Abstract
L-Glutamine, a major energy substrate for intestinal epithelial cells, can be extracted from intraluminal contents across the brush-border membrane and from arterial blood via the basolateral membrane. The purpose of the present study was to characterize glutamine transport by the basolateral membrane of rabbit epithelial cells. Transport of glutamine by isolated basolateral-membrane vesicles was mediated by both Na(+)-dependent and Na(+)-independent carriers. Tests were performed to distinguish glutamine uptake by likely transport agencies, including Systems A, ASC, N, IMINO, NBB, L and asc. The Na(+)-dependent glutamine uptake was strongly inhibited by an excess of 2-(methylamino)isobutyric acid (MeAIB), and glutamine was equally effective in inhibiting MeAIB transport. The reciprocal inhibition analysis, as well as a sensitivity to increased H+ concentration, indicates that Na(+)-dependent glutamine transport across the basolateral membrane is mediated by System A. The saturable Na(+)-independent glutamine transport was markedly inhibited by 2-aminobicyclo-[2,2,1]-heptane-2-carboxylic acid ('BCH') and insensitive to changes in assay pH, suggesting uptake via System L rather than System asc. The presence of a Na(+)-dependent carrier to mediate active transport of glutamine across the basolateral membrane is probably essential to ensure a continuous supply of this vital substrate to the enterocyte in the post-absorptive state.
Full text
PDFSelected References
These references are in PubMed. This may not be the complete list of references from this article.
- Ardawi M. S., Newsholme E. A. The transport of glutamine into rat mesenteric lymphocytes. Biochim Biophys Acta. 1986 Apr 25;856(3):413–420. doi: 10.1016/0005-2736(86)90131-8. [DOI] [PubMed] [Google Scholar]
- Ardawi M. S. The transport of glutamine and alanine into rat colonocytes. Biochem J. 1986 Aug 15;238(1):131–135. doi: 10.1042/bj2380131. [DOI] [PMC free article] [PubMed] [Google Scholar]
- Bannai S., Christensen H. N., Vadgama J. V., Ellory J. C., Englesberg E., Guidotti G. G., Gazzola G. C., Kilberg M. S., Lajtha A., Sacktor B. Amino acid transport systems. 1984 Sep 27-Oct 3Nature. 311(5984):308–308. doi: 10.1038/311308b0. [DOI] [PubMed] [Google Scholar]
- Bradford N. M., McGivan J. D. The transport of alanine and glutamine into isolated rat intestinal epithelial cells. Biochim Biophys Acta. 1982 Jul 14;689(1):55–62. doi: 10.1016/0005-2736(82)90188-2. [DOI] [PubMed] [Google Scholar]
- Christensen H. N., Handlogten M. E. Role of system Gly in glycine transport in monolayer cultures of liver cells. Biochem Biophys Res Commun. 1981 Jan 15;98(1):102–107. doi: 10.1016/0006-291x(81)91875-1. [DOI] [PubMed] [Google Scholar]
- Christensen H. N., Liang M., Archer E. G. A distinct Na+-requiring transport system for alanine, serine, cysteine, and similar amino acids. J Biol Chem. 1967 Nov 25;242(22):5237–5246. [PubMed] [Google Scholar]
- Christensen H. N. Organic ion transport during seven decades. The amino acids. Biochim Biophys Acta. 1984 Sep 3;779(3):255–269. doi: 10.1016/0304-4157(84)90012-1. [DOI] [PubMed] [Google Scholar]
- Ghishan F. K., Arab N., Bulus N., Said H., Pietsch J., Abumrad N. Glutamine transport by human intestinal basolateral membrane vesicle. Am J Clin Nutr. 1990 Apr;51(4):612–616. doi: 10.1093/ajcn/51.4.612. [DOI] [PubMed] [Google Scholar]
- Ghishan F. K., Sutter W., Said H., Leonard D., Pietsch J., Abumrad N. Glutamine transport by rat basolateral membrane vesicles. Biochim Biophys Acta. 1989 Feb 13;979(1):77–81. doi: 10.1016/0005-2736(89)90525-7. [DOI] [PubMed] [Google Scholar]
- Hopfer U., Sigrist-Nelson K., Ammann E., Murer H. Differences in neutral amino acid and glucose transport between brush border and basolateral plasma membrane of intestinal epithelial cells. J Cell Physiol. 1976 Dec;89(4):805–810. doi: 10.1002/jcp.1040890447. [DOI] [PubMed] [Google Scholar]
- Hundal H. S., Rennie M. J., Watt P. W. Characteristics of L-glutamine transport in perfused rat skeletal muscle. J Physiol. 1987 Dec;393:283–305. doi: 10.1113/jphysiol.1987.sp016824. [DOI] [PMC free article] [PubMed] [Google Scholar]
- Joseph S. K., Bradford N. M., McGivan J. D. Characteristics of the transport of alanine, serine and glutamine across the plasma membrane of isolated rat liver cells. Biochem J. 1978 Dec 15;176(3):827–836. doi: 10.1042/bj1760827. [DOI] [PMC free article] [PubMed] [Google Scholar]
- Kilberg M. S., Christensen H. N. Electron-transferring enzymes in the plasma membrane of the Ehrlich ascites tumor cell. Biochemistry. 1979 Apr 17;18(8):1525–1530. doi: 10.1021/bi00575a021. [DOI] [PubMed] [Google Scholar]
- Kilberg M. S., Christensen H. N., Handlogten M. E. Cysteine as a system-specific substrate for transport system ASC in rat hepatocytes. Biochem Biophys Res Commun. 1979 May 28;88(2):744–751. doi: 10.1016/0006-291x(79)92110-7. [DOI] [PubMed] [Google Scholar]
- Kilberg M. S., Handlogten M. E., Christensen H. N. Characteristics of an amino acid transport system in rat liver for glutamine, asparagine, histidine, and closely related analogs. J Biol Chem. 1980 May 10;255(9):4011–4019. [PubMed] [Google Scholar]
- Lazarus P., Panasci L. C. Characterization of L-threonine and L-glutamine transport in murine P388 leukemia cells in vitro. Presence of an N-like amino acid transport system. Biochim Biophys Acta. 1986 Apr 25;856(3):488–495. doi: 10.1016/0005-2736(86)90140-9. [DOI] [PubMed] [Google Scholar]
- Meister A., Tate S. S., Griffith O. W. Gamma-glutamyl transpeptidase. Methods Enzymol. 1981;77:237–253. doi: 10.1016/s0076-6879(81)77032-0. [DOI] [PubMed] [Google Scholar]
- Mircheff A. K., van Os C. H., Wright E. M. Pathways for alanine transport in intestinal basal lateral membrane vesicles. J Membr Biol. 1980 Jan 31;52(1):83–92. doi: 10.1007/BF01869009. [DOI] [PubMed] [Google Scholar]
- OXENDER D. L., CHRISTENSEN H. N. DISTINCT MEDIATING SYSTEMS FOR THE TRANSPORT OF NEUTRAL AMINO ACIDS BY THE EHRLICH CELL. J Biol Chem. 1963 Nov;238:3686–3699. [PubMed] [Google Scholar]
- Orsenigo M. N., Tosco M., Esposito G., Faelli A. The basolateral membrane of rat enterocyte: its purification from brush border contamination. Anal Biochem. 1985 Feb 1;144(2):577–583. doi: 10.1016/0003-2697(85)90156-3. [DOI] [PubMed] [Google Scholar]
- Said H. M., Van Voorhis K., Ghishan F. K., Abumurad N., Nylander W., Redha R. Transport characteristics of glutamine in human intestinal brush-border membrane vesicles. Am J Physiol. 1989 Jan;256(1 Pt 1):G240–G245. doi: 10.1152/ajpgi.1989.256.1.G240. [DOI] [PubMed] [Google Scholar]
- Shotwell M. A., Kilberg M. S., Oxender D. L. The regulation of neutral amino acid transport in mammalian cells. Biochim Biophys Acta. 1983 May 24;737(2):267–284. doi: 10.1016/0304-4157(83)90003-5. [DOI] [PubMed] [Google Scholar]
- Stevens B. R., Kaunitz J. D., Wright E. M. Intestinal transport of amino acids and sugars: advances using membrane vesicles. Annu Rev Physiol. 1984;46:417–433. doi: 10.1146/annurev.ph.46.030184.002221. [DOI] [PubMed] [Google Scholar]
- Stevens B. R., Ross H. J., Wright E. M. Multiple transport pathways for neutral amino acids in rabbit jejunal brush border vesicles. J Membr Biol. 1982;66(3):213–225. doi: 10.1007/BF01868496. [DOI] [PubMed] [Google Scholar]
- Stevens B. R., Wright E. M. Substrate specificity of the intestinal brush-border proline/sodium (IMINO) transporter. J Membr Biol. 1985;87(1):27–34. doi: 10.1007/BF01870696. [DOI] [PubMed] [Google Scholar]
- Taylor P. M., Egan C. J., Rennie M. J. Transport of glutamine across blood-facing membranes of perfused rat jejunum. Am J Physiol. 1989 Apr;256(4 Pt 1):E550–E558. doi: 10.1152/ajpendo.1989.256.4.E550. [DOI] [PubMed] [Google Scholar]
- Vadgama J. V., Christensen H. N. Discrimination of Na+-independent transport systems L, T, and asc in erythrocytes. Na+ independence of the latter a consequence of cell maturation? J Biol Chem. 1985 Mar 10;260(5):2912–2921. [PubMed] [Google Scholar]
- Van Voorhis K., Said H. M., Ghishan F. K., Abumrad N. N. Transport of glutamine in rat intestinal brush-border membrane vesicles. Biochim Biophys Acta. 1989 Jan 16;978(1):51–55. doi: 10.1016/0005-2736(89)90497-5. [DOI] [PubMed] [Google Scholar]
- Windmueller H. G. Glutamine utilization by the small intestine. Adv Enzymol Relat Areas Mol Biol. 1982;53:201–237. doi: 10.1002/9780470122983.ch6. [DOI] [PubMed] [Google Scholar]
- Windmueller H. G., Spaeth A. E. Uptake and metabolism of plasma glutamine by the small intestine. J Biol Chem. 1974 Aug 25;249(16):5070–5079. [PubMed] [Google Scholar]
- ZAK B., COHEN J. Automatic analysis of tissue culture proteins with stable Folin reagents. Clin Chim Acta. 1961 Sep;6:665–670. doi: 10.1016/0009-8981(61)90112-7. [DOI] [PubMed] [Google Scholar]