The human Dnaj homologue (Hdj)-1/heat-shock protein (Hsp) 40 co-chaperone is required for the in vivo stabilization of the cystic fibrosis transmembrane conductance regulator by Hsp70

Biochemical Journal

Volumn 366, Issue 3, 2002, Pages 797-806

  Farinha, Carlos M ^a   Nogueira, Paulo ^a   Mendes, Filipa ^a   Penque, Deborah ^a   Amaral, Margarida D ^a  

^a NATIONAL INSTITUTE OF HEALTH DR RICARDO JORGE   (Portugal)

Author keywords

CFTR; Chaperone; Endoplasmic reticulum associated degradation

Indexed keywords

BIODEGRADATION; BIOLOGICAL MEMBRANES; CHLORINE COMPOUNDS; CONFORMATIONS; MOLECULAR BIOLOGY; PROTEINS;

MUTATIONS;

BIOCHEMISTRY;

15 DEOXYSPERGUALIN; 4 PHENYLBUTYRIC ACID; CHAPERONE; CHLORIDE CHANNEL; HEAT SHOCK PROTEIN 40; HEAT SHOCK PROTEIN 70; PHENYLALANINE; PROTEIN DNAJ; TRANSMEMBRANE CONDUCTANCE REGULATOR;

ANIMAL CELL; ARTICLE; CHO CELL; CONTROLLED STUDY; CYSTIC FIBROSIS; ENDOPLASMIC RETICULUM; NONHUMAN; PRIORITY JOURNAL; PROTEIN CONFORMATION; PROTEIN DEGRADATION; PROTEIN EXPRESSION; PROTEIN FOLDING; PROTEIN GLYCOSYLATION; PROTEIN PROCESSING; PROTEIN STABILITY;

ANIMALS; BLOTTING, WESTERN; CHO CELLS; CRICETINAE; CYSTIC FIBROSIS TRANSMEMBRANE CONDUCTANCE REGULATOR; DENSITOMETRY; DNA, COMPLEMENTARY; ENDOPLASMIC RETICULUM; GLYCOSYLATION; HEAT-SHOCK PROTEINS; HSC70 HEAT-SHOCK PROTEINS; HSP40 HEAT-SHOCK PROTEINS; HSP70 HEAT-SHOCK PROTEINS; HUMANS; IMMUNOHISTOCHEMISTRY; KINETICS; MOLECULAR CHAPERONES; MUTATION; PRECIPITIN TESTS; PROTEIN BINDING; PROTEIN BIOSYNTHESIS; PROTEIN CONFORMATION; PROTEIN FOLDING; TIME FACTORS; TRANSFECTION;

ANIMALIA;

EID: 0037106481     PISSN: 02646021     EISSN: None     Source Type: Journal    
DOI: 10.1042/BJ20011717     Document Type: Article

References (49)

1. Collins, F. S. (1992) Cystic fibrosis: molecular biology and therapeutic implications. Science 256, 774-779
2. Klein, I., Sarkadi, B. and Varadi, A. (1999) An inventory of the human ABC proteins. Biochim. Biophys. Acta 1461, 237-262
3. Lu, Y., Xiong, X., Helm, A., Kimani, K., Bragin, A. and Skach, W. R. (1998) Co- and posttranslational translocation mechanisms direct cystic fibrosis transmembrane conductance regulator N terminus transmembrane assembly. J. Biol. Chem. 273, 568-576
4. Hammond, C. and Helenius, A. (1995) Quality control in the secretory pathway. Curr. Opin. Cell Biol. 7, 523-529
5. 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
6. 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
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) Detective intracellular transport and processing of CFTR is the molecular basis of most cystic fibrosis. Cell 63, 827-834
8. Qu, B. H. and Thomas, P. J. (1996) Alteration of the cystic fibrosis transmembrane conductance regulator folding pathway. J. Biol. Chem. 271, 7261-7264
9. Zhang, F., Kartner, N. and Lukacs, G. L. (1998) Limited proteolysis as a probe for arrested conformational maturation of delta F508 CFTR. Nat. Struct. Biol. 5, 180-183
10. Kalin, N., Claass, A., Sommer, M., Puchelle, E. and Tummler, B. (1999) DeltaF508 CFTR protein expression in tissues from patients with cystic fibrosis. J. Clin. Invest. 103, 1379-1389
11. Penque, D., Mendes, F., Beck, S., Farinha, C., Pacheco, P., Nogueira, P., Lavinha, J., Malhó, R. and Amaral, M. D. (2000) Cystic fibrosis F508del patients have apically localized CFTR in a reduced number of airway cells. Lab. Invest. 80, 857-868
12. Denning, G. M., Anderson, M. P., Amara, J. F., Marshall, J., Smith, A. E. and Welsh, M. J. (1992) Processing of mutant cystic fibrosis transmembrane conductance regulator is temperature-sensitive. Nature (London) 358, 761-764
13. Sato, S., Ward, C. L., Krouse, M. E., Wine, J. J. and Kopito, R. R. (1996) Glycerol reverses the misfolding phenotype of the most common cystic fibrosis mutation. J. Biol. Chem. 271, 635-638
14. Veeze, H. J., Halley, D. J., Bijman, J., de Jongste, J. C., de Jonge, H. R. and Sinaasappel, M. (1994) Determinants of mild clinical symptoms in cystic fibrosis patients. Residual chloride secretion measured in rectal biopsies in relation to the genotype. J. Clin. Invest. 93, 461-466
15. Kelley, T. J., Thomas, K., Milgram, L. J. and Drumm, M. L. (1997) In vivo activation of the cystic fibrosis transmembrane conductance regulator mutant deltaF508 in murine nasal epithelium. Proc. Natl. Acad. Sci. U.S.A. 94, 2604-2608
16. Brodsky, J. L. and McCracken, A. A. (1999) ER protein quality control and proteasome-mediated protein degradation. Semin. Cell Dev. Biol. 10, 507-513
17. 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
18. Ward, C. L., Omura, S. and Kopito, R. R. (1995) Degradation of CFTR by the ubiquitin-proteasome pathway. Cell 83, 121-127
19. Zhang, Y., Nijbroek, G., Sullivan, M. L., McCracken, A. A., Watkins, S. C., Michaelis, S. and Brodsky, J. L. (2001) Hsp70 molecular chaperone facilitates endoplasmic reticulum-associated protein degradation of cystic fibrosis transmembrane conductance regulator in yeast. Mol. Biol. Cell 12, 1303-1314
20. Yang, Y., Janich, S., Cohn, J. A. and Wilson, J. M. (1993) The common variant of cystic fibrosis transmembrane conductance regulator is recognized by hsp70 and degraded in a pre-Golgi nonlysosomal compartment. Proc. Natl. Acad. Sci. U.S.A. 90, 9480-9484
21. Meacham, G. C., Lu, Z., King, S., Sorscher, E., Tousson, A. and Cyr, D. M. (1999) The Hdj-2/Hsc70 chaperone pair facilitates early steps in CFTR biogenesis. EMBO J. 18, 1492-1505
22. Loo, M. A., Jensen, T. J., Gui, 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, 6879-8887
23. 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
24. Strickland, E., Qu, B. H., Millen, L. and Thomas, P. J. (1997) The molecular chaperone Hsc70 assists the in vitro folding of the N-terminal nucleotide-binding domain of the cystic fibrosis transmembrane conductance regulator. J. Biol. Chem. 272, 25421-25424
25. Brown, C. R., Hong-Brown, L. Q., Biwersi, J., Verkman, A. S. and Welch, W. J. (1996) Chemical chaperones correct the mutant phenotype of the delta F508 cystic fibrosis transmembrane conductance regulator protein. Cell Stress Chaperones 1, 117-125
26. Michels, A. A., Kanon, B., Konings, A. W., Ohtsuka, K., Bensaude, O. and Kampinga, H. H. (1997) Hsp70 and Hsp40 chaperone activities in the cytoplasm and the nucleus of mammalian cells. J. Biol. Chem. 272, 33283-33289
27. Nollen, E. A., Brunsting, J. F., Roelofsen, H., Weber, L. A. and Kampinga, H. H. (1999) In vivo chaperone activity of heat shock protein 70 and thermotolerance. Mol. Cell. Biol. 19, 2069-2079
28. Rubenstein, R. C. and Zeitlin, P. L. (2000) Sodium 4-phenylbutyrate downregulates Hsc70: implications for intracellular trafficking of DeltaF508-CFTR. Am. J. Physiol. Cell Physiol. 278, C259-C267
29. Jiang, C., Fang, S. L., Xiao, Y. F., O'Connor, S. P., Nadler, S. G., Lee, D. W., Jefferson, D. M., Kaplan, J. M., Smith, A. E. and Cheng, S. H. (1998) Partial restoration of cAMP-stimulated CFTR chloride channel activity in DeltaF508 cells by deoxyspergualin. Am. J. Physiol. 275, C171-C178
30. Chang, X. B., Tabcharani, J. A. Hou, Y. X., Jensen, T. J., Kartner, N., Alon, N., Hanrahan, J. W. and Riordan, J. R. (1993) Protein kinase A (PKA) still activates CFTR chloride channel after mutagenesis of all 10 PKA consensus phosphorylation sites. J. Biol. Chem. 268, 11304-11311
31. Haardt, M., Benharouga, M., Lechardeur, D., Kartner, N. and Lukacs, G. L. (1999) C-terminal truncations destabilize the cystic fibrosis transmembrane conductance regulator without impairing its biogenesis. A novel class of mutation. J. Biol. Chem. 274, 21873-21877
32. Hunt, C. and Morimoto, R. I. (1985) Conserved features of eukaryotic hsp70 genes revealed by comparison with the nucleotide sequence of human hsp70. Proc. Natl. Acad. Sci. U.S.A. 82, 6455-6459
33. Crawford, I., Maloney, P. C., Zeitlin, P. L., Guggino, W. B., Hyde, S. C., Turley, H., Gatter, K. C., Harris, A. and Higgins, C. F. (1991) Immunocytochemical localization of the cystic fibrosis gene product CFTR. Proc. Natl. Acad. Sci. U.S.A. 88, 9262-9266
34. Baler, R., Dahl, G. and Voellmy, R. (1993) Activation of human heat shock genes is accompanied by oligomerization, modification, and rapid translocation of heat shock transcription factor HSF1. Mol. Cell. Biol. 17, 2486-2496
35. Kleinbaum, D. G., Kupper, L. L. and Muller, K. E. (1988) Applied Regression Analysis and Other Multivariated Methods, 2nd edn, Duxburry Press, Pacific Grove, CA
36. Helliwell, P. S. and Jackson, S. (1994) Relationship between weakness and muscle wasting in rheumatoid arthritis. Ann. Rheum. Dis. 53, 726-728
37. Glantz, S. (1997) Primer of Biostatistics, 4th edn, McGraw Hill, New York
38. Morimoto, R. I. (1998) Regulation of the heat shock transcriptional response: cross talk between a family of heat shock factors, molecular chaperones, and negative regulators. Genes Dev. 12, 3788-3796
39. Dworniczak, B. and Mirault, M. E. (1987) Structure and expression of a human gene coding for a 71 kd heal shock 'cognate' protein. Nucleic Acids Res. 15, 5181-5197
40. Morimoto, R. I. and Santoro, M. G. (1998) Stress-inducible responses and heat shock proteins: new pharmacologic targets for cytoprotection. Nat. Biotechnol. 16, 833-838
41. Thomas, J. G. and Baneyx, F. (1996) Protein misfolding and inclusion body formation in recombinant Escherichia coli cells overexpressing heat-shock proteins. J. Biol. Chem. 271, 11141-11147
42. Silberg, J. J., Hoff, K. G. and Vickery, L. E. (1998) The Hsc66-Hsc20 chaperone system in Escherichia coli: chaperone activity and interactions with the DnaK-DnaJ-grpE system J. Bacteriol. 180, 6617-6624
43. Michels, A. A., Kanon, B., Bensaude, O. and Kampinga, H. H. (1999) Heat shock protein (Hsp) 40 mutants inhibit hsp70 in mammalian cells. J. Biol. Chem. 274, 36757-36763
44. Satyal, S. H., Schmidt, E. Kitagawa, K., Sondheimer, N., Lindquist, S., Kramer, J. M. and Morimoto, R. I. (2000) Polyglutamine aggregates alter protein folding homeostasis in Caenorhabditis elegans. Proc. Natl. Acad. Sci. U.S.A. 97, 5750-5755
45. Cyr, D. M., Langer, T. and Douglas, M. G. (1994) DnaJ-like proteins: molecular chaperones and specific regulators of Hsp70. Trends Biochem. Sci. 19, 176-181
46. Ohtsuka, K. and Hata, M. (2000) Molecular chaperone function of mammalian Hsp70 and Hsp40 - a review. Int. J. Hyperthermia 16, 231-245
47. Meacham, G. C., Patterson, C., Zhang, W., Younger, J. M. and Cyr, D. M. (2001) The Hsc70 co-chaperone CHIP targets immature CFTR for proteasomal degradation. Nat. Cell Biol. 3, 100-105
48. Jiang, J., Ballinger, C. A., Wu, Y., Dai, Q., Cyr, D. M., Hohfeld, J. and Patterson, C. (2001) CHIP is a U-box-dependent E3 ubiquitin ligase: identification of Hsc70 as a target for ubiquitylation. J. Biol. Chem. 276, 42938-42944
49. Wei, H., Kemp, S., McGuinness, M. C., Moser, A. B. and Smith, K. D. (2000) Pharmacological induction of peroxisomes in peroxisome biogenesis disorders. Ann. Neurol. 47, 286-296