 1 of the cycle and also with the meiotic index (r = 0.92). Although relatively high (r = 0.79), DSP did not correlate (P > 0.05) with the ratio of round spermatids per Sertoli cell. Also, no significant correlation (P > 0.05) was observed between the number of Leydig cells per testis and DSP (r = 0.49).
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DISCUSSION |
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TOPABSTRACTINTRODUCTIONMATERIALS AND METHODSRESULTSDISCUSSIONREFERENCES |
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Seminiferous tubules comprise the main compartment of the testis and occupy from 
70% to 90% of testis parenchyma in most mammals investigated [11, 31]. In this regard, compared with other mammalian species, the value found for this parameter in domestic cats is situated in the upper level. The value observed for tubular diameter in the present investigation is similar to that found in other reports for domestic cats [16] and is in the range cited for most mammals investigated (180–350 µm) [32, 33]. In general, 10–15 m of seminiferous tubules are found per gram of testis parenchyma [11, 33]. However, probably due to the fact that the tubular diameter in domestic cats is not high and that almost 90% of seminiferous tubules are found in testis parenchyma, approximately 20 m of tubules per gram are observed in this species.
Compared with most mammals investigated, Leydig cell size and volume density in domestic cats are not low [11, 34]. The organization of Leydig cells observed in the present work, where the lymphatic vessel is located near clusters of Leydig cells, is similar to the type II pattern according to Fawcett and collaborators [35]. Besides producing testosterone, Leydig cells secrete steroids and pheromones that are important for other reproductive functions such as sexual behavior and maintenance of sexual accessory gland function. For instance, it was recently demonstrated that estrogen is important for the male reproductive tract function (see review in Hess et al. [36]). It is also established in the literature that Leydig cell volume is correlated with the amount of smooth endoplasmic reticulum and with its capacity to secrete testosterone [37, 38]. However, it remains to be elucidated why very high variation in Leydig cell organization in the testis [34, 35] is observed in mammals. Also, there is very little knowledge regarding the reason why dramatic variation is observed for Leydig cell volume density (1% in rams to 35% in capybaras) and Leydig cell number per gram of testis (6 million in guinea pigs to 100 million in boars) [11, 34, 39, 40].
To our knowledge, there is only one report in the literature showing the stages of the seminiferous epithelium cycle in domestic cats [15]. In this report, eight stages were characterized according to the acrosomic system and stage frequencies were not determined. From the stage classification herein presented and from the germ cells present at each stage of the cycle, it seems that the criteria utilized by Böhme and Pier [15] were merely an adaptation from the tubular morphology system. As mentioned for other species [41–44], high variation of stage frequencies was observed among different animals investigated in the present work. It is suggested in the literature that stage frequencies grouped in premeiotic and postmeiotic phases of spermatogenesis might be phylogenetically determined among members of the same mammalian family [11, 41–44]. However, because this is the first report in the literature regarding stage frequencies in felines, this aspect of spermatogenesis could not be comparatively analyzed.
A recent study using the spermatogonial transplantation technique showed that the spermatogenic cycle length is under the control of the germ cell genotype [13]. From about 4000 mammalian species alive [45], the duration of spermatogenesis was estimated for only approximately 1% of them. To our knowledge, the spermatogenic cycle length was not determined for any feline species. The data available for the mammalian species investigated to date [46] show that the cycle length ranges from 9 to 12 days in approximately 50% of them. Predominantly, the value found for each spermatogenic cycle in these species is from 10 to 11 days. In this regard, the cycle length found for domestic cats is situated in the predominant range observed for other mammalian species investigated. It should be mentioned that, in mammals in general [11] and in cats in particular, each one of the three phases of spermatogenesis (spermatogonial, meiotic, and spermiogenic) lasts approximately one third of the entire process.
Apoptosis occurs normally during specific steps of germ cell development [47, 48] and can be estimated comparing the ratio of germ cell numbers before and after a given developmental step [11, 49]. In mammals, only 2 or 3 of 10 spermatozoa are produced from differentiated type A1 spermatogonia and, as also observed in cats [17], the highest level of cell degeneration occurs during the spermatogonial proliferative phase and during meiosis [11]. In this regard, similar to what is found for most mammals [11, 48], the meiotic index observed for cats in the present work showed that 30% of cell loss occurred during the two meiotic divisions. We did not investigate the kinetics of spermatogonia in domestic cats. However, compared with other mammals investigated, such as stallions, donkeys, and rabbits [11, 46], the number of primary spermatocytes at preleptotene/leptotene found per each type A spermatogonia present at stage 1 suggests that at least five generations of differentiated spermatogonia are present in this species.
According to Wildt et al. [21], the normal cat ejaculate contains 20–30% abnormally shaped sperm and it is not unusual to find males showing more than 60% sperm pleiomorphisms, which characterizes animals considered as teratospermic. The present study did not aim to investigate these aspects of germ cell development. However, it was not uncommon to find abnormally shaped spermatids in the present investigation. Also, it was not unusual to find missing generations of germ cells. In humans, it is considered that missing generations of germ cells contribute to the low efficiency of spermatogenesis [50]. Missing generations of germ cells are also a common finding after germ cell transplantation in mice [51, 52] and are probably related to the enhanced self-renewing stem cells carry out at the cost of producing differentiating spermatogonia. Missing generations that are most often seen at early time points after colonization begins and at the ends of colonies could also be related to the failure of stem cell division or stem cell degeneration [53]. Although a recent publication has suggested that glial cell line-derived neurotrophic factor is involved with the regulation of spermatogonial stem cell self-renewal and differentiation [54], the biology of stem cell function remains largely unknown [55, 56]. In this regard, it remains to be investigated why, in some species, including the domestic cat, missing generations of germ cells are not a rare finding.
It is currently accepted that the number of Sertoli cells established during testis development determines the rate of sperm production in sexually mature animals [57, 58]. This assumption is based on the fact that each Sertoli cell supports a limited number of germ cells in a species-specific manner [11, 59]. The literature shows that spermatogenic efficiency, expressed as the number of sperm produced daily per gram of testis, is usually positively correlated with the number of germ cells supported by each Sertoli cell [11, 59, 60]. Other important aspects correlated with spermatogenic efficiency are the volume density of seminiferous tubules, the length of spermatogenic cycle, the number of spermatogonial generations, the rate of germ cell loss during spermatogenesis, the number of Sertoli cells per gram of testis, and the size of Sertoli cells [11, 61]. Paradoxically, the higher the Sertoli cell size is, the lower its support capacity for germ cells [31]. Also, as found in the present work, higher numbers of Sertoli cells per gram of testis among individuals from the same species correlate negatively with tubular diameter and consequently with the number of germ cells per tubule cross section.
In general, the number of Sertoli cells per gram of testis found for cats is situated in an intermediate level compared with the values found for most mammalian species investigated [11, 31]. However, Sertoli cell efficiency in domestic cats is one of the lowest among mammals already investigated [11, 59, 60]. In spite of that and probably due to the high seminiferous tubule volume density and the fact that the cycle length is not long in domestic cats, spermatogenic efficiency in this species is moderate.
The significant and positive correlation found in the present work between DSP and the number of germ cells per seminiferous tubule cross sections and the rate of germ cell loss during meiosis showed that these parameters are good predictors of spermatogenic efficiency in domestic cats. Perhaps due to the sample size utilized in the present work, the number of spermatids per Sertoli cell showed no significant correlation with DSP.
In conclusion, the results found in the present investigation will probably provide the baseline for comparative studies with other feline species. Also, these results might help future research in which the spermatogonial transplantation technique could be utilized as a tool to better understand testis function and to preserve the genetic stock from endangered feline species.
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ACKNOWLEDGMENTS |
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FOOTNOTES |
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Received: 31 August 2002.
First decision: 24 September 2002.
Accepted: 13 November 2002.
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REFERENCES |
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TOPABSTRACTINTRODUCTIONMATERIALS AND METHODSRESULTSDISCUSSIONREFERENCES |
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and ß in the reproductive tracts of adult male dogs and cats. Biol Reprod 2002 66:1161-1168This article has been cited by other articles:
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P. Comizzoli, D. E. Wildt, and B. S. Pukazhenthi Poor Centrosomal Function of Cat Testicular Spermatozoa Impairs Embryo Development In Vitro after Intracytoplasmic Sperm Injection Biol Reprod, August 1, 2006; 75(2): 252 - 260. [Abstract] [Full Text] [PDF]
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