Structural cues involved in endoplasmic reticulum degradation of G85E and G91R mutant cystic fibrosis transmembrane conductance regulator

Journal of Clinical Investigation

Volumn 100, Issue 5, 1997, Pages 1079-1088

  Xiong, Ximing ^a   Bragin, Alvina ^a   Widdicombe, Jonathan H ^b   Cohn, Jonathan ^c   Skach, William R ^a  

^a UNIVERSITY OF PENNSYLVANIA   (United States)

^b UNIVERSITY OF CALIFORNIA   (United States)

^c DUKE UNIVERSITY SCHOOL OF MEDICINE   (United States)

Author keywords

CFTR; Cystic fibrosis; ER degradation; Protein biogenesis; Protein folding

Indexed keywords

TRANSMEMBRANE CONDUCTANCE REGULATOR;

ANIMAL CELL; ARTICLE; CYSTIC FIBROSIS; ENDOPLASMIC RETICULUM; GENE MUTATION; NONHUMAN; PRIORITY JOURNAL; PROTEIN ASSEMBLY; PROTEIN FOLDING; PROTEIN STRUCTURE; STRUCTURE ANALYSIS;

EID: 0030931382     PISSN: 00219738     EISSN: None     Source Type: Journal    
DOI: 10.1172/JCI119618     Document Type: Article

References (53)

1. Riordan, J.R., J.M. Rommens, B.-S. Kerem, N. Alon, R. Rozmahel, Z. Grzelczak, J. Zielenski, S. Lok, F.S. Collins, and L.-C. Tsui. 1989. Identification of the cystic fibrosis gene: cloning and characterization of complementary DNA. Science (Wash. DC). 245:1066-1072.
2. Marino, C., L. Matovich, F. Goerlick, and J. Cohn. 1991. Localization of the cystic fibrosis transmembrane conuctance regulator in the pancreas. J. Clin. Invest. 88:712-716.
3. Denning, G., L. Ostedgaard, S. Cheng, A. Smith, and M. Welsh. 1992. Localization of cystic fibrosis transmembrane conductance regulator in chloride secretory epithelia. J. Clin. Invest. 89:339-349.
4. Higgins, C. 1992. ABC transporters: from microorganisms to man. Ann. Rev. Cell Biol. 8:67-113.
5. Hyde, S.C., P. Emsley, M.J. Hartshorn, M.M. Mimmack, U. Gileadi, S.R. Pearce, M.P. Gallagher, D.R. Gill, R.E. Hubbard, and C.F. Higgins. 1990. Structural model of ATP-binding proteins associated with cystic fibrosis, multidrug resistance and bacterial transport. Nature (Lond.). 346:362-365.
6. Anderson, M.P., R.J. Gregory, S. Thompson, D.W. Souza, S. Paul, R.C. Mulligan, A.E. Smith, and M.J. Welsh. 1991. Demonstration that CFTR is a chloride channel by alteration of its anion selectivity. Science (Wash. DC). 253: 202-204.
7. Hasegawa, H., W. Skach, O. Baker, M.C. Cayalag, V. Lingappa, and A. Verkman. 1992. A multifunctional aqueous channel formed by CFTR. Science (Wash. DC). 258:1477-1479.
8. Reisin, I., A. Prat, E. Abraham, J. Amara, R. Gregory, D. Ausiello, and H. Cantiello. 1994. The cystic fibrosis transmembrane conductance regulator is a dual ATP and chloride channel. J. Biol. Chem. 269:20584-20691.
9. Ohrui, T., W. Skach, M. Thompson, J. Matsumoto-Pon, M.C. Calayag, and J. Willicombe. 1994. Radiotracer studies of CFTR expressed in Xenopus oocytes. Am. J. Physiol. (Cell. Physiol.) C1586-C1593.
10. Cystic Fibrosis Genetic Analysis Consortium. 1997. Cystic fibrosis mutation data base. www.genet.sickkids.on.ca/cftr
11. Welsh, M., and A. Smith. 1993. Molecular mechanisn of CFTR chloride channel dysfunction in cystic fibrosis. Cell. 73:1251-1254.
12. Denning, G., M. Anderson, J. Amara, J. Marshall, A. Smith, and M. Welsh. 1992. Processing of mutant cytsic fibrosis transmembrane conductance regulator is temperature-sensitive. Nature (Lond.). 358:761-763.
13. Cheng, S.H., R.J. Gregory, J. Marshall, S. Paul, D.W. Souza, G.A. White, C.R. O'Riordan, and A.E. Smith. 1990. Defective intracellular transport and processing on CFTR is the molecular basis of most cystic fibrosis. Cell. 63: 827-834.
14. - channel is functional when retained in the endoplasmic reticulum of mammalian cells. J. Biol. Chem. 270:12347-12350.
15. Ward, C., and R. Kopito. 1994. Intracellular turnover of cystic fibrosis transmembrane conductance regulator. J. Biol. Chem. 269:25710-25718.
16. Ward, C., C. Omura, and R. Kopito. 1995. Degradation of CFTR by the ubiquitin-proteosome pathway. Cell. 83:121-128.
17. Jensen, T., M. Loo, S. Pind, D. Williams, A. Goldberg, and J. Riordan. 1995. Multiple proteolytic systems, including the proteosome, contribute to CFTR processing. Cell. 83:129-136.
18. Lukacs, G., A. Mohamed, N. Kartner, X. Chang, J. Riordan, and S. Grinstein. 1994. Conformational maturation of CFTR but not its mutant counterpart (delta F508) occurs in the endoplasmic reticulum and requires ATP. EMBO J. 13:6076-6086.
19. Yang, Y., S. Janach, J. Cohn, and J. Wilson. 1993. The common variant of cystic fibrosis transmembrane conductance regulator is recognized by hsp70 and degraded in a pre-Golgi nonlysosomal compartment. Proc. Nat. Acad. Sci. USA. 90:9480-9484.
20. Pind, S., J. Riordan, and D. Williams. 1994. Participation of the endoplasmic reticulum chaperone calnexin (p88, IP90) in the biogenesis of the cystic fibrosis transmembrane conductance regulator. J. Biol. Chem. 269:12784-12788.
21. Brown, C.R., L. Hong-Brown, J. Biwersi, A. Verkman, and W. Welch. 1996. Chemical chaperones correct the mutant phenotype of the ΔF508 cystic fibrosis transmembrane conductance regulator protein. Cell Stress and Chaperones. 1:117-125.
22. Sato, S., C. Ward, M. Krouse, J. Wine, and R. Kopito. 1996. Glycerol reverses the misfolding phenotype of the most common cystic fibrosis mutation. J. Biol. Chem. 271:635-638.
23. Thomas, P., P. Shenbagamurthi, J. Sondek, J. Hullihen, and P. Pederson. 1992. The cystic fibrosis transmembrane conductance regulator. Effects of the most common cystic fibrosis-causing mutation on the secondary structure and stability of a synthetic peptide. J. Biol. Chem. 267:5727-5730.
24. Hartman, J., Z. Huang, T. Rado, S. Peng, T. Jiling, D. Muccio, and E. Sorscher. 1992. Recombinant synthesis, purification, and nucleotide binding characteristics of the first nucleotide binding domain of the cystic fibrosis gene product. J. Biol. Chem. 267:6455-6458.
25. Blobel, G. 1980. Intracellular protein topogenesis. Proc. Natl. Acad. Sci. USA. 77:1496-1500.
26. Bibi, E., G. Verner, C.-Y. Chang, and H. Kaback. 1991. Organization and stability of a polytopic membrane protein: deletion and analysis of the lactose permease of Escherichia coli. Proc. Natl. Acad. Sci. USA. 88:7271-7275.
27. Bibi, E., S. Stearns, and H. Kaback. 1992. The N-terminal 22 amino acid residues in the lactose permease of Escherichia coli are not obligatory for membrane insertion or transport activity. Proc. Natl. Acad. Sci. USA. 89:3180-3184.
28. Calamia, J., and C. Manoil. 1992. Membrane protein spanning segments as export signals. J. Mol. Biol. 224:539-543.
29. Skach, W., and V. Lingappa. 1993. Intracellular trafficking of pre(pro-) proteins across RER membranes. In Mechanisms of Intracellular Trafficking and Processing of Pro-proteins. Y.P. Loh, editor. CRC Press, Inc., Boca Raton, FL. 19-77.
30. Rothman, R.E., D.W. Andrews, M.C. Calayag, and V.R. Lingappa. 1988. Construction of defined polytopic integral transmembrane proteins. J. Biol. Chem. 263:10470-10480.
31. Hartmann, E., T.A. Rapoport, and H.F. Lodish. 1989. Predicting the orientation of eukaryotic membrane-spanning proteins. Proc. Natl. Acad. Sci. USA. 86:5786-5790.
32. Skach, W., and V. Lingappa. 1993. Amino terminus assembly of human P-glycoprotein at the endoplasmic reticulum is directed by cooperative actions of two internal sequences. J. Biol. Chem. 268:23552-23561.
33. Guillermit, H., M. Jehanne, I. Quere, M. Audrezet, B. Mercier, and C. Ferec. 1993. A novel mutation in exon 3 of the CFTR gene. Hum. Genet. 91: 233-235.
34. Zielenski, J., D. Bozon, B. Kerem, D. Markiewicz, P. Durie, J.M. Rommens, and L.-C. Tsui. 1991. Identification of Mutations in exons 1 through 8 of the cystic fibrosis transmembrane conductance regulator (CFTR) gene. Genomics. 10:229-235.
35. Barth, L.G., and L.J. Barth. 1959. Differentiation of cells of the Rana pipiens gastrula in unconditioned medium. J. Embryol. Exp. Morphol. 7:210-222.
36. Cohn, J., A. Narin, C. Marino, O. Melhus, and J. Kole. 1992. Characterization of the cystic fibrosis transmembrane conductance regulator in a colonocyte cell line. Proc. Natl. Acad. Sci. USA. 89:2340-2344.
37. Drumm, M., D. Wilkenson, L. Smit, R. Woeerll, T. Strong, R. Frizzell, D. Dawson, and F. Collins. 1991. Chloride conductance expressed by ΔF508 and other mutant CFTRs in Xenopus oocytes. Science (Wash. DC). 254:1797-1799.
38. Bear, C., F. Duguay, A. Naismith, N. Kartner, J. Hanrahan, and J. Riordan. 1991. CL-channel activity in Xenopus oocytes expressing the cystic fibrosis gene. J. Biol. Chem. 266:19142-19145.
39. Walter, P., and G. Blobel. 1983. Preparation of microsomal membranes for cotranslational protein purification. In Methods in Enzymology. Vol. 96. S. Fleischer and B. Fleischer, editors. Academic Press, Inc., New York. 84-93.
40. Skach, W., and V. Lingappa. 1994. Transmembrane orientation and topogenesis of the 3rd and 4th membrane-spanning regions of human P-glycoprotein (MDR1). Cancer Res. 54:3202-3209.
41. Chang, X.-B., Y.-X. Hou, T. Jensen, and J. Riordan. 1994. Mapping of cystic fibrosis transmembrane conductance regulator membrane topology by glycosylation site insertion. J. Biol. Chem. 269:18572-18575.
42. Wahle, S., and W. Stoffel. 1996. Membrane topology of the high-affinity L-glutamate transporter (GLAST-1) of the central nervous system. J. Cell Biol. 135:1867-1877.
43. Klausner, R., and R. Sita. 1990. Protein degredation in the endoplasmic reticulum. Cell. 62:611-614.
44. Lippincott-Schwartz, J., J. Bonifacino, L. Yuan, and R. Klausner. 1988. Degredation from the endoplasmic reticulum: disposing of newly synthesized proteins. Cell. 54:209-220.
45. Chalkley, G., and A. Harris. 1991. A cystic fibrosis patient who is homozygous for the G85E mutation has very mild disease. J. Med. Genet. 28:875-877.
46. Skach, W., M.C. Calayag, and V. Lingappa. 1993. Evidence for an alternate model of human P-glycoprotein structure and biogenesis. J. Biol. Chem. 268:6903-6908.
47. Carroll, T., M. Morales, S. Fulmer, S. Allen, T. Flotte, G. Cutting, and W. Guggino. 1995. Alternate translation initiation codons can create functional forms of cystic fibrosis transmembrane conductance regulator. J. Biol. Chem. 270:11941-11946.
48. Adams, G.A., and J.K. Rose. 1985. Incorporation of a charged amino acid into the membrane-spanning domain blocks cell surface transport but not membrane anchoring of a viral glycoprotein. Mol. Cell. Biol. 5:1442-1448.
49. Davis, G.L., and E. Hunter. 1987. A charged amino acid substitution within the transmembrane anchor of the rous sarcoma virus envelope glycoprotein affects surface expression but not intracellular transport. J. Cell Biol. 105: 1191-1203.
50. Bonifacino, J., C. Suzuki, and R. Klausner. 1990. A peptide sequence confers retention and rapid degradation in the endoplasmic reticulum. Science (Wash. DC). 247:79-82.
51. Bonifacino, J., P. Cosson, and R. Klausner. 1990. Colocalized transmembrane determinants for ER degradation and subunit assembly explain the intracellular fate of TCR chains. Cell. 63:503-513.
52. Akabas, M., C. Kaufmann, A. Cook, and P. Archdeacon. 1994. Amino acid residues lining the chloride channel of the cystic fibrosis transmembrane conductance regulator. J. Biol. Chem. 269:14865-14868.
53. - channel. Cell. 76:1091-1098.