Construction and characterization of secreted and chimeric transmembrane forms of Drosophila acetylcholinesterase: A large truncation of the C-terminal signal peptide does not eliminate glycoinositol phospholipid anchoring

Molecular Biology of the Cell

Volumn 7, Issue 4, 1996, Pages 595-611

  Incardona, John P ^a   Rosenberry, Terrone L ^a  

^a CASE WESTERN RESERVE UNIVERSITY SCHOOL OF MEDICINE   (United States)

Author keywords

[No Author keywords available]

Indexed keywords

ACETYLCHOLINESTERASE; GLYCOSYLPHOSPHATIDYLINOSITOL; ISOENZYME; SIGNAL PEPTIDE;

ANIMAL CELL; ARTICLE; DROSOPHILA; ENZYME ACTIVITY; ENZYME ANALYSIS; ENZYME STRUCTURE; ENZYME SYNTHESIS; IMMUNOCYTOCHEMISTRY; MEMBRANE BINDING; NONHUMAN; PRIORITY JOURNAL; PROTEIN EXPRESSION; PROTEIN QUATERNARY STRUCTURE;

ACETYLCHOLINESTERASE; AMINO ACID SEQUENCE; ANIMALS; ANIMALS, GENETICALLY MODIFIED; BASE SEQUENCE; CELL LINE; CENTRIFUGATION, DENSITY GRADIENT; DNA, COMPLEMENTARY; DROSOPHILA; ECHOTHIOPHATE IODIDE; ELECTROPHORESIS, POLYACRYLAMIDE GEL; GLYCOSYLPHOSPHATIDYLINOSITOLS; MOLECULAR SEQUENCE DATA; PHOSPHATIDYLINOSITOL DIACYLGLYCEROL-LYASE; PHOSPHORIC DIESTER HYDROLASES; PROTEIN PROCESSING, POST-TRANSLATIONAL; RECOMBINANT FUSION PROTEINS; RESTRICTION MAPPING; SIGNAL TRANSDUCTION; SIMPLEXVIRUS; VIRAL ENVELOPE PROTEINS;

ANIMALIA; HERPES; HUMAN HERPESVIRUS 1;

EID: 0029930873     PISSN: 10591524     EISSN: None     Source Type: Journal    
DOI: 10.1091/mbc.7.4.595     Document Type: Article

References (63)

1. Abrams, J.M., Lux, A., Steller, H., and Krieger, M. (1992). Macrophages in Drosophila and L2 cells exhibit scavenger receptor-mediated endocytosis. Proc. Natl. Acad. Sci. USA 89, 10375-10379.
2. Anderson, R.G.W. (1993). Plasmalemmal caveolae and GPI-anchored membrane proteins. Curr. Opin. Cell Biol. 5, 647-652.
3. Ashburner, M. (1989). Drosophila: A Laboratory Manual, Cold Spring Harbor, NY: Cold Spring Harbor Laboratory Press, 143-145.
4. Berger, J., Howar, A.D., Brink, L., Gerber, L., Hauber, J., Cullen, B.R., and Udenfriend, S. (1988). COOH-terminal requirements for the correct processing of a phosphatidylinositol-glycan-anchored membrane protein. J. Biol. Chem. 263, 10016-10021.
5. Berger, J., Micanovic, R., Greenspan, R.J., and Udenfriend, S. (1989). Conversion of placental alkaline phosphatase from a phosphatidylinositol-glycan-anchored protein to an integral transmembrane protein. Proc. Natl. Acad. Sci. USA 86, 1457-1460.
6. Bordier, C. (1988). Analytical and preparative phase separation of glycolipid-anchored membrane proteins in Triton X-114 solution. In: Post-translational Modification of Proteins by Lipids, ed. U. Brodbeck and C. Bordier, Berlin, Germany: Springer-Verlag.
7. Brockman, S.K., Przybylski, R.J., and Younkin, S.G. (1982). Cellular localization of the molecular forms of acetylcholinesterase in cultured embryonic rat myotubes. J. Neurosci. 2, 1775-1785.
8. Brown, D.A., Crise, B., and Rose, J.K. (1989). Mechanism of membrane anchoring affects polarized expression of two proteins in MLXK cells. Science 245, 1499-1501.
9. Brown, D.A., and Rose, J.K. (1992). Sorting of GPI-anchored proteins to glycolipid-enriched membrane subdomains during transport to the apical cell surface. Cell 68, 533-544.
10. Butters, T.D., Hughes, R.C., and Vischer, P. (1981). Steps in the biosynthesis of mosquito cell membrane glycoproteins and the effects of tunicamycin. Biochim. Biophys. Acta 640, 672-686.
11. Caras, I.W., Weddell, G.N., and Williams, S.R. (1989). Analysis of the signal for attachment of a glycophospholipid membrane anchor. J. Cell Biol. 108, 1387-1396.
12. Cinek, T., and Hořejší, V. (1992). The nature of large noncovalent complexes containing glycosyl-phosphatidylinositol-anchored membrane glycoproteins and protein tyrosine kinases. J. Immunol. 149, 2262-2270.
13. Crise, B., Ruusala, A., Zagouras, P., Shaw, A., and Rose, J.K. (1989). Oligomerization of glycolipid-anchored and soluble forms of the vesicular stomatitis virus glycoprotein. J. Virol. 63, 5328-5333.
14. Davitz, M.A., Horn, J., and Schenkman, S. (1989). Purification of a glycosyl-phosphatidylinositol-specific phospholipase D from human plasma. J. Biol. Chem. 264, 13760-13764.
15. Deeg, M.A., Humphrey, D.R., Yang, S.H., Ferguson, T.R., Reinhold, V.N., and Rosenberry, T.L. (1992). Glycan components in the glycoinositol phospholipid anchor of human erythrocyte acetylcholinesterase. J. Biol. Chem. 267, 18573-18580.
16. Dotti, C.G., Parton, R.G., and Simons, K. (1991). Polarized sorting of glypiated proteins in hippocampal neurons. Nature 349, 158-161.
17. Dupree, P., Parton, R.G., Raposo, G., Kurzchalia, T.V., and Simons, K. (1993). Caveolae and sorting in the trans-Golgi network of epithelial cells. EMBO J. 12, 1597-1605.
18. Ellman, G.L., Courtney, K.D., Andress, V., and Featherstone, R.H. (1961). A new and rapid colorimetric determination of acetylcholinesterase activity. Biochem. Pharmacol. 7, 88-95.
19. Englund, P.T. (1993). The structure and biosynthesis of glycosyl phophatidylinositol protein anchors. Annu. Rev. Biochem. 62, 121-138.
20. Fox, J.A., Soliz, N.M., and Saltiel, A.R. (1987). Purification of a phosphatidylinositol-glycan-specific phospholipase C from liver plasma membranes: a possible target of insulin action. Proc. Natl. Acad. Sci. USA 84, 2663-2667.
21. Frink, R.J., Eisenberg, R., Cohen, G., and Wagner, E.K. (1983). Detailed analysis of the portion of the herpes simplex virus type 1 genome encoding glycoprotein C. J. Virol. 45, 634-647.
22. Gnagey, A.L., Forte, M., and Rosenberry, T.L. (1987). Isolation and characterization of acetylcholinesterase from Drosophila. J. Biol. Chem. 262, 13290-13298.
23. Gritz, L., and Davies, J. (1983). Plasmid-encoded hygromycin B resistance: the sequence of hygromycin B phosphotransferase gene and its expression in Escherichia coli and Saccharomyces cerevisiae. Gene 25, 179-188.
24. Guan, J.-L., Machamer, C.E., and Rose, J.K. (1985). Glycosylation allows cell-surface transport of an anchored secretory protein. Cell 42, 489-496.
25. Hall, L.M.C., and Spierer, P. (1986). The Ace locus of Drosophila melanogaster: structural gene for acetylcholinesterase with an unusually long 5′ leader. EMBO J. 5, 2949-2954.
26. Herald, D., Krakow, J.L., Bangs, J.D., Hart, G.W., and Englund, P.T. (1986). A phospholipase C from Trypanosoma brucei which selectively cleaves the glycolipid on the variant surface glycoprotein. J. Biol. Chem. 261, 13813-13819.
27. Hoener, M.C., Stieger, S., and Brodbeck, U. (1990). Isolation and characterisation of a phosphatidylinositol-glycan-anchor-specific phopholipase D from bovine brain. Eur. J. Biochem. 190, 593-601.
28. Holland, T.C., Lerch, R.J., and Earhart, K. (1988). The cytoplasmic domain of herpes simplex virus type 1 glycoprotein C is required for membrane anchoring. J. Virol. 62, 1753-1761.
29. Homa, F.L., Purifoy, D.J.M., Glorioso, J.C., and Levine, M. (1986). Molecular basis of the glycoprotein C-negative phenotypes of herpes simplex virus type 1 mutants selected with a virus-neutralizing monoclonal antibody. J. Virol. 58, 281-289.
30. Hsieh, P., and Robbins, P.W. (1984). Regulation of asparagine-linked oligosaccharide processing. J. Biol. Chem. 259, 2375-2382.
31. Incardona, J.P., and Rosenberry, T.L. (1996). Replacement of the glycoinositol phospholipid anchor of Drosophila acetylcholinesterase with a transmembrane domain does not alter sorting in neurons and epithelia but results in behavioral defects. Mol. Biol. Cell. 7, 613-630.
32. Jaeger, J.A., Turner, D.H., and Zuker, M. (1989). Improved predictions of secondary structures for RNA. Proc. Natl. Acad. Sci. USA 86, 7706-7710.
33. Karnovsky, M.J., and Roots, L. (1964). A "direct-coloring" thiocholine method for cholinesterases. J. Histochem. Cytochem. 12, 219-222.
34. Kemble, G.W., Henis, Y.I., and White, J.M. (1993). GPI- and transmembrane-anchored influenza hemagglutinin differ in structure and receptor binding activity. J. Cell Biol. 122, 1253-1265.
35. Kikuchi, G.E., Glorioso, J.C., and Nairn, R. (1990). Cross-linking studies show that herpes simplex virus type I glycoprotein C molecules are clustered in the membrane of infected cells. J. Gen. Virol. 71, 455-458.
36. Krasnow, M.A., Saffman, E.E., Korenfeld, K., and Hogness, D.S. (1989). Transcriptional activation and repression by Ultrabithorax proteins in cultured Drosophila cells. Cell 57, 1031-1043.
37. Kuroda, K., Geyer, H., Geyer, R., Doerfler, W., and Klenk, H.-D. (1990). The oligosaccharides of influenza virus hemagglutinin expressed in insect cells by a baculovirus vector. Virology 174, 418-429.
38. Laemmli, U.K. (1970). Cleavage of structural proteins during the assembly of the head of bacteriophage T4. Nature 227, 680-685.
39. Lisanti, M.P., Caras, I.W., Davitz, M.A., and Rodriguez-Boulan, E. (1989). A glycophospholipid membrane anchor acts as an apical targeting signal in polarized epithelial cells. J. Cell. Biol. 109, 2145-2156.
40. Low, M.G., and Prasad, A.R.S. (1988). A phospholipase D specific for the phosphatidylinositol anchor of cell-surface proteins is abundant in plasma. Proc. Natl. Acad. Sci. USA 85, 980-984.
41. Morgan, C., Holden, M., and Jones, E.P. (1959). Electron microscopic observations on the development of herpes simplex virus. J. Exp. Med. 110, 643-656.
42. Mutero, A., and Fournier, D. (1992). Post-translational modifications of Drosophila acetylcholinesterase. J. Biol. Chem. 267, 1695-1700.
43. Peltola, M., Chiatayat, D., Peltonen, L., and Jalanko, A. (1994). Characterization of a point mutation in aspartylglucosaminidase gene: evidence for a read through of a translational stop codon. Hum. Mol. Genet. 3, 2237-2242.
44. Restifo, L.L., and White, K. (1990). Molecular and genetic approaches to neurotransmitter and neuromodulator systems in Drosophila. Adv. Insect Physiol. 22, 115-219.
45. Robinson, P.J. (1991). Phosphatidylinositol membrane anchors and T-cell activation. Immunol. Today 12, 35-41.
46. Robinson, P.J., Millrain, M., Antoniou, J., Simpson, E., and Mellor, A.L. (1989). A glycophospholipid anchor is required for Qa-2-mediated T cell activation. Nature 342, 85-87.
47. Rosenberry, T.L., and Scoggin, D.M. (1984). Structure of human erythrocyte acetylcholinesterase. J. Biol. Chem. 259, 5643-5652.
48. Rotundo, R.L. (1988). Biogenesis of acetylcholinesterase molecular forms in muscle. J. Biol. Chem. 263, 19398-19406.
49. Sargiacomo, M., Sudol, M., Tang, Z.L., and Lisanti, M.P. (1993). Signal transducing molecules and glycosyl-phosphatidylinositol-linked proteins form a caveolin-rich insoluble complex in MDCK cells. J. Cell Biol. 122, 789-807.
50. Shields, D., and Sang, J.H. (1977). Improved medium for culture of Drosophila embryonic cells. Drosophila Inf. Service 52, 161.
51. Srivinas, R.V., Balachandran, N., Alonso-Caplen, F.V., and Cornpans, R.W. (1986). Expression of herpes simplex virus glycoproteins in polarized epithelial cells. J. Virol. 58, 689-693.
52. Štefanová, I., Hořejší, V., Ansotegui, I.J., Knapp, W., and Stockinger, H. (1991). GPI-anchored cell-surface molecules complexed to protein tyrosine kinases. Science 254, 1016-1019.
53. Su, B., and Bothwell, A.L.M. (1989). Biosynthesis of a phosphatidylinositol-glycan-linked membrane protein: signals for posttranslational processing of the Ly-6E antigen. Mol. Cell. Biol. 9, 3369-3376.
54. Tago, H., Kimura, H., and Maeda, T. (1986). Visualization of detailed acetylcholinesterase fiber and neuron staining in rat brain by a sensitive histochemical procedure. J. Histochem. Cytochem. 34, 1431-1438.
55. Thomas, D.C., Brewer, C.B., and Roth, M.G. (1993). Vesicular stomatitis virus glycoprotein contains a dominant cytoplasmic basolateral sorting signal critically dependent on a tyrosine. J. Biol. Chem. 268, 3313-3320.
56. fyn protein tyrosine kinase in T cells. J. Biol. Chem. 267, 12317-12322.
57. Toutant, J.-P., Richards, M.K., Krall, J.A., and Rosenberry, T.L. (1990). Molecular forms of acetylcholinesterase in two sublines of human erythroleukemia K562 cells. Eur. J. Biochem. 187, 31-38.
58. Vigny, M., Bon, S., Massoulie, J., and Gisiger, V. (1979). The subunit structure of mammalian acetylcholinesterase: catalytic subunits, dissociating effects of proteolysis and disulfide reduction of the polymeric forms. J. Neurochem. 33, 559-565.
59. Vigny, M., Bon, S., Massoulie, J., and Leterrier, F. (1978). Active-site catalytic efficiency of acetylcholinesterase molecular forms in Electrophorus, Torpedo, rat and chicken. Eur. J. Biochem. 85, 317-323.
60. Weiss, R.B. (1991). Ribosomal frameshifting, jumping and readthrough. Curr. Opin. Cell Biol. 3, 1051-1055.
61. Whitt, M.A., Chong, L., and Rose, J.K. (1989). Glycoprotein cytoplasmic domain sequences required for rescue of vesicular stomatitis virus glycoprotein mutant. J. Virol. 63, 3569-3578.
62. Yang, M., Allen, H., and DiCoccio, R.A. (1992). A mutation generating a stop codon in the α-L-fucosidase gene of a fucosidosis patient. Biochem. Biophys. Res. Commun. 189, 1063-1068.
63. Younkin, S.G., Rosenstein, C., Collins, P.L., and Rosenberry, T.L. (1982). Cellular localization of the molecular forms of acetylcholinesterase in rat diaphragm. J. Biol. Chem. 257, 13630-13637.