Improved maturation of CFTR by an ER export signal

FASEB Journal

Volumn 21, Issue 10, 2007, Pages 2352-2358

  Wendeler, Markus W ^a   Nufer, Oliver ^a,b   Hauri, Hans Peter ^a  

^a UNIVERSITY OF BASEL   (Switzerland)

^b ASTRAZENECA   (United Kingdom)

Author keywords

Cystic fibrosis; Membrane traffic; Transport signal

Indexed keywords

TRANSMEMBRANE CONDUCTANCE REGULATOR; VALINE;

ARTICLE; CARBOXY TERMINAL SEQUENCE; CELL MEMBRANE; CONTROLLED STUDY; CYTOPLASM; ENDOPLASMIC RETICULUM; HUMAN; HUMAN CELL; MUTATIONAL ANALYSIS; PRIORITY JOURNAL; PROTEIN DEGRADATION; PROTEIN EXPRESSION; PROTEIN LOCALIZATION; PROTEIN PROCESSING; PROTEIN STABILITY; PROTEIN TRANSPORT; SIGNAL TRANSDUCTION; SURFACE PROPERTY; WILD TYPE;

CELL LINE; CELL MEMBRANE; CYSTIC FIBROSIS TRANSMEMBRANE CONDUCTANCE REGULATOR; ENDOPLASMIC RETICULUM; HUMANS; KIDNEY; RECOMBINANT PROTEINS; TRANSFECTION;

EID: 34547760398     PISSN: 08926638     EISSN: None     Source Type: Journal    
DOI: 10.1096/fj.07-8128com     Document Type: Article

References (55)

1. Jilling, T., and Kirk, K. L. (1997) The biogenesis, traffic, and function of the cystic fibrosis transmembrane conductance regulator. Int. Rev. Cytol. 172, 193-241
2. Mickle, J. E., Macek, M., Jr., Fulmer-Smentek, S. B., Egan, M. M., Schwiebert, E., Guggino, W., Moss, R., and Cutting, G. R. (1998) A mutation in the cystic fibrosis transmembrane conductance regulator gene associated with elevated sweat chloride concentrations in the absence of cystic fibrosis. Hum. Mol. Genet. 7, 729-735
3. Riordan, J. R. (2005) Assembly of functional CFTR chloride channels. Annu. Rev. Physiol. 67, 701-718
4. Riordan, J. R., Rommens, J. M., Kerem, B., Alon, N., Rozmahel, R., Grzelczak, Z., Zielenski, J., Lok, S., Plavsic, N., Chou, J. L., et al. (1989) Identification of the cystic fibrosis gene: cloning and characterization of complementary DNA. Science 245, 1066-1073
5. Riordan, J. R. (1999) Cystic fibrosis as a disease of misprocessing of the cystic fibrosis transmembrane conductance regulator glycoprotein. Am. J. Hum. Genet. 64, 1499-1504
6. Bobadilla, J. L., Macek, M., Jr., Fine, J. P., and Farrell, P. M. (2002) Cystic fibrosis: a worldwide analysis of CFTR mutations-correlation with incidence data and application to screening. Hum. Mutat. 19, 575-606
7. Cheng, S. H., Gregory, R. J., Marshall, J., Paul, S., Souza, D. W., White, G. A., O'Riordan, C. R., and Smith, A. E. (1990) Defective intracellular transport and processing of CFTR is the molecular basis of most cystic fibrosis. Cell 63, 827-834
8. Lukacs, G. L., Mohamed, A., Kartner, N., Chang, X. B., Riordan, J. R., and Grinstein, S. (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
9. Ward, C. L., and Kopito, R. R. (1994) Intracellular turnover of cystic fibrosis transmembrane conductance regulator. Inefficient processing and rapid degradation of wild-type and mutant proteins. J. Biol. Chem. 269, 25710-25718
10. Kopito, R. R. (1999) Biosynthesis and degradation of CFTR. Physiol. Rev. 79, S167-173
11. Gilbert, A., Jadot, M., Leontieva, E., Wattiaux-De Coninck, S., and Wattiaux, R. (1998) Delta F508 CFTR localizes in the endoplasmic reticulum-Golgi intermediate compartment in cystic fibrosis cells. Exp. Cell Res. 242, 144-152
12. Bradbury, N. A. (1999) Intracellular CFTR: localization and function. Physiol. Rev. 79, S175-191
13. Bannykh, S. I., Bannykh, G. I., Fish, K. N., Moyer, B. D., Riordan, J. R., and Balch, W. E. (2000) Traffic pattern of cystic fibrosis transmembrane regulator through the early exocytic pathway. Traffic 1, 852-870
14. Ward, C. L., Omura, S., and Kopito, R. R. (1995) Degradation of CFTR by the ubiquitin-proteasome pathway. Cell 83, 121-127
15. Jensen, T. J., Loo, M. A., Pind, S., Williams, D. B., Goldberg, A. L., and Riordan, J. R. (1995) Multiple proteolytic systems, including the proteasome, contribute to CFTR processing. Cell 83, 129-135
16. Gelman, M. S., Kannegaard, E. S., and Kopito, R. R. (2002) A principal role for the proteasome in endoplasmic reticulum-associated degradation of misfolded intracellular cystic fibrosis transmembrane conductance regulator. J. Biol. Chem. 277, 11709-11714
17. Yang, Y., Devor, D. C., Engelhardt, J. F., Ernst, S. A., Strong, T. V., Collins, F. S., Cohn, J. A., Frizzell, R. A., and Wilson, J. M. (1993) Molecular basis of defective anion transport in L cells expressing recombinant forms of CFTR. Hum. Mol. Genet. 2, 1253-1261
18. Pind, S., Riordan, J. R., and Williams, D. B. (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
19. Loo, M. A., Jensen, T. J., Cui, L., Hou, Y., Chang, X. B., and Riordan, J. R. (1998) Perturbation of Hsp90 interaction with nascent CFTR prevents its maturation and accelerates its degradation by the proteasome. EMBO J. 17, 6879-6887
20. Riordan, J. R. (1999) Therapeutic strategies for treatment of CF based on knowledge of CFTR. Pediatr. Pulmonol. Suppl. 18, 83-87
21. Cyr, D. M. (2005) Arrest of CFTRDeltaF508 folding. Nat. Struct. Mol. Biol. 12, 2-3
22. Younger, J. M., Chen, L., Ren, H. Y., Rosser, M. F., Turnbull, E. L., Fan, C. Y., Patterson, C., and Cyr, D. M. (2006) Sequential quality-control checkpoints triage misfolded cystic fibrosis transmembrane conductance regulator. Cell 126, 571-582
23. Sun, F., Zhang, R., Gong, X., Geng, X., Drain, P. F., and Frizzell, R. A. (2006) Derlin-1 promotes the efficient degradation of CFTR and CFTR folding mutants. J. Biol. Chem. 281, 36856-36863
24. Yoo, J. S., Moyer, B. D., Bannykh, S., Yoo, H. M., Riordan, J. R., and Balch, W. E. (2002) Non-conventional trafficking of the cystic fibrosis transmembrane conductance regulator through the early secretory pathway. J. Biol. Chem. 277, 11401-11409
25. Wang, X., Matteson, J., An, Y., Moyer, B., Yoo, J. S., Bannykh, S., Wilson, I. A., Riordan, J. R., and Balch, W. E. (2004) COPII-dependent export of cystic fibrosis transmembrane conductance regulator from the ER uses a di-acidic exit code. J. Cell Biol. 167, 65-74
26. Kleizen, B., Braakman, I., and de Jonge, H. R. (2000) Regulated trafficking of the CFTR chloride channel. Eur. J. Cell Biol. 79, 544-556
27. Varga, K., Jurkuvenaite, A., Wakefield, J., Hong, J. S., Guimbellot, J. S., Venglarik, C. J., Niraj, A., Mazur, M., Sorscher, E. J., Collawn, J. F., and Bebok, Z. (2004) Efficient intracellular processing of the endogenous cystic fibrosis transmembrane conductance regulator in epithelial cell lines. J. Biol. Chem. 279, 22578-22584
28. Nufer, O., Guldbrandsen, S., Degen, M., Kappeler, F., Paccaud, J. P., Tani, K., and Hauri, H. P. (2002) Role of cytoplasmic C-terminal amino acids of membrane proteins in ER export. J. Cell Sci. 115, 619-628
29. Barlowe, C. (2003) Signals for COPII-dependent export from the ER: what's the ticket out? Trends Cell Biol. 13, 295-300
30. Nishimura, N., and Balch, W. E. (1997) A di-acidic signal required for selective export from the endoplasmic reticulum. Science 277, 556-558
31. Kappeler, F., Klopfenstein, D. R., Foguet, M., Paccaud, J. P., and Hauri, H. P. (1997) The recycling of ERGIC-53 in the early secretory pathway. ERGIC-53 carries a cytosolic endoplasmic reticulum-exit determinant interacting with COPII. J. Biol. Chem. 272, 31801-31808
32. Mu, Y., Otsuka, T., Horton, A. C., Scott, D. B., and Ehlers, M. D. (2003) Activity-dependent mRNA splicing controls ER export and synaptic delivery of NMDA receptors. Neuron 40, 581-594
33. Zhao, W., Chen, T. L., Vertel, B. M., and Colley, K. J. (2006) The CMP-sialic acid transporter is localized in the medial-trans golgi and possesses two specific endoplasmic reticulum export motifs in its carboxy-terminal cytoplasmic tail. J. Biol. Chem.
34. Chang, X. B., Cui, L., Hou, Y. X., Jensen, T. J., Aleksandrov, A. A., Mengos, A., and Riordan, J. R. (1999) Removal of multiple arginine-framed trafficking signals overcomes misprocessing of delta F508 CFTR present in most patients with cystic fibrosis. Mol. Cell 4, 137-142
35. Short, D. B., Trotter, K. W., Reczek, D., Kreda, S. M., Bretscher, A., Boucher, R. C., Stutts, M. J., and Milgram, S. L. (1998) An apical PDZ protein anchors the cystic fibrosis transmembrane conductance regulator to the cytoskeleton. J. Biol. Chem. 273, 19797-19801
36. Wang, S., Raab, R. W., Schatz, P. J., Guggino, W. B., and Li, M. (1998) Peptide binding consensus of the NHE-RF-PDZ1 domain matches the C-terminal sequence of cystic fibrosis transmembrane conductance regulator (CFTR). FEBS Lett. 427, 103-108
37. Fanning, A. S., and Anderson, J. M. (1999) PDZ domains: fundamental building blocks in the organization of protein complexes at the plasma membrane. J. Clin. Invest. 103, 767-772
38. Wang, S., Yue, H., Derin, R. B., Guggino, W. B., and Li, M. (2000) Accessory protein facilitated CFTR-CFTR interaction, a molecular mechanism to potentiate the chloride channel activity. Cell 103, 169-179
39. Bezprozvanny, I., and Maximov, A. (2001) PDZ domains: more than just a glue. Proc. Natl. Acad. Sci. U. S. A. 98, 787-789
40. Sun, W., Anderson, B., Redman, J., Milunsky, A., Buller, A., McGinniss, M. J., Quan, F., Anguiano, A., Huang, S., Hantash, F., and Strom, C. (2006) CFTR 5T variant has a low penetrance in females that is partially attributable to its haplotype. Genet. Med. 8, 339-345
41. Reddy, M. M., Light, M. J., and Quinton, P. M. (1999) Activation of the epithelial Na+ channel (ENaC) requires CFTR Cl-channel function. Nature 402, 301-304
42. Swiatecka-Urban, A., Duhaime, M., Coutermarsh, B., Karlson, K. H., Collawn, J., Milewski, M., Cutting, G. R., Guggino, W. B., Langford, G., and Stanton, B. A. (2002) PDZ domain interaction controls the endocytic recycling of the cystic fibrosis transmembrane conductance regulator. J. Biol. Chem. 277, 40099-40105
43. Songyang, Z., Fanning, A. S., Fu, C., Xu, J., Marfatia, S. M., Chishti, A. H., Crompton, A., Chan, A. C., Anderson, J. M., and Cantley, L. C. (1997) Recognition of unique carboxyl-terminal motifs by distinct PDZ domains. Science 275, 73-77
44. Miller, E., Antonny, B., Hamamoto, S., and Schekman, R. (2002) Cargo selection into COPII vesicles is driven by the Sec24p subunit. EMBO J. 21, 6105-6113
45. Mossessova, E., Bickford, L. C., and Goldberg, J. (2003) SNARE selectivity of the COPII coat. Cell 114, 483-495
46. Nufer, O., Kappeler, F., Guldbrandsen, S., and Hauri, H. P. (2003) ER export of ERGIC-53 is controlled by cooperation of targeting determinants in all three of its domains. J. Cell Sci. 116, 4429-4440
47. Wang, X., Venable, J., Lapointe, P., Hutt, D. M., Koulov, A. V., Coppinger, J., Gurkan, C., Kellner, W., Matteson, J., Plutner, H., et al. (2006) Hsp90 Cochaperone Aha1 downregulation rescues misfolding of CFTR in cystic fibrosis. Cell 127, 803-815
48. Ma, D., Zerangue, N., Lin, Y. F., Collins, A., Yu, M., Jan, Y. N., and Jan, L. Y. (2001) Role of ER export signals in controlling surface potassium channel numbers. Science 291, 316-319
49. Griesenbach, U., Ferrari, S., Geddes, D. M., and Alton, E. W. (2002) Gene therapy progress and prospects: cystic fibrosis. Gene Ther. 9, 1344-1350
50. Davies, J. C., Geddes, D. M., and Alton, E. W. (2001) Gene therapy for cystic fibrosis. J. Gene Med. 3, 409-417
51. Davies, J. C. (2006) Gene and cell therapy for cystic fibrosis. Paediatr. Respir. Rev. 7 Suppl. 1, S163-165
52. Liu, X., Jiang, Q., Mansfield, S. G., Puttaraju, M., Zhang, Y., Zhou, W., Cohn, J. A., Garcia-Blanco, M. A., Mitchell, L. G., and Engelhardt, J. F. (2002) Partial correction of endogenous DeltaF508 CFTR in human cystic fibrosis airway epithelia by spliceosome-mediated RNA trans-splicing. Nat. Biotechnol. 20, 47-52
53. Ostrowski, L. E., Hutchins, J. R., Zakel, K., and O'Neal, W. K. (2003) Targeting expression of a transgene to the airway surface epithelium using a ciliated cell-specific promoter. Mol. Ther. 8, 637-645
54. Liu, S., Veilleux, A., Zhang, L., Young, A., Kwok, E., Laliberte, F., Chung, C., Tota, M. R., Dube, D., Friesen, R. W., and Huang, Z. (2005) Dynamic activation of cystic fibrosis transmembrane conductance regulator by type 3 and type 4D phosphodiesterase inhibitors. J. Pharmacol. Exp. Ther. 314, 846-854
55. Liu, X., Alexander, C., Serrano, J., Borg, E., and Dawson, D. C. (2006) Variable reactivity of an engineered cysteine at position 338 in cystic fibrosis transmembrane conductance regulator reflects different chemical states of the thiol. J. Biol. Chem. 281, 8275-8285