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Research Article |
Laboratory of Cellular Biology, Department of Morphology, Institute of Biological Sciences, Federal University of Minas Gerais, 31270–901 Belo Horizonte MG, Brazil
ABSTRACT
Marmosets are New World small primates phylogenetically close to humans and are commonly used in biomedical research. Although the reproductive biology of the common marmoset Callithrix jacchus is fairly well investigated, there are few data available for testis function for its close relative, Callithrix penicillata. In this regard, the present study was performed to investigate testis structure, spermatogenic cycle length, and spermatogenic and Sertoli cell efficiencies in eight captive C. penicillata. These animals received 3H-thymidine injections and had their testes perfused-fixed with glutaraldehyde and embedded in plastic at different time periods after 3H-thymidine injections, for histomorphometric and autoradiographic evaluation. The analysis of the different germ cell associations showed that two or more stages were observed in about 30% of the seminiferous tubule cross sections investigated. The values found for spermatogenic cycle length and for total duration of spermatogenesis in the marmoset C. penicillata, 15.4 and 69.3 days respectively, were very close to those cited in the literature for humans. However, the results observed for Sertoli cell efficiency (number of round spermatids per Sertoli cell; 8:1) and spermatogenic efficiency (daily sperm production per gram of testis; 18.4 million) were substantially higher than those observed for humans. The results found in the present investigation suggest that the black tufted-ear marmoset C. penicillata might represent an alternative and useful experimental model to perform comparative studies regarding the spermatogenic process, particularly in investigations related to the expansion of spermatogonial stem cells and the establishment of spermatogenic waves.
Leydig cells, male reproductive tract, marmoset C. penicillata, morphometry, Sertoli cells, sperm production, spermatogenesis, spermatogenic cycle length, testis
INTRODUCTION
The black tufted-ear marmoset Callithrix penicillata [1] is a small primate belonging to the family Callithricidae of New World monkeys. This is the species of the genus Callithrix with the largest distribution in nature [2]. Another member of the family Callithricidae, the common marmoset Callithrix jacchus, is commonly used in reproductive biology investigations, including testis function, because of the relatively short period necessary for this species to attain sexual maturity (12–18 mo of age) and because of its high fecundity, ease of handling, relatively low cost when compared with other nonhuman primates, and close phylogenetic relationship with humans [3–6]. The reproductive biology in the C. jacchus is fairly well investigated (see review by Li et al. [7]). Despite the very close phylogenetic relationship between C. penicillata and C. jacchus [8], there is little information in the literature regarding the male reproductive tract, and especially spermatogenesis, for the black tufted-ear marmoset C. penicillata. With the development of new technologies such as germ cell transplantation [9, 10] and interspecies testis tissue grafts [11, 12], the marmoset C. penicillata could represent an alternative experimental model to be employed as a receptor for other primates. Also, like its close relative C. jacchus, C. penicillata could be used as a model for comparative and toxicological studies related to the spermatogenic process.
Spermatogenesis is a cyclic, well-organized, highly coordinated process that encompasses different cell associations called stages. In mammals, the stages of the cycle of seminiferous epithelium might be characterized 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 [13–15], and also according to the development of the acrosomic system and the morphology of developing spermatids [16, 17]. The estimation of the spermatogenic cycle length is fundamental to determine spermatogenic efficiency and to perform comparative studies among different species. The total duration of spermatogenesis, which takes approximately 4.5 cycles, is 30–75 days in mammals [17, 18] and has been generally considered to be constant for a given species [19]. Although it is not established yet which genes regulate the duration of spermatogenesis, recent work has demonstrated that the spermatogenic cycle length is under the control of germ cell genotype [20].
Besides being very useful for comparative studies, accurate quantitative evaluation of the testis can provide answers to important questions about testis structure and function and their correlations with physiological and biochemical findings [18, 21]. Most quantitative investigation of the testis requires identification of the stages of the seminiferous epithelium cycle and the knowledge of its duration [14, 18]. Another very important parameter to evaluate testis function is the determination of Sertoli cell efficiency, which is the best indicator of spermatogenic efficiency (daily sperm production per gram of testis [DSP/G/T]). This approach is based on the knowledge that each Sertoli cell is able to support a limited number of germ cells in a species-specific manner, and also because of the fact that the number of Sertoli cells per testis is established before puberty in mammals [18, 22, 23].
Unlike C. jacchus, which has been fairly well investigated, little is known about reproductive biology in the male marmoset C. penicillata. With this in mind, the objectives of the present study were to perform a careful and accurate histological and morphometrical investigation of the testis and to determine the duration of spermatogenesis and Sertoli cell and spermatogenic efficiencies in this species.
MATERIALS AND METHODS
Animals
Seven fully sexually mature and one puberal marmosets (Callithrix penicillata) were used in the present work. These animals were captive and kept in the vivarium of the Federal University of Minas Gerais following approved guidelines for the ethical treatment of animals. Because sperm production in marmosets appears to be unaffected by season [24], the testis samples were not taken at any specific period of the year.
Thymidine Injections and Tissue Preparation
To estimate the duration of the seminiferous epithelium cycle, six animals received intratesticular injections of tritiated thymidine (Thymidine [methyl-3H], specific activity 82.0 Ci/mmol; Amersham Life Science). Injections of 50 µCi of tritiated thymidine in 0.1 ml of aqueous solution were performed in the region of the testis close to the epididymis cauda, using a hypodermic needle. One testis from two different animals was used for each time period interval considered (2–3 h and 10, 14, 15, 16 and 17 days) after thymidine injections. Testes were perfused-fixed by gravity-fed perfusion through the left ventricle with 0.9% saline and abdominal aorta with 4% buffered glutaraldehyde during 25–30 min. Before surgery, all animals received i.p. injection of heparin (125 IU/kg body weight [BW]) and pentobarbital (50 mg/kg BW). After fixation, the testes were trimmed out from the epididymis, weighed, and cut longitudinally by hand with a razor blade. Tissue samples measuring 1–3 mm thick 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 (4 µm) were dipped in autoradiography emulsion (Kodak NTB-2; Eastman Kodak Company) at 45°C. After drying for approximately 1 hour at 25°C, sections were placed in sealed black boxes and stored in a refrigerator at 4°C for approximately 4 weeks. Subsequently, testis sections were developed in Kodak D-19 solution at 15°C [25] 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 time periods post-thymidine 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 as mentioned before. Subsequently, sections of 4 µm in thickness were obtained and stained with toluidine blue. The tubular diameter and the height of seminiferous tubule epithelium were measured at 100x magnification using an ocular micrometer calibrated with a stage micrometer. Thirty 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 used 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. Twenty fields chosen randomly (8820 points) were scored for each animal at 400x magnification. Artifacts were rarely seen and were not considered in the total number of points used 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 [15]. To obtain a more precise measure of testis volume the testis capsule (
7%) was excluded from the testis weight. The total length of seminiferous tubule (m) was obtained by dividing seminiferous tubule volume by the squared radius of the tubule times 
[26].
Stages and the Length of the Seminiferous Epithelium Cycle
Stages of the cycle in marmosets were characterized based on the shape and location of spermatid nuclei, presence of meiotic divisions, and overall seminiferous epithelium composition [13–15]. This method provides eight stages of the seminiferous epithelium cycle, as follows: stage 1, from the release of mature spermatids (spermiation) from the seminiferous epithelium up to the beginning of spermatid nuclei elongation; stage 2, from the beginning of spermatid nuclei elongation to the formation of spermatids bundles; stage 3, from the formation of spermatid bundles to the beginning of the first meiotic divisions; stage 4, ocurrence of the two meiotic divisions and the presence of secondary spermatocytes; stage 5, presence of newly formed round spermatids and spermatid bundles located deeply in the seminiferous epithelium and close to the Sertoli cells nuclei; stage 6, start of spermatid bundles' dissociation and migration toward the tubular lumen; stage 7, complete dissociation and migration of spermatid bundles toward the tubular lumen and beginning of the formation of residual bodies; and stage 8, from the beginning to the end of spermiation. The relative stage frequencies were determined from the analysis of approximately 210 seminiferous tubule cross sections per animal, at 190x or 400x magnification. The camera lucida was used at 190x magnification to draw the seminiferous tubule cross sections containing more than one stage of the cycle, allowing the determination of stage frequencies in these sections [27, 28]. Both testes were analyzed for each animal. The histological sections used were those that presented better quality and more tubular cross sections. We have attempted to characterize the stages of the cycle according to the acrosomic system using periodic acid-Schiff-stained slides. However, because of the very high degree of variation of the acrosome develoment in spermatids observed in the same seminiferous tubule cross section and stage, we did not feel confident in using this system for C. penicillata.
The duration of the spermatogenic cycle was estimated based on the stage frequencies and the most advanced germ cell type labeled at different time periods post-thymidine injections. The total duration of spermatogenesis took into account that approximately 4.5 cycles are necessary for this process to be completed, from type A spermatogonia to spermiation [29]. Because primary spermatocytes' nuclear volume grows markedly during meiotic prophase [18, 30, 31], the size of their nuclei was used to determine more precisely the location of the most advanced labeled germ cell, particularly when these cells were present in stages showing high frequency.
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 [32], as modified by Amann [33]. For this purpose, 10 nuclei or nucleoli diameters were measured per animal for each cell type analyzed. 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 sections and the total length of seminiferous tubules according to Hochereau-de Reviers and Lincoln [34]. The daily sperm production (DSP) per testis and DSP/G/T (spermatogenic efficiency) were obtained according to the formula developed by França [35], as follows: DSP = total number of Sertoli cells per testis x ratio of round spermatids to Sertoli cells at stage 1 x stage 1 relative frequency (%)/Stage 1 duration (days).
Individual volume of the Leydig cell was obtained from nucleus volume and the proportion between nucleus and cytoplasm. Because the Leydig cell nucleus in marmosets 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 diameter measured for each animal. Leydig cell nuclear volume was expressed in µm3 and obtained by the formula 4/3R3, 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 cell in the testis parenchyma.
Statistical Analysis
All data are presented as the mean ± SEM. Analysis of correlation were made using the program STATISTICA for windows (StatSoft, Inc.). The significance level considered was P < 0.05.
RESULTS
Biometric Data and Testis Volume Density
All data are presented in Table 1. The mean testis weight found for the marmosets was approximately 540 mg, providing a gonadosomatic index (GSI; testes mass divided by body weight) of approximately 0.36%. The mean percentage found for the tunica albuginea was approximately 7%. It was not possible to observe the testis mediastinum macroscopically, so its weight was not obtained. The volume density of seminiferous tubules and Leydig cells was approximately 92% and 2%, respectively (Table 1). This means that Leydig cells occupied only 25% of the intertubular compartment. In this compartment, Leydig cells are organized in clusters (not shown). The mean tubular diameter and epithelium height were 260 µm and 87 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 9 m of seminiferous tubules were found per testis and 18 m per testis gram (Table 1). It should be mentioned that because the testis parenchyma weight was aproximatelly 0.5 g in the animals investigated in the present work, the values expressed per gram of testis were basically twice the values obtained per testis. The total length of seminiferous tubules per testis showed significant correlation (P < 0.05) with testis weight, tubular volume, and GSI (r = 0.97, 0.95, and 0.93, respectively).
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Stages of the Seminiferous Epithelium Cycle and Relative Stage Frequencies
The eight stages of the cycle in marmosets, characterized according to the tubular morphology system, are briefly described in the legend to Figure 1. The mean percentages of the seminiferous epithelium cycle for each stage were as follows: stage 1, 24.0 ± 3; stage 2, 12.5 ± 1; stage 3, 22.7 ± 2; stage 4, 8.1 ± 1; stage 5, 9.6 ± 1; stage 6, 4.9 ± 1; stage 7, 5.5 ± 1; and stage 8, 12.7 ± 1. As it can be observed, stage 1 was the most frequent (25%) and stages 6 and 7 presented the lowest frequencies (5%). The frequencies of premeiotic (stage 1 to stage 3), meiotic (stage 4) and postmeiotic (stage 5 to stage 8) stages were 60%, 8%, and 30%, respectively.
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Approximately 70% of 1200 tubular profiles analyzed in marmosets showed only one stage per seminiferous tubule cross section, whereas 30% showed two or three cellular associations (stages) per cross section. In the latter, approximately 80% showed two stages per cross section, and 20% showed three stages (Fig. 2). In these cross sections, the most predominant germ cell associations were stages 2–3 (20%), 4–5 (14%), and 3–4–5 (13%). Although present, germ cells associations such as stages 1–5–8, 5–6–8, and 1–5–7 were rarely seen (0.3%). We have not observed any tubular cross sections with more than three different germ cells associations.
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Seminiferous Epithelium Cycle Length
The most advanced germ cells labeled at different time periods investigated after thymidine injections are shown in Table 2 and Figure 3. Two to three hours after injection, the most advanced germ cells labeled were identified as preleptotene/leptotene spermatocytes. These cells were present at the beginning of stage 2 and were located in the basal compartment (Fig. 3a). The most advanced germ cells labeled observed between 10 and 17 days after thymidine injection were pachytene spermatocyte at the end of stage 7 (10 days; Fig. 3b), in the last third of stage 1 (14 days; Fig. 3c), at the beginning of stage 2 (15 days; Fig. 3d), in the second half of stage 2 (16 days; Fig. 3e), and at the beginning of stage 3 (17 days; Fig. 3f). Based on the most advanced labeled germ cells observed at each time period investigated post-thymidine injections, and the stages' frequencies, the mean duration of the seminiferous epithelium cycle was estimated to be 15.4 ± 0.1 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). As expected, the stage with the shortest duration was stage 6 (0.76 days), whereas the longest stage was stage 1 (3.69 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 69.1 days. The approximate duration of the spermatogonial phase was 23 days, whereas the lifespans of primary spermatocytes and spermatids was 26 days and 20 days, respectively. The meiotic divisions, corresponding to the duration of stage 4, lasted 1.24 days.
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Testis Morphometry
Leydig cell nuclear volume and Leydig cell individual size were approximately 330 µm3 and 1400 µm3, respectively (Table 3). The number of Leydig and Sertoli cells per testis were 7.2 and 17.1 million and per gram of testis were 13.9 and 34.7 million, respectively (Table 3). Significant and positive correlation (P < 0.05) was observed between Sertoli cell number per testis and body weight, testis weight, and seminiferous tubule volume (r = 0.82, 0.84, and 0.85, respectively). Leydig cell number per testis showed significant correlation (P < 0.05) with body weight and blood vessels volume (r = 0.85 and 0.91, respectively). However, the correlation between Leydig cell number per testis and seminiferous tubule volume was not significant (r = 0.63).
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The meiotic index, measured as the number of round spermatids produced per pachytene primary spermatocyte, was 3.4 ± 0.1. This result shows that 15% of germ cell loss occurs during the two meiotic divisions. The Sertoli cell efficiency in marmosets, estimated from the number of round spermatids per Sertoli cell, was 8.0 ± 0.4. Approximately six primary spermatocytes at the preleptotene/leptotene phase were found per each type A spermatogonia present at stage 1 of the cycle.
DSP per testis and DSP/G/T in captive marmosets was approximately 9 and 18 million, respectively (Table 3). DSP/G/T showed significant and positive correlation (P < 0.05) with the ratio of round spermatids per Sertoli cell (r = 0.88).
DISCUSSION
The common marmoset C. jacchus is a well-established experimental model for performing toxicological studies and investigating reproductive biology in primates. In the present work we performed a careful and accurate histological and morphometrical investigation of the testis in the marmoset C. penicillata, including the determination of spermatogenic cycle length and Sertoli cell and spermatogenic efficiencies, and suggest that this species might also be useful for comparative studies involving primates, particularly for studies related to the spermatogenic process.
The GSI found for the marmosets investigated in the present study is high when compared with that of primate species such as men and gorillas (Gorilla gorilla beringei) [36, 37]. At least in part, the higher GSI observed for C. penicillata is related to the very high seminiferous tubule volume density observed for this species, which is 50% higher than the values observed for men [37]. The value observed for tubular diameter in the present investigation is similar to that found for the common marmoset [38].
Little information is available in the literature concerning the cytoarchitecture and the volume density of Leydig cells in primates, and it still remains to be elucidated why very high variation in Leydig cell organization in the testis, and Leydig cell size and number per gram of testis, is observed in mammals [39, 40–44]. The organization of Leydig cells observed in the present work is similar to that of humans [40] and to the type II pattern according to Fawcett et al. [39]. Comparatively, the values found for Leydig cell size and number per gram of testis in C. penicillata are very low. Particularly, the Leydig cell size observed for C. penicillata in the present work represents 50% of the mean value observed for men [45–47].
Two different topographical arrangements of the stages of the seminiferous epithelium cycle are observed in mammals. In the first, named segmental and present in the vast majority of mammalian species investigated up to the present moment, only one stage is usually found per seminiferous tubule cross section, whereas in the helical arrangement, found in humans and some primates such as chimpanzees (Pan troglodytes), two or more stages are present per tubule cross section [5, 27, 48–50]. There are yet other primate species (Papio anubis and Macaca fascicularis), including the marmoset C. penicillata, in which an intermediate situation between segmental and helical is observed [51, 52]. Differently from what is cited for the common marmoset C. jacchus [5] and similarly to what was observed in the cynomolgus monkey (M. fascicularis) [52] and in the olive baboon (P. anubis) [51], only 30% of the tubular cross sections analyzed in C. penicillata showed more than one germ cell association. Recent investigation [53] indicates that the variation observed for stage arrangement in primates is not related to phylogeny, spermatogenic efficiency, or mating system. Surely, more studies are necessary to elucidate this interesting aspect of spermatogenesis observed in some primate species.
As mentioned for other mammalian species [15, 31, 54], a 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 [15, 18, 31, 54]. In this aspect, the premeiotic and postmeiotic phases frequencies obtained for C. penicillata in this study were similar to those of the other investigated species of the Callitrichidae family [C. jacchus; 53].
Although we attempted to do so, because of the lack of rigid synchronization and less-organized spermatogenesis, we did not succeed in precisely characterizing the stages of the cycle using acrosomic system methodology. Indeed, this is a common difficulty found in other studies with primates, including humans [27] and the marmoset C. jacchus [5, 55]. In fact, the methodologies used in these studies are similar to the tubular methodology system employed in the present work, and adjustment of the stages frequencies would provide results similar to the ones found for C. penicillata.
The spermatogenic cycle length is under the control of the germ cell genotype [20], and this parameter has been determined for only 1.5% of the 4000 of mammalian species still alive [56]. For the mammalian species already investigated, the predominant value observed for each spermatogenic cycle is from 10 to 11 days. Thus, although very similar to that observed for men [57], in general the cycle length found for marmosets in the present study is higher than the values found for several mammalian species investigated, including most primates and the marmoset C. jacchus (10 days). This is a good illustration of the assumption that the duration of spermatogenesis is a species-specific event and is not phylogenetically determined [29]. However, in all species investigated up to date, 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 [58, 59] and can be estimated comparing the ratio of germ cell numbers before and after a given developmental step [18, 60]. In mammals, only 2 or 3 out of 10 spermatozoa are produced from the initial differentiated type A spermatogonia, and the highest level of cell degeneration occurs during the spermatogonial proliferative phase and during meiosis [18]. The germ cell loss observed for marmoset in the present work (15%) was similar to that found for the marmoset C. jacchus [5] and much lower than the value observed for men (70%) [61] and most other mammalian species (25%) [18, 62–64]. Similarly to what has been observed for C. jacchus [4, 5], our quantitative results suggest the existence of approximately four generations of differentiated spermatogonia in C. penicillata.
The number of Sertoli cells established before puberty determines the rate of sperm production in adult animals [22, 65, 66], because each Sertoli cell supports a limited number of germ cells in a species-specific manner [18, 66, 67]. In this regard, as found in the present work, spermatogenic efficiency, expressed as the number of sperm produced daily per gram of testis, usually correlates positively with the number of germ cells supported by each Sertoli cell [18, 49, 67]. The volume density of seminiferous tubules, the length of the 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 are also important factors in the determination of spermatogenic efficiency [18, 66, 68].
The number of Sertoli cells per gram of testis found for C. penicillata is situated at an intermediate level compared to the values found for most mammalian species already investigated [18, 66, 69], being, however, 25% lower than the value observed for men [64], and similar to the value found for the marmoset C. jacchus [5]. Also, compared with other mammals already investigated [18, 49, 67], Sertoli cell efficiency in C. penicillata is situated at an intermediate level. However, the value found for Sertoli cell efficiency in this species is 2.5 times higher than that found for humans [61, 64].
The daily sperm production per gram of testis (DSP/G/T or spermatogenic efficiency) observed for C. penicillata is four times higher than the values cited for humans and 25% lower when compared with rhesus monkey (M. mulatta) [64, 70]. Although the spermatogenic cycle length in C. penicillata and humans is similar, the much higher spermatogenic efficiency (DSP/G/T) found for C. penicillata is probably because of the higher volume density of seminiferous tubules and the higher efficiency of Sertoli cells observed for this marmoset species.
Marmosets are considered an excellent experimental model for toxicological and comparative studies involving several aspects of primate reproductive biology. However, when they are compared to humans, it is important to mention that there are important differences of the reproductive system of marmosets, which may limit the use of this species in such studies. For instance, among the particularities of marmosets can be cited the generation of uniplacental twins, the primitive testicular differentiation at birth, the deletion of exon 10 in the LH receptor, and the dependence on hCG for testis maturation and function [see review in Li et al. 2005 (7)].
Finally, although the values observed for several parameters investigated in the present work differ significantly from those observed for humans, the arrangement of germ cells associations and particularly the duration of spermatogenesis are similar in these two primate species. These aspects and the phylogenetic proximity between humans and the marmoset C. penicillata [5, 71] suggest that this species might represent an alternative and useful experimental model for performing comparative studies regarding the spermatogenic process, particularly investigations related to the expansion of spermatogonial stem cells and the establishment of spermatogenic waves. Also, the results found in the present study might be useful for biomedical research in which the spermatogonial transplantation and testis graft techniques could be used as a tool to better understand testis function and to preserve the genetic stock from endangered primate species.
ACKNOWLEDGMENTS
Technical help from Rubens Miranda and Adriano Ferreira is highly appreciated.
FOOTNOTES
1 Supported by the Brazilian Foundations CAPES and CNPq 
2 Correspondence. FAX: 55 31 34992780; lrfranca{at}icb.ufmg.br
Received: 29 September 2005.
First decision: 14 October 2005.
Accepted: 29 November 2005.
REFERENCES
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