The apical sorting of lactase-phlorizin hydrolase implicates sorting sequences found in the mature domain

European Journal of Cell Biology

Volumn 72, Issue 1, 1997, Pages 54-60

  Jacob, Ralf ^a   Zimmer, Klaus Peter ^b   Naim, Hussein ^c   Naim, Hassan Y ^a  

^a HEINRICH HEINE UNIVERSITY   (Germany)

^b UNIVERSITY OF MÜNSTER   (Germany)

^c UNIVERSITY OF TEXAS AT DALLAS   (United States)

Author keywords

Apical sorting; Lactase phlorizin hydrolase; Mature enzyme

Indexed keywords

CELL SURFACE PROTEIN; COMPLEMENTARY DNA; GLYCOSYLCERAMIDASE; LACTASE; MEMBRANE PROTEIN; PROTEIN PRECURSOR;

ANIMAL CELL; APICAL MEMBRANE; ARTICLE; BRUSH BORDER; CONTROLLED STUDY; ENZYME LOCALIZATION; ENZYME SYNTHESIS; EPITHELIUM CELL; GENE EXPRESSION; NONHUMAN; PRIORITY JOURNAL; PROTEIN FOLDING; PROTEIN GLYCOSYLATION; PROTEIN STRUCTURE; PROTEIN TRANSPORT; SMALL INTESTINE MUCOSA;

ANIMALIA;

EID: 0031017823     PISSN: 01719335     EISSN: None     Source Type: Journal    
DOI: None     Document Type: Article

References (39)

1. Brewer, C., D. Thomas, M. A. Roth: A single amino acid change in the cytoplasmic domain alters the polarized delivery of influenza virus hemagglutinin. J. Cell Biol. 114, 413-421 (1991).
2. Büller, H. A., R. K. Montgomery, W. V. Sasak, R. J. Grand: Biosynthesis, glycosylation, and intracellular transport of intestinal lactase-phlorizin hydrolase in rat. J. Biol. Chem. 262, 17206-17211 (1987).
3. [2a] Caplan M., K. S. Matlin: Functional Epithelial Cells in Culture. pp. 71-127. Liss. New York 1989.
4. Casanova, J. E., G. Apodaca, K .E. Mostov: An autonomous signal for basolateral sorting in the cytoplasmic domain of the polymeric immunoglobulin receptor. Cell 66, 65-75 (1991).
5. Cool, D. R., Y. P. Loh: Identification of a sorting signal for the regulated secretory pathway at the N-terminus of proopiomelanocortin. Biochimie 76, 265-270 (1994).
6. Dahlqvist, A.: Assay of intestinal disaccharidases. Anal. Biochem. 22, 99-107 (1968).
7. Danielsen, E. M., H. Skovbjerg, O. Norén, H. Sjöström: Biosynthesis of intest inal microvillar proteins. Intracellular processing of lactase-phlorizin hydrolase. Biochem. Biophys. Res. Commun. 122, 82-90 (1984).
8. Fransen, J. A. M., H. P. Hauri, L. A. Ginsel, H. Y. Naim: Naturally occurring mutations in intestinal sucrase-isomaltase provide evidence for the existence of an intracellular sorting signal in the isomaltase sub-unit. J. Cell Biol. 115, 45-57 (1991).
9. Grünberg, J., U. Luginbühl, E. Sterchi: Proteolytic processing of human intestinal lactase-phlorizin hydrolase precursor is not a prerequisite for correct sorting in Madin Darby canine kidney (MDCK) cells. FEBS Lett. 314, 224-228 (1992).
10. Hauri, H. P., E. E. Sterchi, D. Bienz, J. A. M. Fransen, A. Marxer: Expression and intracellular transport of microvillus membrane hydrolases in human intestinal epithelial cells. J. Cell Biol. 101, 838-851 (1985).
11. Hunziker, W., C. Harter, K. Matter, I. Mellman: Basolateral sort-ing in MDCK cells requires a distinct cytoplasmic domain determinant. Cell 66, 907-920 (1991).
12. Jacob, R., C. Brewer, J. A. M. Fransen, H. Y. Naim: Transport, function and sorting of lactase phlorizin-hydrolase in Madin-Darby canine kidney (MDCK) cells. J. Biol. Chem. 269, 2712-2721 (1994).
13. Jacob, R., N. J. Bulleid, H. Y. Naim: Folding of human intestinal lactase-phlorizin hydrolase. J. Biol. Chem. 270, 18678-18684 (1995).
14. Jacob, R., I. Radebach, M. Wüthrich, J. Grünberg, E. E. Sterchi, H. Y. Naim: Maturation of human intestinal lactase-phlorizin hydrolase. Generation of the brush border form of the enzyme involves at least two proteolytic cleavage steps. Eur. J. Biochem. 236, 789-795 (1996).
15. Kundu, A.,D. P. Nayak: Analysis of the signals for polarized transport of influenza virus (A/WSN/33) neuraminidase and human transferrin receptor, type II transmembrane proteins. J. Virol. 68, 1812-1818 (1994).
16. Le Bivic, A., Y. Sambuy, K. Mostov, E. Rodriguez-Boulan: Vectorial targeting of an endogenous apical membrane sialoglycoprotein und uvomorulin in MDCK cells. J. Cell Biol. 110, 1533-1539 (1990).
17. Lisanti, M. P., M. Sargiacomo, L. Graeve, A. Saltiel, E. Rodriguez-Boulan: Polarized epithelial distribution of glycosyl phosphatidylinositol anchored proteins in a renal epithelial line. Proc. Natl. Acad. Sci. USA 85, 9557-9561 (1988).
18. Lisanti, M. P., I. W. Caras, M. A. Davitz, E. Rodriguez-Boulan: A glycophospholipid membrane anchor acts as an apical targeting signal in polarized epithelial cells. J. Cell Biol. 109, 2145-2156 (1989).
19. Lottaz, D., T. Oberholzer, P. Bähler, G. Semenza, E. E. Sterchi: Maturation of human lactase-phlorizin hydrolase. FEBS Lett. 313, 270-276 (1992).
20. Low, S. H., S. H. Wong, B. L. Tang, V. N. Subramaniam, W. Hong: Apical cell surface expression of rat dipeitidyl peptidase IV in transfected Madin-Darby canine kidney cells. J. Biol. Chem. 266, 13391-13396 (1991).
21. Mantei, N., M. Villa, T. Enzler, H. Wacker, W. Bol, P. James W. Hunziker, G. Semenza: Complete primary structure of human and rabbit lactase-phlorizin hydrolase. Implications for biosynthesis, membrane anchoring and evolution of the enzyme. EMBO J. 7, 2705-2713 (1988).
22. Matlin, K. S., K. Simons: Sorting of an apical plasma membrane glycoprotein occurs before it reaches the cell surface in cultured epithelial cells. J. Cell Biol. 99, 2131-2139 (1984).
23. Matter, K., W. Hunziker, I. Mellman: Basolateral sorting of LDL-receptor in MDCK cells: The cytoplasmic domain contains two tyrosine-dependent targeting determinants. Cell 71, 741-753 (1992).
24. Mostov. K., G. Apodaca, B. Aroeti. C. Okamoto: Plasma membrane protein sorting in polarized epithelial cells. J. Cell Biol. 116, 577-583 (1992).
25. Naim, H. Y.. E. E. Sterchi, M. J. Lentze: Biosynthesis and maturation of lactase-phlorizin hydrolase in the human small intestinal epithelial cells. Biochem. J. 241, 427-434 (1987).
26. Naim, H. Y., S. Lacey, J. F. Sambrook, M. J. H. Gething: Expression of a full-length cDNA coding for human intestinal lactase-phlorizin hydrolase reveals an uncleaved, enzymatically active, and transport-competent protein. J. Biol. Chem. 266, 12313-12320 (1991).
27. Naim, H. Y.: Processing of human pro-lactase-phlorizin hydrolase at reduced temperatures: cleavage is preceded by complex glycosylation. Biochem. J. 285, 13-16 (1992).
28. Naim, H. Y., M. J. Lentze: Impact of O-glycosylation on the function of human intestinal lactase-phlorizin hydrolase. J. Biol. Chem. 267, 25494-25504 (1992).
29. Naim,. H. Y., R. Jacob, H. Naim, J. F. Sambrook, M. J. Gething: The proregion of human intestinal lactase-phlorizin hydrolase. J. Biol. Chem. 269, 26933-26943 (1994).
30. Oberholzer, T., N. Mantei, G. Semenza: The pro sequence of lactase-phlorizin hydrolase is required for the enzyme to reach the plasma membrane. FEBS Lett. 333, 127-131 (1993).
31. Richardson, J. C., V. Scalera, N. L. Simmons: Identification of two strains of MDCK cells which resemble separate nephron tubule segments. Biochim. Biophys. Acta 673, 26-36 (1981).
32. Soole, K. L., M. A. Jepson, G. P. Hazlewood, H. J. Gilbert, B. H. Hirst: Epithelial sorting of a phospatidylinositol-anchored bacterial protein expressed in polarized renal MDCK and intestinal Caco-2 cells. J. Cell Sci. 108, 369-377 (1995).
33. Sambrook, J., E. F. Fritsch, T. Maniatis: Molecular Cloning: A Laboratory Manual. 2nd ed. Cold Spring Harbor Laboratory Cold Spring Harbor, NY 1989.
34. Semenza, G.: Anchoring and biosynthesis of stalked brush border membrane protein glycosidases and peptidases of enterocytes and renal tubuli. Annu. Rev. Cell Biol. 2, 255-313 (1986).
35. Valls, L. A., J. R. Winter, T. H. Stevens: Yeast carboxypeptidase Y vacuolar targeting signal is defined by four propeptide amino acids. J. Cell Biol. 111, 361-368 (1990).
36. Vogel, L. K., M. Spiess, H. Sjöström, O. Norén: Evidence for an apical sorting signal on the ectodomain of human aminopeptidase N. J. Biol. Chem. 267, 2794-2797 (1992).
37. Weisz, O. A., C. E. Machamer, A. L. Hubbard: Rat liver dipeptidase IV contains competing apical and basolateral targeting information. J. Biol. Chem. 267, 22282-22288 (1992).
38. Wessels, H. P., G. H. Hansen, C. Fuhrer, A. T. Look, H. Sjöström, O. Norén. M. Spiess: Aminopeptidase N is directly sorted to the apical domain in MDCK cells. J. Cell Biol. 111, 2923-2930 (1990).
39. Zimmer, K.-P., I. Matsuda, T. Matsuura, M. Mori, J. P. Colombo, H. D. Fahimi, H.-G. Koch, K. Ullrich, E. Harms: Ultrastructural, immunocytochemical and stereological investigation of hepatocytes in a patient with the mutation of the ornithine transcarbamylase gene. Eur. J. Cell Biol. 67, 73-83 (1995).