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BOR - Papers in Press, published online ahead of print March 31, 2004.
Biol Reprod 2004, 10.1095/biolreprod.104.027490
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BIOLOGY OF REPRODUCTION 71, 410–416 (2004)
DOI: 10.1095/biolreprod.104.027490
© 2004 by the Society for the Study of Reproduction, Inc.

Male Reproductive Tract

Fluid Reabsorption by the Ductuli Efferentes Testis of the Rat Is Dependent on Both Sodium and Chlorine1

Lyall A. Hansen3, Françoise Dacheux4, Suet Yee Man3, John Clulow3, and Russell C. Jones2,3

Discipline of Biological Sciences,3 University of Newcastle, Callaghan, New South Wales, Australia 2308 Equipe «Gamète Mâle et Fertilitè»,4 UMR 6175 INRA-CNRS Université-Haras Nationaux, 37/380 Nouzilly, France


   ABSTRACT
TOP
 ABSTRACT
INTRODUCTION
 MATERIALS AND METHODS
 RESULTS
 DISCUSSION
 REFERENCES
 
The role of Na+ and Cl– in fluid reabsorption by the efferent ducts was examined by perfusing individual ducts in vivo with preparations of 160 mM NaCl in which the ions were replaced, together or individually, with organic solutes while maintaining the osmolality at 300 mmol/kg. Progressively replacing NaCl with mannitol reduced net reabsorption of water and the ions in a concentration-dependent manner, and caused net movement into the lumen at concentrations of NaCl less than 80 mM. The net rates of flux were lower for Na+ than for Cl–. In collectates, [Na+] was greater than [Cl–], indicating that Cl– transport is probably linked with another anion. Replacing either Na+ or Cl– in perfusates (with choline and isethionate, respectively) while maintaining the other inorganic ion at 160 mM also reduced net rates of reabsorption in a concentration-dependent manner to zero when either ion was completely replaced. There were no significant differences in the osmolality of perfusate and collectate, and collectates contained a mean of 3.4 mM K+, indicating a backflux of K+ into the lumen. It is concluded that fluid reabsorption from the efferent ducts is dependent on the transport of both Na+ and Cl– from the lumen (from a luminal concentration of at least 70–80 mM), and that Cl– transport is dependent on another anion. The epithelium is permeable to K+ and has a higher permeability to a range of organic solutes (mannitol, choline, and isethionate) than epithelium in the proximal kidney tubules.

epididymis, male reproductive tract


   INTRODUCTION
TOP
 ABSTRACT
 INTRODUCTION
MATERIALS AND METHODS
 RESULTS
 DISCUSSION
 REFERENCES
 
The ductuli efferentes are essential for male fertility in mammals [1]. The ducts reabsorb most of the fluid transported from the testis so that spermatozoa are delivered in a relatively small volume to the ductus epididymidis that modifies the milieu to effect sperm maturation and storage [2–6]. In the rat, 96% of the fluid leaving the testis is reabsorbed by the efferent ducts [6]. Most of the fluid is reabsorbed in the initial zone, the region between the rete testis and the coni vasculosi [7]. The rate of reabsorption is high (17.2 µl cm–2 h–1) compared to that of most epithelium, being 170 times greater than in the cauda epididymidis [8]. Studies involving microperfusion of the ducts in the initial zone showed that the rate of reabsorption is flow-dependent, the rate being greater from native fluid collected from the rete testis (nRTF) than from Krebs-Ringer bicarbonate (KRB) [9]. Reabsorption from both solutions was isosmolar for Na+ and Cl–, but K+ was reabsorbed at a greater rate than water from the nRTF [9]. Including amiloride in the KRB perfusate reduced reabsorption up to 70% in a dose-dependent manner [10], indicating that a significant proportion of the process is effected by an amiloride-sensitive Na+-H+ exchanger (NHE) that has been localized in the efferent duct epithelium [11].

The studies described in this report examine the role of Na+ and Cl– in fluid reabsorption, because they are the main ions present in the lumen and are reabsorbed from the efferent ducts, and the transport of Na+ is implicated in the process of reabsorption (see above). The effect of the ions was determined by replacing them, together or individually, with other solutes in the perfusates. Further, determinations of the composition of collectates were used to interpret the permeability of the ducts to K+ and organic compounds.


   MATERIALS AND METHODS
TOP
 ABSTRACT
 INTRODUCTION
 MATERIALS AND METHODS
RESULTS
 DISCUSSION
 REFERENCES
 
The studies were carried out on outbred Male Wistar rats with the approval of the Institute's Animal Ethics Committee, and using methods of anesthesia and surgery that have been described previously [9, 12]. Briefly, rats were anesthetized with sodium pentobarbitone by an initial i.p. injection (60 mg/kg), and then via a cannula in the jugular vein. Microperfusion of an efferent duct involved its cannulation near the rete testis with a cannula connected to a 50-µl syringe on a perfusion pump (Sage Instruments, Beverly, MA) and perfusing the duct at a rate of 0.1 µl/min. The duct was identified at the distal end of the initial zone and cannulated with an empty cannula in order to collect fluid leaving the duct (collectate). Each rat was perfused sequentially by three different solutions each for at least 30 min (in random order). When the solution was changed, the new solution was perfused for 30 to 40 min to allow equilibration before continuing to sample the collectate [12]. On completion of a perfusion, the volume of collectate was determined by measuring the length of the column of fluid in the collecting cannula. The duct was then dissected free and its length was measured. The rate of fluid reabsorption was calculated from the difference in volume of the perfusate and collectate divided by duct length and the duration of perfusion. Positive values indicate net reabsorption from the duct, and negative values indicate net flux into the duct ("secretion"). When appropriate, the concentrations of Na+, Cl–, and K+ in collectate were determined by energy-dispersive x-ray microanalysis [6]. Osmolality was determined by freezing-point depressions using a nanoliter osmometer (Clifton Technical Physics, New York, NY).

Preparation of Perfusates

Rete testis native fluid was perfused as a "control" perfusate for the studies. The method described by Free and Jaffe [13] was used to collect and prepare [9] nRTF from the rat. The total osmolality of the fluid was 307 mmol/kg, and the main constituents were 137 mM Na+, 13 mM K+, 130 mM Cl–, 1.5 mM Mg2+, 0.9 mM Ca2+, and 2.4 g/L protein [6]. The other solutions were prepared from analytical reagents (Sigma Chemical Co, St. Louis, MO) to a total osmolality of 300 mmol/kg. In the first experiment, the concentration of NaCl was varied by successively replacing 40 mM NaCl with 72 mM mannitol to achieve concentrations of 160, 120, 80, 40, and 0 mM NaCl. In the second experiment, the concentrations of Na+ and Cl– were varied independently by replacing NaCl with equal concentrations of choline chloride and sodium isothionate, respectively (see Table 4).


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  		TABLE 4. Estimates of the rate of solute transport from the lumen of efferent ducts perfused with solutions in which [Na+] and [Cl–] varied independently by replacing NaCl with choline chloride and sodium isethionate, respectively.a

Calculation of Rates of Reabsorption of Na+, K+, and Cl–

Reabsorption was calculated (in the case of Na+, for example) as follows:

where t = perfusion time (in minutes), l = length of duct perfused (in millimeters), and Naperf and Nacoll are, respectively, the number of picomoles of Na perfused or collected.

Calculation of Reabsorption Rates for Organic Solutes

The (maximum) concentrations of mannitol, choline, and isethionate in collectates were estimated from the differences between the measured osmotic pressure and the osmolality calculated for the total concentrations of Na+, Cl–, and K+. For example, the (maximum) [mannitol] in the collectate (in millimoles) was calculated using the formula:

where 0.93 is the value of the constant used to convert electrolyte concentrations to equivalent units of osmolality, and 0.96 is the value used to convert mannitol osmolality to an equivalent mannitol concentration [14]. The estimate is considered to be the maximum [mannitol], as other solutes may be present in the collectate.

The percentage reabsorption of mannitol was calculated as follows:

The value for mannitol is the minimum rate of reabsorption possible, as the calculation employs the highest possible residual concentration of mannitol in the collectate.

The reabsorption (minimum) of mannitol (pmol mm–1 min–1) was calculated as follows:

The reabsorption rates of choline and isethionate were calculated in the same manner as for mannitol. The reliability of the method was confirmed by determining the concentration of isethionate directly by x-ray microanalysis using the sulfur atom in the molecule to determine its concentration.

Epithelial Structure

Individual ducts were perfused for 30 to 40 min with nRTF, KRB, or 288 mM mannitol, then fixed by immersion in phosphate-buffered formaldehyde (3%)-glutaraldehyde (3%) [15], processed into Spurr resin (Agar Scientific, Essex, U.K.), sectioned at 0.5 µm, and stained with toluidine blue. Each treatment was replicated using three rats.

Statistical Analyses

Differences between treatments were determined by analyses of variance using the variance between animals as the estimate of error. The variance between treatments was partitioned into individual degrees of freedom using orthogonal polynomial coefficients. The standard errors shown in the figures and tables were calculated from the variance between animals.


   RESULTS
TOP
 ABSTRACT
 INTRODUCTION
 MATERIALS AND METHODS
 RESULTS
DISCUSSION
 REFERENCES
 
A preliminary study assessed the effect of perfusing efferent ducts and varying the composition of the perfusate on the structure of the duct epithelium. Figure 1 shows that nonciliated cells in epithelium from unperfused duct possessed regular microvilli facing the lumen, and numerous vacuoles and dense bodies occurred throughout the cytoplasm as described in earlier reports [16, 17]. Perfusing the duct mildly disrupted the arrangement of the microvilli, but had little effect on the cytoplasm, except that there were generally fewer vacuoles in epithelium perfused with nRTF than in the unperfused duct, and the supranuclear vacuoles were enlarged by perfusion with 288 mM mannitol.



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  		FIG. 1. Transmission light micrograph of efferent duct epithelium from an (A) unperfused duct, and ducts perfused with (B) nRTF, (C) KRB, and (D) 288 mM mannitol. Stained with toluidine blue. Bar = 0.1 µm

Subsequent studies examined the effects of replacing NaCl with mannitol in perfusates (Figs. 2 and 3, and Tables 1 and 2), and the effects of varying the concentration of Na+ and Cl– independent of one another in perfusates, while maintaining the concentration of the other ion at 160 mM (Fig. 3 and Tables 3 and 4). In these studies, the mean rate of fluid reabsorption from ducts perfused with 160 mM NaCl (33.5 ± 5.1 nl 10 mm–1 min–1) was less than for ducts perfused with nRTF (41.7 ± 2.9 nl 10 mm–1 min–1), and the values are consistent with previous studies [9]. The composition of the collectates were similar (Table 1), and the rates of reabsorption of Na+ and Cl– from ducts perfused with nRTF were about the same as from ducts perfused with 160 mM NaCl (Table 2). K+ was reabsorbed from the nRTF so that its concentration in the collectate was much the same as in blood, but there was a net flux of K+ into perfusates containing no K+ (see below).



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  		FIG. 2. Fluid reabsorption from efferent ducts perfused with varying concentrations of NaCl made 300 mOsm/kg using mannitol. Values are means ± SEM for individual ductules in 5–6 rats



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  		FIG. 3. Rates of transport of Na+ and Cl– from efferent ducts perfused with varying concentrations of NaCl made 300 mOsm/kg using mannitol. Data are derived from the experiment shown in Figure 2


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  		TABLE 1. Osmolality and elemental concentrations in blood plasma and collectates obtained after perfusing a single efferent duct with nRTF and solutions containing various concentrations of NaCl adjusted to 300 mOsm/kg with mannitol


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  		TABLE 2. Estimates of rates of solute transport from the lumen of efferent ducts perfused with nRTF and solutions containing varying concentrations of NaCl adjusted to 300 mmol/kg with mannitol.a


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  		TABLE 3. Osmolalities and elemental concentrations in blood plasma and collectates obtained after perfusing a single efferent duct in vivo with solutions at 300 mOsm/kg in which the concentrations of Na+ and Cl– were varied independently by replacing NaCl with choline chloride and sodium isethionate, respectively

Replacement of NaCl with Mannitol (Na+ and Cl– at Equimolar Concentrations)

Figure 2 shows that progressive replacement of NaCl with mannitol in perfusates caused a decline in reabsorption (P < 0.001) until reabsorption was abolished at about 80 mM NaCl. Fluid fluxed into the lumen of the duct when the perfusates contained less than 80 mM NaCl. Varying the [NaCl] in perfusates did not affect the osmolality of collectates (Table 1). However, both the [Na+] (P < 0.001) and [Cl–] (P < 0.001) in collectates declined significantly as the [NaCl] in perfusates was reduced. Nevertheless, even for perfusates that contained only mannitol, the [Na+] and [Cl–] in the collectate was 85 ± 10 mM and 76 ± 6 mM, respectively (Table 1). [Na+] in collectates was at least as high as in the perfusates, but in collectates the [Cl–] was lower than [Na+]. K+ was present in all collectates at 50%– 100% of [K+] in blood (P < 0.05–0.001 for the difference between blood and collectate for all perfusates, except for 160 mM NaCl). The net rate of flux of K+ into the lumen was not affected by [NaCl] in the perfusate.

Figure 3 shows that the net rate of flux was greater for Cl– than Na+ (P < 0.01) for all concentrations of NaCl. Table 2 shows that reducing [NaCl] in the perfusate to 80 mM reduced the net rates of reabsorption of Na+ (P < 0.001) and Cl– (P < 0.001). At lower [NaCl] the Na+ and Cl– fluxes became negative, and this net flux into the lumen increased until mannitol completely replaced NaCl in perfusates. The fluxes of Na+ and Cl– into the lumen were very high for perfusates that contained only mannitol, and in absolute terms, they exceeded the highest rates of reabsorption of Na+ and Cl– when 160 mM NaCl was perfused. Net fluxes of mannitol increased as Na+ and Cl– were replaced by mannitol in the perfusate (P < 0.001) so that mannitol was fluxed in the opposite direction to Na+ and Cl– for perfusates containing more than 72 mM mannitol. The estimates of mannitol fluxes indicate that up to 40% of mannitol was removed from perfusates. Luminal iso-osmolality (Table 1) was maintained by NaCl and mannitol fluxing in opposite directions across the duct epithelium (Table 2). The net flux of fluid (water) into the lumen was also important for perfusates containing low [NaCl]. For example, for the perfusate containing only mannitol, its net reabsorption (921 pmol mm–1 min–1) was higher in absolute terms than any net flux for Na+ or Cl–. However, the total flux of Na+ and Cl– into the lumen (–1541 pmol mm–1 min–1) exceeded the net reabsorptive flux of mannitol (921 pmol mm–1 min–1).

Replacement of Na+ and Cl– Independently (Different Concentrations of Na+ and Cl–)

Figure 4 shows that progressively replacing either Na+ or Cl– in perfusates with an organic ion while maintaining the other inorganic ion at 160 mM (see Table 3) progressively reduced net rates of fluid reabsorption in a concentration-dependent manner. The rates were reduced to zero when either Na+ or Cl– were completely replaced (P < 0.001). The reduction occurred without a significant change in osmolality of the collectate (Table 3). Tables 3 and 4 show that replacing Na+ in perfusates with choline increased the net flux of Na+ (P < 0.001) into the lumen and reduced net reabsorption of Cl– (P < 0.001), so that the [Na+] in collectates was higher than in their corresponding perfusates, while [Cl–] in all collectates was much the same (and about 30 mM lower than in perfusates). A corresponding response was obtained when Cl– in perfusates was replaced with isethionate. The flux of Cl– into the lumen increased (P < 0.001) and reabsorption of Na+ decreased, so that the [Cl–] in collectates was higher than in perfusates, while [Na+] in all collectates was much the same (and about the same as in the perfusates). The general effect of replacing either Na+ or Cl– with more than 80 mM organic ion was, for the net fluxes of Na+ and Cl–, shown to occur in opposite directions.



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  		FIG. 4. Fluid reabsorption from efferent ducts perfused with varying [Cl–] and [Na+] as shown in Table 3. Values are means ± SEM for individual ductules in 5–6 rats

Table 3 shows that K+ was present in all collectates at 57%–88% of its concentration in blood (P < 0.05 for all perfusates except those containing 160 mM Na+ and 40 mM Cl–). Also, the [K+] was higher in collectates when the perfusate contained 160 mM Na+ than 160 mM Cl– (P < 0.05; Table 3), suggesting a link between luminal Na+ and K+ entry into the ducts.

The minimum rate of reabsorption of choline and isethionate from perfusates ranged from 44% to 63% of the solute in the perfusate, and the rates were dependent on their concentration in the perfusate (P < 0.001; Table 4). Further, the highest estimates of mean minimum rate of reabsorption of choline and isethionate (597 ± 24 and 697 ± 60 pmol mm–1 min–1, respectively; Table 4) were higher than mean values for the reabsorption of Na+ or Cl– from perfusates containing 160 mM NaCl.


   DISCUSSION
TOP
 ABSTRACT
 INTRODUCTION
 MATERIALS AND METHODS
 RESULTS
 DISCUSSION
REFERENCES
 
Fluid Reabsorption Is Dependent on Both Na+ and Cl– Transport

These studies demonstrate that NaCl plays a major role in fluid reabsorption from the efferent ducts. The findings are consistent with our previous work [10] showing the importance of the Na+-H+ antiport, NHE3 [11], in fluid reabsorption by the ducts. The present studies also demonstrate that fluid reabsorption from the efferent ducts is dependent on both Na+ and Cl– transport, and that the transport of the ions is interdependent (i.e., the flux rates are parallel). This dependence on both Na+ and Cl– is a different mechanism of fluid transport than in the caudal ductus epididymidis [18–20] and proximal kidney tubules [21–23]. They are mainly dependent on the transepithelial transport of Na+, and removal of intraluminal Na+ abolishes fluid transport, whereas omission of chloride from the perfusion fluid has no effect on Na+ or water reabsorption. Our finding (in the present study and in an earlier study [9]) that fluid reabsorption was greater from efferent ducts perfused with nRTF than inorganic solutions suggests that a portion of fluid transport may depend on cotransport of Na+ and organic solutes as in the proximal tubules [24]. Rete testis fluid also contains numerous regulatory steroids and peptides that could affect ion and fluid transport [25– 27].

Anion Exchanger to Achieve Electroneutral Movement of Na+ and Cl–

It is suggested that, as in the proximal kidney tubules [28], there is probably some form of apical anion antiporter operating in parallel with the Na+-H+ antiporter [10, 11] in order to achieve an electroneutral movement of Na+ and Cl– across the efferent duct epithelium. Such a linkage would explain why Cl– was fluxed at a greater rate than Na+ during reabsorption, and at a lower rate than Na+ during movement into the lumen, and why [Na+] in the collectate is greater than [Cl–]. It is also consistent with the finding that high levels of are found in the efferent duct fluid, some of which may be contributed by fluxing into the lumen, even though most entering the efferent ducts is ultimately reabsorbed at about the same rate as fluid [29]. Consequently, it is suggested that during reabsorption, enters the lumen in exchange for Cl–, resulting in a greater net reabsorption of Cl– than Na+ under normal physiological conditions. Conversely, when there is a net flux of Na+ and Cl– into the lumen, a co-flux of Cl– and the putative anion would result in the entry into the lumen of less Cl– than Na+.

Backflux of Na+ and Cl–

This report shows that there can be considerable backflux of Na+, Cl–, and K+ into the lumen of the efferent ducts. Tables 1 and 3 show that when either or both Na+ and Cl– are replaced by organic solute, the backflux of Na+ and Cl– can maintain their intraluminal concentrations at 85–99 mM and 67–76 mM, respectively, but this does not sustain fluid reabsorption. The demonstration of the backflux suggests that Na+ and Cl– are continually fluxing into and out of the lumen under normal physiological conditions when there is net fluid reabsorption (i.e., when the luminal concentration of NaCl exceeds ~80 mM). The backflux is probably due to leaky epithelium (involving paracellular fluxes through intercellular junctions that are relatively permeable to small ions), and may be responsible for fluid secretion when the [NaCl] in perfusate is less than 80 mM. These findings are in agreement with work on the proximal kidney tubule, which investigated the relationship between the transtubular [Na+] gradient and the net movement of luminal fluid [30]. Zero reabsorption occurred at approximately 95 mM Na+ when a transtubular concentration difference of 50 mM was exceeded [30].

K+ Equilibrates with Blood

The behavior of K+ both in the intact system of efferent ducts [6] and during microperfusion of individual ducts (this study and [8, 9]) indicates that K+ equilibrates across the epithelium as a simple diffusible solute. Indeed, under normal conditions, K+ undergoes the largest relative change in concentration of any electrolyte along the efferent duct system (from 13.3 to 5.7 to 11.6 mM in the rete testis, coni vasculosi, and proximal ductus epididymidis, respectively [6]). Tables 1 and 4 indicate that when the ducts are perfused with solutions containing no K+, there is a flux of K+ into the lumen, where its concentration equilibrates close to that in blood plasma (a mean of 3.4 mM and 4.8 mM, respectively). This is in agreement with a model of K+ transport for the proximal kidney tubule [28, 29]. The model integrates active K+ uptake by the epithelial cells from the serosal side and passive (paracellular) K+ flux through the intercellular spaces, and predicts an equilibration of [K+] occurring in the lumen within 1 mM blood plasma through a balance between the flux of K+ in opposite directions across the epithelium.

Permeability to Organic Solutes

The studies described here and in our earlier reports [8, 9] indicate that the efferent ducts have a higher permeability to a range of organic solutes (mannitol, choline, isethionate, inulin) than transporting epithelia such as the proximal kidney tubules [30–36]. For example, whereas only 0.05% of inulin is reabsorbed during microperfusion of the proximal tubules [35], up to 30% of inulin [8], about 40% of mannitol, 55–60% of isethionate, and 45%–60% of choline can be reabsorbed during microperfusion of an efferent duct. There is evidence for carrier-mediated reabsorption of choline [37] from the lumen of the proximal tubules, but mannitol efflux is believed to be diffusive, and there is no evidence for carrier-mediated absorption [30, 36]. It is possible that in the efferent ducts these solutes have different pathways or combinations of pathways through transcellular routes (such as through aquaporin 9 [38–40]), paracellular routes [41], or both. It is also possible that they may all be transported by fluid phase endocytosis, because 80% of the protein entering the efferent ducts is reabsorbed [6], probably mainly by endocytosis [42–44].

Structure and Function of Perfused Duct

It is reassuring that the reabsorption rates determined for perfusions with nRTF and 160 mM NaCl were similar in this study to the reabsorption rates for nRTF and KRB, respectively, in a previous study [9]. It is also reassuring that the perfusions had little effect on epithelial structure. Indeed, we did not observe an increase in lateral, intercellular spaces as reported for the ductus epididymidis [45, 46], and suggest that this may be because we used a perfusion rate that is about the same as it occurs in situ, and is much lower than that used by earlier workers. The large intracellular vacuoles that formed in ducts perfused with 288 mM mannitol indicates a change in the role of these structures under the conditions. The vacuoles may indicate an intracellular accumulation of mannitol that did not affect the integrity of the epithelium during the 30-min perfusion, but could not develop further during a longer period of perfusion. It is suggested that the perturbation of microvilli in perfused ducts is unlikely to be due to a redistribution of transporters in the membrane, as we saw no significant differences between perfusions with nRTF and the synthetic solutions.


   FOOTNOTES
 
1 This work was supported by grants from the Australian Research Grants Committee, postgraduate scholarships, and an RMC Research Visitor grant from the University of Newcastle. Back

2 Correspondence. FAX: 61 2 4921 6923; bircj{at}cc.newcastle.edu.au Back

Received: 16 January 2004.

First decision: 2 February 2004.

Accepted: 16 March 2004.


   REFERENCES
TOP
 ABSTRACT
 INTRODUCTION
 MATERIALS AND METHODS
 RESULTS
 DISCUSSION
 REFERENCES
 

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