The role of the cytosolic HSP70 chaperone system in diseases caused by misfolding and aberrant trafficking of ion channels

DMM Disease Models and Mechanisms

Volumn 7, Issue 3, 2014, Pages 319-329

  Young, Jason C ^a  

^a MCGILL UNIVERSITY   (Canada)

Author keywords

Chaperone; Cystic fibrosis; Degradation; Intracellular trafficking; Long QT syndrome; Protein folding

Indexed keywords

ADENOSINE TRIPHOSPHATASE; CHAPERONE; CYSTIC FIBROSIS TRANSMEMBRANE CONDUCTANCE REGULATOR; DEGENERIN SODIUM CHANNEL; EPITHELIAL SODIUM CHANNEL; HEAT SHOCK COGNATE PROTEIN 70; HEAT SHOCK PROTEIN 70; ION CHANNEL; POTASSIUM CHANNEL HERG; VOLTAGE GATED POTASSIUM CHANNEL;

CELL CYCLE; CELL MIGRATION; CYSTIC FIBROSIS; CYTOSOL; HUMAN; LONG QT SYNDROME; NONHUMAN; PRIORITY JOURNAL; PROTEIN DEGRADATION; PROTEIN FOLDING; REVIEW; ANIMAL; GENETICS; METABOLISM; PROTEIN TRANSPORT; PROTEOSTASIS DEFICIENCY;

ANIMALS; CYSTIC FIBROSIS TRANSMEMBRANE CONDUCTANCE REGULATOR; CYTOSOL; ETHER-A-GO-GO POTASSIUM CHANNELS; HSP70 HEAT-SHOCK PROTEINS; HUMANS; ION CHANNELS; PROTEIN TRANSPORT; PROTEOSTASIS DEFICIENCIES;

EID: 84897133734     PISSN: 17548403     EISSN: 17548411     Source Type: Journal    
DOI: 10.1242/dmm.014001     Document Type: Review

References (98)

1. Akhavan, A., Atanasiu, R., Noguchi, T., Han, W., Holder, N. and Shrier, A. (2005). Identification of the cyclic-nucleotide-binding domain as a conserved determinant of ion-channel cell-surface localization. J. Cell Sci. 118, 2803-2812.
2. Alberti, S., Böhse, K., Arndt, V., Schmitz, A. and Höhfeld, 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. Anderson, C. L., Delisle, B. P., Anson, B. D., Kilby, J. A., Will, M. L., Tester, D. J., Gong, Q., Zhou, Z., Ackerman, M. J. and January, C. T. (2006). Most LQT2 mutations reduce Kv11.1 (hERG) current by a class 2 (trafficking-deficient) mechanism. Circulation 113, 365-373. (Pubitemid 43803197)
4. Arndt, V., Daniel, C., Nastainczyk, W., Alberti, S. and Höhfeld, J. (2005). BAG-2 acts as an inhibitor of the chaperone-associated ubiquitin ligase CHIP. Mol. Biol. Cell 16, 5891-5900. (Pubitemid 41752235)
5. Baaklini, I., Wong, M. J., Hantouche, C., Patel, Y., Shrier, A. and Young, J. C. (2012). The DNAJA2 substrate release mechanism is essential for chaperone-mediated folding. J. Biol. Chem. 287, 41939-41954.
6. Bhangoo, M. K., Tzankov, S., Fan, A. C., Dejgaard, K., Thomas, D. Y. and Young, J. C. (2007). Multiple 40-kDa heat-shock protein chaperones function in Tom70-dependent mitochondrial import. Mol. Biol. Cell 18, 3414-3428. (Pubitemid 47378681)
7. Brelidze, T. I., Gianulis, E. C., DiMaio, F., Trudeau, M. C. and Zagotta, W. N. (2013). Structure of the C-terminal region of an ERG channel and functional implications. Proc. Natl. Acad. Sci. USA 110, 11648-11653.
8. Brychzy, A., Rein, T., Winklhofer, K. F., Hartl, F. U., Young, J. C. and Obermann, W. M. (2003). Cofactor Tpr2 combines two TPR domains and a J domain to regulate the Hsp70/Hsp90 chaperone system. EMBO J. 22, 3613-3623. (Pubitemid 36898338)
9. Caplan, A. J., Cyr, D. M. and Douglas, M. G. (1993). Eukaryotic homologues of Escherichia coli dnaJ: a diverse protein family that functions with hsp70 stress proteins. Mol. Biol. Cell 4, 555-563. (Pubitemid 23183603)
10. Chang, L., Miyata, Y., Ung, P. M., Bertelsen, E. B., McQuade, T. J., Carlson, H. A., Zuiderweg, E. R. and Gestwicki, J. E. (2011). Chemical screens against a reconstituted multiprotein complex: myricetin blocks DnaJ regulation of DnaK through an allosteric mechanism. Chem. Biol. 18, 210-221.
11. Chanoux, R. A., Robay, A., Shubin, C. B., Kebler, C., Suaud, L. and Rubenstein, R. C. (2012). Hsp70 promotes epithelial sodium channel functional expression by increasing its association with coat complex II and its exit from endoplasmic reticulum. J. Biol. Chem. 287, 19255-19265.
12. Cho, H. J., Gee, H. Y., Baek, K. H., Ko, S. K., Park, J. M., Lee, H., Kim, N. D., Lee, M. G. and Shin, I. (2011). A small molecule that binds to an ATPase domain of Hsc70 promotes membrane trafficking of mutant cystic fibrosis transmembrane conductance regulator. J. Am. Chem. Soc. 133, 20267-20276.
13. Choo-Kang, L. R. and Zeitlin, P. L. (2001). Induction of HSP70 promotes DeltaF508 CFTR trafficking. Am. J. Physiol. 281, L58-L68.
14. Chung, K. T., Shen, Y. and Hendershot, L. M. (2002). BAP, a mammalian BiP-associated protein, is a nucleotide exchange factor that regulates the ATPase activity of BiP. J. Biol. Chem. 277, 47557-47563. (Pubitemid 36159275)
15. Connell, P., Ballinger, C. A., Jiang, J., Wu, Y., Thompson, L. J., Höhfeld, J. and Patterson, C. (2001). The co-chaperone CHIP regulates protein triage decisions mediated by heat-shock proteins. Nat. Cell Biol. 3, 93-96. (Pubitemid 32114838)
16. Coppinger, J. A., Hutt, D. M., Razvi, A., Koulov, A. V., Pankow, S., Yates, J. R., III and Balch, W. E. (2012). A chaperone trap contributes to the onset of cystic fibrosis. PLoS ONE 7, e37682.
17. Dai, Q., Qian, S. B., Li, H. H., McDonough, H., Borchers, C., Huang, D., Takayama, S., Younger, J. M., Ren, H. Y., Cyr, D. M. et al. (2005a). Regulation of the cytoplasmic quality control protein degradation pathway by BAG2. J. Biol. Chem. 280, 38673-38681. (Pubitemid 43853770)
18. Dai, Y. S., Xu, J. and Molkentin, J. D. (2005b). The DnaJ-related factor Mrj interacts with nuclear factor of activated T cells c3 and mediates transcriptional repression through class II histone deacetylase recruitment. Mol. Cell. Biol. 25, 9936-9948. (Pubitemid 41572741)
19. Daugaard, M., Rohde, M. and Jäättelä, M. (2007). The heat shock protein 70 family: Highly homologous proteins with overlapping and distinct functions. FEBS Lett. 581, 3702-3710. (Pubitemid 47081009)
20. Davis, P. B. (2006). Cystic fibrosis since 1938. Am. J. Respir. Crit. Care Med. 173, 475-482.
21. Dominguez, L. M. and Dodson, K. M. (2012). Genetics of hearing loss: focus on DFNA2. Appl. Clin. Genet. 5, 97-104.
22. Dragovic, Z., Broadley, S. A., Shomura, Y., Bracher, A. and Hartl, F. U. (2006). Molecular chaperones of the Hsp110 family act as nucleotide exchange factors of Hsp70s. EMBO J. 25, 2519-2528.
23. Du, K., Sharma, M. and Lukacs, G. L. (2005). The DeltaF508 cystic fibrosis mutation impairs domain-domain interactions and arrests post-translational folding of CFTR. Nat. Struct. Mol. Biol. 12, 17-25. (Pubitemid 40082912)
24. Farinha, C. M., Nogueira, P., Mendes, F., Penque, D. and Amaral, M. D. (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.
25. Farrell, P. M. (2008). The prevalence of cystic fibrosis in the European Union. Journal of Cystic Fibrosis 7, 450-453.
26. Ficker, E., Dennis, A. T., Obejero-Paz, C. A., Castaldo, P., Taglialatela, M. and Brown, A. M. (2000). Retention in the endoplasmic reticulum as a mechanism of dominant-negative current suppression in human long QT syndrome. J. Mol. Cell. Cardiol. 32, 2327-2337. (Pubitemid 32039783)
27. Ficker, E., Dennis, A. T., Wang, L. and Brown, A. M. (2003). Role of the cytosolic chaperones Hsp70 and Hsp90 in maturation of the cardiac potassium channel HERG. Circ. Res. 92, e87-e100.
28. Gao, Y., Yechikov, S., Vazquez, A. E., Chen, D. and Nie, L. (2013). Distinct roles of molecular chaperones HSP90á and HSP90â in the biogenesis of KCNQ4 channels. PLoS ONE 8, e57282.
29. Goeckeler, J. L., Petruso, A. P., Aguirre, J., Clement, C. C., Chiosis, G. and Brodsky, J. L. (2008). The yeast Hsp110, Sse1p, exhibits high-affinity peptide binding. FEBS Lett. 582, 2393-2396.
30. Goldberg, A. L. (2003). Protein degradation and protection against misfolded or damaged proteins. Nature 426, 895-899.
31. Goldfarb, S. B., Kashlan, O. B., Watkins, J. N., Suaud, L., Yan, W., Kleyman, T. R. and Rubenstein, R. C. (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.
32. Goloudina, A. R., Demidov, O. N. and Garrido, C. (2012). Inhibition of HSP70: a challenging anti-cancer strategy. Cancer Lett. 325, 117-124.
33. Gong, Q., Jones, M. A. and Zhou, Z. (2006). Mechanisms of pharmacological rescue of trafficking-defective hERG mutant channels in human long QT syndrome. J. Biol. Chem. 281, 4069-4074. (Pubitemid 43847832)
34. Graf, C., Stankiewicz, M., Nikolay, R. and Mayer, M. P. (2010). Insights into the conformational dynamics of the E3 ubiquitin ligase CHIP in complex with chaperones and E2 enzymes. Biochemistry 49, 2121-2129.
35. Grifoni, S. C., McKey, S. E. and Drummond, H. A. (2008). Hsc70 regulates cell surface ASIC2 expression and vascular smooth muscle cell migration. Am. J. Physiol. 294, H2022-H2030.
36. Grove, D. E., Fan, C. Y., Ren, H. Y. and Cyr, D. M. (2011). The endoplasmic reticulum-associated Hsp40 DNAJB12 and Hsc70 cooperate to facilitate RMA1 E3-dependent degradation of nascent CFTRDeltaF508. Mol. Biol. Cell 22, 301-314.
37. Hageman, J., van Waarde, M. A., Zylicz, A., Walerych, D. and Kampinga, H. H. (2011). The diverse members of the mammalian HSP70 machine show distinct chaperone-like activities. Biochem. J. 435, 127-142.
38. Hampton, R. Y. and Sommer, T. (2012). Finding the will and the way of ERAD substrate retrotranslocation. Curr. Opin. Cell Biol. 24, 460-466.
39. Harley, C. A., Jesus, C. S., Carvalho, R., Brito, R. M. and Morais-Cabral, J. H. (2012). Changes in channel trafficking and protein stability caused by LQT2 mutations in the PAS domain of the HERG channel. PLoS ONE 7, e32654.
40. Hartl, F. U., Bracher, A. and Hayer-Hartl, M. (2011). Molecular chaperones in protein folding and proteostasis. Nature 475, 324-332.
41. Hirota, Y., Kurata, Y., Kato, M., Notsu, T., Koshida, S., Inoue, T., Kawata, Y., Miake, J., Bahrudin, U., Li, P. et al. (2008). Functional stabilization of Kv1.5 protein by Hsp70 in mammalian cell lines. Biochem. Biophys. Res. Commun. 372, 469-474.
42. Höhfeld, J. and Jentsch, S. (1997). GrpE-like regulation of the hsc70 chaperone by the anti-apoptotic protein BAG-1. EMBO J. 16, 6209-6216. (Pubitemid 27458341)
43. Höhfeld, J., Minami, Y. and Hartl, F. U. (1995). Hip, a novel cochaperone involved in the eukaryotic Hsc70/Hsp40 reaction cycle. Cell 83, 589-598.
44. Howard, R. J., Clark, K. A., Holton, J. M. and Minor, D. L., Jr (2007). Structural insight into KCNQ (Kv7) channel assembly and channelopathy. Neuron 53, 663-675. (Pubitemid 46283377)
45. Johnson, J. N., Ahrendt, E. and Braun, J. E. (2010). CSPalpha: the neuroprotective J protein. Biochem. Cell Biol. 88, 157-165.
46. Kabani, M., McLellan, C., Raynes, D. A., Guerriero, V. and Brodsky, J. L. (2002). HspBP1, a homologue of the yeast Fes1 and Sls1 proteins, is an Hsc70 nucleotide exchange factor. FEBS Lett. 531, 339-342.
47. Kampinga, H. H. and Craig, E. A. (2010). The HSP70 chaperone machinery: J proteins as drivers of functional specificity. Nat. Rev. Mol. Cell Biol. 11, 579-592.
48. Kapoor, N., Lee, W., Clark, E., Bartoszewski, R., McNicholas, C. M., Latham, C. B., Bebok, Z., Parpura, V., Fuller, C. M., Palmer, C. A. et al. (2011). Interaction of ASIC1 and ENaC subunits in human glioma cells and rat astrocytes. Am. J. Physiol. 300, C1246-C1259.
49. Kellenberger, S. and Schild, L. (2002). Epithelial sodium channel/degenerin family of ion channels: a variety of functions for a shared structure. Physiol. Rev. 82, 735-767. (Pubitemid 34743337)
50. Kharkovets, T., Dedek, K., Maier, H., Schweizer, M., Khimich, D., Nouvian, R., Vardanyan, V., Leuwer, R., Moser, T. and Jentsch, T. J. (2006). Mice with altered KCNQ4 K+ channels implicate sensory outer hair cells in human progressive deafness. EMBO J. 25, 642-652. (Pubitemid 43237670)
51. Kim, H. J., Lv, P., Sihn, C. R. and Yamoah, E. N. (2011). Cellular and molecular mechanisms of autosomal dominant form of progressive hearing loss, DFNA2. J. Biol. Chem. 286, 1517-1527.
52. Leu, J. I., Pimkina, J., Frank, A., Murphy, M. E. and George, D. L. (2009). A small molecule inhibitor of inducible heat shock protein 70. Mol. Cell 36, 15-27.
53. Li, P., Ninomiya, H., Kurata, Y., Kato, M., Miake, J., Yamamoto, Y., Igawa, O., Nakai, A., Higaki, K., Toyoda, F. et al. (2011). Reciprocal control of hERG stability by Hsp70 and Hsc70 with implication for restoration of LQT2 mutant stability. Circ. Res. 108, 458-468.
54. 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.
55. Lu, J. T. and Kass, R. S. (2010). Recent progress in congenital long QT syndrome. Curr. Opin. Cardiol. 25, 216-221.
56. Lukacs, G. L. and Verkman, A. S. (2012). CFTR: folding, misfolding and correcting the ÄF508 conformational defect. Trends Mol. Med. 18, 81-91.
57. Magga, J. M., Jarvis, S. E., Arnot, M. I., Zamponi, G. W. and Braun, J. E. (2000). Cysteine string protein regulates G protein modulation of N-type calcium channels. Neuron 28, 195-204.
58. Matsumura, Y., David, L. L. and Skach, W. R. (2011). Role of Hsc70 binding cycle in CFTR folding and endoplasmic reticulum-associated degradation. Mol. Biol. Cell 22, 2797-2809.
59. Mayer, M. P. and Bukau, B. (2005). Hsp70 chaperones: cellular functions and molecular mechanism. Cell. Mol. Life Sci. 62, 670-684.
60. 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.
61. 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.
62. Morito, D., Hirao, K., Oda, Y., Hosokawa, N., Tokunaga, F., Cyr, D. M., Tanaka, K., Iwai, K. and Nagata, K. (2008). Gp78 cooperates with RMA1 in endoplasmic reticulum-associated degradation of CFTRDeltaF508. Mol. Biol. Cell 19, 1328-1336. (Pubitemid 351805088)
63. Mornon, J. P., Lehn, P. and Callebaut, I. (2009). Molecular models of the open and closed states of the whole human CFTR protein. Cell. Mol. Life Sci. 66, 3469-3486.
64. Ohtsuka, K. and Hata, M. (2000). Mammalian HSP40/DNAJ homologs: cloning of novel cDNAs and a proposal for their classification and nomenclature. Cell Stress Chaperones 5, 98-112.
65. Okiyoneda, T., Barrière, H., Bagdány, M., Rabeh, W. M., Du, K., Höhfeld, J., Young, J. C. and Lukacs, G. L. (2010). Peripheral protein quality control removes unfolded CFTR from the plasma membrane. Science 329, 805-810.
66. Olson, T. M., Alekseev, A. E., Liu, X. K., Park, S., Zingman, L. V., Bienengraeber, M., Sattiraju, S., Ballew, J. D., Jahangir, A. and Terzic, A. (2006). Kv1.5 channelopathy due to KCNA5 loss-of-function mutation causes human atrial fibrillation. Hum. Mol. Genet. 15, 2185-2191. (Pubitemid 43985509)
67. Palleros, D. R., Reid, K. L., Shi, L., Welch, W. J. and Fink, A. L. (1993). ATP-induced protein-Hsp70 complex dissociation requires K+ but not ATP hydrolysis. Nature 365, 664-666. (Pubitemid 23350540)
68. Park, H. J., Mylvaganum, M., McPherson, A., Fewell, S. W., Brodsky, J. L. and Lingwood, C. A. (2009). A soluble sulfogalactosyl ceramide mimic promotes Delta F508 CFTR escape from endoplasmic reticulum associated degradation. Chem. Biol. 16, 461-470.
69. Pearl, L. H. and Prodromou, C. (2006). Structure and mechanism of the Hsp90 molecular chaperone machinery. Annu. Rev. Biochem. 75, 271-294. (Pubitemid 44118034)
70. Powers, M. V., Clarke, P. A. and Workman, P. (2008). Dual targeting of HSC70 and HSP72 inhibits HSP90 function and induces tumor-specific apoptosis. Cancer Cell 14, 250-262.
71. Qiu, X. B., Shao, Y. M., Miao, S. and Wang, L. (2006). The diversity of the DnaJ/Hsp40 family, the crucial partners for Hsp70 chaperones. Cell. Mol. Life Sci. 63, 2560-2570. (Pubitemid 44800711)
72. Ravens, U. and Wettwer, E. (2011). Ultra-rapid delayed rectifier channels: molecular basis and therapeutic implications. Cardiovasc. Res. 89, 776-785.
73. Riordan, J. R. (2008). CFTR function and prospects for therapy. Annu. Rev. Biochem. 77, 701-726.
74. Rossier, B. C., Pradervand, S., Schild, L. and Hummler, E. (2002). Epithelial sodium channel and the control of sodium balance: interaction between genetic and environmental factors. Annu. Rev. Physiol. 64, 877-897. (Pubitemid 34259252)
75. Sahi, C. and Craig, E. A. (2007). Network of general and specialty J protein chaperones of the yeast cytosol. Proc. Natl. Acad. Sci. USA 104, 7163-7168. (Pubitemid 47186026)
76. Sanguinetti, M. C. and Tristani-Firouzi, M. (2006). hERG potassium channels and cardiac arrhythmia. Nature 440, 463-469.
77. Saxena, A., Banasavadi-Siddegowda, Y. K., Fan, Y., Bhattacharya, S., Roy, G., Giovannucci, D. R., Frizzell, R. A. and Wang, X. (2012). Human heat shock protein 105/110 kDa (Hsp105/110) regulates biogenesis and quality control of misfolded cystic fibrosis transmembrane conductance regulator at multiple levels. J. Biol. Chem. 287, 19158-19170.
78. Scheufler, C., Brinker, A., Bourenkov, G., Pegoraro, S., Moroder, L., Bartunik, H., Hartl, F. U. and Moarefi, I. (2000). Structure of TPR domain-peptide complexes: critical elements in the assembly of the Hsp70-Hsp90 multichaperone machine. Cell 101, 199-210. (Pubitemid 32004747)
79. Schmidt, B. Z., Watts, R. J., Aridor, M. and Frizzell, R. A. (2009). Cysteine string protein promotes proteasomal degradation of the cystic fibrosis transmembrane conductance regulator (CFTR) by increasing its interaction with the C terminus of Hsp70-interacting protein and promoting CFTR ubiquitylation. J. Biol. Chem. 284, 4168-4178.
80. Smith, M. H., Ploegh, H. L. and Weissman, J. S. (2011). Road to ruin: targeting proteins for degradation in the endoplasmic reticulum. Science 334, 1086-1090.
81. Szabo, A., Langer, T., Schröder, H., Flanagan, J., Bukau, B. and Hartl, F. U. (1994). The ATP hydrolysis-dependent reaction cycle of the Escherichia coli Hsp70 system DnaK, DnaJ, and GrpE. Proc. Natl. Acad. Sci. USA 91, 10345-10349.
82. Takayama, S. and Reed, J. C. (2001). Molecular chaperone targeting and regulation by BAG family proteins. Nat. Cell Biol. 3, E237-E241. (Pubitemid 32952248)
83. Terada, K., Kanazawa, M., Bukau, B. and Mori, M. (1997). The human DnaJ homologue dj2 facilitates mitochondrial protein import and luciferase refolding. J. Cell Biol. 139, 1089-1095. (Pubitemid 27523199)
84. Tzankov, S., Wong, M. J., Shi, K., Nassif, C. and Young, J. C. (2008). Functional divergence between co-chaperones of Hsc70. J. Biol. Chem. 283, 27100-27109.
85. Ungewickell, E., Ungewickell, H., Holstein, S. E., Lindner, R., Prasad, K., Barouch, W., Martin, B., Greene, L. E. and Eisenberg, E. (1995). Role of auxilin in uncoating clathrin-coated vesicles. Nature 378, 632-635.
86. Vila-Carriles, W. H., Zhou, Z. H., Bubien, J. K., Fuller, C. M. and Benos, D. J. (2007). Participation of the chaperone Hsc70 in the trafficking and functional expression of ASIC2 in glioma cells. J. Biol. Chem. 282, 34381-34391. (Pubitemid 350159465)
87. Walker, V. E., Wong, M. J., Atanasiu, R., Hantouche, C., Young, J. C. and Shrier, A. (2010). Hsp40 chaperones promote degradation of the HERG potassium channel. J. Biol. Chem. 285, 3319-3329.
88. 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. (Pubitemid 44716255)
89. Wang, L., Liu, Y. T., Hao, R., Chen, L., Chang, Z., Wang, H. R., Wang, Z. X. and Wu, J. W. (2011). Molecular mechanism of the negative regulation of Smad1/5 protein by carboxyl terminus of Hsc70-interacting protein (CHIP). J. Biol. Chem. 286, 15883-15894.
90. Ward, C. L., Omura, S. and Kopito, R. R. (1995). Degradation of CFTR by the ubiquitin-proteasome pathway. Cell 83, 121-127.
91. Westhoff, B., Chapple, J. P., van der Spuy, J., Höhfeld, J. and Cheetham, M. E. (2005). HSJ1 is a neuronal shuttling factor for the sorting of chaperone clients to the proteasome. Curr. Biol. 15, 1058-1064. (Pubitemid 40772155)
92. Xu, X., Sarbeng, E. B., Vorvis, C., Kumar, D. P., Zhou, L. and Liu, Q. (2012). Unique peptide substrate binding properties of 110-kDa heat-shock protein (Hsp110) determine its distinct chaperone activity. J. Biol. Chem. 287, 5661-5672.
93. Yamamoto, Y. H., Kimura, T., Momohara, S., Takeuchi, M., Tani, T., Kimata, Y., Kadokura, H. and Kohno, K. (2010). A novel ER J-protein DNAJB12 accelerates ER-associated degradation of membrane proteins including CFTR. Cell Struct. Funct. 35, 107-116.
94. Yang, Y., Li, J., Lin, X., Yang, Y., Hong, K., Wang, L., Liu, J., Li, L., Yan, D., Liang, D. et al. (2009). Novel KCNA5 loss-of-function mutations responsible for atrial fibrillation. J. Hum. Genet. 54, 277-283.
95. Young, J. C. (2010). Mechanisms of the Hsp70 chaperone system. Biochem. Cell Biol. 88, 291-300.
96. Young, J. C., Barral, J. M. and Ulrich Hartl, F. (2003). More than folding: localized functions of cytosolic chaperones. Trends Biochem. Sci. 28, 541-547. (Pubitemid 38366280)
97. 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. (Pubitemid 44163603)
98. Zhang, H., Schmidt, B. Z., Sun, F., Condliffe, S. B., Butterworth, M. B., Youker, R. T., Brodsky, J. L., Aridor, M. and Frizzell, R. A. (2006). Cysteine string protein monitors late steps in cystic fibrosis transmembrane conductance regulator biogenesis. J. Biol. Chem. 281, 11312-11321. (Pubitemid 43855556)