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Vertebrate Renal System

Eldon J. Braun, William H. Dantzler

10.1002/cphy.cp130108

Source: Supplement 30: Handbook of Physiology, Comparative Physiology

Originally published: 1997

Published online: January 2011

Full Article on Wiley Online Library



Abstract

The sections in this article are:

1 External and Internal Gross Morphology of Vertebrate Kidneys
1.1 Fishes
1.2 Amphibians
1.3 Reptiles
1.4 Birds
1.5 Mammals
2 Glomerular Ultrafiltration
2.1 Glomerular Filtration Rate: Stability and Variability
2.2 Changes in the Number of Filtering Nephrons
2.3 Regulation of SNGFRs and the Number of Filtering Nephrons
3 Tubular Transport
3.1 Fine Structure of Tubule Cells
3.2 Transport of Inorganic Ions
3.3 Transport of Fluid
3.4 Transport of Organic Substances
4 Concentration and Dilution of the Urine
5 Integrative Summary of Some Renal Functions
5.1 Fishes
5.2 Amphibians
5.3 Reptiles
5.4 Birds
5.5 Mammals
Figure 1. Figure 1.

Diagrams of an elasmobranch nephron in the bundle zone (dorsal portion of the kidney) and in the sinus zone (the more ventral aspect of the kidney). a: Stylized nephron emphasizes the countercurrent folding pattern of four loops labeled I–IV(RC, renal corpuscle). A peritubular sheath surrounds the countercurrent system of nephron segments and the capillary loops in the bundle zone. Arrows indicate direction of flow in tubules and capillaries. b: Complexity of skate nephron in bundle and sinus zones. (from ref. 264, with permission).
Figure 2. Figure 2.

Three‐dimensional illustration of the avian kidney based on the anatomy of the desert quail (Callipepla gambelii); depicted is the extreme morphological heterogeneity of the nephron population within the quail kidney, which exists in all avian kidneys.

From ref. 58, with permission
Figure 3. Figure 3.

Drawings of proximal tubule ultrastructure in mammalian kidney. Cellular interdigitation is demonstrated by stippling over neighboring cells and their processes. a: S1 (P1) segment. Cellular interdigitation is most extensive and extends to apical ends of cells. Brush border is dense and high. b: S2 (P2) segment. Cellular interdigitation is decreased; cells have smooth apical outline. Brush border is less dense and reduced in height. Peroxysomes (cross‐hatched profiles) art numerous. c, d: S3 (P3) segments. Cellular interdigitation is markedly reduced. Considerable interspecies differences in brush border occur. In rabbit (c) and most other mammals, microvilli are short and scanty. In rat (d), brush border of S3 (P3) segment is highest among all proximal segments.

From ref. 263, with permission
Figure 4. Figure 4.

Schematic drawings comparing proximal tubule cells in two urodele amphibian species, Ambystoma tigrinum (tiger salamander) and Necturus maculosus (mudpuppy). Note higher, more uniform, and more dense brush border of apical membrane and greater amplification of basal membrane in A. tigrinum than in N. maculosus. Neither species has the large amplification and intercellular interdigitation of the lateral cell membranes observed in mammals (see Fig. 3).

From ref. 121, after ref. 301, with permission
Figure 5. Figure 5.

Schematic drawings showing characteristics of surfaces of proximal and distal tubule cells of mammals and reptiles. A: Mammalian cell type (less detailed than in Fig. 1). B: Gecko (Hemidactylus sp.) proximal cell. Note amplification of basal surface area. C: Horned lizard (Phrynosoma cornutum) and Galapagos lizard (Tropidurus sp.) proximal cells. Note lack of amplification of basal surface area. D: Mammalian thick ascending limb or early distal convoluted cell. E: Gecko (Hemidactylus sp.) distal cell. Note deep basolateral infoldings with elongated mitochondria, similar to those in mammalian cells. F: Horned lizard (P. cornutum) and Galapagos lizard (Tropidurus sp.) distal cell type. Note lack of deep basal infolding but presence of extensive lateral interdigitations.

From ref. 383, with permission
Figure 6. Figure 6.

Distal nephron of Amphiuma means (Congo eel). Glomerulus and proximal tubule are drawn in outline for reference. Shading indicates distal nephron segments. Lines from schematics to tubule segments indicate cellular composition of each segment. EDT, early distal tubule or “diluting segment”; LDT, late distal tubule.

From ref. 451, with permission
Figure 7. Figure 7.

Model for sodium and chloride reabsorption in nonmammalian proximal tubules based primarily on work with amphibians. Filled circle with solid arrows and breakdown of ATP to ADP, primary active transport; open circles, carrier‐mediated transport that may involve carrier‐mediated diffusion or secondary active transport; broken arrows, movement down an electrochemical gradient; solid arrows, movement against an electrochemical gradient; lines with bar at end, inhibition; VT, transepithelial potential difference, with sign enclosed in circle indicating whether lumen is negative or positive relative to peritubular fluid.
Figure 8. Figure 8.

Model for net sodium chloride secretion by proximal tubules based on studies of elasmobranch proximal tubules by Beyenbach 31. Filled circle with solid arrows, primary active transport; open circles, carrier‐mediated transport; broken arrows, movement down electrochemical gradient; solid arrows, movement against electrochemical gradient; lines with bar at end, inhibition; VT, transepithelial potential difference, with sign in circle indicating whether lumen is negative or positive relative to peritubular fluid. Note that transepithelial potential difference changes from lumen‐positive to lumen‐negative when chloride conductance across the luminal membrane is increased by cAMP.
Figure 9. Figure 9.

Model for sodium, chloride, potassium, and hydrogen ion transport by early distal tubules of nephrons of nonmammalian vertebrates and thick ascending limbs of loops of Henle of long‐looped (mammalian‐type) avian nephrons and mammalian nephrons. Filled circle with solid arrows, primary active transport; open circles, carrier‐mediated transport; broken arrows, movement down electrochemical gradient; solid arrows, movement against electrochemical gradient; lines with bar at end, inhibition; VT, transepithelial potential difference, with sign in circle indicating whether lumen is negative or positive relative to peritubular fluid. Although details are based primarily on studies with amphibian and mammalian nephrons, the steps for sodium chloride reabsorption apparently are the same for early distal tubules of teleost nephrons, amphibian nephrons, and loopless (reptilian‐type) avian nephrons; the thick ascending limb of Henle's loop of mammalian‐type avian nephrons and mammalian nephrons; and possibly the thin intermediate segment or early distal tubule of reptilian nephrons.
Figure 10. Figure 10.

Model for sodium, chloride, potassium, and hydrogen ion transport by late distal tubules, collecting tubules, and collecting ducts. Filled circle with solid arrows, primary active transport; open circles, carrier‐mediated transport; broken arrows, movement down electrochemical gradient; solid arrows, movement against electrochemical gradient; lines with bar at end, inhibition; VT, transepithelial potential difference, with sign in circle indicating whether lumen is negative or positive relative to peritubular fluid. Uncertainty about processes in different cell types in nonmammalian vertebrates, particularly in intercalated cells, is indicated by question marks.
Figure 11. Figure 11.

Model for potassium reabsorption by proximal tubules based on studies of mammals and amphibians. Filled circle with solid arrows, primary active transport; broken arrows, movement down electrochemical gradient; solid arrows, movement against electrochemical gradient; lines with bar at end, inhibition; VT, transepithelial potential difference, with sign in circle indicating whether lumen is negative or positive relative to peritubular fluid. Note that transepithelial potential difference changes from lumen‐negative in early proximal tubule to lumen‐positive in late proximal tubules in mammals but remains lumen‐negative in proximal tubules of amphibians. See text for differences between mammals and amphibians in transport steps pictured.
Figure 12. Figure 12.

Model for hydrogen ion secretion and bicarbonate reabsorption by proximal tubules based on studies on mammals and amphibians. Filled circle with solid arrows, primary active transport; open circles, carrier‐mediated transport; broken arrows, movement down electrochemical gradient; solid arrows, movement against electrochemical gradient. C.A., carbonic anhydrase. Question marks, uncertainty about role of carbonic anhydrase in amphibians and about exit step for bicarbonate across peritubular membrane in both mammals and amphibians.
Figure 13. Figure 13.

Net fluid movement in isolated, perfused garter snake (Thamnophis sp.) proximal renal tubules. Composition of solution in lumen and bath in terms of sodium and chloride and of substitutes for them is shown at sides of figure for each experiment. Each bar represents mean net fluid movement, with lumen and bath composition shown. Horizontal lines at end of each bar represent SE. From six to thirteen tubules were used in each experiment.

From ref. 115, with permission
Figure 14. Figure 14.

Electron micrographs of cross‐section of isolated, perfused proximal renal tubules of garter snake (Thamnophis sp.). A: Proximal tubule perfused and bathed with medium containing sodium. B: Proximal tubule perfused and bathed with medium in which sodium has been replaced with choline. Both tubules are shown at same magnification. Note increase in cell height and widening of intercellular spaces in B, the tubule perfused and bathed with medium in which choline replaced sodium. Bar = 2.0 mm.

From ref. 139, with permission
Figure 15. Figure 15.

Model for net tubular reabsorption of glucose based on studies on amphibians, reptiles, and fish. Open circles, carrier‐mediated transport; broken arrows, movement down electrochemical gradient; solid arrows, movement against electrochemical gradient. Question marks, tentative suggestions. Apparent permeabilities of luminal membrane in lumen‐to‐cell ) and cell‐to‐lumen directions and of peritubular membrane in bath‐to‐cell direction are shown for various conditions for snake renal tubules.
Figure 16. Figure 16.

Model for amino acid entry across luminal membrane based on studies on amphibians and fish. Open circles, carrier‐mediated transport; solid arrows, movement against electrochemical gradient. Absence of positive charge on sodium indicates electroneutral entry step.
Figure 17. Figure 17.

Model for net taurine secretion based on studies on teleosts. Open circles, carrier‐mediated transport; broken arrows, movement down electrochemical gradient; solid arrows, movement against electrochemical gradient.
Figure 18. Figure 18.

Model for net tubular secretion of urea based on studies on amphibians. Open circles, carrier‐mediated transport; broken arrows, movement down electrochemical gradient; solid arrows, movement against electrochemical gradient.
Figure 19. Figure 19.

Model for net tubular secretion of organic anions, with para‐aminohippurate (PAH) as the prototype anion, based on studies on fish, amphibians, reptiles, and birds. A−, anion of unspecified nature. Arrows from K+, Na+, and Ca2+, sites of effects of alterations in concentrations of these inorganic cations. Broken arrow with question mark leading from transport step at luminal membrane to transport step at peritubular membrane, possible feedback coupling between transport steps. Electrical potentials at top of figure refer to peritubular fluid at 0 mV. Values for apparent permeabilities to PAH of luminal (PL) and peritubular (PF) membranes and for Km and Jmax for net secretion are from studies on snake and frog renal tubules. Filled circle with solid arrows, primary active transport; open circles, carrier‐mediated transport; broken arrows, movement down electrochemical gradient; solid arrows, movement against electrochemical gradient.
Figure 20. Figure 20.

Model for net tubular secretion of urate in reptiles. Open circles, carrier‐mediated transport; broken arrows, movement down electrochemical gradient; solid arrows, movement against electrochemical gradient. A−, anion of unspecified nature; broken arrow with question mark, uncertainty at transport step across luminal membrane.
Figure 21. Figure 21.

Model for net tubular secretion of urate in birds. Filled circle with solid arrows, primary active transport; open circles, carrier‐mediated transport; broken arrows, movement down electrochemical gradient; solid arrows, movement against electrochemical gradient.
Figure 22. Figure 22.

Model for net tubular transport of tetraethylammonium (TEA+) and N1‐methylnicotinamide (NMN+) in snake proximal renal tubules. C+, cation of unspecified nature. Open circles, carrier‐mediated transport; broken arrows, movement down electrochemical gradient; solid arrows, movement against electrochemical gradient. A−, anion of unspecified nature; broken arrow with question mark, possible feedback coupling between transport steps. Maximum unidirectional fluxes for TEA and NMN are given and illustrated by the lengths of the arrows at the top and bottom of model, respectively. Km value for each unidirectional flux is also given.
Figure 23. Figure 23.

Model for net secretion of tetraethylammonium (TEA+) and N1‐methylnicotinamide (NMN+) (and most other organic cations) and for net reabsorption of choline in rabbit proximal renal tubules. Filled circle with solid arrows, primary active transport; open circles, carrier‐mediated transport; broken arrows, movement down electrochemical gradient; solid arrows, movement against electrochemical gradient.
Figure 24. Figure 24.

Model for net secretion of tetraethylammonium (TEA+) and N1‐methylnicotinamide (NMN+) in fish proximal renal tubules. Open circles, carrier‐mediated transport; broken arrows, movement down electrochemical gradient; solid arrows, movement against electrochemical gradient.


Figure 1.

Diagrams of an elasmobranch nephron in the bundle zone (dorsal portion of the kidney) and in the sinus zone (the more ventral aspect of the kidney). a: Stylized nephron emphasizes the countercurrent folding pattern of four loops labeled I–IV(RC, renal corpuscle). A peritubular sheath surrounds the countercurrent system of nephron segments and the capillary loops in the bundle zone. Arrows indicate direction of flow in tubules and capillaries. b: Complexity of skate nephron in bundle and sinus zones. (from ref. 264, with permission).



Figure 2.

Three‐dimensional illustration of the avian kidney based on the anatomy of the desert quail (Callipepla gambelii); depicted is the extreme morphological heterogeneity of the nephron population within the quail kidney, which exists in all avian kidneys.

From ref. 58, with permission


Figure 3.

Drawings of proximal tubule ultrastructure in mammalian kidney. Cellular interdigitation is demonstrated by stippling over neighboring cells and their processes. a: S1 (P1) segment. Cellular interdigitation is most extensive and extends to apical ends of cells. Brush border is dense and high. b: S2 (P2) segment. Cellular interdigitation is decreased; cells have smooth apical outline. Brush border is less dense and reduced in height. Peroxysomes (cross‐hatched profiles) art numerous. c, d: S3 (P3) segments. Cellular interdigitation is markedly reduced. Considerable interspecies differences in brush border occur. In rabbit (c) and most other mammals, microvilli are short and scanty. In rat (d), brush border of S3 (P3) segment is highest among all proximal segments.

From ref. 263, with permission


Figure 4.

Schematic drawings comparing proximal tubule cells in two urodele amphibian species, Ambystoma tigrinum (tiger salamander) and Necturus maculosus (mudpuppy). Note higher, more uniform, and more dense brush border of apical membrane and greater amplification of basal membrane in A. tigrinum than in N. maculosus. Neither species has the large amplification and intercellular interdigitation of the lateral cell membranes observed in mammals (see Fig. 3).

From ref. 121, after ref. 301, with permission


Figure 5.

Schematic drawings showing characteristics of surfaces of proximal and distal tubule cells of mammals and reptiles. A: Mammalian cell type (less detailed than in Fig. 1). B: Gecko (Hemidactylus sp.) proximal cell. Note amplification of basal surface area. C: Horned lizard (Phrynosoma cornutum) and Galapagos lizard (Tropidurus sp.) proximal cells. Note lack of amplification of basal surface area. D: Mammalian thick ascending limb or early distal convoluted cell. E: Gecko (Hemidactylus sp.) distal cell. Note deep basolateral infoldings with elongated mitochondria, similar to those in mammalian cells. F: Horned lizard (P. cornutum) and Galapagos lizard (Tropidurus sp.) distal cell type. Note lack of deep basal infolding but presence of extensive lateral interdigitations.

From ref. 383, with permission


Figure 6.

Distal nephron of Amphiuma means (Congo eel). Glomerulus and proximal tubule are drawn in outline for reference. Shading indicates distal nephron segments. Lines from schematics to tubule segments indicate cellular composition of each segment. EDT, early distal tubule or “diluting segment”; LDT, late distal tubule.

From ref. 451, with permission


Figure 7.

Model for sodium and chloride reabsorption in nonmammalian proximal tubules based primarily on work with amphibians. Filled circle with solid arrows and breakdown of ATP to ADP, primary active transport; open circles, carrier‐mediated transport that may involve carrier‐mediated diffusion or secondary active transport; broken arrows, movement down an electrochemical gradient; solid arrows, movement against an electrochemical gradient; lines with bar at end, inhibition; VT, transepithelial potential difference, with sign enclosed in circle indicating whether lumen is negative or positive relative to peritubular fluid.



Figure 8.

Model for net sodium chloride secretion by proximal tubules based on studies of elasmobranch proximal tubules by Beyenbach 31. Filled circle with solid arrows, primary active transport; open circles, carrier‐mediated transport; broken arrows, movement down electrochemical gradient; solid arrows, movement against electrochemical gradient; lines with bar at end, inhibition; VT, transepithelial potential difference, with sign in circle indicating whether lumen is negative or positive relative to peritubular fluid. Note that transepithelial potential difference changes from lumen‐positive to lumen‐negative when chloride conductance across the luminal membrane is increased by cAMP.



Figure 9.

Model for sodium, chloride, potassium, and hydrogen ion transport by early distal tubules of nephrons of nonmammalian vertebrates and thick ascending limbs of loops of Henle of long‐looped (mammalian‐type) avian nephrons and mammalian nephrons. Filled circle with solid arrows, primary active transport; open circles, carrier‐mediated transport; broken arrows, movement down electrochemical gradient; solid arrows, movement against electrochemical gradient; lines with bar at end, inhibition; VT, transepithelial potential difference, with sign in circle indicating whether lumen is negative or positive relative to peritubular fluid. Although details are based primarily on studies with amphibian and mammalian nephrons, the steps for sodium chloride reabsorption apparently are the same for early distal tubules of teleost nephrons, amphibian nephrons, and loopless (reptilian‐type) avian nephrons; the thick ascending limb of Henle's loop of mammalian‐type avian nephrons and mammalian nephrons; and possibly the thin intermediate segment or early distal tubule of reptilian nephrons.



Figure 10.

Model for sodium, chloride, potassium, and hydrogen ion transport by late distal tubules, collecting tubules, and collecting ducts. Filled circle with solid arrows, primary active transport; open circles, carrier‐mediated transport; broken arrows, movement down electrochemical gradient; solid arrows, movement against electrochemical gradient; lines with bar at end, inhibition; VT, transepithelial potential difference, with sign in circle indicating whether lumen is negative or positive relative to peritubular fluid. Uncertainty about processes in different cell types in nonmammalian vertebrates, particularly in intercalated cells, is indicated by question marks.



Figure 11.

Model for potassium reabsorption by proximal tubules based on studies of mammals and amphibians. Filled circle with solid arrows, primary active transport; broken arrows, movement down electrochemical gradient; solid arrows, movement against electrochemical gradient; lines with bar at end, inhibition; VT, transepithelial potential difference, with sign in circle indicating whether lumen is negative or positive relative to peritubular fluid. Note that transepithelial potential difference changes from lumen‐negative in early proximal tubule to lumen‐positive in late proximal tubules in mammals but remains lumen‐negative in proximal tubules of amphibians. See text for differences between mammals and amphibians in transport steps pictured.



Figure 12.

Model for hydrogen ion secretion and bicarbonate reabsorption by proximal tubules based on studies on mammals and amphibians. Filled circle with solid arrows, primary active transport; open circles, carrier‐mediated transport; broken arrows, movement down electrochemical gradient; solid arrows, movement against electrochemical gradient. C.A., carbonic anhydrase. Question marks, uncertainty about role of carbonic anhydrase in amphibians and about exit step for bicarbonate across peritubular membrane in both mammals and amphibians.



Figure 13.

Net fluid movement in isolated, perfused garter snake (Thamnophis sp.) proximal renal tubules. Composition of solution in lumen and bath in terms of sodium and chloride and of substitutes for them is shown at sides of figure for each experiment. Each bar represents mean net fluid movement, with lumen and bath composition shown. Horizontal lines at end of each bar represent SE. From six to thirteen tubules were used in each experiment.

From ref. 115, with permission


Figure 14.

Electron micrographs of cross‐section of isolated, perfused proximal renal tubules of garter snake (Thamnophis sp.). A: Proximal tubule perfused and bathed with medium containing sodium. B: Proximal tubule perfused and bathed with medium in which sodium has been replaced with choline. Both tubules are shown at same magnification. Note increase in cell height and widening of intercellular spaces in B, the tubule perfused and bathed with medium in which choline replaced sodium. Bar = 2.0 mm.

From ref. 139, with permission


Figure 15.

Model for net tubular reabsorption of glucose based on studies on amphibians, reptiles, and fish. Open circles, carrier‐mediated transport; broken arrows, movement down electrochemical gradient; solid arrows, movement against electrochemical gradient. Question marks, tentative suggestions. Apparent permeabilities of luminal membrane in lumen‐to‐cell ) and cell‐to‐lumen directions and of peritubular membrane in bath‐to‐cell direction are shown for various conditions for snake renal tubules.



Figure 16.

Model for amino acid entry across luminal membrane based on studies on amphibians and fish. Open circles, carrier‐mediated transport; solid arrows, movement against electrochemical gradient. Absence of positive charge on sodium indicates electroneutral entry step.



Figure 17.

Model for net taurine secretion based on studies on teleosts. Open circles, carrier‐mediated transport; broken arrows, movement down electrochemical gradient; solid arrows, movement against electrochemical gradient.



Figure 18.

Model for net tubular secretion of urea based on studies on amphibians. Open circles, carrier‐mediated transport; broken arrows, movement down electrochemical gradient; solid arrows, movement against electrochemical gradient.



Figure 19.

Model for net tubular secretion of organic anions, with para‐aminohippurate (PAH) as the prototype anion, based on studies on fish, amphibians, reptiles, and birds. A−, anion of unspecified nature. Arrows from K+, Na+, and Ca2+, sites of effects of alterations in concentrations of these inorganic cations. Broken arrow with question mark leading from transport step at luminal membrane to transport step at peritubular membrane, possible feedback coupling between transport steps. Electrical potentials at top of figure refer to peritubular fluid at 0 mV. Values for apparent permeabilities to PAH of luminal (PL) and peritubular (PF) membranes and for Km and Jmax for net secretion are from studies on snake and frog renal tubules. Filled circle with solid arrows, primary active transport; open circles, carrier‐mediated transport; broken arrows, movement down electrochemical gradient; solid arrows, movement against electrochemical gradient.



Figure 20.

Model for net tubular secretion of urate in reptiles. Open circles, carrier‐mediated transport; broken arrows, movement down electrochemical gradient; solid arrows, movement against electrochemical gradient. A−, anion of unspecified nature; broken arrow with question mark, uncertainty at transport step across luminal membrane.



Figure 21.

Model for net tubular secretion of urate in birds. Filled circle with solid arrows, primary active transport; open circles, carrier‐mediated transport; broken arrows, movement down electrochemical gradient; solid arrows, movement against electrochemical gradient.



Figure 22.

Model for net tubular transport of tetraethylammonium (TEA+) and N1‐methylnicotinamide (NMN+) in snake proximal renal tubules. C+, cation of unspecified nature. Open circles, carrier‐mediated transport; broken arrows, movement down electrochemical gradient; solid arrows, movement against electrochemical gradient. A−, anion of unspecified nature; broken arrow with question mark, possible feedback coupling between transport steps. Maximum unidirectional fluxes for TEA and NMN are given and illustrated by the lengths of the arrows at the top and bottom of model, respectively. Km value for each unidirectional flux is also given.



Figure 23.

Model for net secretion of tetraethylammonium (TEA+) and N1‐methylnicotinamide (NMN+) (and most other organic cations) and for net reabsorption of choline in rabbit proximal renal tubules. Filled circle with solid arrows, primary active transport; open circles, carrier‐mediated transport; broken arrows, movement down electrochemical gradient; solid arrows, movement against electrochemical gradient.



Figure 24.

Model for net secretion of tetraethylammonium (TEA+) and N1‐methylnicotinamide (NMN+) in fish proximal renal tubules. Open circles, carrier‐mediated transport; broken arrows, movement down electrochemical gradient; solid arrows, movement against electrochemical gradient.

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Article Title: Vertebrate Renal System
 

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Eldon J. Braun, William H. Dantzler. Vertebrate Renal System. Compr Physiol 2011, Supplement 30: Handbook of Physiology, Comparative Physiology: 481-576. First published in print 1997. doi: 10.1002/cphy.cp130108