The effect of intraluminal flow rate on glomerulotubular balance in the proximal tubule of the rat kidney

Romano, Giulio; Favret, G; Federico, Edda; Bartoli, Ettore

doi:10.1113/expphysiol.1996.sp003921

Cited by 13 publications

(12 citation statements)

References 34 publications

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“…MIJ of ET-1 into the early proximal tubule caused the exposure of the full length of the proximal tubule to the peptide. Absolute and percentage reabsorption rose strikingly during MIJ, and this cannot be accounted for by the presence of glomerulotubular balance which would have been expected to cause a rise in absolute and a fall in fractional reabsorption [24]. Therefore, this seems a direct effect of ET-1 on proximal reabsorption.…”

Section: Resultsmentioning

confidence: 94%

Effect of Endothelin 1 on Proximal Reabsorption and Tubuloglomerular Feedback

Romano¹,

Giagu²,

Favret³

et al. 2000

Kidney Blood Press Res

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Endothelin 1 (ET–1) is a powerful constrictor of the afferent glomerular artery, implicated in the occurrence of both functional and acute renal failure. Besides being produced by the endothelium, ET–1 is also secreted by proximal tubular cells, suggesting that it may act as an endoluminal messenger. The present study is intended to verify whether ET–1 may play a role in the tubuloglomerular feedback system. The experiments were performed in rat superficial glomeruli. In 25 nephrons we measured by the total collection technique the single–nephron glomerular filtration rate (SNGFR; nl/min) and reabsorption rates before (control) and during microinjection (MIJ) of ET–1 10^–7 M into the first proximal convolution or Bowman’s space. The SNGFR rose from 27±3 to 61±11 nl/min (p<0.01), the percent proximal reabsorption rose from 43 to 74%, and the absolute reabsorption rose from 13±2 to 46±11 nl/min (p<0.01). In additional 23 nephrons the collections were performed at the earliest distal convolution accessible on the renal surface, while MIJ was performed in the last proximal convolution of the same nephrons. The SNGFR rose during MIJ from 22±3 to 40±6 nl/min (p<0.01), the percent reabsorption rose from 61 to 66% (p>0.77), and the absolute reabsorption rose from 12±2 to 26±4 nl/min, (p<0.003). Exposure of the macula densa to intraluminally injected ET–1 causes an abrupt increase in SNGFR of the experimental nephron, in the absence of changes in systemic and renal hemodynamics. During proximal MIJ, ET–1 may have reached the macula densa during the time preceding the beginning of collection and interruption of the delivery of fluid to the distal nephron. ET–1 directly stimulates fractional and absolute volume reabsorption along the proximal tubule. Proximal secretion and/or filtration of ET–1 could represent a physiological mechanism to activate the tubuloglomerular feedback, eliciting a response opposite to that triggered by systemic and intrarenal infusion.

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Section: Resultsmentioning

confidence: 94%

Effect of Endothelin 1 on Proximal Reabsorption and Tubuloglomerular Feedback

Romano¹,

Giagu²,

Favret³

et al. 2000

Kidney Blood Press Res

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“…Because water reabsorption is driven by Na ϩ transport, a prerequisite for precise glomerulotubular balance is that luminal fluid flow modulates proximal tubule epithelial cell Na ϩ reabsorption. This flow effect has been termed ''perfusion-absorption balance'' (2,3) and has been demonstrated in microperfusion studies in rats (4)(5)(6)(7)(8). In mammalian kidneys, the primary pathway for proximal Na ϩ transport is into the cell through the Na ϩ -H ϩ exchanger isoform 3 (NHE-3) within the luminal cell membrane and out across the peritubular cell membrane via the Na ϩ , K ϩ -ATPase.…”

mentioning

confidence: 99%

Mechanosensory function of microvilli of the kidney proximal tubule

Duan

Yan

et al. 2004

Proc. Natl. Acad. Sci. U.S.A.

104

128

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Normal variations in glomerular filtration induce proportional changes in proximal tubule Na ؉ reabsorption. This ''glomerulotubular balance'' derives from flow dependence of Na ؉ uptake across luminal cell membranes; however, the underlying physical mechanism is unknown. Our hypothesis is that flow-dependent reabsorption is an autoregulatory mechanism that is independent of neural and hormonal systems. It is signaled by the hydrodynamic torque (bending moment) on epithelial microvilli. Such signals need to be transmitted to the terminal web to modulate Na ؉ -H ؉ -exchange activity. To investigate this hypothesis, we examined Na ؉ transport and tubular diameter in response to different flow rates during the microperfusion of isolated S2 proximal tubules from mouse kidneys. The data were analyzed by using a mathematical model to estimate the microvillous torque as function of flow. In this model, increases in luminal diameter have the effect of blunting the impact of flow velocity on microvillous shear stress and, thus, microvillous torque. We found that variations in microvillous torque produce nearly identical fractional changes in Na ؉ reabsorption. Furthermore, the flow-dependent Na ؉ transport is increased by increasing luminal fluid viscosity, diminished in Na ؉ -H ؉ exchanger isoform 3 knockout mice, and abolished by nontoxic disruption of the actin cytoskeleton. These data support our hypothesis that the ''brush-border'' microvilli serve a mechanosensory function in which fluid dynamic torque is transmitted to the actin cytoskeleton and modulates Na ؉ absorption in kidney proximal tubules. glomerulotubular balance ͉ flow-dependent transport ͉ Na ϩ -H ϩ exchange

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“…This is consistent with the known fact that GTB is not perfect, and there is a slight resetting of reabsorption (Bartoli & Earley, 1972). This resetting causes reabsorption to increase and to fall less than SNGFR when filtration is changed by experimental manoeuvres (Romano et al 1996). Therefore, the relationship between reabsorption and filtration should be different, in conditions where the GTB is expressed, from that observed in conditions where these changes are random and attributable to experimental errors in measurements, as during collection-recollection sampling.…”

Section: Discussionmentioning

confidence: 99%

“…The major difficulty with these experiments is to produce changes in native flow of tubular fluid without modification of the peritubular environment, and vice versa. In order to dissociate these factors we devised appropriate experiments by inducing hydronephrosis (Bartoli et al 1978) or partial obstruction of the lumen of single tubules (Romano, Favret, Federico & Bartoli, 1996). Finally, we resorted to double-collecting proximal tubular fluid to reduce its delivery to the last proximal convolution .…”

Section: Discussionmentioning

confidence: 99%

“…2 ) and reproduced by others (Haberle et al 1981) without EAO, should already represent conclusive evidence in favour of the intraluminal theory. Furthermore, this would allow us to consider as fully valid the experiments involving manipulation of intraluminal flow rate per se, such as those using single nephron hydronephrosis (Bartoli et al 1978) and single nephron external compression (Romano et al 1996), which invariably demonstrated a strong correlation between the fall in reabsorption and that in SNGFR. The single nephron function hypothesis states that each proximal convoluted tubule is perfused by the parent efferent arteriolar blood.…”

Section: Discussionmentioning

confidence: 99%

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Proximal reabsorption with changing tubular fluid inflow in rat nephrons

Romano¹,

Favret²,

D’Amato³

et al. 1998

Experimental Physiology

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SUMMARYThe relative contribution of intraluminal versus peritubular factors in mediating glomerulo-tubular balance (GTB) is still controversial. We modulated the load of tubular fluid to the proximal tubule of single nephrons of rats by injecting oil into the efferent arteries (EAO). In fifty nephrons the changes in reabsorption induced by obstruction occurred in the same direction as, and were significantly correlated with, the simultaneous changes in single nephron glomerular filtration rate (SNGFR) (y = -0-54 + 0-92x, R = 0-91, P < 0-0001). In an additional set of thirty-nine nephrons the load of tubular fluid was changed, during EAO, by partial collection from Bowman's space or from the early proximal convolution. Thus, the rate of tubular fluid delivery along the proximal tubule was changed in an experimental situation that prevented any modification in the oncotic pressure of peritubular capillaries. The changes in proximal deliveries during this experimental condition were significantly correlated with those during reabsorption (y = -2-87 + 0-7 lx, R = 0-82, P < 0.0001). These data demonstrate that GTB is fully expressed even when the native peritubular environment is kept constant while the rate of perfusion of proximal tubular segments with native tubular fluid is changed.

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The effect of intraluminal flow rate on glomerulotubular balance in the proximal tubule of the rat kidney

Cited by 13 publications

References 34 publications

Effect of Endothelin 1 on Proximal Reabsorption and Tubuloglomerular Feedback

Effect of Endothelin 1 on Proximal Reabsorption and Tubuloglomerular Feedback

Mechanosensory function of microvilli of the kidney proximal tubule

Proximal reabsorption with changing tubular fluid inflow in rat nephrons

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