The capacity for paracellular absorption in the insectivorous bat Tadarida brasiliensis

Springer Science and Business Media LLC - Tập 183 - Trang 289-296 - 2012
Verónica Fasulo1,2, ZhiQiang Zhang1,3,4, Juan G. Chediack1,5,3, Fabricio D. Cid1,5,3, William H. Karasov6, Enrique Caviedes-Vidal1,5,3
1Laboratorio de Biología “Professor E. Caviedes Codelia”, Facultad de Ciencias Humanas, Universidad Nacional de San Luis, San Luis, Argentina
2Departamento de Psicobiología, Facultad de Ciencias Humanas, Universidad Nacional de San Luis, San Luis, Argentina
3Laboratorio de Biología Integrativa, Instituto Multidisciplinario de Investigaciones Biológicas de San Luis, Consejo Nacional de Investigaciones Científicas y Técnicas, San Luis, Argentina
4College of Animal Science and Technology, Anhui Agricultural University, Hefei, People’s Republic of China
5Departamento de Bioquímica y Ciencias Biológicas, Universidad Nacional de San Luis, San Luis, Argentina
6Department of Forestry and Wildlife Ecology, University of Wisconsin, Madison, Madison, USA

Tóm tắt

Water-soluble nutrients are absorbed by the small intestine via transcellular and paracellular processes. The capacity for paracellular absorption seems greater in fliers than in nonfliers, although that conclusion rests mainly on a comparison of flying birds and nonflying mammals because only two frugivorous bat species have been studied. Furthermore, the bats studied so far were relatively large (>85 g, compared with most bat species which are <20 g) and were not insectivores (like about 70 % of bat species). We studied the small (11 g) insectivorous bat Tadarida brasiliensis and tested the prediction that the capacity for paracellular absorption would be as high as in the other bat and avian species studied so far, well above that in terrestrial, nonflying mammals. Using standard pharmacokinetic technique, we measured the extent of absorption (fractional absorption = f) of inert carbohydrate probes: L-arabinose (MM = 150.13) absorbed exclusively by paracellular route and 3OMD-glucose (MM = 194) absorbed both paracellularly and transcellularly. As predicted, the capacity of paracellular absorption in this insectivorous bat was high (L-arabinose f = 1.03 ± 0.14) as in other frugivorous bats and small birds. Absorption of 3OMD-glucose was also complete (f = 1.09 ± 0.17), but >80 % was accounted for by paracellular absorption. We conclude that passive paracellular absorption of molecules of the size of amino acids and glucose is extensive in this bat and, generally in bats, significantly higher than that in nonflying mammals, although the exact extent can be somewhat lower or higher depending on molecule size, polarity and charge.

Tài liệu tham khảo

Anumula KR (1994) Quantitative determination of monosaccharides in glycoproteins by high-performance liquid chromatography with highly sensitive fluorescence detection. Anal Biochem 220:275–283 Barry RE (1976) Mucosal surface areas and villous morphology of the small intestine of small mammals: functional interpretations. J Mammal 57:273–290 Bijlsma PB, Peeters RA, Groot JA, Dekker PR, Taminiau JAJM, Van Der Meer R (1995) Differential in vivo and in vitro intestinal permeability to lactulose and mannitol in animals and humans: a hypothesis. Gastroenterology 108:687–696 Caviedes-Vidal E, McWhorter TJ, Lavin SR, Chediack JG, Tracy CR, Karasov WH (2007) The digestive adaptation of flying vertebrates: high intestinal paracellular absorption compensates for smaller guts. Proc Natl Acad Sci USA 104:19132–19137 Caviedes-Vidal E, Karasov WH, Chediack JG, Fasulo V, Cruz-Neto AP, Otani L (2008) Paracellular absorption: a bat breaks the mammal paradigm. PLoS One 3:e1425 Chang MH, Karasov WH (2004) How the house sparrow Passer domesticus absorbs glucose. J Exp Biol 207:3109–3121 Chediack JG, Caviedes-Vidal E, Fasulo V, Yamin LJ, Karasov WH (2003) Intestinal passive absorption of water-soluble compounds by sparrows: effect of molecular size and luminal nutrients. J Comp Physiol [B] 173:187–197 Chediack JG, Caviedes-Vidal E, Karasov WH (2006) Electroaffinity in paracellular absorption of hydrophilic D-dipeptides by sparrow intestine. J Comp Physiol [B] 176:303–309 Colegio OR, Van Itallie CM, McCrea HJ, Rahner C, Anderson JM (2002) Claudins create charge-selective channels in the paracellular pathway between epithelial cells. Am J Physiol Cell Physiol 283:C142–C147 Fanning AS, Mitic LL, Anderson JM (1999) Transmembrane proteins in the tight junction barrier. J Am Soc Nephrol 10:1337–1345 Ferraris RP (1994) Regulation of intestinal nutrient transport Chapter 54. In: Johnson LR (ed) Physiology of the gastrointestinal tract. Raven Press, New York, pp 1821–1844 Fine KD, Santa Ana CA, Porter JL, Fordtran JS (1993) Effect of D-glucose on intestinal permeability and its passive absorption in human small intestine in vivo. Gastroenterology 105:1117–1125 Hamilton I, Rothwell J, Archer D, Axon TR (1987) Permeability of the rat small intestine to carbohydrate probe molecules. Clin Sci 73:189–196 He YL, Murby S, Gifford L, Collett A, Warhurst G, Douglas KT, Rowland M, Ayrton J (1996) Oral absorption of D-oligopeptides in rats via the paracellular route. Pharm Res 13:1673–1678 Hopfer U (1987) Membrane transport mechanisms for hexoses and aminoacids in the small intestine. In: Johnson LR (ed) Physiology of the gastrointestinal tract. Raven Press, New York, pp 1499–1526 Jones G, Rydell J (2003) Attack and defense: Interactions between echolocation bats and their insect prey. In: Kunz TH, Fenton MB (eds) Bat ecology. The University of Chicago Press, Chicago, pp 301–345 Karasov WH, Caviedes-Vidal E, Bakken BH, Izhaki I, Samuni-Blank M, Arad Z (2012) Capacity for absorption of water-soluble secondary metabolites greater in birds than in rodents. PLoS One 7:e32417 Lane JS, Whang EE, Rigberg DA, Hines OJ, Kwan D, Zinner MJ, McFadden DW, Diamond J, Ashley SW (1999) Paracellular glucose transport plays a minor role in the unanesthetized dog. Am J Physiol Gastrointest Liver Physiol 276:G789–G794 Lavin SR (2007) Small intestine morphometrics and paracellular absorption in birds and mammals. PhD Dissertation. Department of Wildlife Ecology. University of Wisconsin, Madison Lavin SR, Karasov WH (2008) Allometry of paracellular absorption in birds. Physiol Biochem Zool 81:551–560 Lavin SR, McWhorter TJ, Karasov WH (2007) Mechanistic bases for differences in passive absorption. J Exp Biol 210:2754–2764 Maina JN (2000) What it takes to fly: the structural and functional respiratory refinements in birds and bats. J Exp Biol 203:3045–3064 Makanya AN (1997) The morphology of the intestine of the entomophagous longfingered bat, Miniopterus inflatus : mucosal topography and possible landmarks. Acta Biol Hung 48:15–27 Mayhew TM, Middleton C (1985) Crypts, villi and microvilli in the small intestine of the rat. A stereological study of their variability within and between animals. J Anat 141:1–17 McWhorter TJ, Karasov WH (2007) Paracellular nutrient absorption in a gum-feeding new world primate, the common marmoset Callithrix jacchus. Am J Primatol 69:1399–1411 McWhorter TJ, Green AK, Karasov WH (2010) Assessment of radiolabeled D-glucose and the nonmetabolizable analog 3-O-methyl-D-glucose as tools for in vivo absorption studies. Physiol Biochem Zool 83:376–384 Pappenheimer JR (1990) Paracellular intestinal absorption of glucose, creatinine, and mannitol in normal animals: relation to body size. Am J Physiol 259:G290–G299 Pappenheimer JR, Reiss KZ (1987) Contribution of solvent drag through intercellular junctions to absorption of nutrients by the small intestine of the rat. J Membr Biol 100:123–136 Pencek RR, Koyama Y, Lacy DB, James FD, Fueger PT, Jabbour K, Williams PE, Wasserman DH (2002) Transporter-mediated absorption is the primary route of entry and is required for passive absorption of intestinal glucose into the blood of conscious dogs. J Nutr 132:1929–1934 Schondube JE, Herrera LG, Martínez del Rio C (2001) Diet and the evolution of digestion and the renal function in phyllostomid bats. Zoology 104:59–73 Simmons NB, Conway TM (2003) Evolution of ecological diversity in bats. In: Kunz TH, Fenton MB (eds) Bat ecology. The University of Chicago Press, Chicago, pp 493–535 Smulders AP, Wright EM (1971) The magnitude of nonelectrolyte selectivity in the gallbladder epithelium. J Membr Biol 5:297–318 Snipes RL, Chivers DJ, Langer P (1994) Morphometric methods for determining surface enlargement at the microscopic level in the large intestine and their application. In: Anonymous (ed) The digestive system in mammals: food, form, and function. Cambridge University Press, pp 234–263 Stuart A, Ord K (1994) Kendall’s advanced theory of statistics. Distribution Theory. Arnold, London Tracy CR, McWhorter TJ, Korine C, Wojciechowski MS, Pinshow B, Karasov WH (2007) Absorption of sugars in the Egyptian fruit bat (Rousettus aegyptiacus): a paradox explained. J Exp Biol 210:1726–1734 Uhing MR, Kimura RE (1995) Active transport of 3-O-methyl-glucose by the small intestine in chronically catheterized rats. J Clin Invest 95:2799–2805