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From the Department of Anatomy and Cell Biology, McGill University, Montréal, Québec, Canada.
| Correspondence to: Dr Louis Hermo, Department of Anatomy and Cell Biology, McGill University, 3640 University Street, Montréal, Québec, Canada, H3A 2B2 (e-mail: louis.hermo{at}mcgill.ca). |
| Received for publication January 21, 2003; accepted for publication March 4, 2003. |
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Abstract |
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Key words: Light microscopy, immunocytochemistry
GSTs are a family of soluble isozymes involved in cellular detoxification. They prevent the build up of potentially toxic substances by catalyzing the conjugation of reduced glutathione with various electrophilic substances, thereby protecting cellular components such as DNA, proteins, and lipids. The electrophilic substances can be of cellular origin, such as free radicals formed during normal metabolism or exogenous chemical compounds (Daniel, 1993). In addition to their main function in detoxification, they also play an important role in steroid isomerization (Benson et al, 1977); glutathione peroxidation (Prohaska and Ganther, 1976); leukotriene C biosynthesis (Pemble et al, 1986); and binding noncovalently to a number of nonsubstrate ligands, including steroids (Homma et al, 1986).
Cytosolic, microsomal, and nuclear forms of GSTs have been identified
(Hayes and Strange, 2000). They are dimeric proteins from a family of 16 genes grouped into five classes
(
, µ, 
, 
, and 
) according to the amino acid
homology of their subunits (Mannervik and
Danielson, 1988; Buetler and
Eaton, 1992; Daniel,
1993). GSTs form homo- or heterodimers from subunits that are
members of 1 gene family but not between gene families
(Mantle et al, 1990). GSTs
have similar molecular weights but differ with respect to isoelectric point
and substrate specificities (Jakoby et al,
1976). The vast number of different GST subunits implies their
importance in the protection of cells against a wide variety of potentially
harmful substances that they can encounter.
In previous studies, Hales et al (1980) had shown that the epididymis–vas deferens contains high GST activity, approximately 50% of that found in the liver on a protein weight basis, and that there are a large number of different GSTs in the epididymis–vas deferens, which are differentially localized along the length of this tissue. Recently, we examined with light microscopic immunocytochemistry the distribution of different GST subunits along the epididymis and vas deferens of adult rats. Our studies revealed that the expression of the different GSTs in the epididymis and vas deferens was often cell type– and region-specific (Veri et al, 1993, 1994; Papp et al, 1995; Andonian and Hermo, 1999). The absence of reactivity in 1 cell type of a given region was usually compensated for by the reactivity in another cell type of that region. The varied GST expression in the different cell types was thought to ensure that sperm would be protected from a wide variety of blood-borne electrophiles as they traversed the epididymis and during storage in the cauda region and vas deferens (Papp et al, 1995; Andonian and Hermo, 1999).
Although the activity of GSTs in the epididymis has been shown to be androgen-dependent and at times region-specific (Hales et al, 1980; Robaire and Hales, 1982), the regulation of expression of the different GST subunits has not been examined in a cell-type and region-specific manner, with only one exception. Indeed, in the epididymis, although basal cells were shown to be unaffected in their expression of Yf-GST by the absence of testicular and pituitary factors, the expression of Yf-GST by principal cells was shown to be dependent on testosterone (Hermo and Papp, 1996). However, little is known about the regulation of other GST subunits according to the different cell types and regions of the epididymis.
The purpose of the present study was, therefore, to examine the regulation of the Yb1-GST subunit in the epididymis of adult rats following orchidectomy with or without testosterone supplementation and efferent duct ligation using light microscope immunocytochemistry in conjunction with an anti-Yb1–GST antibody. The experimental procedures were designed to evaluate the role of androgens on Yb1-GST expression, well known regulators of many epididymal functions (Cornwall et al, 2002), as well as luminal testicular factors, other than androgens, which enter the epididymis via the lumen of the seminiferous tubules of the testis and efferent ducts and which have recently been defined as lumicrine factors (Hinton et al, 1998). The data from experimentally treated animals were qualitatively compared with those obtained for control adult rats based on numerous images generated from the 4 animals of each treatment group.
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Materials and Methods |
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All experimentation was carried out with minimal stress and discomfort being placed on the animals both during and after surgery as set up by the guidelines and approval of the McGill University Animal Care Committee.
Tissue Preparation for Light Microscope Immunocytochemistry
At the end of each experiment, the epididymides of each rat were fixed by
perfusion with Bouin's fixative via the abdominal aorta for 10 minutes.
Following perfusion, the epididymides were removed and cut so that given
sections would include all of the major regions of the epididymis (ie, the
initial segment, intermediate zone, caput, corpus, and cauda;
Hermo et al, 1991). The tissue
was then immersed in Bouin fixative for 72 hours, after which it was
dehydrated and embedded in paraffin.
Light Microscope Immunostaining— Sections 5 µm thick were cut and mounted on glass slides. They were then depar-affinized with xylene and hydrated in graded concentrations of ethanol (from 100% to 50%). During hydration, immersing the tissues in 70% ethanol containing 1% lithium carbonate for 5 minutes neutralized residual picric acid. In order to inactivate any endogenous peroxidase activity, the tissue sections were incubated for 5 minutes in 70% ethanol containing 1% (vol/vol) hydrogen peroxide. Following hydration, the sections were incubated (5 minutes) in a 300 mM glycine solution in order to block free aldehyde groups. The tissue was then blocked with 40 µL of 10% goat serum, diluted in TBS (20 mM Tris-HCl saline containing 0.1% bovine serum albumin) at pH 7.4, for 25 minutes at room temperature. The slides were then washed with Tween buffer solution (TBS with 0.1% Tween-20; TWBS). A dilution factor of 1:100 in TBS was used for the affinity-purified polyclonal anti-Yb1 antibody, which was kindly provided by Dr J. Hayes (University of Edinburgh, Scotland). Its purification and specificity are described in Hayes and Mantle (1986), and the anti-Yb1–GST antibody has already been used in one of our previous studies on control animals (Papp et al, 1995).
Each tissue section was incubated in the primary antibody for 1.5 hours. After incubation, the sections were immersed in 4 consecutive wells of TWBS for 2 minutes each. The sections were then blocked with 40 µL of 10% goat serum and subsequently incubated with goat anti-rabbit IgG conjugated to peroxidase (Sigma, St. Louis, MO) at a dilution of 1:250 in TBS and incubated for 30 minutes at 35°C in a humidified incubator. After incubation with a secondary antibody, the tissue was washed by immersion in 4 wells of TWBS for 2 minutes each.
The final reaction product was obtained by incubating the slides for 10 minutes in 250 mL of TBS containing 0.03% hydrogen peroxide, 0.1 M imidazole, and 0.05% diaminobenzidine tetrahydrochloride (DAB), pH 7.4. The sections were counterstained with 0.1% methylene blue (2 minutes) and then dehydrated in a graded series of ethanol solutions (30 seconds each) and xylene (3 minutes). Cover slips were mounted onto glass slides using Permount.
Incubation of epididymal tissues with normal rabbit serum at a dilution of 1:100 in TBS and in secondary antibody alone, without primary antibody, served as negative controls.
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Results |
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Principal cells of the distal initial segment in control animals revealed a weak checkerboard staining pattern of their cytoplasm, whereas their nuclei were intensely reactive; there was no staining of basal or narrow/apical cells. After each of the different experimental treatments at the various time points examined, no change in the staining pattern of Yb1-GST, as compared with control animals, was observed for any epithelial cell type of the distal initial segment (Figure 2a). In the caput epididymidis of control animals immunostained with anti-Yb1–GST antibody, principal cells also revealed a checkerboard-staining pattern showing a variable cytoplasmic reaction ranging from intense to moderate to weak reactivity to a complete absence of reaction; their nuclei were at times more reactive than the cytoplasm; basal and clear cells of the caput region were unreactive in control animals. No change was noted in the expression of Yb1-GST in any cell type after each experimental treatment at the different time points (Figure 2b).
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In the corpus (Figure 3a) and cauda (Figure 4a) epididymidis of control animals immunostained with anti-Yb1–GST antibody, principal cells maintained a checkerboard staining pattern, with their nuclei at times being more reactive than their cytoplasm. Although basal cells of the corpus epididymidis were intensely reactive (Figure 3a), these cells were unreactive in the cauda (Figure 4a) region. Clear cells of all regions were consistently unreactive (Figures 3a, 4a).
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At all time points after orchidectomy, no change in the staining pattern for Yb1-GST expression was noted for principal and clear cells of the caput (Figure 2b), corpus (Figure 3b), and cauda (Figure 4b) regions. However, basal cells displayed a region-specific difference after orchidectomy. Although these cells continued to be unreactive in the caput (Figure 2b) and cauda (Figure 4b) regions, they became unreactive in the corpus epididymidis at all time points after orchidectomy (Figure 3b). In the case of basal cells of the corpus epididymidis, these cells became intensely reactive in orchidectomized rats supplemented with testosterone (Figure 3c), and they were seen to be intensely reactive at all time points after efferent duct ligation (not shown). These data suggest that Yb1-GST expression in basal cells of the corpus region is regulated by testosterone or one of its metabolites.
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Discussion |
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This data contrasts with data obtained for Yf-GST expression, where principal cells noted to be reactive for Yf GST in control animals became unreactive after orchidectomy. The administration of testosterone to these animals restored Yf-GST expression, indicating that androgens were responsible for regulating Yf-GST expression in principal cells (Hermo and Papp, 1996). Clearly differences in the regulation of the various isoforms of GST appear to occur in the case of principal cells. Although it is well established that many epididymal functions are under the control of androgens (Robaire and Hermo, 1988; Orgebin-Crist, 1996; Cornwall et al, 2002; Ezer and Robaire, 2002), several proteins have been shown to be unaffected by androgen withdrawal in a cell-specific manner, such as SGP-1, cystatin c, SGP-2, and cathepsins A and D (Hermo et al, 2000b; Luedtke et al, 2000; Cornwall et al, 2002; Hermo and Andonian, in press). This also appears to be the case for Yb1-GST expression by principal cells.
However, in addition to the regulation mediated by androgens, factors
emanating from the testis that enter the epididymis via the lumen of the duct,
defined as lumicrine factors, also play a role in regulating epididymal
functions (Hinton et al, 1998; Cornwall et al, 2002). In the
present study, efferent duct ligation also had no effect on Yb1-GST
expression in principal cells, eliminating a role for lumicrine factors on its
expression (Figure 5, Table),
and this was also observed to be the case for Yf-GST
(Hermo and Papp, 1996) and
several other proteins expressed by the epididymis
(Ezer and Robaire,
2002).
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In the present study, the anti-Yb1 antibody often showed a nuclear reaction in principal cells that was more intense than the reaction seen in the cytoplasm (Figure 5, Table), and this was noted throughout most of the epididymis. It has been demonstrated that Yb1 proteins exist in a soluble form in both the nucleus and cytoplasm; however, they also exist in a bound form in the nucleus, where they bind to DNA (Bennett et al, 1986; Hayes and Mantle, 1986; Ketterer et al, 1990). It has also been shown that Yb1 in carcinoma cells migrates into the nucleus, providing further evidence for their strong nuclear affinity (Bennett et al, 1986; Bennett and Yeoman, 1987). In the epididymis, the Yb1 protein may protect DNA and RNA from harmful electrophiles that may be encountered by principal cells. In the present study, at no time was the expression of Yb1-GST noted to be different in experimentally treated animals as compared with controls, suggesting that testicular factors did not regulate Yb1-GST expression in the nucleus of principal cells.
Narrow/apical cells are found only in the initial segment and intermediate zone of the epididymis (Adamali and Hermo, 1996). Aside from a function in endocytosis, these cells also express GSTs in a region-specific manner (Papp et al, 1995; Hermo et al, 2000a). Apical cells express Yf-GST in the initial segment and intermediate zone, whereas narrow cells do not. In the proximal initial segment only, both apical and narrow cells express Yo GST (Adamali and Hermo, 1996). In the present study, Yb1-GST was expressed in narrow/apical cells of the proximal initial segment only. We did not separate these cells from each other, as both the thin narrow cells as well as the cup-shaped apical cells, which did not reach the basement membrane, were reactive (Adamali and Hermo, 1996). Although little is known about the regulation of the functions of these cells, the present data indicate that Yb1-GST expression is not regulated by androgens. Indeed, expression was lost after orchidotomy and not restored following testosterone supplementation. However, since a lack of expression was also noted after efferent duct ligation (Figure 5, Table), it was concluded that regulation of Yb1-GST in narrow/apical cells of the proximal initial segment was via a lumicrine factor. Lumicrine factors derived from the testis have been shown to regulate several proteins synthesized by the epididymis. Indeed, ligation of the efferent ducts induces changes in epididymal gene and protein expression (Cornwall et al, 2002). The luminal testicular factors that may regulate gene expression in the initial segment include ions, solutes, proteins, steroids, and even germ cells. These factors can up- or down-regulate gene expression after efferent duct ligation (Brooks, 1983). Expression of cystatin-related lipocalin and proenkephalin are among the proteins that have already been shown to be regulated by lumicrine factors (Garrett et al, 1991; Lareyre et al, 2001; Cornwall et al, 2002), and to this list may be now added Yb1-GST expression by narrow/apical cells of the proximal initial segment.
Basal cells are small hemispherical cells that reside on the basement membrane and do not reach the lumen of the duct. They also send thin, footlike processes along the basement membrane that collectively encompass a large portion of the circumference of each tubule (Veri et al, 1993). In this way they form a barrier, albeit an incomplete one, between the blood vessels and other contents of the intertubular space and the epididymal lumen. They can, therefore, to a degree effectively eliminate potentially harmful substances emanating from the blood that are trying to access the sperm in the lumen. In this context, basal cells express various isoforms of GSTs, such as the Yf, Ya, Yb2, and Yc subunits (Papp et al, 1995), as well as superoxide dismutase (Nonogaki et al, 1992).
Basal cells of control animals express Yb1-GST, but only in the proximal initial segment and corpus regions (Figure 5, Table). After orchidectomy and efferent duct ligation, these cells showed a differential response to androgens and lumicrine factors, dependent on their location along the duct. In the proximal initial segment, Yb1-GST expression was not restored to orchidectomized animals supplemented with testosterone, and expression was also absent after efferent duct ligation (Figure 5, Table). However, in the corpus region, expression was restored to control levels in orchidectomized animals that received testosterone, and there was no effect on expression in efferent duct–ligated animals (Figure 5, Table). Taken together, the data suggest that in the corpus region, Yb1-GST expression in basal cells is regulated by testosterone or one of its metabolites, but in the proximal initial segment, expression is regulated by a lumicrine factor. These data differ dramatically from that obtained for the Yf-GST subunit, where its expression in basal cells was unaltered after orchidectomy and efferent duct ligation, as well as hypophysectomy, indicating that neither testicular nor pituitary factors governed Yf-GST expression in basal cells (Hermo and Papp, 1996). Thus basal cells of different regions show differential responses to the absence of androgens or testicular lumicrine factors in their expression of a given GST as well as between different GSTs. Very little is known about what regulates basal cell functions, as data on the functions of these cells is only slowly being gathered. However, the expression of metallothionein by basal cells, although detectable in all epididymal regions, was shown to be androgen-dependent according to specific regions (Cyr et al, 2001).
Aside from the family of GSTs, the expression of glutathione peroxidase at the message and protein levels has also been noted to be androgen-dependent (Vernet et al, 1997; Schwaab et al, 1998). At the mRNA level, gamma glutamyl-transpeptidases, which show multiple transcripts, are also differentially regulated by androgens and/or lumicrine factors in the different epididymal regions (Palladino and Hinton, 1994), as is their secretion and activity (Agrawal and Vanha-Perttula, 1988). Thus various antioxidant enzymes show a differential regional response in their expression to the presence or absence of testicular factors. However, their regulation has not as yet been determined on a cell-type and region-specific manner. In summary, the present study has revealed that the expression of Yb1-GST is regulated along the epididymis in a cell-type and region-specific manner.
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Acknowledgments |
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Footnotes |
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