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First published online July 26, 2004
Journal of Experimental Biology 207, 3109-3121 (2004)
Published by The Company of Biologists 2004
doi: 10.1242/jeb.01154
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How the house sparrow Passer domesticus absorbs glucose

Min-Hwang Chang1 and William H. Karasov2,*

1 Department of Zoology, University of Wisconsin-Madison, USA
2 Department of Wildlife Ecology, 221 Russell Labs, 1630 Linden Drive, University of Wisconsin-Madison, Madison, WI 53706, USA



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  		Fig. 1. The time course for absorption of radiolabeled 3OMD-glucose and L-glucose differs according to whether most glucose absorption is mediated by the Na+-glucose cotransporter or is passive. The predicted patterns shown were generated using a chemical reactor model of intestinal absorption of radiolabeled probes, with a starting substrate concentration of 100 mmol l-1 (see Discussion). (A,B) Mediated uptake is assumed to dominate and so the maximal rate of 3OMD-glucose transport (Vmax) was taken to be 5x that which was measured in house sparrow small intestine in vitro (2.083 nmol min-1 µl-1; Caviedes-Vidal and Karasov, 1996Go) whereas the passive permeability coefficient (Ka) was taken to be the measured value (0.05 nmol µl-1). In this situation, percent cumulative absorption of the 3OMD-glucose (A), whose uptake is both mediated and passive (broken line), increases faster and is overall greater than the percent cumulative absorption of L-glucose, whose uptake is only passive (solid line). The apparent absorption rate (i.e. instantaneous slope; B) of 3OMD-glucose exceeds that of L-glucose. (C,D) Passive uptake is assumed to dominate and so the Vmax was taken to be the measured value and Ka was taken to be 5x the measured value. In this situation, the percent cumulative absorption of the 3OMD-glucose is only marginally faster and higher than L-glucose (C), and the apparent absorption rate of the 3OMD-glucose is only marginally higher than that of L-glucose (D). The Michaelis constant for mediated uptake (apparent Km) was fixed at 16.5 mmol l-1, 3x the measured value. These figures are shown because these types of data can be empirically generated using the pharmacokinetic methods described in Materials and methods and Results.

 


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  		Fig. 2. Plots of plasma [3H]3OMD-glucose and [14C]L-glucose concentration (mean ± S.E.M.) as a function of time since feeding the probes (gavage). The units for concentration are proportion per gram plasma, because values of d.p.m. g-1 plasma were normalized to d.p.m. dose for each individual. (A) Measurements made under relatively nonsaturating conditions (200 mmol l-1 mannitol in the gavage solution, N=7 birds); (B) measurements made under more saturating conditions (i.e. 200 mmol l-1 3OMD-glucose replaced mannitol in the gavage solution, N=6). Filled symbols and solid lines, [14C]L-glucose; unfilled symbols and broken lines, [3H]3OMD-glucose.

 


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  		Fig. 3. Plots, and semi-log inset plots, of plasma [3H]3OMD-glucose and [14C]L-glucose concentration as a function of time since injecting the probes. The units for concentration are proportion per gram plasma, because values of d.p.m. g-1 plasma were normalized to d.p.m. dose for each individual. (A) Measurements made under relatively nonsaturating conditions (200 mmol l-1 mannitol in the gavage solution, N=6 birds); (B) measurements made under more saturating conditions (i.e. 200 mmol l-1 3OMD-glucose replaced mannitol in the gavage solution, N=4). Filled symbols and solid lines, [14C]L-glucose; unfilled symbols and broken lines, [3H]3OMD-glucose.

 


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  		Fig. 4. The cumulative absorption (inset plots) and apparent rates of absorption of [3H]3OMD-glucose and [14C]L-glucose as a function of time since gavage of the probes to house sparrows. (A) Measurements made under relatively nonsaturating conditions (200 mmol l-1 mannitol in the gavage solution, N=7 birds); (B) measurements made under more saturating conditions (i.e. 200 mmol l-1 3OMD-glucose replaced mannitol in the gavage solution, N=6). Filled symbols and solid lines, [14C]L-glucose; unfilled symbols and dashed lines, [3H]3OMD-glucose. The absorption of 3OMD-glucose was slightly but significantly higher than that of L-glucose. The asterisk in A designates the significantly higher apparent absorption rate of [3H]3OMD-glucose (P=0.015) than of [14C]L-glucose at the 15 min sampling point.

 


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  		Fig. 5. The majority of 3OMD-glucose absorption is passive, as indicated by the high ratio of apparent absorption rates for L-glucose and 3OMD-glucose. Assuming that absorption of L-glucose is passive whereas the absorption of 3OMD-glucose represents the sum of passive + mediated absorption, the ratio of the apparent absorption rates (L/D) indicates the proportion of 3OMD-glucose absorption that occurs via the passive pathway. The ratios were calculated from the apparent rates shown in Fig. 4, for measurements made under relatively nonsaturating conditions (filled squares, solid line), and for measurements made under relatively more saturating conditions (unfilled circles, broken line).

 


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  		Fig. 6. The simulated pattern of D- and L-glucose radiolabeled probe absorption at the apical membrane in the presence of an initial low substrate concentration (CC0=1 mmol l-1) varies according to whether absorption is primarily mediated or primarily passive. The initial probe concentration used in the modeling was 0.001 nmol µl-1 (i.e. tracer level). (A) Cumulative absorption (%); (B) probe absorption rate. Four different situations are shown. (Ai,Bi) Absorption described by kinetic values (Vmax, Km and Ka) that have been measured in vitro using isolated sparrow intestine (Caviedes-Vidal and Karasov, 1996Go). We used the Vmax measured in that study because in vitro rates of uptake of 3OMD-glucose and D-glucose under saturating conditions were comparable (Chang et al., 2004Go). (Aii,Bii) Analogous to Ai,Bi but for the D-glucose analogue 3-O-methyl-D-glucose, which has lower affinity (approximately 3x higher Km, determined in rats, rabbits, guinea pigs and hamsters; Jorgensen et al., 1961Go; Syme and Levin, 1980Go; Thomson et al., 1982Go). (Aiii,Biii) Absorption based on the assumption that the Vmax was underestimated in vitro due to handling effects on tissue viability (Starck et al., 2000Go), uses a 5x higher Vmax, and thus represents absorption dominated by the mediated pathway. (Aiv,Biv) Absorption based on the assumption that the Ka was underestimated in vitro due to absence of solvent drag (Pappenheimer, 1993Go), uses a 5x higher Ka, and thus represents absorption dominated by the passive pathway. Notice that when passive absorption dominates (Aiv,Biv) the predicted cumulative absorption of D- and L-glucose probes as a function of time (Aiv) are much more similar than when mediated absorption dominates (Aiii). Analogously, when passive absorption dominates, the predicted absorption rates of D- and L-glucose probes as a function of time (Biv) are much closer to each other than when mediated absorption dominates (Biii).

 


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  		Fig. 7. The simulated pattern of D- and L-glucose radiolabeled probe absorption at the apical membrane in the presence of an initial high substrate concentration (100 mmol l-1) varies according to whether absorption is primarily mediated or primarily passive. The same four different situations as shown in Fig. 6 are modeled, but the starting concentration of unlabeled D-glucose is 100 times higher. Notice that when passive absorption dominates (Aiv,Biv), the predicted cumulative absorption of D- and L-glucose probes as a function of time (Aiv) are much more similar than when mediated absorption dominates (Aiii). Analogously, when passive absorption dominates, the predicted absorption rates of D- and L-glucose probes as a function of time (Biv) are much closer than when mediated absorption dominates (Biii).

 

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© The Company of Biologists Ltd 2004