Dissection of de novo membrane insertion activities of internal transmembrane segments of ATP-binding-cassette transporters: Toward understanding topological rules for membrane assembly of polytopic membrane proteins

Molecular Biology of the Cell

Volumn 9, Issue 4, 1998, Pages 853-863

  Zhang, Jian Ting ^a   Chen, Mingang ^a   Han, Ernest ^a   Wang, Changsen ^a  

^a UNIVERSITY OF TEXAS MEDICAL BRANCH   (United States)

Author keywords

[No Author keywords available]

Indexed keywords

ABC TRANSPORTER; GLYCOPROTEIN P; MEMBRANE PROTEIN; TRANSMEMBRANE CONDUCTANCE REGULATOR;

ARTICLE; CELL MEMBRANE; MEMBRANE BINDING; MEMBRANE STRUCTURE; MOLECULAR MODEL; NONHUMAN; PRIORITY JOURNAL; PROTEIN DOMAIN;

EID: 0031946150     PISSN: 10591524     EISSN: None     Source Type: Journal    
DOI: 10.1091/mbc.9.4.853     Document Type: Article

References (40)

1. Audigier, Y., Friedlander, M. and Blobel, G. (1987). Multiple topogenic sequences in bovine opsin. Proc. Natl. Acad. Sci. USA. 84, 5783-5787.
2. Bibi, E., and Béjà, O. (1994). Membrane topology of multidrug resistance protein expressed in Escherichia coli. J. Biol. Chem. 269, 19910-19915.
3. Blobel, G. (1980). Intracellular protein topogenesis. Proc. Natl. Acad. Sci. USA 77, 1496-1500.
4. Borel, A.C., and Simon. M. (1996a). Biogenesis of polytopic membrane proteins: membrane segments of P-glycoprotein sequentially translocate to span the ER membrane. Biochemistry 35, 10587-10594.
5. Borel, A.C., and Simon. M. (1996b). Biogenesis of polytopic membrane proteins: membrane segments assemble within translocation channels prior to membrane integration. Cell 85, 379-389.
6. Braell, W.A., and Lodish, H.F. (1982). The erythrocyte anion transport protein is cotranslationally inserted into microsomes. Cell 28, 23-31.
7. Brown, D., and Simoni, R. (1984). Biogenesis of 3-hydroxy-3-methyl-glutaryl coenzyme A reductase, an integral glycoprotein of the endoplasmic reticulum. Proc. Natl. Acad. Sci. USA 81, 1674-1678.
8. Chang X.-B., Hou, Y.-X., Jensen, T.J., and Riordan, J.R. (1994). Mapping of cystic fibrosis transmembrane conductance regulator membrane topology by glycosylation site insertion. J. Biol. Chem. 269, 18572-18575.
9. Chen, M.A., and Zhang, J.T. (1996). Membrane insertion, processing, and topology of cystic fibrosis transmembrane conductance regulator (CFTR) in microsomal membranes. Mol. Memb. Biol. 13, 33-40.
10. Childs, S., and Ling, V. (1994). The MDR superfamily of genes and its biological implications. In: Important Advances in Oncology, ed. V.T. DeVita, S. Hellman, and S.A. Rosenberg, Philadelphia: J.B. Lippincott Co.
11. Corsi, A.K., and Schekman, R. (1996). Mechanism of polypeptide translocation into the endoplasmic reticulum. J. Biol. Chem. 271, 30299-30302.
12. Doige, C.A., and Ames, G.F.-L. (1993). ATP-dependent transport systems in bacteria and humans: relevance to cystic fibrosis and multidrug resistance. Annu. Rev. Microbiol. 47, 291-319.
13. Friedlander, M., and Blobel, G. (1985). Bovine opsin has more than one signal sequence. Nature 318, 338-343.
14. Gafvelin, G., Sakaguchi, M., Andersson, H., and von Heijne, G. (1997). Topological rules for membrane assembly in eukaryotic cells. J. Biol. Chem. 272, 6119-6127.
15. Gafvelin, G., and von Heijne, G. (1994). Topological "frustration" in multispanning E. coli inner membrane proteins. Cell 77, 401-412.
16. Geller, D., Taglicht, D., Edgar, R., Tarn, A., Pines, O., Michaelis, S., and Bibi, E. (1996). Comparative topology studies in Saccharomyces cerevisiae and in Escherichia coli, the N-terminal half of the yeast ABC protein Ste6. J. Biol. Chem. 271, 13746-13753.
17. Goldman, G., and Blobel, G. (1981). In vitro biogenesis, core glycosylation and membrane integration of opsin. J. Cell Biol. 90, 236-242.
18. Hartmann, E., Rapoport, T.A., and Lodish, H.F. (1989). Predicting the orientation of eukaryotic membrane spanning proteins. Proc. Natl. Acad. Sci. USA 86, 5786-5790.
19. Higgins, C. (1992). ABC transporters: from microorganisms to man. Annu. Rev. Cell Biol. 8, 67-113.
20. Johnson, A.E. (1997). Protein translocation at the ER membrane: a complex process becomes more so. Trends Cell Biol. 7, 90-95.
21. Kast, C., Canfield, V., Levenson, R., and Gros, P. (1995). Membrane topology of P-glycoprotein as determined by epitope insertion: transmembrane organization of the N-terminal domain of mdr3. Biochemistry 34, 4402-4401.
22. Lipp, J., Flint, N., Haeuptle, M.-T., and Dobberstein, B. (1989). Structural requirements for membrane assembly of proteins spanning the membrane several times. J. Cell Biol. 109, 2013-2022.
23. Loo, T.W., and Clarke, D.M. (1995). Membrane topology of a cysteine-less mutant of human P-glycoprotein. J. Biol. Chem. 270, 843-848.
24. McGovern K., Ehrmann, M., and Beckwith, J. (1991). Decoding signals for membrane protein assembly using alkaline phosphatase fusions. EMBO J. 10, 2773-2782.
25. Rapoport, T.A., Jungnickel, B., and Kutay, U. (1996). Protein transport across the eukaryotic endoplasmic reticulum and bacterial inner membranes. Annu. Rev. Biochem. 65, 271-303.
26. Schatz, G., and Dobberstein, B. (1996). Common principles of protein translocation across membranes. Science 271, 1519-1526.
27. Seligman, L., and Manoil, C. (1994). An amphipathic sequence determinant of membrane protein topology. J. Biol. Chem. 269, 19888-19896.
28. Simon, S.M., and Blobel, G. (1991). A protein-conducting channel in the endoplasmic reticulum. Cell 65, 371-380.
29. Skach, W.R., Calayag, M.C., and Lingappa, V.R. (1993). Evidence for an alternate model of human P-glycoprotein structure and biogenesis. J. Biol. Chem. 268, 6903-6908.
30. Skach, W.R., and Lingappa, V.R. (1993). Intracellular trafficking of pre-(pro) proteins across RER membranes. In: Mechanisms of Intracellular Trafficking and Processing of Proproteins, ed. Y. Peng Loh, Boca Raton, FL: CRC Press Inc., 19-77
31. Skach, W.R., and Lingappa, V.R. (1994). Transmembrane orientation and topogenesis of the third and fourth membrane-spanning regions of human P-glycoprotein (MDR1). Cancer Res. 54, 3202-3209.
32. von Heijne, G. and Gavel, Y. (1988). Topogenic signals in integral membrane proteins. Eur. J. Biochem. 174, 671-678.
33. Wessels, H., and Spiess, M. (1988). Insertion of a multispanning membrane protein occurs sequentially and requires only one signal sequence. Cell 55, 61-70.
34. Walter, P., and Johnson, A.E. (1994). Signal sequence recognition and protein targeting to the endoplasmic reticulum membrane. Annu. Rev. Cell Biol. 10, 87-119.
35. Wang, G., Pincheira, R., Zhang, M., and Zhang, J.T. (1997). Conformational changes of P-glycoprotein by nucleotide binding. Biochem. J. 328, 897-904.
36. Zhang, J.T. (1996). Sequence requirements for membrane assembly of polytopic membrane proteins: molecular dissection of the membrane insertion process and topogenesis of the human MDR3 P-glycoprotein. Mol. Biol. Cell 7, 1709-1721.
37. Zhang, J.T., and Ling, V. (1991). Study of membrane orientation and glycosylated extracellular loops of mouse P-glycoprotein by in vitro translation. J. Biol. Chem. 266, 18224-18232.
38. Zhang, J.T., Duthie, M., and Ling, V. (1993). Membrane topology of the N-terminal half of the hamster P-glycoprotein molecule. J. Biol. Chem. 268, 15101-15110.
39. Zhang, J.T., Lee, C-H., Duthie, M., and Ling, V. (1995). Topological determinants of internal transmembrane segments in P-glycoprotein sequences. J. Biol. Chem. 270, 1742-1746.
40. Zhang, M., Wang, G.C., Shapiro, A., and Zhang, J.T. (1996). Topological folding and proteolysis profile of P-glycoprotein in membranes of multidrug-resistant cells: implications for the drug-transport mechanism. Biochemistry 35, 9728-9736.