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Biol Reprod 2003, 10.1095/biolreprod.103.019711
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BIOLOGY OF REPRODUCTION 69, 1714–1718 (2003)
DOI: 10.1095/biolreprod.103.019711
© 2003 by the Society for the Study of Reproduction, Inc.

Male Reproductive Tract

Signal Transduction in the Ductuli Efferentes Testis of the Rat: Inhibition of Fluid Reabsorption by Cyclic Adenosine 3', 5'-Monophosphate1

S.Y. Man, J. Clulow, and R.C. Jones2

Discipline of Biological Sciences, University of Newcastle, NSW, Australia 2308


   ABSTRACT
TOP
 ABSTRACT
INTRODUCTION
 MATERIALS AND METHODS
 RESULTS
 DISCUSSION
 REFERENCES
 
It is important to identify the signal transduction pathway involved in the regulation of fluid reabsorption by the ductuli efferentes of the testis because they reabsorb most of the fluid leaving the testis and are essential for male fertility. Microperfusion studies of the ducts in vivo showed that 0.1 or 1.0 mM dibutyryl (db)-cGMP in the perfusate had no effect on fluid reabsorption, but 0.1 mM db-cAMP significantly reduced fluid reabsorption, 0.25 mM abolished reabsorption, and 0.5–1.0 mM caused secretion. The inhibitory effect of db-cAMP was reversible. Although the presence of db-cAMP in the perfusate did not affect the concentration of Na+ in the collectate, the concentrations of K+ and Cl- increased, indicating that their transport is at least partly regulated by cAMP. Including the phosphodiesterase inhibitor pentoxifylline in the perfusate decreased fluid reabsorption by the ducts in a dose-dependent manner, and it also increased the concentration of cAMP (5.5-fold) in collectate. Pentoxifylline also increased the production of cAMP (4-fold) by ducts incubated in vitro. It is concluded that cAMP, but probably not cGMP, is an intracellular messenger regulating fluid reabsorption in the efferent ducts.

epididymis, male reproductive tract, signal transduction


   INTRODUCTION
TOP
 ABSTRACT
 INTRODUCTION
MATERIALS AND METHODS
 RESULTS
 DISCUSSION
 REFERENCES
 
The efferent ducts of mammals play an essential role in male fertility [1]. They reabsorb most of the fluid and protein from the fluid leaving the testis [2–4]. Net fluid reabsorption from the ducts determines the concentration of sperm delivered to the ductus epididymidis and is determined by the relative rates of fluid reabsorption and secretion by the duct epithelium. It is interpreted that fluid reabsorption is mainly determined by sodium/hydrogen exchanger 3 (NHE3), an amiloride-sensitive Na+-H+ antiport that accounts for 70% of the fluid reabsorbed by the proximal efferent ducts [5, 6]. Secretion of fluid into the duct is probably determined by secretion of Cl- via the cystic fibrosis transmembrane conductance regulator, CFTR [7, 8]. Na+-K+-ATPase is probably the main source of energy driving the solute transport, as its activity has been localized in the basolateral membranes of the ducts [9–11].

Chronic control of net fluid reabsorption by the ducts is dependent on both androgen and estrogen [11–14] but not on corticosteroids [15]. Receptors for both sex hormones have been identified in the duct epithelium [16–19]. Local, acute regulation of fluid reabsorption is determined by load, including the concentration of Na+, and the rate of flow of fluid into the ducts [20]. However, although there is evidence, from studies of epithelium cultured in vitro, that cAMP can affect fluid reabsorption by acting on Cl- channels to stimulate fluid secretion into the ducts [8], the role of cyclic nucleotides in net fluid reabsorption has not been resolved. Consequently, we have examined the role of cyclic-nucleotides in net fluid reabsorption in vivo. It has been established that both cyclic adenosine 3',5'-monophosphate (cAMP) and cyclic guanosine 3',5'-monophosphate (cGMP) are involved in regulating fluid transport in a number of other tissues. Both stimulate fluid secretion in intestines of humans [21] and rats [22–25], causing diarrhoea, and both inhibit fluid reabsorption in the proximal tubules of the kidney of a number of vertebrate species [26–31]. However, cAMP alone activates fluid secretion in canine pancreatic [32] and gallbladder epithelium [33], equine sweat glands [34], rat submandibular acinar cells [35], frog retinal pigment epithelium [36], and insect salivary glands [37, 38], but activates fluid absorption in lung aveolar epithelium [39, 40]. On the other hand, cGMP alone stimulates fluid secretion in rat hepatocyte couplets [41].

The studies described in this report examined the effects of permeant forms of cyclic nucleotides, dibutyryl-cAMP (db-cAMP) and dibutyryl-cGMP (db-cGMP), and the phosphodiesterase inhibitor pentoxyfylline on fluid reabsorption in the efferent ducts of the rat and the effect of pentoxyfylline on the production of cAMP by the ducts.


   MATERIALS AND METHODS
TOP
 ABSTRACT
 INTRODUCTION
 MATERIALS AND METHODS
RESULTS
 DISCUSSION
 REFERENCES
 
Microperfusion In Vivo

Outbred, male Wistar rats, between 5 and 10 mo old, were used in the studies with the approval of the Institute's Animal Ethics Committee. The rats were anesthetized with sodium pentobarbitone (60 mg/kg i.p.) and then maintained under anesthesia via a cannula in the jugular vein. A testis with attached epididymis was delivered through a longitudinal incision in the scrotum and placed in a testis-cup lined with cotton gauze saturated with 0.91% saline and maintained at 35°C. The microperfusion procedure [20] involved cannulating an efferent duct near the rete testis with a polyethylene cannula (outer diameter = 0.8 mm, inner diameter = 0.4 mm; Dural Plastics and Engineering, Auburn, NSW, Australia) filled with Krebs Ringer bicarbonate (KRB: 130 mM NaCl, 25 mM NaHCO3, 4.7 mM KCl, 2.56 mM CaCl2, 1.13 mM MgSO4, 1.17 mM NaH2PO4) colored with Lissamine Green (Sigma Chemical Co., St. Louis, MO). The cannula was connected to a 50-µl syringe on a perfusion pump (Sage Instruments, Beverly, MA) and the duct perfused at a rate of 0.1 µl/min. The same 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). The duct (10–20 mm long) was then perfused with KRB (perfusate) containing any additional compounds (from Sigma Chemical Co.) determined by the design of the experiment: db-cAMP (catalogue number D3501), db-cGMP (catalogue number D3510) or pentoxyfylline (catalogue number P1784) or no additions. When different compounds, or different concentrations of a compound, were perfused sequentially in the same experiment, the new solution was perfused for 30–40 min to allow equilibration before continuing to sample the collectate. On completion of the perfusion, the duct was dissected free while immersed in KRB and its length 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. When appropriate, the concentrations of Na+, Cl-, and K+ in the collectate were determined by energy-dispersive x-ray microanalysis [4], and cAMP was determined as described below.

Production of cAMP In Vitro

The vascular system of rats, deeply anesthetized with sodium pentobarbitol, was cleared of blood by perfusing with cold (5°C) Hank solution (137 mM NaCl, 5 mM KCl, 0.33 mM Na2HPO4, 1 mM MgCl2, 0.8 mM MgSO4, 10 mM Tris Cl, 1 mM CaCl2, 0.1% BSA) via a cannula in the abdominal aorta and at a hydrostatic pressure of 150 mm Hg. After the perfusion, a testis and its epididymis was recovered and transferred to a Petri dish containing cold Hank solution containing 0.05% collagenase and 0.2 mM CaCl2. A length of about 10 mm of the initial zone of the efferent ducts [2] was dissected out, trimmed free from fat, and the length measured. Two pieces of duct were transferred to 40 µl KRB (pH 7.4, 37°C, bubbled with 5% CO2 before use), incubated for 5 min under 5% CO2 in air, then diluted with 40 µl of KRB containing 0 or 10 mM pentoxifylline and incubated for 5 min. A sample of the incubation medium (40 µl) was prepared for cAMP determination by mixing with 50 µl 10% trichloroacetic acid (TCA) at 4°C in order to stop the reaction, and extracting the product four times with 0.5 ml diethyl ether. A sample of the ducts was prepared for cAMP determination by homogenization (for 1–2 min at 0–4°C using a glass hand homogenizer), washing once with KRB:TCA mixed 5:4, centrifuging (60 x g, 15 min, 4°C) and extracting the supernatant four times with 1 ml water-saturated diethyl ether.

Determination of cAMP

Samples for analysis were dried with nitrogen at 40°C and stored at -80°C until assay. Cyclic AMP was determined using the commercial cAMP EIA system (Amersham Biosciences, Sydney, Australia) after dissolving in 0.05 M acetate buffer. The concentration of cAMP was corrected according to the length of efferent duct studied and expressed as fmol/mm.

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
 
Perfusions In Vivo

Figure 1 shows that the mean net reabsorption of fluid from a perfused efferent duct decreased from 36.19 ± 1.49 nl 10 mm-1 min-1 when the perfusate contained no db-cAMP to 23.37 ± 3.85 nl 10 mm-1 min-1 when the perfusate contained 0.1 mM db-cAMP. Reabsorption was abolished when the perfusate contained 0.25 mM db-cAMP, and higher concentrations of db-cAMP caused net fluid secretion. When no db-cAMP was included in the perfusate, the concentrations of Cl- and K+ were lower in the collectate (Table 1) than perfusate (115.9 vs. 140 mM and 3.8 vs. 4.7 mM, respectively), indicating that these ions were being reabsorbed at a greater rate than Na+. However, there was a significant increase in concentrations of luminal Cl- and K+ when the perfusion fluid contained db-cAMP (Table 1).



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  		FIG. 1. Reabsorption of fluid in efferent ducts perfused in vivo with KRB containing various millimolar concentrations of db-cAMP. Each perfusion period was 30 min. Mean ± SEM for the number of rats shown in parentheses. *P < 0.05 for comparison with 0 mM db-cAMP


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  		TABLE 1. Concentrations of the three major ions in collectates from efferent ducts perfused with KRB containing 0–1 mM db-cAMP.a

The inhibition of fluid reabsorption by db-cAMP was shown to be reversible in a second experiment in which lengths of duct were perfused sequentially with KRB containing 0 mM, 0.1 mM, and then 0 mM db-cAMP (Fig. 2). This indicates that db-cAMP inhibits fluid reabsorption without damaging cellular function.



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  		FIG. 2. Reabsorption of fluid in efferent ducts perfused sequentially with KRB containing 0, 0.1, and 1.0 mM db-cAMP. Each perfusion period was 30 min. Mean ± SEM for 6 rats. *P < 0.05 for comparison with 0 mM db-cAMP

Figure 3 shows that fluid reabsorption was not affected by including db-cGMP in the perfusion fluid using concentrations at which db-cAMP would completely abolish reabsorption. Furthermore, there was no significant difference in the concentrations of Na+, Cl-, or K+ in the collectates when 0, 0.1, or 1.0 mM db-cGMP was included in the perfusion fluids (data not shown).



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  		FIG. 3. Reabsorption of fluid in efferent ducts perfused in vivo with KRB containing 0, 0.1, and 1.0 mM concentrations of db-cGMP. Each perfusion period was 30 min. Mean ± SEM for 8 rats. P < 0.05 for comparison with 0 mM db-cGMP

Pentoxifylline was used to confirm that the efferent duct epithelium could produce cAMP to suppress fluid reabsorption. Figure 4 shows that including pentoxifylline in the perfusate decreased fluid reabsorption in a dose-dependent manner and that the effect was reversible. When 5 mM pentoxifylline was included in the perfusate, the amount of cAMP in the collectate increased from 0.53 ± 0.14 fmol/mm to 3.01 ± 0.52 fmol/mm during a 90-min collection, indicating that pentoxifylline increased cAMP secretion into the lumen from the duct epithelium. The average rate of secretion of cAMP into the lumen when the perfusion fluids contained 0 and 5 mM pentoxifylline were, respectively, 0.34 ± 0.10 and 2.01 ± 0.37 fmol mm-1 h-1.



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  		FIG. 4. Reabsorption of fluid in efferent ducts perfused sequentially with 0, 1, 5, and 0 mM pentoxifylline in KRB. Mean ± SEM for 6 rats. *P < 0.05 for comparison with 0 mM pentoxifylline

Incubation In Vitro

A study in vitro was carried out to confirm that pentoxifylline stimulates cAMP production in the efferent ducts. Table 2 shows that a 5-min exposure of the ducts (with their vascular system cleared of blood) to 5 mM pentoxifylline caused a 4-fold increase in the total amount of cAMP measured. The ratio of the amount of cAMP released into the bathing solution to the amount of cAMP remaining in the duct was similar (1:13) in the presence and absence of pentoxyfylline. The results suggest that cAMP production is enhanced by pentoxifylline, most of the cAMP remains in the duct epithelium, and that pentoxifylline does not change the mechanism of cAMP release from the epithelium.


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  		TABLE 2. Concentration of cAMP after incubation of efferent ducts in vitro for 5 min in KRB containing 0 and 5 mM pentoxifylline.a


   DISCUSSION
TOP
 ABSTRACT
 INTRODUCTION
 MATERIALS AND METHODS
 RESULTS
 DISCUSSION
REFERENCES
 
This article demonstrates that db-cAMP can completely and reversibly inhibit fluid reabsorption (Figs. 1 and 2) in a perfused efferent duct, and so it indicates that cAMP is the main regulator of net fluid reabsorption in the efferent ducts. This report also provides evidence that cGMP is either not involved in regulating fluid and solute transport across the efferent ducts or is much less potent than cAMP. Consequently, in this respect, intracellular signal transduction is significantly different in the efferent ducts from their homologue, the proximal kidney tubules. In the latter, both cAMP [26–30] and cGMP [31] inhibit fluid reabsorption at about the same concentrations.

Further work is required to determine the mechanism of action of cAMP in the efferent ducts. It may act the same as in the proximal kidney tubules. The proximal tubules have the same principal transporter for Na+ and fluid reabsorption, NHE3, and cAMP inhibits this Na+/H+ antiporter [42–45], causing a reduction in Na+ and fluid reabsorption [26–30]. However, cAMP probably acts on more than NHE3 in the efferent ducts, as inhibition of NHE3 by amiloride can only reduce fluid reabsorption by 70% [5], whereas db-cAMP completely inhibits reabsorption at a concentration of 0.25 mM or more (Fig. 1). Further, cAMP has also been implicated in stimulating Cl- secretion in the efferent ducts [8], and this would drive fluid secretion into the duct. Support for this mechanism is indicated in Table 1, which shows that db-cAMP in the perfusate increased the concentration of Cl- in collectate. As CFTR is the main Cl- channel in the efferent ducts, the water channel, aquaporin, may also be a (secondary) target for cAMP as CFTR has been implicated in activating acquaporin-3 in airway epithelium [46] and aquaporin-1 has been localized in efferent duct epithelium [47, 48].

Table 1 indicates that the concentration of Na+ in the efferent ducts is not altered by cAMP as the inclusion of db-cAMP in the perfusate did not affect the concentration of Na+ in the collectate. However, the finding that inclusion of db-cAMP in the perfusate affected the reabsorption of Cl- and K+ indicates that regulation of their transport is more complicated than the regulation of Na+ transport. Indeed, it seems that K+ reabsorption is completely inhibited by (high) levels of db-cAMP that support net reabsorption of Cl- (Table 1). The increased concentration of Cl- in the collectates can be explained by cAMP stimulation of Cl- secretion in the efferent ducts (see above) as in other tissues including the cauda epididymidis [49, 50] respiratory epithelium [39, 51] and small and large intestine [52]. In the absence of db-cAMP in the perfusate, Cl- reabsorption in the efferent ducts is so much greater than secretion that there is no obvious movement of Cl- into the lumen when net transport is determined (Table 1). In this condition, reabsorption is greater for Cl- than Na+, as Cl- movement is not only determined by its attraction to Na+. When cAMP blocks the Na+ transporters and Cl- secretion is promoted, net reabsorption is reduced, but Cl- is still driven out of the duct. As our findings show that net reabsorption decreases with an increasing concentration of db-cAMP in the perfusate, it is suggested that cAMP inhibits Na+ and fluid reabsorption and stimulates Cl- secretion at the same time. Further, it is suggested that cAMP is normally maintained at a low level in the ducts (Table 2), permitting a high rate of fluid reabsorption and ensuring that sperm are concentrated before entering the ductus epididymidis.


   FOOTNOTES
 
1 This work was supported by a grant from the Australian Research Grants Committee and a postgraduate scholarship from the University of Newcastle. Back

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

Received: 29 May 2004.

First decision: 20 June 2003.

Accepted: 30 June 2003.


   REFERENCES
TOP
 ABSTRACT
 INTRODUCTION
 MATERIALS AND METHODS
 RESULTS
 DISCUSSION
 REFERENCES
 

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