Role of the kidney in human leptin metabolism

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1 Role of the kidney in human metabolism CHRISTIAN MEYER, 1 DAVE ROBSON, 1 NOYA RACKOVSKY, 1 VEENA NADKARNI, 1 AND JOHN GERICH 1,2 Departments of 1 Medicine and 2 Physiology and Pharmacology, University of Rochester School of Medicine, Rochester, New York Meyer, Christian, Dave Robson, Noya Rackovsky, Veena Nadkarni, and John Gerich. Role of the kidney in human metabolism. Am. J. Physiol. 273 (Endocrinol. Metab. 36): E903 E907, To assess the role of the human kidney in metabolism, we measured renal net balance and urinary excretion in 16 normal postabsorptive volunteers with varying degrees of obesity. Arterial concentrations ( ng/ml) significantly exceeded renal vein concentrations ( ng/ml, P 0.001). Renal fractional extraction averaged %, and renal net balance (uptake) averaged 1, ng/min. Lineweaver-Burk analysis indicated that renal uptake followed saturation kinetics with an apparent Michaelis-Menten constant of 10.9 ng/ml and maximal velocity of 1,730 ng/min. Leptin was generally undetectable in urine. Using literature values for systemic clearance, we calculated that renal uptake could account for 80% of all removal from plasma. These data indicate that the human kidney plays a substantial role in removal from plasma by taking up and degrading the peptide. obesity LEPTIN, THE 16-kDa product of the obese gene, is currently believed to be involved in the regulation of appetite and energy expenditure (3, 7, 15, 18). Although it is well established that is secreted exclusively by adipocytes (12, 21), little is known regarding its metabolism in humans aside from its systemic clearance rate, half-life, and volume of distribution (8). Mouse kidney has been reported to have a substantial number of receptors (19). This observation and the fact that bilateral nephrectomy reduced plasma clearance 80% in rats (5) suggest that, in these species, the kidneys may play an important role in removal of from plasma. However, in humans with end-stage renal failure of various etiologies, plasma has been reported to be increased only about twofold, and no correlation was found between plasma levels and creatinine clearance (13). These latter observations suggest that the human kidney may play a less important role in metabolism. To date, neither renal extraction nor urinary excretion of has been reported in humans. If kidneys were the major route of clearance of plasma in humans and if was quantitatively excreted in urine, urinary could be used to assess secretion. Therefore, in the present studies, we measured urinary excretion and the net balance of across the kidney in normal postabsorptive volunteers with varying degrees of obesity. METHODS Subjects. Informed written consent was obtained from 16 normal volunteers (6 men and 10 women) after the protocol had been approved by the University of Rochester Institutional Review Board. The subjects were (means SE) 40 3 yr of age, weighed 74 4 kg (body mass index kg/m 2 ), and had normal glucose tolerance tests according to World Health Organization criteria (20) and no family history of diabetes mellitus. For 3 days before the study, all had been on a weight-maintaining diet containing at least 200 g carbohydrate and had abstained from alcohol. Protocol. Subjects were admitted to the University of Rochester General Clinical Research Center the evening before experiments. They consumed a standard meal (10 kcal/kg, 50% carbohydrate, 35% fat, and 15% protein) between 6:00 and 7:00 PM and were fasted overnight until experiments were completed. Between 8:00 and 9:00 AM, a renal vein was catheterized through the right femoral vein under fluoroscopy, and the position of the catheter tip was ascertained by injecting a small amount of iodinated contrast material. The catheter was then continuously infused with a saline solution (heparinized at 5.6 U/min) to maintain patency. At 9:00 AM, a dorsal hand vein was cannulated and kept in a thermoregulated Plexiglas box at 65 C for sampling arterialized venous blood (1), and an antecubital venous infusion of p-aminohippuric acid (PAH; 12 mg/min) was started for determination of renal plasma flow. After we allowed 1 h for PAH to achieve steady state, three blood samples were collected simultaneously from the dorsal hand vein and the renal vein at 30-min intervals (0, 30, and 60 min) for determination of plasma and PAH. Urine was collected in sterile containers between 6:00 and 10:00 AM for the determination of and creatinine in the urine and immediately frozen at 20 C. Analytic procedures. Blood samples for PAH and concentrations were collected in oxalate-fluoride tubes immediately placed in a 4 C ice bath. Plasma was separated within 30 min by centrifugation at 4 C. Plasma PAH concentrations were measured by a colorimetric method (2). Plasma and urine concentrations were measured by a commercial radioimmunoassay (RIA) (Linco Research, St. Louis, MO). The assay limits of detection and linearity were 0.5 and 100 ng/ml, respectively (10). The day-to-day precision of the assay, expressed as coefficients of variation, ranged from 3.6 to 6.2% (10). Serum and urine creatinine were measured by standard laboratory methods. Stability of in the urine and validation of urinary analysis. To determine whether urine degrades, 0.5 ml 125 I-labeled from the RIA kit containing 60,000 disintegrations per minute was incubated in 0.5 ml urine at 37 C for 15 h and subjected to gel permeation chromatography. A 1 29 cm column of Sephadex G-50 coarse, equilibrated with incubation buffer for the RIA (0.05 M phosphosaline, ph 7.4, containing M EDTA, 0.05% Triton X-100, and 1% RIA-grade bovine serum albumin), was used. The flow rate was 20 ml/h, and the eluate was collected as 375-µl fractions. Application of 0.5 ml of 125 I- from the RIA kit directly onto the column served as a control /97 $5.00 Copyright 1997 the American Physiological Society E903

2 E904 RENAL LEPTIN METABOLISM Fig. 1. Gel permeation chromatography of 125 I-labeled without (A) and with (B) prior incubation in urine at 37 C for 15 h. dpm, Disintegrations/min. To determine whether urine interferes with the RIA kit, known quantities of were added to urine and incubated for 15 h at 37 C. Aliquots of urine were assayed before and after addition of 25 ng. Calculations. Renal plasma flow was determined by the PAH clearance technique (6). Renal uptake was calculated as renal plasma flow (arterial concentration renal venous concentration). Because the kidney does not produce (12), renal fractional extraction of was calculated as (arterial concentration renal venous concentration) arterial concentration 100. Renal tissue degradation was calculated as renal net balance urinary excretion. The contribution of the kidney to overall systemic removal of from plasma was calculated as renal uptake overall systemic removal of from plasma 100. Overall systemic removal of from plasma was calculated as mean plasma concentration mean plasma clearance mean body weight. Plasma clearance was assumed to be 1.50 ml kg 1 min 1, based on the mean value obtained by Klein et al. (8) in 14 normal volunteers. Statistical analysis. Unless stated otherwise, data are expressed as means SE. Least-square regression analysis was used for correlations and determinations of Michaelis- Table 1. Recovery of 20 ng/ml incubated in urine at 37 C for 15 h and concentrations of urine to which had not been added Urine Sample Urine Leptin Concentrations, ng/ml Without With Recovery, % 1 ND ND ND ND ND ND ND ND Means SE ND, not detectable. Menten constant (K m ) and maximal velocity (V max ) for renal uptake from Lineweaver-Burk plots. A P value 0.05 was considered to be statistically significant. RESULTS To assess whether urine degrades, the recovery and elution profile of 125 I- incubated with urine were determined. As shown in Fig. 1, 125 I- incubated with urine eluted as a single peak and its recovery (88%) was comparable with that of 125 I- not incubated with urine. These observations indicate that urine does not appreciably degrade. To determine whether urine interferes with the assay, measurements of known amounts of added to urine were made. As shown in Table 1, the recovery of added to the urine averaged 106 3%. Additionally, 250 µl standard were incubated in urine for 15 h at 37 C and were serially diluted with incubation buffer for the RIA. Serial dilutions from 250 µl urine from the same urine to which the standard had not been added served as controls. Leptin was then analyzed by RIA on all dilutions. As shown in Table 2, the samples diluted proportionately and recovery averaged 98 4%. Renal plasma flow and creatinine clearance averaged ml/min and ml/min, respectively. Fasting arterial plasma concentrations ranged from 0.75 to 36.1 ng/ml (mean ng/ml; Table 3). As expected (11, 14), there was a positive correlation Table 2. Serial dilutions of 25 ng incubated in urine and of urine to which had not been added Dilution Factor Urine Leptin Concentrations, ng/ml Without With Recovery, % 2 ND ND ND ND ND

3 RENAL LEPTIN METABOLISM E905 Table 3. Renal plasma flow; arterial, renal vein, and urinary concentrations; renal fractional extraction; and renal uptake on normal postabsorptive volunteers Subject Gender BMI, kg/m 2 RPF, ml/min Leptin Concentrations, ng/ml Artery Renal vein Urine Fx, % RU, ng/min 1 M , ND F ND M M ND M , ND F ND F ND M , ND F ND F ND , F M , , F ND , F , F , F ND 6.8 1,787 Mean SE , BMI, body mass index; RPF, renal plasma flow; Fx, fractional extraction; RU, renal uptake; M, male; F, female. between arterial plasma concentrations and body mass index (r 0.88, P 0.001). Renal venous concentrations ( ng/ml) were significantly lower than arterial concentrations (P 0.001), indicating net renal uptake of. Renal fractional extraction averaged % and was inversely related to arterial plasma concentrations (r 0.58, P 0.03; Fig. 2). There was no correlation between renal fractional extraction of and creatinine clearance (r 0.034, P 0.9). Renal clearance averaged ml/min and was greater in men than in women ( vs ml/min). Renal uptake averaged 1, ng/min. Urinary was detectable in only four cases and ranged in these subjects between 0.8 and 1.0 ng/ml, which corresponded to excretion rates of ng/min. In the other 12 subjects, urinary was 0.5 ng/ml and thus below the sensitivity of the RIA. With the assumption of values at the sensitivity of the assay, this could account at most for only ng/min urinary excretion. Consequently, renal tissue uptake (overall uptake minus urinary excretion) closely approximated overall renal uptake (1, ng/min). The decrease in renal fractional extraction as a function of arterial concentrations suggested that renal uptake may be a saturable process subject to Michaelis-Menten kinetics. This was therefore assessed by the Lineweaver-Burk analysis (Fig. 3). There was a highly significant inverse correlation between 1/renal net balance and 1/arterial plasma concentration (r 0.93, P 0.001). The calculated apparent K m and V max were 10.9 ng/ml and 1,730 ng/min, respectively, consistent with Michaelis- Menten kinetics for the removal of plasma by the kidney. The mean estimated overall systemic removal of from plasma in our subjects, calculated by using the mean clearance data of Klein et al. (8), was 1,288 ng/min (11.6 ng/ml 1.50 ml kg 1 min 1 74 kg). Renal uptake accounted for 80% of this. Fig. 2. Correlation between renal fractional extraction and arterial concentrations. Fig. 3. Lineweaver-Burk analysis of renal uptake. K m, Michaelis-Menten constant; V max, maximal velocity.

4 E906 RENAL LEPTIN METABOLISM DISCUSSION The present studies indicate that, in postabsorptive normal human volunteers, 1) the kidneys account for a substantial proportion of overall systemic removal from the circulation, 2) little or no cleared by the kidneys appears in the urine, 3) thus renal removal of from plasma involves tissue degradation rather than mere urinary excretion, and, finally, 4) the removal of from plasma by the kidneys is a saturable process following Michaelis-Menten kinetics. We found that the kidneys could account for 80% of the overall systemic removal of from plasma. This calculation was based on the use of a mean value for systemic clearance from the data of Klein et al. (8). Such an approach assumes that systemic clearance does not vary with plasma concentrations and could actually underestimate the contribution of the kidney in people with high levels if systemic clearance decreases as plasma increases. This appears to be the case, since we found that renal fractional extraction decreased as plasma increased. Moreover, we found that renal uptake could be ascribed to a saturable process as assessed by the Lineweaver-Burk analysis. It is of interest that the calculated apparent K m of 10.2 ng/ml for renal uptake approximates the mean arterial plasma concentration in our subjects. This indicates that renal uptake would be half-maximal at physiological plasma concentrations and that small increases in secretion or small decrements in renal uptake would result in relative disproportional increases in plasma. In general, we found urinary excretion to be negligible compared with overall renal uptake. We also found that renal fractional extraction was unrelated to creatinine clearance. These observations strongly suggest that is taken up and degraded by renal parenchymal cells independently of glomerular filtration rate and are consistent with the finding of Merabet et al. (13). Although the renal metabolic pathway for is not known, there is evidence for glomerular filtration followed by tubular reabsorption and peritubular extraction of various hormones such as insulin, C-peptide, glucagon, and parathyroid hormone (16). Similar to the finding in the present study, few of these hormones are found in the urine compared with their overall clearance by the kidney (16). It is of interest to note that men had greater renal clearance of than women. Because renal fractional extraction of was not significantly different, this appears to be explicable on the basis of greater renal plasma flow in men ( vs ml/min, P 0.031). From our data suggesting an important role of the human kidney in metabolism, one would expect that plasma levels should be markedly increased in people with end-stage renal disease. The fact that Merabet et al. (13) found only a twofold elevation of plasma in such patients suggests that in endstage renal disease, either other tissues become more important for removal from plasma or there may be reduced release from adipose tissue. Altered body composition with a reduction of adipose tissue and/or reduced food intake, as is commonly observed in people with end-stage renal disease (4, 9, 17), might also affect plasma concentrations. In conclusion, the results of the present study indicate that, in postabsorptive normal volunteers, the kidneys account for a substantial proportion of the overall systemic removal from the circulation. Renal removal from plasma is due to renal tissue uptake and degradation rather than glomerular filtration and urinary excretion and is subject to a saturable process following Michaelis-Menten kinetics. The present work was supported in part by Grants DK and 5MOI-RR from the National Institutes of Health. Address for reprint requests: J. E. Gerich, Univ. of Rochester School of Medicine, 601 Elmwood Ave., Box MED/CRC, Rochester, NY Received 21 April 1997; accepted in final form 23 July REFERENCES 1. Brooks, D. C., P. R. Black, M. A. Arcangeli, T. T. Aoki, and D. W. Wilmore. The heated dorsal hand vein: an alternative arterial sampling site. J. Parenter. Enteral Nutr. 13: , Brun, C. A rapid method for the determination of paraaminohippuric acid in kidney function tests. J. Lab. Clin. Med. 37: , Campfield, L. A., F. J. Smith, Y. Guisez, R. Devos, and P. Burn. Recombinant mouse OB protein: evidence for a peripheral signal linking adiposity and central neural networks. Science 269: , Coles, G. A. Body composition in chronic renal failure. Q. J. Med. 41: 25 47, Cumin, F., H.-P. Baum, and N. Levens. Leptin is cleared from the circulation primarily by the kidney. Int. J. Obes. 20: , Earle, J., and R. W. Berliner. A simplified clinical procedure for measurement of glomerular filtration rate and renal plasma flow. Proc. Soc. Exp. 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5 RENAL LEPTIN METABOLISM E Ostlund, R. E., J. W. Yang, S. Klein, and R. Gingerich. Relation between plasma concentration and body fat, gender, diet, age, and metabolic covariates. J. Clin. Endocrinol. Metab. 81: , Pelleymounter, M. A., M. J. Cullen, M. B. Baker, R. Hecht, D. Winters, T. Boone, and F. Collins. Effects of the obese gene product on body weight regulation in ob/ob mice. Science 269: , Rabkin, R., and J. Kitaji. Renal metabolism of peptide hormones. Miner. Electrolyte Metab. 9: , Schoenfeld, P. Y., R. R. Henry, N. M. Laird, and D. M. Roxe. Assessment of nutritional status of the national cooperative dialysis study population. Kidney Int. 23, Suppl. 13: S80 S88, Stephens, T. W., M. Basinski, P. K. Bristow, J. M. Bue- Valleskey, S. G. Burgett, L. Craft, J. Hale, J. Hoffmann, H. M. Hsiung, A. Kriauciunas, W. McKellar, P. R. Rosteck, B. Schoner, D. Smith, F. C. Tinsley, X.-Y. Zhang, and M. Heiman. The role of neuropeptide Y in the antiobesity action of the obese gene product. Nature 377: , Tartaglia, L. A., M. Dembski, X. Weng, N. Deng, J. Culpepper, R. Devos, G. J. Richards, A. Campfield, F. T. Clark, J. Deeds, C. Muir, S. Sanker, A. Moriarty, K. J. Moore, J. S. Smutko, G. G. Mays, E. A. Woolf, C. A. Monroe, and R. I. Tepper. Identification and expression cloning of a receptor, OB-R. Cell 83: , World Health Organization Expert Committee. Second Report on Diabetes Mellitus. Geneva, Switzerland: WHO, (Tech. Rep. Ser ) 21. Zhang, Y., R. Proenca, M. Maffei, M. Barone, L. Leopold, and J. M. Friedman. Positional cloning of the mouse obese gene and its human homologue. Nature 372: , 1994.

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