Role of Hsc70 binding cycle in CFTR folding and endoplasmic reticulum-associated degradation

Molecular Biology of the Cell

Volumn 22, Issue 16, 2011, Pages 2797-2809

  Matsumura, Yoshihiro ^a   David, Larry L ^a   Skach, William R ^a  

^a OREGON HEALTH AND SCIENCE UNIVERSITY   (United States)

Author keywords

[No Author keywords available]

Indexed keywords

BAG 1 PROTEIN; CHAPERONE; HEAT SHOCK COGNATE PROTEIN 70; TRANSMEMBRANE CONDUCTANCE REGULATOR; UBIQUITIN;

ARTICLE; CARBOXY TERMINAL SEQUENCE; CELL FREE SYSTEM; ENDOPLASMIC RETICULUM; GENE EXPRESSION; HUMAN; NONHUMAN; PRIORITY JOURNAL; PROTEIN BINDING; PROTEIN DEGRADATION; PROTEIN DOMAIN; PROTEIN FOLDING; PROTEIN FUNCTION; PROTEIN PROCESSING; UBIQUITINATION;

ANIMALS; CELL LINE; CELL-FREE SYSTEM; CYSTIC FIBROSIS TRANSMEMBRANE CONDUCTANCE REGULATOR; DNA-BINDING PROTEINS; ENDOPLASMIC RETICULUM; HSC70 HEAT-SHOCK PROTEINS; HUMANS; MICROSOMES; PEPTIDE FRAGMENTS; PROTEIN BINDING; PROTEIN FOLDING; PROTEIN STRUCTURE, TERTIARY; PROTEOLYSIS; RATS; TRANSCRIPTION FACTORS; UBIQUITINATION;

EID: 80051689133     PISSN: 10591524     EISSN: 19394586     Source Type: Journal    
DOI: 10.1091/mbc.E11-02-0137     Document Type: Article

References (95)

1. Ahner A, Nakatsukasa K, Zhang H, Frizzell RA, Brodsky JL (2007). Small heat-shock proteins selectΔF508-CFTR for endoplasmic reticulum-associated degradation. Mol Biol Cell 18, 806-814. (Pubitemid 46399487)
2. Alberti S, Bohse K, Arndt V, Schmitz A, Hohfeld J (2004). The cochaperone HspBP1 inhibits the CHIP ubiquitin ligase and stimulates the maturation of the cystic fibrosis transmembrane conductance regulator. Mol Biol Cell 15, 4003-4010. (Pubitemid 39122006)
3. Andreasson C, Fiaux J, Rampelt H, Druffel-Augustin S, Bukau B (2008). Insights into the structural dynamics of the Hsp110-Hsp70 interaction reveal the mechanism for nucleotide exchange activity. Proc Natl Acad Sci USA 105, 16519-16524.
4. Arndt V, Daniel C, Nastainczyk W, Alberti S, Hohfeld J (2005). BAG-2 acts as an inhibitor of the chaperone-associated ubiquitin ligase CHIP. Mol Biol Cell 16, 5891-5900. (Pubitemid 41752235)
5. Balch WE, Morimoto RI, Dillin A, Kelly JW (2008). Adapting proteostasis for disease intervention. Science 319, 916-919. (Pubitemid 351263754)
6. Ballinger CA, Connell P, Wu Y, Hu Z, Thompson LJ, Yin LY, Patterson C (1999). Identification of CHIP, a novel tetratricopeptide repeat-containing protein that interacts with heat shock proteins and negatively regulates chaperone functions. Mol Cell Biol 19, 4535-4545. (Pubitemid 29242026)
7. Bhangoo MK, Tzankov S, Fan AC, Dejgaard K, Thomas DY, Young JC (2007). Multiple 40-kDa heat-shock protein chaperones function in Tom70-dependent mitochondrial import. Mol Biol Cell 18, 3414-3428. (Pubitemid 47378681)
8. Bimston D, Song J, Winchester D, Takayama S, Reed JC, Morimoto RI (1998). BAG-1, a negative regulator of Hsp70 chaperone activity, uncouples nucleotide hydrolysis from substrate release. EMBO J 17, 6871-6878. (Pubitemid 28550281)
9. Brehmer D, Rudiger S, Gassler CS, Klostermeier D, Packschies L, Reinstein J, Mayer MP, Bukau B (2001). Tuning of chaperone activity of Hsp70 proteins by modulation of nucleotide exchange. Nat Struct Biol 8, 427-432. (Pubitemid 32381290)
10. Briknarova K et al. (2001). Structural analysis of BAG1 cochaperone and its interactions with Hsc70 heat shock protein. Nat Struct Biol 8, 349-352. (Pubitemid 32275022)
11. Brive L, Takayama S, Briknarova K, Homma S, Ishida SK, Reed JC, Ely KR (2001). The carboxyl-terminal lobe of Hsc70 ATPase domain is sufficient for binding to BAG1. Biochem Biophys Res Commun 289, 1099-1105. (Pubitemid 34076304)
12. Brown CR, Martin RL, Hansen WJ, Beckmann RP, Welch WJ (1993). The constitutive and stress inducible forms of hsp 70 exhibit functional similarities and interact with one another in an ATP-dependent fashion. J Cell Biol 120, 1101-1112. (Pubitemid 23064165)
13. Buck TM, Skach WR (2005). Differential stability of biogenesis intermediates reveals a common pathway for aquaporin-1 topological maturation. J Biol Chem 280, 261-269. (Pubitemid 40164988)
14. Caohuy H, Jozwik C, Pollard HB (2009). Rescue ofΔF508-CFTR by the SGK1/Nedd4-2 signaling pathway. J Biol Chem 284, 25241-25253.
15. Carlson E, Bays N, David L, Skach WR (2005). Reticulocyte lysate as a model system to study endoplasmic reticulum membrane protein degradation. Methods Mol Biol 301, 185-205.
16. Carlson EJ, Pitonzo D, Skach WR (2006). p97 functions as an auxiliary factor to facilitate TM domain extraction during CFTR ER-associated degradation. EMBO J 25, 4557-4566. (Pubitemid 44498129)
17. Carvalho P, Goder V, Rapoport TA (2006). Distinct ubiquitin-ligase complexes define convergent pathways for the degradation of ER proteins. Cell 126, 361-373. (Pubitemid 44092963)
18. Chen JS, Faller DV, Spanjaard RA (2003). Short-chain fatty acid inhibitors of histone deacetylases: promising anticancer therapeutics? Curr Cancer Drug Targets 3, 219-236. (Pubitemid 36565763)
19. Chiang HL, Terlecky SR, Plant CP, Dice JF (1989). A role for a 70-kilodalton heat shock protein in lysosomal degradation of intracellular proteins. Science 246, 382-385.
20. Choo-Kang LR, Zeitlin PL (2001). Induction of HSP70 promotes ΔF508 CFTR trafficking. Am J Physiol Lung Cell Mol Physiol 281, L58-L68.
21. Connell P, Ballinger CA, Jiang J, Wu Y, Thompson LJ, Hohfeld J, Patterson C (2001). The co-chaperone CHIP regulates protein triage decisions mediated by heat-shock proteins. Nat Cell Biol 3, 93-96. (Pubitemid 32114838)
22. Cross BC, Sinning I, Luirink J, High S (2009). Delivering proteins for export from the cytosol. Nat Rev Mol Cell Biol 10, 255-264.
23. Dai Q et al. (2005). Regulation of the cytoplasmic quality Control protein degradation pathway by BAG2. J Biol Chem 280, 38673-38681. (Pubitemid 43853770)
24. Demand J, Alberti S, Patterson C, Hohfeld J (2001). Cooperation of a ubiquitin domain protein and an E3 ubiquitin ligase during chaperone/proteasome coupling. Curr Biol 11, 1569-1577. (Pubitemid 32978521)
25. Denic V, Quan EM, Weissman JS (2006). A luminal surveillance complex that selects misfolded glycoproteins for ER-associated degradation. Cell 126, 349-359. (Pubitemid 44092967)
26. Dittmar KD, Hutchison KA, Owens-Grillo JK, Pratt WB (1996). Reconstitution of the steroid receptor.hsp90 heterocomplex assembly system of rabbit reticulocyte lysate. J Biol Chem 271, 12833-12839. (Pubitemid 26175857)
27. Eisenberg E, Greene LE (2007). Multiple roles of auxilin and hsc70 in clathrin-mediated endocytosis. Traffic 8, 640-646. (Pubitemid 46785147)
28. Fan CY, Lee S, Cyr DM (2003). Mechanisms for regulation of Hsp70 function by Hsp40. Cell Stress Chaperones 8, 309-316. (Pubitemid 38222877)
29. Farinha CM, Nogueira P, Mendes F, Penque D, Amaral MD (2002). 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. Biochem J 366, 797-806.
30. Frydman J, Hohfeld J (1997). Chaperones get in touch: the Hip-Hop connection. Trends Biochem Sci 22, 87-92. (Pubitemid 27107858)
31. Frydman J, Nimmesgern E, Ohtsuka K, Hartl FU (1994). Folding of nascent polypeptide chains in a high molecular mass assembly with molecular chaperones. Nature 370, 111-117. (Pubitemid 24229115)
32. Gamerdinger M, Hajieva P, Kaya AM, Wolfrum U, Hartl FU, Behl C (2009). Protein quality control during aging involves recruitment of the macroautophagy pathway by BAG3. EMBO J 28, 889-901.
33. Goldfarb SB, Kashlan OB, Watkins JN, Suaud L, Yan W, Kleyman TR, Rubenstein RC (2006). Differential effects of Hsc70 and Hsp70 on the intracellular trafficking and functional expression of epithelial sodium channels. Proc Natl Acad Sci USA 103, 5817-5822.
34. Grove DE, Fan CY, Ren HY, Cyr DM (2011). The ER-associated Hsp40 DNAJB12 and Hsc70 cooperate to facilitate RMA1 E3 dependent degradation of nascent CFTRΔF508. Mol Biol Cell 22, 301-314.
35. Grove DE, Rosser MF, Ren HY, Naren AP, Cyr DM (2009). Mechanisms for rescue of correctable folding defects in CFTRΔF508. Mol Biol Cell 20, 4059-4069.
36. Hartl FU (1996). Molecular chaperones in cellular protein folding. Nature 381, 571-579.
37. Hohfeld J, Jentsch S (1997). GrpE-like regulation of the hsc70 chaperone by the anti-apoptotic protein BAG-1. EMBO J 16, 6209-6216. (Pubitemid 27458341)
38. Hutt DM, Powers ET, Balch WE (2009). The proteostasis boundary in misfolding diseases of membrane traffic. FEBS Lett 583, 2639-2646.
39. Hutt DM et al. (2010). Reduced histone deacetylase 7 activity restores function to misfolded CFTR in cystic fibrosis. Nat Chem Biol 6, 25-33.
40. Jiang C, Fang SL, Xiao YF, O'Connor SP, Nadler SG, Lee DW, Jefferson DM, Kaplan JM, Smith AE, Cheng SH (1998). Partial restoration of cAMP-stimulated CFTR chloride channel activity in. F508 cells by deoxyspergualin. Am J Physiol 275, C171-C178.
41. Kampinga HH, Craig EA (2010). The HSP70 chaperone machinery: J proteins as drivers of functional specificity. Nat Rev Mol Cell Biol 11, 579-592.
42. Kingston RE, Chen CA, Okayama H (2003). Calcium phosphate transfection. In: Current Protocols in Cell Biology, ed. JS Bonifacino, M Dasso, J Lippincott-Schwartz, JB Harford, and KM Yamada, New York: John Wiley & Sons, 20.3.1-20.3.8.
43. Kleizen B, van Vlijmen T, de Jonge HR, Braakman I (2005). Folding of CFTR is predominantly cotranslational. Mol Cell 20, 277-287. (Pubitemid 41484172)
44. Kopito RR (1997). ER quality control: the cytoplasmic connection. Cell 88, 427-430.
45. Lee RJ, Liu CW, Harty C, McCracken AA, Latterich M, Romisch K, DeMartino GN, Thomas PJ, Brodsky JL (2004). Uncoupling retro-translocation and degradation in the ER-associated degradation of a soluble protein. EMBO J 23, 2206-2215. (Pubitemid 38833230)
46. Matsumura Y, Ban N, Inagaki N (2008). Aberrant catalytic cycle and impaired lipid transport into intracellular vesicles in ABCA3 mutants associated with nonfatal pediatric interstitial lung disease. Am J Physiol Lung Cell Mol Physiol 295, L698-L707.
47. Matsumura Y, Ban N, Ueda K, Inagaki N (2006). Characterization and classification of ATP-binding cassette transporter ABCA3 mutants in fatal surfactant deficiency. J Biol Chem 281, 34503-34514. (Pubitemid 46036658)
48. Matsumura Y, Rooney LA, Skach WR (2011). In vitro methods for CFTR biogenesis. Methods Mol Biol 741, 233-253.
49. Matsumura Y, Skach WR (2009). Protein export from endoplasmic reticulum to the cytosol: In vitro methods. In: Encyclopedia of Life Sciences, ed. A Finazzi-Agrò, New York: John Wiley & Sons.
50. Meacham GC, Lu Z, King S, Sorscher E, Tousson A, Cyr DM (1999). The Hdj-2/Hsc70 chaperone pair facilitates early steps in CFTR biogenesis. EMBO J 18, 1492-1505.
51. Meacham GC, Patterson C, Zhang W, Younger JM, Cyr DM (2001). The Hsc70 co-chaperone CHIP targets immature CFTR for proteasomal degradation. Nat Cell Biol 3, 100-105. (Pubitemid 32114840)
52. Meusser B, Hirsch C, Jarosch E, Sommer T (2005). ERAD: the long road to destruction. Nat Cell Biol 7, 766-772. (Pubitemid 41079045)
53. Morito D, Hirao K, Oda Y, Hosokawa N, Tokunaga F, Cyr DM, Tanaka K, Iwai K, Nagata K (2008). Gp78 cooperates with RMA1 in endoplasmic reticulum-associated degradation of CFTRΔF508. Mol Biol Cell 19, 1328-1336. (Pubitemid 351805088)
54. Mu TW, Ong DS, Wang YJ, Balch WE, Yates JR 3rd, Segatori L, Kelly JW (2008). Chemical and biological approaches synergize to ameliorate protein-folding diseases. Cell 134, 769-781.
55. Nakatsukasa K, Huyer G, Michaelis S, Brodsky JL (2008). Dissecting the ER-associated degradation of a misfolded polytopic membrane protein. Cell 132, 101-112.
56. Nimmesgern E, Hartl FU (1993). ATP-dependent protein refolding activity in reticulocyte lysate. Evidence for the participation of different chaperone components. FEBS Lett 331, 25-30. (Pubitemid 23285619)
57. Oberdorf J, Carlson EJ, Skach WR (2001). Redundancy of mammalian proteasome beta subunit function during endoplasmic reticulum associated degradation. Biochemistry 60, 13397-13405. (Pubitemid 33043556)
58. Oberdorf J, Carlson EJ, Skach WR (2006). Uncoupling proteasome peptidase and ATPase activities results in cytosolic release of an ER polytopic protein. J Cell Sci 119, 303-313. (Pubitemid 43210699)
59. Oberdorf J, Pitonzo D, Skach WR (2005). An energy-dependent maturation step is required for release of the cystic fibrosis transmembrane conductance regulator from early endoplasmic reticulum biosynthetic machinery. J Biol Chem 280, 38193-38202. (Pubitemid 43853714)
60. Oberdorf J, Skach WR (2002). In vitro reconstitution of CFTR biogenesis and degradation. Methods Mol Med 70, 295-310.
61. Okiyoneda T, Barrière H, Bagdány M, Rabeh WM, Du K, Höhfeld J, Young JC, Lukacs GL (2010). Peripheral protein quality control removes unfolded CFTR from the plasma membrane. Science 329, 805-810.
62. Osborne AR, Rapoport TA, van den Berg B (2005). Protein translocation by the Sec61/SecY channel. Annu Rev Cell Dev Biol 21, 529-550. (Pubitemid 41740645)
63. Palleros DR, Welch WJ, Fink AL (1991). Interaction of hsp70 with unfolded proteins: effects of temperature and nucleotides on the kinetics of binding. Proc Natl Acad Sci USA 88, 5719-5723. (Pubitemid 21914817)
64. Pratt EB, Yan FF, Gay JW, Stanley CA, Shyng SL (2009). Sulfonylurea receptor 1 mutations that cause opposite insulin secretion defects with chemical chaperone exposure. J Biol Chem 284, 7951-7959.
65. Riordan JR (2008). CFTR function and prospects for therapy. Annu Rev Biochem 77, 701-726.
66. Rosser MF, Washburn E, Muchowski PJ, Patterson C, Cyr DM (2007). Chaperone functions of the E3 ubiquitin ligase CHIP. J Biol Chem 282, 22267-22277. (Pubitemid 47267320)
67. Rubenstein RC, Egan ME, Zeitlin PL (1997). In vitro pharmacologic restoration of CFTR-mediated chloride transport with sodium 4-phenylbutyrate in cystic fibrosis epithelial cells containing ΔF508-CFTR. J Clin Invest 100, 2457-2465. (Pubitemid 27514885)
68. Rubenstein RC, Lyons BM (2001). Sodium 4-phenylbutyrate downregulates HSC70 expression by facilitating mRNA degradation. Am J Physiol Lung Cell Mol Physiol 281, L43-L51.
69. Rubenstein RC, Zeitlin PL (1998). A pilot clinical trial of oral sodium 4-phenylbutyrate (Buphenyl) in. F508-homozygous cystic fibrosis patients: partial restoration of nasal epithelial CFTR function. Am J Respir Crit Care Med 157, 484-490. (Pubitemid 28090539)
70. Rubenstein RC, Zeitlin PL (2000). Sodium 4-phenylbutyrate downregulates Hsc70: implications for intracellular trafficking of ΔF508-CFTR. Am J Physiol Cell Physiol 278, C259-C267. (Pubitemid 30131142)
71. Schmid D, Baici A, Gehring H, Christen P (1994). Kinetics of molecular chaperone action. Science 263, 971-973. (Pubitemid 24094562)
72. Shomura Y, Dragovic Z, Chang HC, Tzvetkov N, Young JC, Brodsky JL, Guerriero V, Hartl FU, Bracher A (2005). Regulation of Hsp70 function by HspBP1: structural analysis reveals an alternate mechanism for Hsp70 nucleotide exchange. Mol Cell 17, 367-379. (Pubitemid 40193308)
73. Skach WR (2009). Cellular mechanisms of membrane protein folding. Nat Struct Mol Biol 16, 606-612.
74. Smith DF, Sullivan WP, Marion TN, Zaitsu K, Madden B, McCormick DJ, Toft DO (1993). Identification of a 60-kilodalton stress-related protein, p60, which interacts with hsp90 and hsp70. Mol Cell Biol 13, 869-876. (Pubitemid 23040252)
75. Sondermann H, Scheufler C, Schneider C, Hohfeld J, Hartl FU, Moarefi I (2001). Structure of a Bag/Hsc70 complex: convergent functional evolution of Hsp70 nucleotide exchange factors. Science 291, 1553-1557. (Pubitemid 32179223)
76. Strickland E, Qu BH, Millen L, Thomas PJ (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. (Pubitemid 27438842)
77. Summers DW, Douglas PM, Ramos CH, Cyr DM (2009). Polypeptide transfer from Hsp40 to Hsp70 molecular chaperones. Trends Biochem Sci 34, 230-233.
78. Takayama S, Bimston DN, Matsuzawa S, Freeman BC, Aime-Sempe C, Xie Z, Morimoto RI, Reed JC (1997). BAG-1 modulates the chaperone activity of Hsp70/Hsc70. EMBO J 16, 4887-4896. (Pubitemid 27348398)
79. Takayama S, Reed JC (2001). Molecular chaperone targeting and regulation by BAG family proteins. Nat Cell Biol 3, E237-E241. (Pubitemid 32952248)
80. Terada K, Kanazawa M, Bukau B, Mori M (1997). The human DnaJ homologue dj2 facilitates mitochondrial protein import and luciferase refolding. J Cell Biol 139, 1089-1095. (Pubitemid 27523199)
81. Tzankov S, Wong MJ, Shi K, Nassif C, Young JC (2008). Functional divergence between co-chaperones of Hsc70. J Biol Chem 283, 27100-27109.
82. Vembar SS, Brodsky JL (2008). One step at a time: endoplasmic reticulum-associated degradation. Nat Rev Mol Cell Biol 9, 944-957.
83. Ward CL, Kopito RR (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.
84. Ward CL, Omura S, Kopito RR (1995). Degradation of CFTR by the ubiquitin-proteasome pathway. Cell 83, 121-127.
85. Xiong X, Bragin A, Widdicombe JH, Cohn J, Skach WR (1997). Structural cues involved in endoplasmic reticulum degradation of G85E and G91R mutant cystic fibrosis transmembrane conductance regulator. J Clin Invest 100, 1079-1088. (Pubitemid 27386291)
86. Xiong X, Chong E, Skach WR (1999). Evidence that endoplasmic reticulum (ER)-associated degradation of cystic fibrosis transmembrane conductance regulator is linked to retrograde translocation from the ER membrane. J Biol Chem 274, 2616-2624. (Pubitemid 29075338)
87. Ye Y, Meyer HH, Rapoport TA (2001). The AAA ATPase Cdc48/p97 and its partners transport proteins from the ER into the cytosol. Nature 414, 652-656. (Pubitemid 33151262)
88. Youker RT, Walsh P, Beilharz T, Lithgow T, Brodsky JL (2004). Distinct roles for the Hsp40 and Hsp90 molecular chaperones during cystic fibrosis transmembrane conductance regulator degradation in yeast. Mol Biol Cell 15, 4787-4797. (Pubitemid 39392196)
89. Young JC, Agashe VR, Siegers K, Hartl FU (2004). Pathways of chaperone-mediated protein folding in the cytosol. Nat Rev Mol Cell Biol 5, 781-791. (Pubitemid 39336272)
90. Young JC, Hartl FU (2000). Polypeptide release by Hsp90 involves ATP hydrolysis and is enhanced by the co-chaperone p23. EMBO J 19, 5930-5940.
91. Young JC, Hoogenraad NJ, Hartl FU (2003). Molecular chaperones Hsp90 and Hsp70 deliver preproteins to the mitochondrial import receptor Tom70. Cell 112, 41-50. (Pubitemid 36106417)
92. Younger JM, Chen L, Ren HY, Rosser MF, Turnbull EL, Fan CY, Patterson C, Cyr DM (2006). Sequential quality-control checkpoints triage misfolded cystic fibrosis transmembrane conductance regulator. Cell 126, 571-582. (Pubitemid 44163603)
93. Younger JM, Ren HY, Chen L, Fan CY, Fields A, Patterson C, Cyr DM (2004). A foldable CFTRΔF508 biogenic intermediate accumulates upon inhibition of the Hsc70-CHIP E3 ubiquitin ligase. J Cell Biol 167, 1075-1085. (Pubitemid 40066623)
94. Zhang H, Schmidt BZ, Sun F, Condliffe SB, Butterworth MB, Youker RT, Brodsky JL, Aridor M, Frizzell RA (2006). Cysteine string protein monitors late steps in cystic fibrosis transmembrane conductance regulator biogenesis. J Biol Chem 281, 11312-11321. (Pubitemid 43855556)
95. Zhang Y, Nijbroek G, Sullivan ML, McCracken AA, Watkins SC, Michaelis S, Brodsky JL (2001). Hsp70 molecular chaperone facilitates endoplasmic reticulum-associated protein degradation of cystic fibrosis transmembrane conductance regulator in yeast. Mol Biol Cell 12, 1303-1314. (Pubitemid 33044412)