Comprehensive Physiology Wiley Online Library

The Kidney During Development

Full Article on Wiley Online Library



Abstract

The sections in this article are:

1 Historical Perspective
2 Standards of Reference for Comparison of Renal Function Between Infants and Adults
3 Morphogenesis of the Kidney
3.1 Embryologic Origin of the Kidney
3.2 Subsequent Development of the Kidney
3.3 Glomerulus
3.4 Renal Tubule
4 Renal Blood Flow and its Control During Development
4.1 Total Renal Blood Flow
4.2 Intrarenal Distribution of Blood Flow
4.3 Renal Microvasculature
4.4 Control of Renal Circulation
5 Glomerular Filtration
5.1 Net Ultrafiltration Pressure
5.2 Hydraulic Conductivity and Ultrafiltration Coefficient
5.3 Glomerular Capillary Surface Area
5.4 Factors That Affect GFR during Development
5.5 Autoregulation of GFR
6 Renal Energy Metabolism
6.1 Development of Renal Cortical Metabolic Pathways
7 Tubular Functions
7.1 Renal Reabsorption of Sodium
7.2 Reabsorption of Bicarbonate and Excretion of Hydrogen Ions
7.3 Glucose Transport
7.4 Transport of Amino Acids
7.5 Transport of Organic Acids
7.6 Phosphate Transport
7.7 Control of Renal Transport during Development
7.8 Calcium Transport
7.9 Magnesium Transport
7.10 Potassium Transport
7.11 Concentration of Urine
8 Developmental Renal Physiology as A Tool for Understanding the Emergence and Integration of Renal Transport Systems
Figure 1. Figure 1.

Changes in mean values for GFR with age. Note difference between values corrected for total body water and for body surface area.

From McCrory 357
Figure 2. Figure 2.

Embryologic development of kidney. A: pronephros consists of several tubules with rudimentary glomeruli connected to a primary nephric duct. B: mesonephros develops caudally to pronephros, which degenerates. C: mesonephric nephrons are connected to the mesonephric (wolffian) ducts, which drain into the cloaca. D: metanephric kidney is derived from metanephric blastema, which gives rise to glomeruli and uriniferous tubules, and metanephric ducts (ureteric buds) that form the pelvis, calyces, and the first generation of collecting ducts. Mesonephric ducts give rise to muellerian ducts from which oviducts, uterus, and vagina are formed in females. In males, mesonephric ducts give rise to epididymis and ductus deferens; mesonephric tubules participate in formation of efferent ductiles of testis.

Figure 3. Figure 3.

Drawings of glomeruli at various developmental stages as seen by light microscopy. A: renal vesicles (rv) on each side of a collecting duct (cd). B: S‐shaped body. Cells to left of cleft (cl) become glomerular epithelium; and those to right of cleft become proximal tubule. C: capillary loop stage. Mesenchymal cells differentiate into endothelium and mesangium, leading to formation of capillary loops. D: maturing stage. Number of capillary loops increases; density of cells decreases.

From Reeves et al. 424
Figure 4. Figure 4.

Oliver's renal abacus: successive division of collecting tubules and their ampullae accounts for advancement of newly formed nephrons toward kidney surface; older nephrons accumulate on advancing tips

From Oliver 390
Figure 5. Figure 5.

Oldest nephron in arcade of 38‐week‐old human fetus (A) and nephron from adult (B). Note differences in complexity of proximal convoluted tubule and in length of loop of Henle.

From Potter 412
Figure 6. Figure 6.

Histogram of r/R values for infant nephron population (shaded area) superimposed on that of adult (heavy line), r = gs/pv, where gs is glomerular surface area calculated from measurements of glomerular diameter, and pv is volume of proximal tubule calculated from measurements of tubule length and tubule diameter. R, mean value of r for all nephrons.

From Fetterman et al. 167
Figure 7. Figure 7.

Transmission electron micrographs of proximal tubules from 2‐day‐old rabbits. A: outer cortical; cells have few apical microvilli (MV), small mitochondria (M), large nuclei (N), and few basolateral processes (arrow) (actual magnification x8,400). B: inner cortical; cells have elaborate apical brush border (MV), numerous mitochondria (M), and moderate number of basolateral processes (arrows) (actual magnification x10,000).

From Evan et al. 156
Figure 8. Figure 8.

Decrease in renal vascular resistance in piglet during maturation.

From Gruskin et al. 222
Figure 9. Figure 9.

Relative rate of blood flow per glomerulus in four cortical zones of canine puppy. Zone I is most superficial; zone IV is deepest. Total height of bars in each group is equal.

From Olbing et al. 389
Figure 10. Figure 10.

Cast of cortical vasculature of 1‐week‐old puppy. Sinusoidal vessels (S) connect directly with venous system (V), which in turn joins developing stellate vein.

From Evan 155
Figure 11. Figure 11.

Relationship between postnatal age and GFR in full‐term (y = 33.9 + 94.1) (x − 0.5) and preterm (y = 21.8 + 13.9) (x − 0.5) infants. Slopes of regression lines are significantly different (P < 0.05).

From Aperia et al. 10
Figure 12. Figure 12.

Changes in superficial nephron GFR (SNGFR) as function of age in guinea pig. The regression curve (solid line) was calculated to the least square fit by a polynomial. The dashed line was drawn from inspection.

From Spitzer and Brandis 511
Figure 13. Figure 13.

Theoretical effects on SNGFR of selective changes in glomerular plasma flow (GPF) at low ultrafiltration coefficient (Kf, measured in immature rats) and at high Kf (measured in adult rats). Calculations based on hydraulic pressure difference (ΔP) mm Hg and on afferent arteriolar oncotic pressure of 17 mm Hg.

From Ichikawa et al. 264
Figure 14. Figure 14.

Autoregulation factor for young and adult rats at various ranges of renal perfusion pressure. Factor >1 denotes lack of autoregulation; factor = 0 indicates perfect autoregulation. NX, unilateral nephrectomy.

From Chevalier and Kaiser 95
Figure 15. Figure 15.

Changes in O2 consumption as function of age in suspensions of proximal tubules of rats. FCCP (carbonyl‐cyanide triflurophenylhydrazone) denotes uncoupled oxidative phosphorylation. Ouabain‐dependent oxygen uptake was calculated as difference between control and ouabain.

From Barac‐Nieto and Spitzer 35
Figure 16. Figure 16.

Glycolysis in slices of kidney cortex of newborn and adult animals expressed as rate of CO2 production from NaHCO3 under anaerobic conditions.

From Dicker and Shirley 127
Figure 17. Figure 17.

Gluconeogenesis in renal cortical slices from rats of various ages. Values represent differences in glucose production between media of pH 7.1 and 7.7. Lines within and above the columns represent S.D.

From Goldstein and Harley‐DeWitt 202
Figure 18. Figure 18.

Natriuretic response of newborn (circles) and adult [diamonds) dogs to acute infusion of isotonic solution of saline equal to 10% of body weight. Note retention of Na+ in the young.

From Goldsmith et al. 198
Figure 19. Figure 19.

Fractional reabsorption of fluid (TF/PIN) by end of proximal convoluted tubule in guinea pigs of various ages.

From Spitzer and Brandis 511
Figure 20. Figure 20.

Top: relationship between age‐related changes in rate of fluid transport (Jv) and Na+,K+‐ATPase activity during postnatal maturation in juxtamedullary proximal tubules of maturing rabbits. Bottom: concomitant changes in surface area of basolateral membrane.

Top: Data from Schwartz and Evan 478,479; Bottom: Data from Evan (156 and unpublished observations
Figure 21. Figure 21.

Relationship between age‐related changes in net pressure for reabsorption (solid curve) and absolute reabsorption of fluid (open circles) in proximal tubules of guinea pigs.

From Kaskel et al. 284
Figure 22. Figure 22.

Changes in fraction of Na+ (TF/Pna/In) remaining in early and late distal tubules of hydropenic and volume‐expanded 24‐day‐old (open circles) and 40‐day‐old (closed circles) rats. Steeper slope observed in immature animals reflects larger fractional reabsorption of Na+ along distal convoluted tubule. NS, not significant; ** P < 0.001; *** P < 0.0001.

From Aperia and Elinder 14
Figure 23. Figure 23.

Plasma renin activity (PRA) in nanograms of angiotensin generated per milliliter of plasma in 30 min before (left column) and after (right column) administration of isotonic saline to canine puppies of various ages. Note higher PRA and larger fall in PRA in younger than in older animals.

From Drukker et al. 133
Figure 24. Figure 24.

Sodium balance, plasma sodium concentration, plasma renin activity (PRA), plasma aldosterone concentration (PA), and urinary aldosterone excretion (UAE) in 1‐week‐old newborns of different gestational ages.

From Sulyok et al. 528
Figure 25. Figure 25.

Regression line (y = 18.2 + 0.088x) and 95% confidence limits of plasma in low‐birth‐weight infants as function of postnatal age. Each closed circle represents mean value for respective age interval.

From Schwartz et al. 482
Figure 26. Figure 26.

Reabsorption and excretion of bicarbonate in infants and adults subjected to infusion of NaHCO3. Renal threshold for bicarbonate is ∼22mmol/liter in infants and ∼26 mmol/liter in adults.

From Edelmann et al. 140
Figure 27. Figure 27.

Changes in urinary pH of premature infants during the first 2 weeks of extrauterine life.

From Edelmann and Spitzer 141
Figure 28. Figure 28.

Rates of bicarbonate (JCHO3) and glucose (Jglu) transport in isolated perfused juxtamedullary proximal tubules of rabbits.

From Schwartz and Evan 478
Figure 29. Figure 29.

Maturation of intercalated (IC) and principal (PC) cell pH in rabbit cortical collecting ducts isolated from newborn (NB), 1‐month‐old (1 MO), and adult (A) rabbits. IC pH was greater than that of PC at all ages (mean of 25 of each cell type per tubule). Asterisk denotes significantly higher pH in IC from mature than from neonatal rabbits.

From Satlin and Schwartz 461
Figure 30. Figure 30.

Relationship between maximal glucose reabsorption per unit of GFR (TmG/CIn) and age in canine puppies.

From Arant et al. 21
Figure 31. Figure 31.

Regression line and 95% confidence limits of relationship between reabsorption of Pi per gram kidney weight (g KW) and filtered load of Pi by isolated perfused kidney of newborn (y = 1.25x + 0.09) and mature (y = 0.34x + 3.1) guinea pigs.

From Johnson and Spitzer 273
Figure 32. Figure 32.

Glomerular filtration rates (GFR) and fractional excretions of sodium (FeNa), calcium (FeCa), and phosphate (FePi) during control periods and following addition of parathyroid hormone (PTH) to the fluid perfusing isolated kidneys of newborn and adult guinea pigs. *Significantly different from control values (P < 0.01).

From Johnson and Spitzer 273
Figure 33. Figure 33.

Effect of variations in Pi intake on the maximal velocity (Vmax) of Na+ ‐Pi cotransport in brush border membranes of newborn (3–14‐day‐old) and adult (>57‐day‐old) guinea pigs.

From Neiberger et al. 381
Figure 34. Figure 34.

Relation between maximum urine osmolality and age in healthy infants and children. The curves represent the mean ± 1 S.D.

From Winberg 590
Figure 35. Figure 35.

Schematic representation of nephron maturation in rat. Numbers indicate successive generations of nephrons. Note substantial elongation in loops of Henle of both superficial and juxtamedullary nephrons.

From Edwards et al. 143
Figure 36. Figure 36.

Age‐related changes in variables affecting concentrating ability of rat. A: percentage of superficial nephrons that penetrate outer medulla. B: length of corticomedullary zone. C: osmolality of papillary tip following 8 h of dehydration. D: fraction of total papillary osmolality contributed by urea.

From Edwards et al. 143
Figure 37. Figure 37.

Regression analysis of changes in papillary and urinary osmolalities as function of age in rat. Note discrepancy between papillary and urinary osmolalities at early age.

From Edwards et al. 143
Figure 38. Figure 38.

Plasma concentrations of arginine vasopressin (AVP) before and after dehydration in rat. Smaller vertical bars represent ranges of values; numbers in parentheses represent numbers of animals.

From Edwards et al. 143
Figure 39. Figure 39.

Osmotic hydraulic conductance (Lp) of rabbit outer medullary collecting tubule (OMCT) at three stages of ontogenic differentiation under basal (‐ADH) or activated (+ADH) conductance. Stages are e, early, <4 days old; i, intermediate, 10–15 days, m, mature, 30–35 days. Numbers represent numbers of experiments.

From Horster and Zink 260
Figure 40. Figure 40.

Stimulation of adenylate cyclase by various concentrations of vasopressin in partially purified membranes from adult and neonatal (10‐day‐old) rabbit kidney medulla. Each point represents mean of triplicate determination from 2 to 4 animals.

From Schlondorff et al. 470


Figure 1.

Changes in mean values for GFR with age. Note difference between values corrected for total body water and for body surface area.

From McCrory 357


Figure 2.

Embryologic development of kidney. A: pronephros consists of several tubules with rudimentary glomeruli connected to a primary nephric duct. B: mesonephros develops caudally to pronephros, which degenerates. C: mesonephric nephrons are connected to the mesonephric (wolffian) ducts, which drain into the cloaca. D: metanephric kidney is derived from metanephric blastema, which gives rise to glomeruli and uriniferous tubules, and metanephric ducts (ureteric buds) that form the pelvis, calyces, and the first generation of collecting ducts. Mesonephric ducts give rise to muellerian ducts from which oviducts, uterus, and vagina are formed in females. In males, mesonephric ducts give rise to epididymis and ductus deferens; mesonephric tubules participate in formation of efferent ductiles of testis.



Figure 3.

Drawings of glomeruli at various developmental stages as seen by light microscopy. A: renal vesicles (rv) on each side of a collecting duct (cd). B: S‐shaped body. Cells to left of cleft (cl) become glomerular epithelium; and those to right of cleft become proximal tubule. C: capillary loop stage. Mesenchymal cells differentiate into endothelium and mesangium, leading to formation of capillary loops. D: maturing stage. Number of capillary loops increases; density of cells decreases.

From Reeves et al. 424


Figure 4.

Oliver's renal abacus: successive division of collecting tubules and their ampullae accounts for advancement of newly formed nephrons toward kidney surface; older nephrons accumulate on advancing tips

From Oliver 390


Figure 5.

Oldest nephron in arcade of 38‐week‐old human fetus (A) and nephron from adult (B). Note differences in complexity of proximal convoluted tubule and in length of loop of Henle.

From Potter 412


Figure 6.

Histogram of r/R values for infant nephron population (shaded area) superimposed on that of adult (heavy line), r = gs/pv, where gs is glomerular surface area calculated from measurements of glomerular diameter, and pv is volume of proximal tubule calculated from measurements of tubule length and tubule diameter. R, mean value of r for all nephrons.

From Fetterman et al. 167


Figure 7.

Transmission electron micrographs of proximal tubules from 2‐day‐old rabbits. A: outer cortical; cells have few apical microvilli (MV), small mitochondria (M), large nuclei (N), and few basolateral processes (arrow) (actual magnification x8,400). B: inner cortical; cells have elaborate apical brush border (MV), numerous mitochondria (M), and moderate number of basolateral processes (arrows) (actual magnification x10,000).

From Evan et al. 156


Figure 8.

Decrease in renal vascular resistance in piglet during maturation.

From Gruskin et al. 222


Figure 9.

Relative rate of blood flow per glomerulus in four cortical zones of canine puppy. Zone I is most superficial; zone IV is deepest. Total height of bars in each group is equal.

From Olbing et al. 389


Figure 10.

Cast of cortical vasculature of 1‐week‐old puppy. Sinusoidal vessels (S) connect directly with venous system (V), which in turn joins developing stellate vein.

From Evan 155


Figure 11.

Relationship between postnatal age and GFR in full‐term (y = 33.9 + 94.1) (x − 0.5) and preterm (y = 21.8 + 13.9) (x − 0.5) infants. Slopes of regression lines are significantly different (P < 0.05).

From Aperia et al. 10


Figure 12.

Changes in superficial nephron GFR (SNGFR) as function of age in guinea pig. The regression curve (solid line) was calculated to the least square fit by a polynomial. The dashed line was drawn from inspection.

From Spitzer and Brandis 511


Figure 13.

Theoretical effects on SNGFR of selective changes in glomerular plasma flow (GPF) at low ultrafiltration coefficient (Kf, measured in immature rats) and at high Kf (measured in adult rats). Calculations based on hydraulic pressure difference (ΔP) mm Hg and on afferent arteriolar oncotic pressure of 17 mm Hg.

From Ichikawa et al. 264


Figure 14.

Autoregulation factor for young and adult rats at various ranges of renal perfusion pressure. Factor >1 denotes lack of autoregulation; factor = 0 indicates perfect autoregulation. NX, unilateral nephrectomy.

From Chevalier and Kaiser 95


Figure 15.

Changes in O2 consumption as function of age in suspensions of proximal tubules of rats. FCCP (carbonyl‐cyanide triflurophenylhydrazone) denotes uncoupled oxidative phosphorylation. Ouabain‐dependent oxygen uptake was calculated as difference between control and ouabain.

From Barac‐Nieto and Spitzer 35


Figure 16.

Glycolysis in slices of kidney cortex of newborn and adult animals expressed as rate of CO2 production from NaHCO3 under anaerobic conditions.

From Dicker and Shirley 127


Figure 17.

Gluconeogenesis in renal cortical slices from rats of various ages. Values represent differences in glucose production between media of pH 7.1 and 7.7. Lines within and above the columns represent S.D.

From Goldstein and Harley‐DeWitt 202


Figure 18.

Natriuretic response of newborn (circles) and adult [diamonds) dogs to acute infusion of isotonic solution of saline equal to 10% of body weight. Note retention of Na+ in the young.

From Goldsmith et al. 198


Figure 19.

Fractional reabsorption of fluid (TF/PIN) by end of proximal convoluted tubule in guinea pigs of various ages.

From Spitzer and Brandis 511


Figure 20.

Top: relationship between age‐related changes in rate of fluid transport (Jv) and Na+,K+‐ATPase activity during postnatal maturation in juxtamedullary proximal tubules of maturing rabbits. Bottom: concomitant changes in surface area of basolateral membrane.

Top: Data from Schwartz and Evan 478,479; Bottom: Data from Evan (156 and unpublished observations


Figure 21.

Relationship between age‐related changes in net pressure for reabsorption (solid curve) and absolute reabsorption of fluid (open circles) in proximal tubules of guinea pigs.

From Kaskel et al. 284


Figure 22.

Changes in fraction of Na+ (TF/Pna/In) remaining in early and late distal tubules of hydropenic and volume‐expanded 24‐day‐old (open circles) and 40‐day‐old (closed circles) rats. Steeper slope observed in immature animals reflects larger fractional reabsorption of Na+ along distal convoluted tubule. NS, not significant; ** P < 0.001; *** P < 0.0001.

From Aperia and Elinder 14


Figure 23.

Plasma renin activity (PRA) in nanograms of angiotensin generated per milliliter of plasma in 30 min before (left column) and after (right column) administration of isotonic saline to canine puppies of various ages. Note higher PRA and larger fall in PRA in younger than in older animals.

From Drukker et al. 133


Figure 24.

Sodium balance, plasma sodium concentration, plasma renin activity (PRA), plasma aldosterone concentration (PA), and urinary aldosterone excretion (UAE) in 1‐week‐old newborns of different gestational ages.

From Sulyok et al. 528


Figure 25.

Regression line (y = 18.2 + 0.088x) and 95% confidence limits of plasma in low‐birth‐weight infants as function of postnatal age. Each closed circle represents mean value for respective age interval.

From Schwartz et al. 482


Figure 26.

Reabsorption and excretion of bicarbonate in infants and adults subjected to infusion of NaHCO3. Renal threshold for bicarbonate is ∼22mmol/liter in infants and ∼26 mmol/liter in adults.

From Edelmann et al. 140


Figure 27.

Changes in urinary pH of premature infants during the first 2 weeks of extrauterine life.

From Edelmann and Spitzer 141


Figure 28.

Rates of bicarbonate (JCHO3) and glucose (Jglu) transport in isolated perfused juxtamedullary proximal tubules of rabbits.

From Schwartz and Evan 478


Figure 29.

Maturation of intercalated (IC) and principal (PC) cell pH in rabbit cortical collecting ducts isolated from newborn (NB), 1‐month‐old (1 MO), and adult (A) rabbits. IC pH was greater than that of PC at all ages (mean of 25 of each cell type per tubule). Asterisk denotes significantly higher pH in IC from mature than from neonatal rabbits.

From Satlin and Schwartz 461


Figure 30.

Relationship between maximal glucose reabsorption per unit of GFR (TmG/CIn) and age in canine puppies.

From Arant et al. 21


Figure 31.

Regression line and 95% confidence limits of relationship between reabsorption of Pi per gram kidney weight (g KW) and filtered load of Pi by isolated perfused kidney of newborn (y = 1.25x + 0.09) and mature (y = 0.34x + 3.1) guinea pigs.

From Johnson and Spitzer 273


Figure 32.

Glomerular filtration rates (GFR) and fractional excretions of sodium (FeNa), calcium (FeCa), and phosphate (FePi) during control periods and following addition of parathyroid hormone (PTH) to the fluid perfusing isolated kidneys of newborn and adult guinea pigs. *Significantly different from control values (P < 0.01).

From Johnson and Spitzer 273


Figure 33.

Effect of variations in Pi intake on the maximal velocity (Vmax) of Na+ ‐Pi cotransport in brush border membranes of newborn (3–14‐day‐old) and adult (>57‐day‐old) guinea pigs.

From Neiberger et al. 381


Figure 34.

Relation between maximum urine osmolality and age in healthy infants and children. The curves represent the mean ± 1 S.D.

From Winberg 590


Figure 35.

Schematic representation of nephron maturation in rat. Numbers indicate successive generations of nephrons. Note substantial elongation in loops of Henle of both superficial and juxtamedullary nephrons.

From Edwards et al. 143


Figure 36.

Age‐related changes in variables affecting concentrating ability of rat. A: percentage of superficial nephrons that penetrate outer medulla. B: length of corticomedullary zone. C: osmolality of papillary tip following 8 h of dehydration. D: fraction of total papillary osmolality contributed by urea.

From Edwards et al. 143


Figure 37.

Regression analysis of changes in papillary and urinary osmolalities as function of age in rat. Note discrepancy between papillary and urinary osmolalities at early age.

From Edwards et al. 143


Figure 38.

Plasma concentrations of arginine vasopressin (AVP) before and after dehydration in rat. Smaller vertical bars represent ranges of values; numbers in parentheses represent numbers of animals.

From Edwards et al. 143


Figure 39.

Osmotic hydraulic conductance (Lp) of rabbit outer medullary collecting tubule (OMCT) at three stages of ontogenic differentiation under basal (‐ADH) or activated (+ADH) conductance. Stages are e, early, <4 days old; i, intermediate, 10–15 days, m, mature, 30–35 days. Numbers represent numbers of experiments.

From Horster and Zink 260


Figure 40.

Stimulation of adenylate cyclase by various concentrations of vasopressin in partially purified membranes from adult and neonatal (10‐day‐old) rabbit kidney medulla. Each point represents mean of triplicate determination from 2 to 4 animals.

From Schlondorff et al. 470
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How to Cite

Adrian Spitzer, George J. Schwartz. The Kidney During Development. Compr Physiol 2011, Supplement 25: Handbook of Physiology, Renal Physiology: 475-544. First published in print 1992. doi: 10.1002/cphy.cp080112