Mechanistic bases for differences in passive absorption

Lavin, Shana R.; McWhorter, Todd J.; Karasov, William H.

doi:10.1242/jeb.006114

Cited by 38 publications

(60 citation statements)

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“…The decrease in absorption of paracellular probes with increasing probe size that we observed in rodents is consistent with a sizesieving effect of the tight junction channels, a phenomenon that has been documented in a variety of species (Delahunty and Hollander, 1987;Bijlsma et al, 1995;Chediack et al, 2003;Lavin et al, 2007;Anderson and Van Itallie, 2009;Fasulo et al, 2013a;Fasulo et al, 2013b;Price et al, 2013a). This size-sieving effect seems to diminish at smaller molecule sizes, such that absorption of arabinose and creatinine was similar in M. lucifugus.…”

Section: Whole Animal Paracellular Nutrient Absorptionsupporting

confidence: 89%

“…L-glucose or rhamnose) because of previous reports that they may have some affinity for the D-glucose transporter (Schwartz et al, 1995;Lavin et al, 2007), whereas arabinose does not (present study). The molecule size effect necessarily complicates interpretation of arabinose absorption as an indicator for paracellular glucose absorption; because arabinose is smaller than glucose (M r 150 versus 180), it probably overestimates paracellular glucose absorption.…”

Section: Whole Animal Paracellular Nutrient Absorptionmentioning

confidence: 58%

“…For example, differences in gastric evacuation rates, contact time on the epithelium, and the presence of sufficient dietary water can affect absorption rates of paracellular probes (Pappenheimer and Reiss, 1987;Lennernäs, 1995;Turner et al, 2000;Lavin et al, 2007). Our intestinal perfusions control for these potential differences, and thus serve to confirm that the patterns observed in intact animals are in fact driven by permeability characteristics of the intestine.…”

Section: Paracellular Nutrient Absorption In Isolated Intestinesmentioning

confidence: 75%

“…To verify that our L-arabinose and creatinine probes have no affinity for intestinal transporters, we used an everted sleeve technique to test for saturation kinetics (Karasov and Diamond, 1983;Lavin et al, 2007). Seven naïve M. lucifugus and P. leucopus were euthanized with CO 2 and the entire small intestine was immediately removed and perfused with ice cold Ringer solution (125 mmol l −1 NaCl, 4.7 mmol l −1 KCl, 2.5 mmol l −1 CaCl 2 , 1.2 mmol l −1 KH 2 PO 4 , 1.2 mmol l −1 MgSO 4 and 20 mmol l −1 NaHCO 3 , pH 7.3−7.4).…”

Section: Validation Of Paracellular Probesmentioning

confidence: 99%

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Paracellular nutrient absorption is higher in bats than rodents: integrating from intact animals to the molecular level

Price

Rott

Caviedes‐Vidal

et al. 2014

Journal of Experimental Biology

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Flying vertebrates have been hypothesized to rely heavily on paracellular absorption of nutrients to compensate for having smaller intestines than non-flyers. We tested this hypothesis in an insectivorous bat (Myotis lucifugus) and two insect-eating rodents (Onychomys leucogaster and Peromyscus leucopus). In intact animals, the fractional absorption of orally dosed L-arabinose (M r 150) was 82% in M. lucifugus, which was more than twice that of the rodents. Absorption of creatinine (M r 113) was greater than 50% for all species and did not differ between M. lucifugus and the rodents. We also conducted intestinal luminal perfusions on anesthetized animals. Absorption of L-arabinose per nominal surface area in M. lucifugus was nearly double that of the rodents, while absorption of creatinine was not different among species. Using an everted sleeve preparation, we demonstrated that high concentrations of L-arabinose and creatinine did not inhibit their own uptake, validating their use as passive, paracellular probes. Histological measurements indicated that M. lucifugus has more cells, and presumably more tight junctions, per nominal surface area than P. leucopus. This seems unlikely to explain entirely the higher absorption of L-arabinose in M. lucifugus during perfusions, because L-arabinose absorption normalized to the number of enterocytes was still double that of P. leucopus. As an alternative, we investigated tight junction gene expression. M. lucifugus had higher expression of claudin-1 and claudin-15, and lower expression of claudin-2 relative to P. leucopus. Expression of claudin-7 and occludin did not differ among species. Taken together, our results support the hypothesis that bats have evolved higher paracellular nutrient absorption than non-flying animals, and that this phenomenon might be driven by both histological characteristics and differences in tight junction gene expression.

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Section: Whole Animal Paracellular Nutrient Absorptionsupporting

confidence: 89%

Section: Whole Animal Paracellular Nutrient Absorptionmentioning

confidence: 58%

Section: Paracellular Nutrient Absorption In Isolated Intestinesmentioning

confidence: 75%

Section: Validation Of Paracellular Probesmentioning

confidence: 99%

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Paracellular nutrient absorption is higher in bats than rodents: integrating from intact animals to the molecular level

Price

Rott

Caviedes‐Vidal

et al. 2014

Journal of Experimental Biology

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“…Then, we took several blood samples to analyze the absorption profile (Figure 4). The absorption profile of l-rhamnose determined in this study was in agreement with the results previously reported by other authors in pigeons (Lavin et al, 2007). …”

Section: Application Of the Model In Absorption Experimentssupporting

confidence: 93%

Chronic cannulation in the small intestine of feral pigeons (Columba livia) to assess bioavailability

Chediack¹,

Cid²,

Fasulo³

et al. 2010

Vet. Med. - Czech

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ABSTRACT:We improved a method of chronic duodenal cannulation to study intestinal transport of solutes in an in vivo model (pigeon, Columba livia). A hypoallergenic cannula was inserted into the proximal part of the small intestine of pigeons and used for solution administration. Recovery from surgery was extremely rapid and animals started eating and drinking within a day. After surgery, the body mass of cannulated pigeons was stable, and no adverse effects in the weight could be detected. The method is simple, economical and useful to determine intestinal bioavailability of solutes, for nutritional and ecological studies, in intact animals without influence of anesthesia.

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Comparative Digestive Physiology

Karasov

Douglas

2013

Comprehensive Physiology

243

221

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In vertebrates and invertebrates, morphological and functional features of gastrointestinal (GI) tracts generally reflect food chemistry, such as content of carbohydrates, proteins, fats, and material(s) refractory to rapid digestion (e.g., cellulose). The expression of digestive enzymes and nutrient transporters approximately matches the dietary load of their respective substrates, with relatively modest excess capacity. Mechanisms explaining differences in hydrolase activity between populations and species include gene copy number variations and single-nucleotide polymorphisms. Transcriptional and posttranscriptional adjustments mediate phenotypic changes in the expression of hydrolases and transporters in response to dietary signals. Many species respond to higher food intake by flexibly increasing digestive compartment size. Fermentative processes by symbiotic microorganisms are important for cellulose degradation but are relatively slow, so animals that rely on those processes typically possess special enlarged compartment(s) to maintain a microbiota and other GI structures that slow digesta flow. The taxon richness of the gut microbiota, usually identified by 16S rRNA gene sequencing, is typically an order of magnitude greater in vertebrates than invertebrates, and the interspecific variation in microbial composition is strongly influenced by diet. Many of the nutrient transporters are orthologous across different animal phyla, though functional details may vary (e.g., glucose and amino acid transport with K+ rather than Na+ as a counter ion). Paracellular absorption is important in many birds. Natural toxins are ubiquitous in foods and may influence key features such as digesta transit, enzymatic breakdown, microbial fermentation, and absorption

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Mechanistic bases for differences in passive absorption

Abstract: Whatever the exact mechanism(s), the paracellular pathway of both species limits substantial (>5%) fractional absorption to molecules smaller than about 4.8·Å (M r ca. 350), and permeability to smaller molecules at the tissue level is higher in pigeons than in rats.

Cited by 38 publications

References 50 publications

Paracellular nutrient absorption is higher in bats than rodents: integrating from intact animals to the molecular level

Paracellular nutrient absorption is higher in bats than rodents: integrating from intact animals to the molecular level

Chronic cannulation in the small intestine of feral pigeons (Columba livia) to assess bioavailability

Comparative Digestive Physiology

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