Gut sensing of dietary K⁺ intake increases renal K⁺excretion

Abstract

Dietary K(+) intake may increase renal K(+) excretion via increasing plasma [K(+)] and/or activating a mechanism independent of plasma [K(+)]. We evaluated these mechanisms during normal dietary K(+) intake. After an overnight fast, [K(+)] and renal K(+) excretion were measured in rats fed either 0% K(+) or the normal 1% K(+) diet. In a third group, rats were fed with the 0% K(+) diet, and KCl was infused to match plasma [K(+)] profile to that of the 1% K(+) diet group. The 1% K(+) feeding significantly increased renal K(+) excretion, associated with slight increases in plasma [K(+)], whereas the 0% K(+) diet decreased K(+) excretion, associated with decreases in plasma [K(+)]. In the KCl-infused 0% K(+) diet group, renal K(+) excretion was significantly less than that of the 1% K(+) group, despite matched plasma [K(+)] profiles. We also examined whether dietary K(+) alters plasma profiles of gut peptides, such as guanylin, uroguanylin, glucagon-like peptide 1, and glucose-dependent insulinotropic polypeptide, pituitary peptides, such as AVP, α-MSH, and γ-MSH, or aldosterone. Our data do not support a role for these hormones in the stimulation of renal K(+) excretion during normal K(+) intake. In conclusion, postprandial increases in renal K(+) excretion cannot be fully accounted for by changes in plasma [K(+)] and that gut sensing of dietary K(+) is an important component of the regulation of renal K(+) excretion. Our studies on gut and pituitary peptide hormones suggest that there may be previously unknown humoral factors that stimulate renal K(+) excretion during dietary K(+) intake.

Fig. 1.

Plasma glucose (A), Na⁺ (B), and K⁺ (C) concentrations and renal K⁺ excretion (D) profiles during the 2-h basal (−120 to 0 min) and 5-h postprandial (0 to 300 min) periods in overnight-fasted rats given the 0% (○) or 1% (●) K⁺ diet. Data are expressed as means ± SE for 7 or 8 experiments. *P < 0.05 vs. 0% K⁺ diet.

Fig. 2.

A: plasma [K⁺] profiles with the 1% (●) or 0% K⁺ diet with (□), or without (○) K⁺ infusion (KINF) to match plasma [K⁺] profile to that of the 1% K⁺ group. B: K⁺ infusion profile used. C: renal K⁺ excretion profiles in the three groups. D: increases in renal K⁺ excretion above basal rates. Data are expressed as means ± SE for 7 or 8 experiments. *P < 0.05 vs. zero (i.e., no increase); #P < 0.05 vs. the other groups.

Fig. 3.

A: renal Na⁺ excretion profiles with the 1% (●) or 0% K⁺ diet with (□) or without (○) K⁺ infusion (KINF). B: increases in renal Na⁺ excretion above basal rates. C: urine flow in the three groups. D: increases in urine flow above basal rates. Data are expressed as means ± SE for 7 or 8 experiments. *P < 0.05 vs. zero (i.e., no increase).

Fig. 4.

A: linear relationship between KINF and renal K⁺ excretion (measured after 1 h) rates in rats fed the 0% K⁺ diet (data from Fig. 2, B and C). B: KINF profile (dashed line) predicted to produce renal K⁺ excretion rates matching those with the 1% K⁺ diet (Fig. 2C), compared with the profile used in the earlier experiment. C and D: renal K⁺ excretion and plasma [K⁺] profiles, respectively, in rats fed the 0% K⁺ diet and infused with K⁺, according to the new KINF profile (□), compared with the data with the 1% K⁺ diet (●; from Fig. 2, A and C). Data are expressed as means ± SE for 6–8 experiments.

Fig. 5.

Plasma K⁺ concentrations (A) and renal K⁺ excretion rates (B) after the 1% K⁺ diet with (■) or without (●) amiloride (AR) infusion (2 nmol/min, intravenous) started at the beginning of the feeding (t=0). Data are expressed as means ± SE for 4 experiments. *P < 0.05 between the groups.

Fig. 6.

Plasma glucose-dependent insulinotropic polypeptide (GIP; A), glucagon-like peptide 1 (GLP-1; B), guanylin (C), and uroguanylin (D) profiles in overnight-fasted rats after the 0% (○) or 1% (●) K⁺ diet. A and B: data are expressed as means ± SE for 5 experiments for each group. *#Significant changes (P < 0.05) from basal (i.e., t=0) in the 0% and the 1% K⁺ diet group, respectively. C and D: data from individual rats are shown with open symbols representing the 0% K⁺ diet group, and solid symbols the 1% K⁺ diet group (n=2 and 3, respectively).

Fig. 7.

Plasma [K⁺] (A) and renal K⁺ excretion (B) profiles in overnight-fasted rats before and after an 1-min infusion of pituitary extracts from overnight-fasted rats (○) or overnight-fasted rats refed for 2 h with normal 1% K⁺ diet (●). C: average K⁺ excretion rates before and after the infusion of pituitary extracts. Data are expressed as means ± SE for 5 experiments. B: *#Significant changes (P < 0.05, one-tail t-test) from average K⁺ excretion before the infusion in the fed and the fasted group, respectively. C: *P < 0.05 vs. before.

Fig. 8.

Plasma AVP (A), α-MSH (B), γ-MSH (C), and aldosterone (D) profiles in overnight-fasted rats after the 0% (○) or 1% (●) K⁺ diet. Data are expressed as means ± SE for 4 or 5 experiments for each group.