Summary
In vivo pulse-chase labeling of rabbit jejunum loops was used in conjunction with subcellular fractionation and quantitative immunoprecipitation to determine whether or not the newly synthesized aminopeptidase N transits through the basolateral membrane before it reaches the apical brush border, its final localization. The kinetics of the arrival of the newly synthesized enzyme in the Golgi complex, basolateral and brush border membrane fractions strongly suggest that on leaving the Golgi aminopeptidase N is transiently integrated into the basolateral domain before reaching the brush border.
Similar content being viewed by others
References
Ahnen, D.J., Mirchaff, A.K., Santiago, N.A., Yoshioka, C., Gray, G.H. 1983. Intestinal surface aminooligopeptidase: Distinct molecular forms during assembly on intracellular membranes “in vivo.”J. Biol. Chem. 258:5960–5966
Bernadac, A., Gorvel, J.P., Feracci, H., Maroux, S. 1984. Human blood group A-like determinents as marker of the intracellular pools of glycoproteins on secretory and absorbing of A+ rabbit jejunum.Biol. Cell 50:31–36
Colas, B., Maroux, S. 1980. Simultaneous isolation of brush border and basolateral membrane from rabbit enterocytes: Presence of brush border hydrolases in the basolateral membrane of rabbit enterocytes,Biochim. Biophys. Acta 600:406–420
Coudrier, E., Reggio, H., Louvard, D. 1983. Characterization of an integral membrane glycoprotein associated with the microfilaments of pig intestinal microvilli.EMBO J. 2:469–475
Feracci, H., Bernadac, A., Gorvel, J.P., Maroux, S. 1982. Localization by immunofluorescence and histochemical labeling of aminopeptidase N in relation to its biosynthesis in rabbit and pig enterocytes.Gastroenterology 82:317–324
Feracci, H., Maroux, S. 1980. Rabbit intestinal aminopeptidase N: Purification and molecular properties.Biochim. Biophys. Acta 684:133–136
Feracci, H., Rigal, A., Maroux, S. 1985. Biosynthesis and intracellular pool of aminopeptidase N in rabbit enterocytes.J. Membrane Biol. 83:139–146
Fransen, J., Ginsel, L., Hauri, H.P., Sterchi, E., Block, J. 1985. Immuno-electron microscopical localization of a microvillus membrane disaccharidase in the human small intestinal epithelium with monoclonal antibodies.Eur. J. Cell. Biol. 38:6–15
Fujita, M., Ohta, H., Kawaï, K., Matsui, H., Nakac, M. 1972. Differential isolation of microvillous and basolateral plasma membrane from intestinal mucosa: Mutually exclusive distribution of digestive enzymes and ouabian-sensitive ATPase.Biochim. Biophys. Acta 274:336–347
Gorvel J.P., Liabeuf, A., Massey, D., Liot, D., Goridis, C., Maroux, S., 1983. Recognition of sodium and potassium-dependent adenosine triphosphatase on organs of the mouse by means of a monoclonal antibody,Cell Tissue Res. 234:619–632
Gorvel, J.P., Massey, D., Rigal, A., Maroux, S. 1986. Evidence for selective transport of two brush border glycoproteins from endoplasmic reticulum to Golgi complex in rabbit enterocytes.Biol. Cell 56:251–254
Gorvel, J.P., Sarles, J., Maroux, S., Olive, D., Mawas, C. 1984. Cellular localization of class I (HLA-A,B,C) and class II (HLA-DR and DQ) MHC antigens on the epithelial cells of normal human jejunum.Biol. Cell 52:249–252
Griffiths, G., Pfeiffer, S., Simons, K., Matlin, K. 1985. Exit of a newly synthesized membrane protein from theTrans cisterna of the Golgi complex to the plasma membrane.J. Cell Biol. 101:949–964.
Hauri, H., Quaroni, A., Isselbacher, K. 1979. Biosynthesis of intestinal plasma membrane: Post-translational route and cleavage of sucrase-isomaltase.Proc. Natl. Acad. Sci. USA 76:5183–5186
Hauri, H., Sterchi, E.E., Bienz, D., Fransen, J.A., Marxer, A.. 1985. Expression and intracellular transport of microvillus membrane hydrolases in human intestinal epithelial cells.J. Cell Biol. 101:838–851
Jamieson, J.D., Palade, G. 1971. Synthesis, intracellular transport, and discharge of secretory protein in stimulated pancreatic exocrine cells.J. Cell Biol. 50:135–138
Kenny, J.A., Maroux, S. 1982. Topology of microvillar membrane hydrolases of kidney and intestine.Physiol. Rev. 62:91–128
Kirby, N.N., Parr, E.L. 1979. The occurrence and distribution of H-2 antigens on mouse intestinal epithelial cells.J. Histochem. Cytochem. 27:746–750
Massey, D., Maroux, S. 1985. The carbohydrate moiety of aminopeptidase N of rabbit intestinal brush border membrane.FEBS Lett. 181:207–210
Matlin, K., Bainton, D.F., Personen, M., Louvard, D., Genty, N., Simons, K. 1983. Transepithelial transport of a viral membrane glycoprotein implanted into the apical plasma membrane of Madin-Darby Canine kidney cells: I. Morphological evidence.J. Cell Biol. 97:627–637
Matlin, K., Simons, K. 1984. Sorting of an apical plasma membrane glycoprotein occurs before it reaches the cell surface in cultured epithelial cells.J. Cell Biol. 99:2131–2139
Misek, D.E., Bard, E., Rodriguez-Boulan E. 1984. biogenesis of epithelial cell polarity: Intracellular sorting and vectorial excytosis of an apical plasma membrane glycoprotein.Cell 39:537–546
Moktari, S., Feracci, H., Gorvel, J.-P., Mishal, Z., Rigal, A., Maroux, S. 1986. Subcellular fractionation and subcellular localization of aminopeptidase N in rabbit enterocytes.J. Membrane Biol. 89:53–63
Mouttet, C., Fouchier, F., Nari, J., Ricard, J. 1974. Subunit interactions in enzyme catalysis. Effect of interactions on transient kinetics.Eur. J. Biochem. 49:11–20
Pesonen, M., Ansorge, W., Simons, K. 1984. Transcytosis of the G protein of vesicular stomatitis virus after implantation into the apical membrane of Madin-Darby Canine kidney cells: I. Involvement of endosomes and lysosomes.J. Cell Biol. 99:796–802
Quaroni, A., Kirsch, K., Weiser, M. M. 1979a. Synthesis of membrane glycoprotein in rat small intestinal villus cells: Redistribution ofl-(1,5,6-3H) fucose labelled membrane glycoproteins among Golgi, lateralbasal and microvillus membranes in vivo.Biochem. J. 182:203–212
Quaroni, A., Kirsch, K., Weiser, M.M. 1979b. Synthesis of membrane glycoprotein in rat small intestinal villus cells: Effect of colchicine on the redistribution ofl-(1,5,6-3H) fucose labelled membrane glycoprotein among Golgi, lateralbasal and microvillus membrane in vivo.Biochem. J. 182:213–221
Rindler, M.J., Ivanov, I.E., Plesken H., Sabatini, D.D. 1985. Polarized delivery of viral glycoproteins to the apical and basolateral plasma membrane of Madin-Darby canine kidney cells injected with temperature-sensitive viruses.J. Cell Biol. 100:136–151
Saraste, J., Kuismanen, E. 1984. Pre and post-Golgi vacuoles operate in the transport of Semliki Forest Virus membrane glycoproteins to the cell surface.Cell 38:535–549
Schmitz, J., Preiser, H., Maestracci, D., Ghosh, B.K., Cerda, J.J., Crane, R.K. 1973. Purification of the human intestinal brush border membrane.Biochim. Biophys. Acta 323:98–112
Soulié, J.M., Buc, J., Rivière, M., Ricard, J. 1985. Equilibrium binding of thiorodoxinf B to chloroplastic fructose biphosphatase: Evidence of a thioredoxin site distinct from the active site.Eur. J. Biochem. 152:565–568
Ternynck, T., Avrameas, S. 1972. Polyacrylamide-Protein immunoabsorbents prepared with glutaraldehyde.FEBS Lett. 23:24–28
Author information
Authors and Affiliations
Rights and permissions
About this article
Cite this article
Massey, D., Feracci, H., Gorvel, JP. et al. Evidence for the transit of aminopeptidase N through the basolateral membrane before it reaches the brush border of enterocytes. J. Membrain Biol. 96, 19–25 (1987). https://doi.org/10.1007/BF01869331
Received:
Revised:
Issue Date:
DOI: https://doi.org/10.1007/BF01869331