Water transport in collecting ducts of Japanese quail

Abstract

Previously, we reported that the countercurrent urine concentration mechanism in birds appears to operate by recycling of a single solute (NaCl), in which the thick ascending limb of looped nephrons provides an energy source. To determine the importance of the medullary collecting duct (MCD) in the countercurrent multiplier system, we examined in isolated and perfused MCDs from Japanese quail, Coturnix coturnix, the osmotic and/or diffusional water permeability and whether arginine vasotocin (AVT) regulates water permeability. We noted that dark cells that possess electron-dense cytoplasm and numerous mitochondria and light mucus-secreting cells exist in the cortical collecting duct (CD), whereas only mucus-secreting cells are present in the MCDs. The volume flux (Jv) in the MCDs from intact birds and that from the water-deprived birds were nearly zero; after exposure to a hyperosmotic bath and AVT (2 x 10(-5) M), the Jv was significantly higher in water-deprived birds. The diffusional water permeability (Pdw) was moderately high in MCDs bathed in an isosmotic bath in which the Pdw was increased slightly by AVT (10(-5) M, bath) and more markedly (10(-5) M) by forskolin (Fsk), whereas 1,9-dideoxy Fsk (an inactive analogue) showed no effect. Furthermore, the basal adenosine 3',5'-cyclic monophosphate (cAMP) levels were higher in the medulla than in the cortex and were stimulated only slightly by AVT (10(-5) M) and markedly by Fsk (10(-4) M) in both the cortex and medulla. These results in the C. coturnix CD indicate the following. 1) Two types of cells are present; whereas dark cells resemble mammalian intercalated cells morphologically, it is not certain whether mucus-secreting cells are equivalent to principal cells. 2) AVT increases Pdw via a cAMP mechanism; the relatively high basal Pdw and minor effect of AVT on Jv and Pdw suggest, however, that diffusional water movement across the MCD may occur without significant direct control by AVT.

Urine concentration and avian aquaporin water channels

“…Regulation of avian kidney function by AVT and biological evidence for AVT receptors on preglomerular vasculature and renal tubules have been established in birds (for review, see [21]). In isolated perfused medullary CDs of Coturnix quail kidneys, the volume flux is nearly zero [59]. When medullary CDs are acutely treated with AVT, the volume flux increases only in water-deprived quail.…”

“…Furthermore, the basal diffusional water permeability (tritiated water flux coefficient) in medullary CDs is considerable, whereas the diffusional water permeability is increased slightly by AVT and only modestly by forskolin, which stimulates adenylate cyclase, whereas a forskolin analogue that does not stimulate adenylate cyclase shows no effect [59]. Thus AVT's direct action on water transport in CDs appears less marked in avian kidneys [23,59] than in mammalian kidneys [18,35]. In medullary cones, cAMP levels are also increased only slightly by AVT but markedly by forskolin, suggesting that the relatively low response to AVT is not due to insufficient adenylate cyclase activity [59].…”

“…In the isolated perfused thick AL of the quail kidney, the lumento-bath Na + and Cl − flux increased proportionately to perfusion flow rate and NaCl concentration, suggesting that increased luminal loading of NaCl evoked by increased volume flow or NaCl concentration facilitates NaCl extrusion (reabsorption), which may help enhance the imposition of the medullary osmotic gradient [62]. The CD cells in the cortical zone contain dark electrondense cells that have apical microvilli and vesicles, resembling intercalated cells, and light mucus-secreting cells that have large vacuoles, particularly in the apical side of the nucleus [50,59]. Abundant interdigitation and tight deep junctions are seen between mucus-secreting cells and also between intercalated cells and mucus-secreting cells.…”

“…When medullary CDs are acutely treated with AVT, the volume flux increases only in water-deprived quail. Furthermore, the basal diffusional water permeability (tritiated water flux coefficient) in medullary CDs is considerable, whereas the diffusional water permeability is increased slightly by AVT and only modestly by forskolin, which stimulates adenylate cyclase, whereas a forskolin analogue that does not stimulate adenylate cyclase shows no effect [59]. Thus AVT's direct action on water transport in CDs appears less marked in avian kidneys [23,59] than in mammalian kidneys [18,35].…”

“…Thus AVT's direct action on water transport in CDs appears less marked in avian kidneys [23,59] than in mammalian kidneys [18,35]. In medullary cones, cAMP levels are also increased only slightly by AVT but markedly by forskolin, suggesting that the relatively low response to AVT is not due to insufficient adenylate cyclase activity [59]. cAMP response to AVT also varies among species and ages [23].…”