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In Vivo and Ex Vivo Analysis of Tubule Function

James D. Stockand, Volker Vallon, Pablo Ortiz

10.1002/cphy.c100051

Source: Volume 2, Issue 4, October 2012

Published online: October 2012

Full Article on Wiley Online Library



Abstract

Analysis of tubule function with in vivo and ex vivo approaches has been instrumental in revealing renal physiology. This work allows assignment of functional significance to known gene products expressed along the nephron, primary of which are proteins involved in electrolyte transport and regulation of these transporters. Not only we have learned much about the key roles played by these transport proteins and their proper regulation in normal physiology but also the combination of contemporary molecular biology and molecular genetics with in vivo and ex vivo analysis opened a new era of discovery informative about the root causes of many renal diseases. The power of in vivo and ex vivo analysis of tubule function is that it preserves the native setting and control of the tubule and proteins within tubule cells enabling them to be investigated in a “real‐life” environment with a high degree of precision. In vivo and ex vivo analysis of tubule function continues to provide a powerful experimental outlet for testing, evaluating, and understanding physiology in the context of the novel information provided by sequencing of the human genome and contemporary genetic screening. These tools will continue to be a mainstay in renal laboratories as this discovery process continues and as we continue to identify new gene products functionally compromised in renal disease. © 2012 American Physiological Society. Compr Physiol 2:2495‐2525, 2012.

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Figure 1. Figure 1.

Preparing the kidney for micropuncture. (A) After a flank incision, the left kidney is carefully freed from perirenal fat and the adrenal gland, overturned, and placed in a cup such that the dorsal kidney surface faces up (B). (C) In the rat, the ureter is catheterized for collection of urine; this is less useful in mice because of a tendency of catheters to obstruct. To immobilize the kidney, the cup is lined with moleskin (D) and cotton soaked in saline is carefully placed around the kidney. 2% to 3% agar is dripped onto the cotton, which, after cooling, prevents leakage of the superfused mineral oil or saline (37°C) thereby establishing an oil or saline layer, respectively, over the kidney surface to keep the kidney surface warm and protected. Adapted, with permission, from reference 17.
Figure 2. Figure 2.

Identifying tubular segments accessible to micropuncture on the kidney surface. The Bowman's space of a Munich‐Wistar‐Fromter rat is injected with small amounts of artificial tubular fluid containing a blue dye. The nephron is mapped by following the dye moving along proximal and distal segments (1‐4). Adapted, with permission, from reference 331.
Figure 3. Figure 3.

Reabsorption of glucose along the proximal tubule. (A) Free‐flow collections of tubular fluid were performed along accessible proximal tubules at the kidney surface to establish a profile for fractional reabsorption of glucose versus fluid. (B) Glucose is rapidly and nearly completely reabsorbed within the early proximal tubule in wild‐type mice (WT). Reabsorption of glucose is absent in the early proximal tubule of mice lacking the sodium glucose cotransporter, SGLT2 (Sglt2−/−). (C) Mean fractional reabsorption of glucose for early (<40%) and late (≥40%) proximal tubular collections and up to the urine. *P<0.001 versus WT. Adapted, with permission, from reference 337.
Figure 4. Figure 4.

Reabsorption of Ca2+ along the nephron. (A) Free‐flow collections of tubular fluid were performed in the last surface loop of the proximal tubule (LPT), as well as, along distal segments (DS) using luminal K+ concentration as a reference for puncturing sites. (B) Ca2+ reabsorption was unaffected in Trpv5−/− mice up to the the proximal tubule surface loop (LPT); in contrast, mean Ca2+ delivery to puncturing sites in the distal segments (DS) accessible to micropuncture as well as urine (U) was significantly enhanced in Trpv5−/− mice. *P<0.001 versus wild type (WT). (C) To directly assess Ca2+ reabsorption along the distal segments, luminal K+ concentration was used as a reference with low and high concentrations indicating early and late aspects of the DS, respectively. Whereas, the Ca2+ delivery profile indicated net reabsorption along the distal segments in WT mice, fractional Ca2+ delivery increased in Trpv5−/− mice, indicating Ca2+ back leak along the distal segments in the absence of Trpv5. Finally, comparing the fractional Ca2+ delivery in the late distal segment with the values in urine indicated significant compensation in the collecting duct of Trpv5−/− (consistent with expression of TRPV6 in that segment). Adapted, with permission, from reference 141.
Figure 5. Figure 5.

Role of Na+/H+ exchanger (NHE3) in proximal tubular absorption. (A) Quantitative collection of tubular fluid was performed during perfusion of superficial proximal tubular segments downstream of an obstructing wax block with control and vehicle solution with and without the addition of the unselective NHE inhibitor ethylisopropylamiloride (EIPA) or the selective NHE3 inihitor S3226. (B) Proximal tubule absorption of HCO3− (JHCO3) and fluid (Jv) were greater in wild‐type (WT) compared to NHE3 null mice (Nhe3−/−). Moreover, EIPA (Black bars) inhibits absorption in WT but not in Nhe3−/− mice. (C) S3226 induces a dose‐dependent reduction in proximal tubular absorption of fluid and sodium in normal rats. *P<0.05 versus control/vehicle. #P<0.05 versus WT. Adapted, with permission, from references 362 and 342.
Figure 6. Figure 6.

Role of maxi‐K (BK) channels in K+ secretion in distal nephron. (A) Stationary microperfusion has been used to study distal K+ secretion. A double‐barreled perfusion pipette containing perfusion solution (P; to identify distal surface segments) and castor oil (CO; to fill the downstream segments) was inserted in the late proximal tubule. A double‐barreled microelectrode with K+‐sensitive ion‐exchange resin (IE) and reference solution (ref) is inserted into a distal segment. Another pipette (S) is placed into the distal tubule to split the oil column and add a low K+‐control solution. The increase in luminal K+ activity is followed and analyzed as a measure of secretory K+ flux, JK. In paired experiments, the BK channel blocker IBTX is added to the tubular fluid. (B) Mice lacking the ROMK channel continue to secrete K+, albeit at a reduced rate, by an IBTX‐sensitive mechanism consistent with BK channels. (C) A high K+ diet increases distal K+ secretion primarily by an IBTX‐sensitive K+ flux. * P<0.05 versus Control. #P<0.05 versus WT or 1.2% K+ diet, respectively. Adapted, with permission, from reference 9.
Figure 7. Figure 7.

Isolated split‐open tubule – a segment of the cortical collecting duct isolated from rat is shown here. The middle of this segment has been split open to allow patch clamp access to the apical membranes of the lining epithelial cells. Apical membranes are shown at higher magnification in the inset.
Figure 8. Figure 8.

Patch clamp configurations used in the isolated split‐open tubule preparation. This illustration depicts the five different seal configurations available for probing channel activity with the voltage clamp approach in isolated split‐open tubules: three amenable to single channel recording, cell‐attached, excised inside‐out, and excised outside‐out; and two for macroscopic current recording, perforated and whole cell. In this figure, the cell is represented as a circle and the recording pipette as a V. Gray shading defines the continuity between the solution in the recording pipette and intracellular solution. Arrows represent transition steps during seal formation taken to establish the distinct types of seals. Undershown are representative current data from configurations with single channel (left) and macroscopic (right) resolutions. Closed (C) and open (O) states are noted in the single channel trace. Data adapted, with permission, from J.D. Stockand or published previously in reference 256.
Figure 9. Figure 9.

SK channel in TAL epithelial cells. Shown is a typical single channel current trace of an SK channel in an inside‐out patch held at hyperpolarizing test potentials made from the apical membrane of an epithelial cell lining a split‐open murine TAL. Patch solutions contained 140/5 mmol/L K+ in the pipette/bath. Inward K+ current is downward. Test voltages and closed state are noted in the figure. Figure originally presented in reference 204.
Figure 10. Figure 10.

IK channel in TAL epithelial cells. Shown is a typical single channel current trace of an IK channel in a cell attached patch held on the apical membrane of an epithelial cell lining a split‐open rat TAL. For this experiment, pipette potential was 0 mV and the recording pipette contained 140 mmol/L KCl. Closed state noted with C. Data provided, with permission, by W‐H. Wang.
Figure 11. Figure 11.

Depiction of ion channel and transport proteins in a TAL epithelial cell.
Figure 12. Figure 12.

Basolateral Cl− channels in TAL cells. Shown are typical single channel current traces of the small (∼10 pS; A) and the double‐barreled (B) Cl− channels in cell attached patches formed on the basolateral membranes of epithelial cells in isolated, split‐open TAL. For the current trace containing only the small channel (A), the bath and pipette contained symmetrical NaCl and the patch was exposed to hyperpolarizing test pulses. The patch in B contains both the larger double‐barreled channel, as well as, the smaller Cl− channel (openings for the smaller channel noted with arrows). This patch was held at 50 and −80 mV test potentials also with symmetrical bath and pipette solutions. Closed state noted with C. Data in A and B originally published in references 125 and 127, respectively.
Figure 13. Figure 13.

Apical BK channel in cortical collecting duct (CCD). Shown here is a representative single channel current trace for a BK channel in the absence and presence of exogenous calcium in an excised, inside‐out patch from a principal cell in an isolated split‐open collecting duct. For this experiment, the patch was held at 0 mV, and the pipette and bath solutions contained 140 and 5 mmol/L KCl, respectively. Closed state noted with C. Data adapted, with permission, from W‐H Wang.
Figure 14. Figure 14.

Depiction of ion channel and transport proteins in a CD principal cell.
Figure 15. Figure 15.

Apical ENaC in CCD. (A) Shown here is a representative single channel current trace for ENaC in a cell‐attached patch from a principal cell in an isolated split‐open collecting duct before and after addition of vasopressin. For this experiment, the patch was held at 0 mV, and the pipette and bath solutions contained physiological NaCl. Closed state noted with C and areas below 1 (before) and 2 (after addition of vasopressin) shown at an expanded time scale below. (B) Summary results for change in ENaC Po in response to vasopressin. Data published previously in reference 31.
Figure 16. Figure 16.

Regulation of ENaC by local autocrine/paracrine signaling systems intrinsic to the CCD. Shown here is a representative single channel current trace (A) and summary data (B) for ENaC in cell attached patches from principal cells in an isolated split‐open collecting ducts before and after sequential addition of ATP and the broad‐spectrum P2 antagonist suramin. For these paired experiment, patches were held at 0 mV, and the pipette and bath solutions contained physiological NaCl. Closed state noted with C and areas below 1, 2, and 3 shown at expanded time scale below. Data published previously in reference 255.


Figure 1.

Preparing the kidney for micropuncture. (A) After a flank incision, the left kidney is carefully freed from perirenal fat and the adrenal gland, overturned, and placed in a cup such that the dorsal kidney surface faces up (B). (C) In the rat, the ureter is catheterized for collection of urine; this is less useful in mice because of a tendency of catheters to obstruct. To immobilize the kidney, the cup is lined with moleskin (D) and cotton soaked in saline is carefully placed around the kidney. 2% to 3% agar is dripped onto the cotton, which, after cooling, prevents leakage of the superfused mineral oil or saline (37°C) thereby establishing an oil or saline layer, respectively, over the kidney surface to keep the kidney surface warm and protected. Adapted, with permission, from reference 17.



Figure 2.

Identifying tubular segments accessible to micropuncture on the kidney surface. The Bowman's space of a Munich‐Wistar‐Fromter rat is injected with small amounts of artificial tubular fluid containing a blue dye. The nephron is mapped by following the dye moving along proximal and distal segments (1‐4). Adapted, with permission, from reference 331.



Figure 3.

Reabsorption of glucose along the proximal tubule. (A) Free‐flow collections of tubular fluid were performed along accessible proximal tubules at the kidney surface to establish a profile for fractional reabsorption of glucose versus fluid. (B) Glucose is rapidly and nearly completely reabsorbed within the early proximal tubule in wild‐type mice (WT). Reabsorption of glucose is absent in the early proximal tubule of mice lacking the sodium glucose cotransporter, SGLT2 (Sglt2−/−). (C) Mean fractional reabsorption of glucose for early (<40%) and late (≥40%) proximal tubular collections and up to the urine. *P<0.001 versus WT. Adapted, with permission, from reference 337.



Figure 4.

Reabsorption of Ca2+ along the nephron. (A) Free‐flow collections of tubular fluid were performed in the last surface loop of the proximal tubule (LPT), as well as, along distal segments (DS) using luminal K+ concentration as a reference for puncturing sites. (B) Ca2+ reabsorption was unaffected in Trpv5−/− mice up to the the proximal tubule surface loop (LPT); in contrast, mean Ca2+ delivery to puncturing sites in the distal segments (DS) accessible to micropuncture as well as urine (U) was significantly enhanced in Trpv5−/− mice. *P<0.001 versus wild type (WT). (C) To directly assess Ca2+ reabsorption along the distal segments, luminal K+ concentration was used as a reference with low and high concentrations indicating early and late aspects of the DS, respectively. Whereas, the Ca2+ delivery profile indicated net reabsorption along the distal segments in WT mice, fractional Ca2+ delivery increased in Trpv5−/− mice, indicating Ca2+ back leak along the distal segments in the absence of Trpv5. Finally, comparing the fractional Ca2+ delivery in the late distal segment with the values in urine indicated significant compensation in the collecting duct of Trpv5−/− (consistent with expression of TRPV6 in that segment). Adapted, with permission, from reference 141.



Figure 5.

Role of Na+/H+ exchanger (NHE3) in proximal tubular absorption. (A) Quantitative collection of tubular fluid was performed during perfusion of superficial proximal tubular segments downstream of an obstructing wax block with control and vehicle solution with and without the addition of the unselective NHE inhibitor ethylisopropylamiloride (EIPA) or the selective NHE3 inihitor S3226. (B) Proximal tubule absorption of HCO3− (JHCO3) and fluid (Jv) were greater in wild‐type (WT) compared to NHE3 null mice (Nhe3−/−). Moreover, EIPA (Black bars) inhibits absorption in WT but not in Nhe3−/− mice. (C) S3226 induces a dose‐dependent reduction in proximal tubular absorption of fluid and sodium in normal rats. *P<0.05 versus control/vehicle. #P<0.05 versus WT. Adapted, with permission, from references 362 and 342.



Figure 6.

Role of maxi‐K (BK) channels in K+ secretion in distal nephron. (A) Stationary microperfusion has been used to study distal K+ secretion. A double‐barreled perfusion pipette containing perfusion solution (P; to identify distal surface segments) and castor oil (CO; to fill the downstream segments) was inserted in the late proximal tubule. A double‐barreled microelectrode with K+‐sensitive ion‐exchange resin (IE) and reference solution (ref) is inserted into a distal segment. Another pipette (S) is placed into the distal tubule to split the oil column and add a low K+‐control solution. The increase in luminal K+ activity is followed and analyzed as a measure of secretory K+ flux, JK. In paired experiments, the BK channel blocker IBTX is added to the tubular fluid. (B) Mice lacking the ROMK channel continue to secrete K+, albeit at a reduced rate, by an IBTX‐sensitive mechanism consistent with BK channels. (C) A high K+ diet increases distal K+ secretion primarily by an IBTX‐sensitive K+ flux. * P<0.05 versus Control. #P<0.05 versus WT or 1.2% K+ diet, respectively. Adapted, with permission, from reference 9.



Figure 7.

Isolated split‐open tubule – a segment of the cortical collecting duct isolated from rat is shown here. The middle of this segment has been split open to allow patch clamp access to the apical membranes of the lining epithelial cells. Apical membranes are shown at higher magnification in the inset.



Figure 8.

Patch clamp configurations used in the isolated split‐open tubule preparation. This illustration depicts the five different seal configurations available for probing channel activity with the voltage clamp approach in isolated split‐open tubules: three amenable to single channel recording, cell‐attached, excised inside‐out, and excised outside‐out; and two for macroscopic current recording, perforated and whole cell. In this figure, the cell is represented as a circle and the recording pipette as a V. Gray shading defines the continuity between the solution in the recording pipette and intracellular solution. Arrows represent transition steps during seal formation taken to establish the distinct types of seals. Undershown are representative current data from configurations with single channel (left) and macroscopic (right) resolutions. Closed (C) and open (O) states are noted in the single channel trace. Data adapted, with permission, from J.D. Stockand or published previously in reference 256.



Figure 9.

SK channel in TAL epithelial cells. Shown is a typical single channel current trace of an SK channel in an inside‐out patch held at hyperpolarizing test potentials made from the apical membrane of an epithelial cell lining a split‐open murine TAL. Patch solutions contained 140/5 mmol/L K+ in the pipette/bath. Inward K+ current is downward. Test voltages and closed state are noted in the figure. Figure originally presented in reference 204.



Figure 10.

IK channel in TAL epithelial cells. Shown is a typical single channel current trace of an IK channel in a cell attached patch held on the apical membrane of an epithelial cell lining a split‐open rat TAL. For this experiment, pipette potential was 0 mV and the recording pipette contained 140 mmol/L KCl. Closed state noted with C. Data provided, with permission, by W‐H. Wang.



Figure 11.

Depiction of ion channel and transport proteins in a TAL epithelial cell.



Figure 12.

Basolateral Cl− channels in TAL cells. Shown are typical single channel current traces of the small (∼10 pS; A) and the double‐barreled (B) Cl− channels in cell attached patches formed on the basolateral membranes of epithelial cells in isolated, split‐open TAL. For the current trace containing only the small channel (A), the bath and pipette contained symmetrical NaCl and the patch was exposed to hyperpolarizing test pulses. The patch in B contains both the larger double‐barreled channel, as well as, the smaller Cl− channel (openings for the smaller channel noted with arrows). This patch was held at 50 and −80 mV test potentials also with symmetrical bath and pipette solutions. Closed state noted with C. Data in A and B originally published in references 125 and 127, respectively.



Figure 13.

Apical BK channel in cortical collecting duct (CCD). Shown here is a representative single channel current trace for a BK channel in the absence and presence of exogenous calcium in an excised, inside‐out patch from a principal cell in an isolated split‐open collecting duct. For this experiment, the patch was held at 0 mV, and the pipette and bath solutions contained 140 and 5 mmol/L KCl, respectively. Closed state noted with C. Data adapted, with permission, from W‐H Wang.



Figure 14.

Depiction of ion channel and transport proteins in a CD principal cell.



Figure 15.

Apical ENaC in CCD. (A) Shown here is a representative single channel current trace for ENaC in a cell‐attached patch from a principal cell in an isolated split‐open collecting duct before and after addition of vasopressin. For this experiment, the patch was held at 0 mV, and the pipette and bath solutions contained physiological NaCl. Closed state noted with C and areas below 1 (before) and 2 (after addition of vasopressin) shown at an expanded time scale below. (B) Summary results for change in ENaC Po in response to vasopressin. Data published previously in reference 31.



Figure 16.

Regulation of ENaC by local autocrine/paracrine signaling systems intrinsic to the CCD. Shown here is a representative single channel current trace (A) and summary data (B) for ENaC in cell attached patches from principal cells in an isolated split‐open collecting ducts before and after sequential addition of ATP and the broad‐spectrum P2 antagonist suramin. For these paired experiment, patches were held at 0 mV, and the pipette and bath solutions contained physiological NaCl. Closed state noted with C and areas below 1, 2, and 3 shown at expanded time scale below. Data published previously in reference 255.

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Article Title: In Vivo and Ex Vivo Analysis of Tubule Function
 

How to Cite

James D. Stockand, Volker Vallon, Pablo Ortiz. In Vivo and Ex Vivo Analysis of Tubule Function. Compr Physiol 2012, 2: 2495-2525. doi: 10.1002/cphy.c100051