Department of Biology, University of Virginia, Charlottesville, Virginia
Submitted 21 January 2005 ; accepted in final form 27 June 2005
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ABSTRACT |
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Drosophila; Malpighian tubule; cell volume regulation; G protein-coupled receptor; biogenic amines
Osmoregulation in insects is accomplished through the function of the excretory system, which consists primarily of two epithelial organs, the Malpighian tubules (MTs) and the rectum (8, 40). The MTs are blind-ended epithelial tubes that empty into the gut and are responsible for the production of primary urine. In the fruit fly Drosophila melanogaster, urine is produced by the main segments of the four MTs (16); these segments consist of two cell types, the principal cells and the stellate cells (50, 55). Urine secretion in Drosophila, as in other insects, is driven by the coupled action of a V-type proton ATPase and a proton/alkali metal antiporter in the apical membrane of the principal cells, resulting in the net active transport of potassium into the tubule lumen and the generation of a lumen-positive transepithelial potential (TEP) (3, 17, 34, 38). Chloride ions and water move passively into the lumen following their electrochemical and osmotic gradients, and the resulting urine is approximately isoosmotic with the surrounding hemolymph (28, 34, 36). The precise mechanism of chloride transport in the Drosophila MT remains unclear but is regulated by intracellular calcium levels in the stellate cells; treatment of tubules with agents that cause an increase in cytoplasmic calcium concentrations in the stellate cells result in a rapid increase in transepithelial chloride permeability, a depolarization of the TEP, and an increase in urine secretion (36).
I have previously shown that the biogenic amine tyramine is a potent stimulator of chloride transport and a diuretic agent in the Drosophila MT (7). Application of nanomolar doses of tyramine causes a rapid depolarization of the TEP and an increase in transepithelial chloride conductance, as shown by an increased sensitivity of the TEP to peritubular chloride concentration. Tyramine is synthesized in isolated tubules from tyrosine present in the peritubular bath through the action of the enzyme tyrosine decarboxylase in the principal cells. Tyramine then acts on the tubule with a pharmacology very similar to that of a cloned, G protein-coupled tyramine receptor. The response of MTs to tyramine requires an increase in intracellular calcium levels in the stellate cells (6); it is likely that, like the diuretic peptide leucokinin, tyramine acts by stimulating the release of calcium from intracellular stores in the stellate cells (42). This study shows that the sensitivity of the tubule to tyramine is modulated by the osmolality of the peritubular fluid. This modulatory mechanism could potentially play a role in protecting the insect from dehydration stress. These data demonstrate a novel mechanism for the osmotic control of epithelial function and raise the possibility that such a pathway might function in other secretory epithelial tissues.
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MATERIALS AND METHODS |
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Two solutions were used in these studies, depending on the type of experiment being performed. The first was a dissecting/recording saline containing (in mM) 85 NaCl, 20 KCl, 3 CaCl2, 12 MgSO4, 7.5 NaHCO3, 4 NaH2PO4, 15 glucose, and 10 HEPES, pH 6.75. This saline was used for studies involving acute application of secretagogues. The second solution, SBM, was a 1:1 mixture of Schneider's Drosophila medium (Invitrogen, Carlsbad, CA) and a diluting saline containing (in mM) 36 NaCl, 21 KCl, 15 MgCl2, 5 CaCl2, 4.8 NaHCO3, 2 NaH2PO4, 11.1 glucose, and 15 HEPES, pH 6.75. The composition of SBM, based on the compositions of the diluting saline and Schneider's medium, is the following (in mM): 36 NaCl, 21 KCl, 5.2 CaCl2, 7.5 MgSO4, 7.5 MgCl2, 4.8 NaHCO3, 1.3 KH2PO4, 3.4 sodium phosphate, 7.5 HEPES, 0.7 -ketoglutaric acid, 11.1 D-glucose, 0.43 fumaric acid, 0.38 malic acid, 0.42 succinic acid, 2.9 trehalose, 2.8
-alanine, 1.15 L-arginine, 1.5 L-aspartic acid, 0.25 L-cysteine, 0.21 L-cystine, 2.7 L-glutamic acid, 6.15 L-glutamine, 1.67 glycine, 1.29 L-histidine, 0.58 L-isoleucine, 0.58 L-leucine, 4.5 L-lysine HCl, 2.7 L-methionine, 0.45 L-phenylalanine, 7.4 L-proline, 1.19 L-serine, 1.47 L-threonine, 0.25 L-tryptophan, 1.38 L-tyrosine, 1.32 L-valine, and 1,000 mg/l yeastolate. SBM, which is thought to approximate insect hemolymph in composition, was used for studies of chronically stimulated tubules. The osmolality of both the recording saline and SBM was 255270 mosmol/kgH2O. All osmolality measurements were performed with a vapor-pressure osmometer (Wescor, Logan, UT).
Electrophysiology.
Tubules were dissected under saline and placed in a tissue culture dish, in which a 100-µl drop of 0.125 mg/ml poly-L-lysine had been dried (34). Where appropriate, the bathing saline was then replaced with SBM. The TEP was recorded immediately after dissection by impaling the tubule lumen with a sharp electrode (R > 25 M) pulled from theta-glass and filled with 3 M KCl. Potentials were amplified (Axopatch 200B, Axon Instruments, Union City, CA), digitized at 100 Hz and stored online. Recording and analysis were conducted using pCLAMP software (Axon Instruments). The peritubular bath was continuously perfused during recording.
Urine secretion assays. Urine secretion rates were measured as described previously (16). Tubules were dissected under SBM and placed in a 15-µl droplet of medium under mineral oil. One branch of the tubule was pulled out of the droplet and wrapped around a pin such that the cut end of the ureter and lower section of the other branch were out of the aqueous droplet. At intervals of 1220 min, the secreted urine droplet was removed from the ureter with a glass rod and its diameter was measured with an ocular micrometer. The volume of the urine droplet was calculated assuming spherical geometry. Solution changes were made immediately before the removal of the urine droplet for the second interval by twice removing 12 µl of medium and replacing it with 12 µl of new solution.
Data analysis. The response index, a measure of the TEP response to pulses of drugs, was calculated as previously described (7). The area under the voltage curve was calculated for a period beginning 15 s after drug application began and ending 15 s after drug application ended, using 10 mV as the baseline (drug area). For the same period, the area was calculated under a line extrapolated from the voltage trace for the 30 s immediately preceding drug application (control area). The response index was calculated as (control area drug area)/control area. Records in which the control response to tyramine had a response index of <0.03 were discarded from further analysis.
The average period of the TEP oscillations was calculated using a fast Fourier transform nonlinear least-squares algorithm as previously described (6). Records were analyzed beginning 60 s after each solution change.
Data were plotted and tests for statistical significance were performed with the use of Origin software (OriginLab, Northampton, MA).
Materials. Except where noted, all reagents were purchased from Sigma (St. Louis, MO). Leucokinin IV was purchased from Bachem (King of Prussia, PA).
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RESULTS |
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DISCUSSION |
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There has been one previous report of osmotic modulation of the period of an oscillatory signal. Reetz and coworkers (45) observed that in cultured rat astrocytes, ATP induced calcium oscillations through the activation of a P2 purinergic receptor, and the frequency of these oscillations was sensitive to osmolality. As in the Drosophila MTs, hypertonic media reduced the frequency of the oscillations, although the astrocyte responses were more variable than those of the MTs. No mechanism or functional consequence of this modulation was proposed.
The mechanism through which osmolality acts on tyramine and leucokinin signaling in the MTs remains unknown; however, the data are most easily explained by an effect on either inositol trisphosphate production or intracellular calcium dynamics. In the Drosophila MT, leucokinin stimulates the production of inositol trisphosphate and release of calcium from intracellular stores in the stellate cells (42). Tyramine, because it displays cross-desensitization with leucokinin, is presumed to act on the same pathway (6). The subsequent rise in intracellular calcium levels triggers either an increase in the chloride conductance of the stellate cells or an increase in paracellular chloride conductance. Generally speaking, changes in osmolality could act either on the first part of this pathway, between receptor activation and calcium release, or on the second part, between calcium release and the increase in chloride conductance. However, the current study shows that in the continuous presence of tyrosine, changes in osmolality alter the period of the TEP oscillations; these oscillations are hypothesized to reflect oscillations in intracellular calcium levels due to periodic release from and reuptake into intracellular stores (6). An effect of osmolality on oscillation period is most easily explained by a change in either inositol trisphosphate levels or calcium dynamics; a direct effect of osmolality on chloride conductance would more likely alter the amplitude of the TEP oscillations and not the period. Changes in osmolality are known to affect intracellular calcium dynamics in many systems (24), and modulation of inositol trisphosphate-mediated calcium release has been demonstrated (9, 23). Future experiments measuring intracellular calcium levels will be needed to test this hypothesis directly.
Although the effects of tyramine have not been reported in the MTs of any other insect species, leucokinin signaling has been extensively studied in the MTs of the mosquito Aedes aegypti (4). Leucokinin increases transepithelial chloride conductance in the MTs of both Aedes and Drosophila; however, the mechanistic details of the pathway appear to differ significantly between the two species. In Aedes, stellate cells are not involved in leucokinin signaling, and the resulting chloride conductance is entirely paracellular (39, 60). Nonetheless, in both Aedes and Drosophila MTs, leucokinin causes production of inositol trisphosphate and an increase in intracellular calcium levels (59), and Aedes MTs can also display oscillations in chloride conductance (5). It will be extremely interesting, therefore, to see whether leucokinin signaling in the Aedes MT is also modulated by peritubular osmolality.
It is noteworthy that whereas the response of the MT to acute applications of tyramine was modulated by both increases and decreases in osmolality, when the tyraminergic signaling pathway was continuously activated, the MT responded only to hyperosmotic stimulation. This asymmetric response to changes in osmolality was seen both electrophysiologically, where a drop in osmolality had no effect on the TEP oscillations, and with urine secretion, where inhibition of tyramine signaling by yohimbine did not affect the response of the MTs to a drop in osmolality. Without a direct knowledge of the biochemical pathways responsible for tyramine signaling and the TEP oscillations, one cannot provide any explanation for this difference. However, it is plausible that there exists a lower limit on the period of the TEP oscillations, possibly due to kinetic constraints on processes such as calcium release from and reuptake into intracellular stores, such that an increase in the effective concentration of tyramine caused by a drop in the osmolality would not result in any further acceleration of the oscillations. Whatever the mechanism, it seems likely that in the intact fly, where the tubule is bathed continuously in a hemolymph that contains tyrosine, the modulation of tyramine signaling causes a drop in urine secretion when hemolymph osmolality rises but is not functionally important when hemolymph osmolality falls. The increase in urine secretion that does occur following a drop in osmolality is greater than that predicted by the Boyle-Van't Hoff relationship, meaning either that the rate of ion flux across the epithelium is not constant or that the urine does not remain isoosmotic to the bathing solution. A similar result was reported for the New Zealand alpine weta, in which the flux rates of both potassium and chloride were greatly enhanced by peritubular hypoosmolality (33). This increase in flux was hypothesized to occur, at least in part, due to a drop in intracellular chloride activity, thereby reducing the electrochemical gradient opposing the movement of chloride across the basolateral membrane. In the MTs of Rhodnius, in contrast, the rate of ion flux appears to be invariant across a wide range of peritubular osmolality (27). Thus the Drosophila MTs seem to behave more like those of the alpine weta, and further studies of urine composition and osmolality as well as intracellular ion activities are necessary to identify the mechanisms underlying the response of the MTs to hypoosmolality.
What is the role of the osmotic modulation of MT function in the intact fly? One hypothesis is that it allows for enhanced survival under dehydration stress. Under normal conditions, there is a high flux of water through the insect excretory system, with the large majority of the water that is secreted by the main segments of the tubules being reabsorbed, primarily in the rectum but also in the lower tubules and anterior hindgut (8, 35). It has been hypothesized that this flux is important in the diuretic clearance of toxins from the hemolymph (40). During desiccation stress, Drosophila can lose a large percentage of their total body water; this water loss is associated with a loss of hemolymph volume and an increase in hemolymph osmolality (1, 19). Indeed, dehydrated Drosophila can tolerate increases of >15% in their hemolymph osmolality (1); such an increase is more than sufficient to inhibit tyramine signaling in the MTs. In the intact fly, the tyramine signaling pathway should be constitutively active due to the relatively high concentration of tyrosine in the hemolymph (14, 41). Thus, as a fly becomes dehydrated, tyramine signaling should decrease, leading to a reduction in the rate of urine secretion by the tubules. This, in turn, will reduce the flux of liquid moving into the rectum. I hypothesize that a decreased flow of liquid into and through the rectum will result in a more efficient reabsorption of water into the hemolymph and concentration of the feces. The argument that downregulation of urine secretion by the MTs is an important step in water retention is strengthened by the observation that MT antidiuresis has been observed in other insect species under dehydration stress (51, 54). Thus the sensitivity of the tubule to osmolality would result in an excretory system that combines a high resting flux of water with an enhanced ability to conserve water during dehydration stress.
A final question is why the control of MT secretion rate by osmolality is indirect, acting through the modulation of the frequency of tyramine-dependent TEP oscillations. One possible explanation stems from an analysis of the control of the salivary gland in the blowfly Calliphora erythrocephala (43). In that epithelium, secretion is stimulated by serotonin; serotonin causes oscillations in the TEP of the isolated salivary gland, and the frequency of the oscillations increases with serotonin concentration. Rapp and colleagues (44) demonstrated that the conversion of an analog parameter (serotonin concentration) into the frequency domain allowed for a more stable control of secretion rate in the presence of small fluctuations in serotonin levels. Similarly, in a Drosophila MT that is constitutively activated by tyramine, the conversion of osmotic information into the frequency domain would then allow for a more stable control of excretory function in the presence of small fluctuations in hemolymph osmolality. This modulatory pathway provides an example of the unexpected complexity of insect renal function and its regulation.
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GRANTS |
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ACKNOWLEDGMENTS |
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Present address for E. M. Blumenthal: Department of Biological Sciences, Marquette University, PO Box 1881, Milwaukee, WI 53201-1881.
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FOOTNOTES |
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The costs of publication of this article were defrayed in part by the payment of page charges. The article must therefore be hereby marked "advertisement" in accordance with 18 U.S.C. Section 1734 solely to indicate this fact.
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