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Male Reproductive Tract |
a Center of Electron Microscopy, School of Medical Sciences, National University of Cordoba, C.P. 5000, Córdoba, Argentina
b Division of Immunogenetics, School of Medicine, University of Buenos Aires, C.P. 1120, Buenos Aires, Argentina
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ABSTRACT |
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 TOP ABSTRACT INTRODUCTIONMATERIALS AND METHODSRESULTSDISCUSSIONREFERENCES |
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apoptosis, immunology, Sertoli cells, spermatogenesis
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INTRODUCTION |
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TOPABSTRACTINTRODUCTIONMATERIALS AND METHODSRESULTSDISCUSSIONREFERENCES |
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By cross-linking T-cell surface glycoproteins, Gal-1 induces apoptosis of activated, but not resting, T cells through ERK (extracellular regulated kinase) phosphorylation and activation of specific transcription factors [7, 12–14]. Moreover, at concentrations under its apoptotic threshold, this ß-galactoside-binding protein inhibits T-cell adhesion to extracellular matrix glycoproteins and proinflammatory cytokine secretion [15].
Galectin-1 has immunosuppressive and anti-inflammatory effects in experimental models of autoimmunity and chronic inflammation [16, 17]. We have recently shown, using gene-therapy strategies, that Gal-1 ameliorates inflammation in a collagen-induced arthritis model [16]. Investigation of the molecular mechanisms involved in this process revealed that Gal-1 treatment increases T-cell susceptibility to activation-induced cell death and promotes a shift from a Th1 to a Th2 cytokine profile [16]. We have also shown that Gal-1 plays a key role in the resolution of acute inflammation [18].
Because of its ability to inhibit T-cell effector functions, we hypothesized that expression of endogenous Gal-1 could function as a novel mechanism to confer immune privilege to vulnerable sites such as reproductive cells. Immune privilege is a term applied to several tissues having a unique relationship with the immune response. These sites prevent the spread of inflammation, because even minor episodes can threaten organ integrity and function [19, 20]. The most prominent examples are the eye, the brain, the testis, and the ovary, in which immune responses either do not proceed or proceed in a manner different from that in other areas [20]. It has long been known that the testis is an immunologically privileged site and that the human seminal plasma possesses a generalized immunosuppressive activity [19]. Multiple factors participate in the establishment of immunotolerance in the testis, such as the blood-testis barrier and the local production of immunosuppressive molecules and proapoptotic mediators by Sertoli cells [20–24]. The latter also express high levels of Fas ligand, which has been shown to initiate the killing of Fas-bearing infiltrating T cells and Fas-expressing defective germ cells [25–27]. However, recent findings suggest that Fas ligand has controversial proinflammatory effects, suggesting that other apoptotic mediators might contribute to the establishment of the immune privilege [28]. Interestingly, immunohistochemical studies showed that Gal-1 is expressed profusely at sites of immune privilege, where the regulation of apoptotic processes is crucial [11, 29, 30]. Furthermore, this sugar-binding protein might also contribute to interactions between different cell types at some stages during spermatogenesis and during sperm-egg binding.
In the present study, we investigated the expression and ultrastructural localization of Gal-1 in normal rat testis by Western blot analysis, immunohistochemistry, and immunoelectron microscopy as well as its regulation during postnatal testis development.
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MATERIALS AND METHODS |
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TOPABSTRACTINTRODUCTIONMATERIALS AND METHODSRESULTSDISCUSSIONREFERENCES |
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Male Wistar rats (aged 9, 15, 30, 45, and 60 days) were used in this study. Animals were housed and cared for at the Animal Resource Facilities, Faculty of Medical Sciences, National University of Córdoba, in accordance with the National Research Council publication Guide for Care and Use of Laboratory Animals and institutional guidelines. Animals were maintained under a photoperiod of 14L:10D with food and water available ad libitum.
Tissue Processing
Animals were anesthetized with an i.p. injection of a chloral hydrate solution (0.25 g/kg body weight). One testis was dissected, minced, and homogenized in 1 ml of ice-cold lysis buffer (PBS containing 5 mM EDTA, 1% [w/v] NP40, 0.5% [w/v] sodium deoxycholate, 0.1% [w/v] SDS, 124.5 mM KCl, 5 mM MgCl2, and 10 mM Hepes [pH 7.2]) plus protease-inhibitor cocktail (0.2 mM PMSF, 0.1% [w/v] aprotinin. 0.7 µg/ml of pepstatin, and 1 µg/ml of leupeptin) and incubated for 30 min on ice. Samples were finally centrifuged at 15 000 x g for 20 min at 4°C, and the supernatant fluid of the whole-tissue homogenates was stored at -70°C until use. Protein concentration was estimated by using the micro-BCA Protein Assay reagent kit (Pierce, Rockford, IL).
The other testis was fixed by perfusion with 4% paraformaldehyde in 0.1 M cacodylate buffer at pH 7.4 and then embedded in paraffin for light-microscopic immunocytochemistry. For ultrastructural immunocytochemistry, testes perfused with a mixture of 4% paraformaldehyde and 1.5% glutaraldehyde were cut with razor blades in small pieces (1 x 1 x 2 mm) and embedded in LR-White (London Resin Co, Hampshire, U.K.) after partial dehydration in increasing concentrations of ethanol solutions up to 90%, followed by incubation overnight in pure monomer and polymerization at 50°C.
Western Blot Analysis
The SDS-PAGE was carried out in a Miniprotean II electrophoresis apparatus (Bio-Rad, Richmond, CA) as described by Laemmli [31]. Briefly, total tissue homogenates corresponding to normal rat testis of 9, 15, 30, and 60 days of age (30 µg of protein each) were diluted in electrophoresis sample buffer and boiled for 90 sec. Equal amounts of proteins for each lysate were then resolved on a 15% separating polyacrylamide slab gel. Protein bands were detected using Coomassie brilliant blue R250. After electrophoresis, the separated proteins were transferred onto nitrocellulose membranes, blocked for 1.5 h using 5% (w/v) nonfat dried milk in PBS containing 0.05% (v/v) Tween-20, and probed for 3 h with a 1:2000 dilution of an anti-Gal-1 polyclonal antibody as described elsewhere [16]. Blots were then incubated for 1 h with a 1:3000 dilution of a horseradish peroxidase-conjugated goat anti-rabbit immunoglobulin (Ig) G (Bio-Rad). Finally, the peroxidase reaction product was developed in 50 mM Tris-HCl (pH 7.4) containing 0.05% (w/v) 4-chloro-1-naphthol and 0.03% (v/v) hydrogen peroxide. Recombinant Gal-1 (rGal-1; kindly donated by Drs. J. Hirabayashi and K.I. Kasai, Faculty of Pharmaceutical Sciences, Teikyo University, Japan) was used as a positive control of immunodetection. Control of specific immunoreaction was performed by incubation of the blots with a rabbit preimmune serum without detecting any reactivity. The anti-Gal-1 antibody was monospecific, because it did not recognize other galectins, such as rGal-3 [10]. Equal loading and extract degradation were checked by Ponceau S staining and by using an anti-
-tubulin (DM1A) monoclonal antibody. Rainbow protein molecular weight markers were purchased from Bio-Rad. The immunoreactive protein bands were analyzed with the Fotodyne Image Analyzer (Fotodyne, Inc., Hartland, WI). Results were expressed as relative densitometric values by means of the Image Quant software (Molecular Dynamics, Sunnyvale, CA).
Gold-Complex Preparation
Colloidal gold particles (average diameter, 16 nm) were prepared according to the method of Frens [32] using sodium citrate as a reducing agent. Then, particles were adsorbed to an IgG fraction purified from a goat antiserum raised against rabbit IgG (Sigma Chemical Co., St. Louis, MO). Approximately 0.25 µg of protein was necessary to stabilize 1 µl of colloidal gold solution. Finally, the gold complex was centrifuged at 60 000 x g for 2 h before use and the pellet resuspended in PBS containing 0.01% (w/v) polyethylene glycol.
Light Microscopic Immunocytochemistry
For Gal-1 immunodetection by light microscopic immunocytochemistry, paraffin sections (thickness, 5 µm) were mounted on glass slides coated with 1% polylysine, deparaffinized with xylene, and rehydrated. Then, the sections were incubated with a drop of 1% BSA in PBS for 15 min at room temperature in a humidified chamber to block nonspecific binding sites, followed by incubation with rabbit anti-Gal-1 antibody (diluted 1:1000 in 1% BSA-PBS) for 24 h at 4°C. After three washes with PBS, slides were incubated with a 1:6 dilution of the anti-rabbit IgG-gold complex for 1 h at room temperature. A silver enhancement kit (Sigma) was used to visualize the gold particles at the light-microscopic level. After washing with tridistilled water, the sections were mounted on glass slides and studied in a Zeiss Photomicroscope III (Oberkochen, Germany). Spermatogenic stages were identified according to the method of Leblond and Clermont [33], who defined the 14 stages of the seminiferous cycle in the rat.
Ultrastructural Immunohistochemistry
Thin sections cut from LR-White-embedded tissues were mounted on 300-mesh nickel grids. The grids were floated onto a drop of 1% BSA-PBS for 15 min at room temperature. Then, the sections were incubated with rabbit anti-Gal-1 antibody (diluted 1:3000 in BSA-PBS) for 24 h at 4°C. After washing with PBS, the grids were incubated with anti-rabbit IgG-gold complex diluted 1:20 for 30 min at room temperature. Sections were finally examined in a Siemens Elmiskop 101 transmission electron microscope (Karlsruhe, Germany). Controls of immunoreactivity were performed by incubating LR-White thin sections or paraffin sections with normal rabbit serum or by preadsorbing the anti-Gal-1 antibody with rGal-1.
Pre-Embedding Immunolocalization of Gal-1 in Epididymal Spermatozoa
Spermatozoa were obtained from the caput epididymis after several punctures with a 20-gauge hypodermic needle. The epididymal fluid was collected in a glass vessel containing 25 ml of PBS and then placed in an oven at 34°C for 15 min to allow sedimentation of cellular debris. The upper fraction was collected in a centrifuge tube, spun for 10 min at 1000 rpm, and resuspended in PBS. Cells were then washed through subsequent centrifugations. The collected spermatozoa were resuspended in a blocking solution containing 1% normal goat serum in PBS and incubated for 15 min at room temperature. Blocking solution was discarded, and cells were incubated overnight at 4°C with rabbit anti-Gal-1 antibody diluted 1:1000 or in normal rabbit serum (at the same dilution) for control purposes. After washing, bound antibodies were detected with the anti-rabbit Ig-colloidal complex (1:10 dilution) for 30 min at room temperature.
Following three washes, cells were fixed with 1% glutaraldehyde in 0.1 mM cacodylate buffer at pH 7.4 for 1 h and postfixed for 1 h with 1% osmium tetroxide in the same buffer. Then, the samples were dehydrated in a series of graded acetones and embedded in Araldite (Electron Microscopy Sciences, Fort Washington, PA). Thin sections cut in a Porter-Blum MT2 ultramicrotome (Sorvall Inc., Newtown, CT) were studied in a Siemens Elmiskop 101 electron microscope.
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RESULTS |
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TOPABSTRACTINTRODUCTIONMATERIALS AND METHODSRESULTSDISCUSSIONREFERENCES |
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Testis samples of 9-, 15-, 30-, and 60-day-old rats with equal amounts of protein (30 µg) were analyzed by Western blot. As shown in Figure 1, Gal-1 expression increased in an age-dependent manner in postnatal rat testis. A weak immunoreactivity was found in testes of 9- and 15-day-old rats, but a marked increase in Gal-1 expression was observed when testes were obtained from 30- and 60-day-old rats (Fig. 1). This finding suggests a developmentally regulated expression of this ß-galactoside-binding protein in postnatal testis.
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Immunohistochemistry of Gal-1 at the light- and electron-microscopic levels with colloidal gold/antibody complex and silver enhancement technique revealed that seminiferous tubules of 9-, 15-, and 30-day-old rats were almost negative. Immunostaining of Gal-1 was first detected at 45 days and restricted to a basal portion of the seminiferous epithelium, where it was associated with the nucleus and cytoplasm of Sertoli cells (Fig. 2A). Moreover, interstitial cells exhibited an intense immunolabeling. In contrast, in the testes of 60-day-old rats, a strong Gal-1 immunoreactivity was detected in all seminiferous tubules, with a typical distribution that appeared to be modulated according to different stages of the spermatogenic process. At stages X and II, gold/silver labeling delineated the typical columnar profile of Sertoli cells stretching from the basal membrane to the lumen of seminiferous tubules (Fig. 2B). At these stages, germ cells and luminal space were found to be negative.
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On the other hand, at the following stage of spermiation, immunolabeling progressively increased at the apical regions of the seminiferous epithelium (Fig. 2, C–G), whereas it diminished at the basal and intermediate levels. At stages VI and VII (Fig. 2, D–F), Gal-1 was localized mainly at the level of late spermatid heads and at apical processes of Sertoli cells, which were tightly associated with developing spermatids before their release into the tubular lumen. In Figure 2F, the strong luminal staining highlights two regions: the first corresponding to late spermatid heads and the second associated with spermatid tails projecting toward the lumen of the seminiferous tubules. At these stages, Sertoli cells were negative in their middle segment (stage VI) (Fig. 2, C and D) or their basal areas (stage VII) (Fig. 2, E and F). Finally, when the spermiation process was completed (stage VIII) (Fig. 2G), specific staining was found in spermatozoa that were free in the tubular lumen, whereas the basal seminiferous epithelium, associated to Sertoli cell nuclei, was being replenished with Gal-1. Spermatocytes and round spermatids were negative at all stages. No labeling was detected in control sections incubated with preimmune serum instead of with primary antibody (Fig. 2H).
Immunoelectron microscopy confirmed the distribution of Gal-1 described at the light-microscopic level. The labeling of Sertoli cells was observed at the apical projections during spermiation (Figs. 3–6); Figure 7 shows control sections incubated with normal rabbit serum. Also, an intense labeling was associated with nuclei and tails of late spermatids still anchored to the epithelium (Figs. 3, 4, and 6) or free in the lumen (Figs. 8 and 9). The cytoplasm of late spermatids exhibited a weak immunogold staining, the density of which increased after transformation into residual bodies (Fig. 10). Furthermore, immunostaining was also found at the thin laminar processes of the apical pole of Sertoli cells that engulfed residual bodies (Fig. 10).
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Finally, strong Gal-1 immunoreactivity was found in epididymal spermatozoa processed for pre-embedding immunoelectron microscopy. A marked staining occurred around the head plasma membrane, whereas a weak immunoreactivity was found in spermatozoa tails (Fig. 11, a and b). To investigate whether Gal-1 exists in the cell surface of spermatozoa by ß-galactoside-dependent binding, lactose (100 mM) was added to the buffer when sperm cells were isolated. Immunostaining was partially inhibited (data not shown), suggesting that at least part of the Gal-1 present at the heads of sperm cells are bound to the cell surface through its CRD.
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DISCUSSION |
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TOPABSTRACTINTRODUCTIONMATERIALS AND METHODSRESULTSDISCUSSIONREFERENCES |
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In the present study, we reported the expression of Gal-1 regulated throughout postnatal development and its stage-specific distribution in the seminiferous tubules of adult rat testis. Expression of Gal-1 was first detected by Western blot analysis in 9-day-old testis and increased in an age-dependent manner during postnatal development. By immunocytochemistry, positive staining was detected after 45 days at the level of Sertoli cells. After puberty, Gal-1 expression exhibited a stage-specific pattern at the level of Sertoli cells during spermatogenesis. Moreover, heads and tails of late spermatids and spermatozoids were strongly stained, suggesting a potential role for this immunosuppressive protein in the establishment of immune tolerance not only at the level of the male ejaculatory tract but also in the female reproductive tract.
Sertoli cells are somatic cells that stretch from the basal lamina to the lumen of the seminiferous tubules, with key functions in blood-testis barrier development and spermatogenesis [36]. All stages of spermatogenesis take place while the developing gametes are in intimate relationship with Sertoli cells. This facilitates the progression of germ cells to spermatozoa and the control of the milieu within the compartments of seminiferous tubules by means of paracrine signaling. Many functions of Sertoli cells are apparently carried out through a variety of proteins that are secreted to the adluminal compartment, such as the Müllerian-inhibitory substance and inhibin [37]. They also produce a number of immunosuppressive and homeostatic factors [19].
Wollina et al. [30], using immunohistochemistry, recently described the presence of Gal-1 in human testis. In the present study, we provide evidence that the expression and localization of this sugar-binding protein is modulated throughout the different stages of the tubular seminiferous cycle in tight correlation with spermatogenesis. Although we found that all seminiferous tubules express Gal-1 in Sertoli cells, the whole cell body was only stained at stages X–II, corresponding to stages of meiotic division. Moreover, during spermiation stages (stages V–VII), Gal-1 was restricted to apical processes of Sertoli cells, enveloping the heads of mature spermatids and the eccentric lobes of redundant cytoplasm. Following spermiation, Gal-1 was replenished at the basal portion of Sertoli cells and progressively spread out through the whole cell body.
A cyclic activity has been described for Sertoli cells [38], with many genes being differentially expressed during different stages of spermatogenesis. In this sense, a group of growth factors and immunosuppressive products derived from Sertoli cells are secreted during periods of meiotic division, whereas others are only synthesized during spermiation stages [39]. Our observations concerning a cyclic distribution of Gal-1 in Sertoli cells support the idea that these somatic cells might have two different functional modes: a first mode, with maximal levels of mRNA for specific Sertoli cell products roughly found at stages VII–IX, and a second mode, in which maximal levels are found at stages XIII–III [40]. By the time this paper was submitted, Timmons et al. [41] reported that Gal-1 mRNA levels in the mouse are regulated in concert with the spermatogenic cycle following a biphasic pattern in which transcripts are most abundant in Sertoli cells at stages X–XII and fall to undetectable levels at stages VII–VIII.
To gain insight regarding the potential physiological significance of Gal-1 in Sertoli cells in relation to differentiating gametes, it would be relevant to consider the testis as an immunologically privileged site, like the placenta and the ovary. Multiple factors contribute to the establishment of immune privilege, including the blood-testis barrier and the local production of immunosuppressive cytokines and proapoptotic factors [19, 42]. Because Gal-1 is a master regulator of T-cell homeostasis, it might provide to Sertoli cells an alternative mechanism with which to induce apoptosis of infiltrating T cells. This role could be reinforced by Leydig cells, in which we also found Gal-1. These cells have been associated with immunoregulation and have shown lymphocyte-inhibitory activity [43, 44]. On the other hand, mammalian testis exhibits a high rate of apoptosis of spermatogenic cells and preleptotene spermatocytes to compensate for the abundant mitosis and to eliminate defective cells [45]. Because Gal-1 is mostly expressed in Sertoli cells during postspermiation stages, one might speculate that this lectin contributes to the maintenance of organ integrity in the face of potentially damaging immune reactions or prevents the generation of defective germ cells. Moreover, Gal-1 might participate in Sertoli cell-sperm and sperm-sperm interactions. In this context, Akama et al [46] have recently shown that N-glycan structures play a key role in Sertoli cell-sperm adhesion and that specific carbohydrates are required for spermatogenesis. The precise functional significance of Gal-1 expression during this process is currently under investigation.
Previous studies have indicated that the cyclic activity of Sertoli cells ceases in the absence of germ cells, suggesting that signals originating from germ cells are important in regulating the spermatogenic cycle [47]. Significantly, in our present study, localization of Gal-1 at a basal position of Sertoli cells before puberty (45 days of postnatal development) occurs after the development of the blood-testis barrier and the simultaneous appearance of zygotene-pachytene spermatocytes [48]. As the differentiation of spermatids proceeds, Gal-1 becomes more prominent in structures located at the apical pole of seminiferous tubules. These observations highlight the importance of Sertoli-germ cell interactions in the establishment of the cyclic functional and morphological activity of the seminiferous epithelium. In agreement with these observations, Timmons et al. [41] suggested that the spermatogenic cycle depended exclusively on the Sertoli cells, because the coordinated cyclic patterns of gene expression in these cells was already established in the prepubertal mouse when gonocytes were arrested at a quiescent stage of the cell cycle.
By means of immunoelectron microscopy, we have also demonstrated the presence of Gal-1 in late spermatids and spermatozoa. This novel and intriguing finding puts forward the hypothesis that this proapoptotic protein might play a crucial role in reproduction. It could provide a novel immunosuppressive mechanism based on protein-carbohydrate interactions to prevent inflammation along the ejaculatory tract as well as in the female genital tract. On the other hand, Gal-1 might also be necessary for germ cell maturation by modulating the activity of several glycoproteins through its CRD.
Furthermore, a role has also been suggested for carbohydrate-binding sperm proteins in the sequence of binding events during fertilization [49]. In this context, Gal-1 might play a role in sperm-egg interactions through binding to specific polylactosamine sugars.
Based on our observations, it is still not clear whether Gal-1 is synthesized by spermatids or is transferred from Sertoli cells to late spermatids. It seems to be unlikely that late spermatids containing highly condensed chromatin and scant cytoplasmic organelles could synthesize proteins actively. Moreover, many secretory products that occur in high concentration in the Sertoli cell cytoplasm appear, finally, as an integral component of the seminal fluid [50]. In this sense, it might be speculated that Sertoli cells could transfer Gal-1 to germ cells; although galectins are cytosolic proteins that lack a signal peptide, they are secreted by a novel apocrine mechanism or are targeted to subcytosolic compartments [51]. However, the high immunoreactivity found in residual bodies during the spermiation stage of the cycle might indicate that Gal-1 is actually synthesized by spermatids and is then targeted to the nucleus or the plasma membrane. Both hypotheses are currently under consideration.
Targeted disruption of the Gal-1 gene in knockout mice resulted in the absence of major phenotypic abnormalities [52]. These animals were fertile and showed normal spermatogenesis and no chronic inflammation. This suggests that other members of the family might compensate for the absence of this sugar-binding protein, as suggested for null mutations in particularly important genes.
We conclude that Gal-1 expression and cellular localization are developmentally regulated in postnatal rat testis throughout different stages of spermatogenesis. The regulated expression in Sertoli cells, late spermatids, and spermatozoids suggests an unknown role for this immunosuppressive protein during reproduction. The current wealth of new information regarding the galectin family promises a ripe field that will expose undisclosed mechanisms involved in the control of basic cellular processes, such as proliferation, apoptosis, and signal transduction, in sites of immune privilege [4]. Finally, it could also provide new therapeutic strategies in chronic inflammatory disorders such as autoimmune orchitis.
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ACKNOWLEDGMENTS |
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FOOTNOTES |
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2 Correspondence: Cristina Maldonado, Centro de Microscopía Electrónica, Facultad de Ciencias Médicas, Universidad Nacional de Córdoba, Casilla Postal 362, 5000 Córdoba, Argentina. FAX: 54351 4333021; cmaldon{at}cmefcm.uncor.edu
3 G.A.R. and C.A.M. contributed equally to this work
Received: 11 April 2002.
First decision: 28 April 2002.
Accepted: 30 July 2002.
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REFERENCES |
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TOPABSTRACTINTRODUCTIONMATERIALS AND METHODSRESULTSDISCUSSIONREFERENCES |
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) at the apical portion of the seminiferous tubule in stage IV. Sp, Round spermatid.Ultrastructural immunolocalization of Gal-1 in adult rat testis. Specific gold labeling in a cytoplasmic projection of a Sertoli cell in the lumen of seminiferous tubule. Bar = 0.6 µm.FIG. 6. Ultrastructural immunolocalization of Gal-1 in adult rat testis. Gold labeling is observed in elongated spermatid heads (