Hsp70 and Hsp90 multichaperone complexes sequentially regulate thiazide-sensitive cotransporter endoplasmic reticulum-associated degradation and biogenesis

Journal of Biological Chemistry

Volumn 288, Issue 18, 2013, Pages 13124-13135

  Donnelly, Bridget F ^b   Needham, Patrick G ^a   Snyder, Avin C ^b   Roy, Ankita ^b   Khadem, Shaheen ^b,c   Brodsky, Jeffrey L ^a   Subramanya, Arohan R ^b,c  

^a UNIVERSITY OF PITTSBURGH   (United States)

^b UNIVERSITY OF PITTSBURGH SCHOOL OF MEDICINE   (United States)

^c VETERANS AFFAIRS MEDICAL CENTER   (United States)

Author keywords

[No Author keywords available]

Indexed keywords

CHAPERONE SYSTEMS; COMPLEX TOPOLOGY; ENDOPLASMIC RETICULUM; IMMUNOPRECIPITATES; KEY DETERMINANTS; LOWER TEMPERATURES; UBIQUITIN LIGASES; WILD-TYPE PROTEINS;

BIOSYNTHESIS; BLOOD PRESSURE; CELL MEMBRANES; QUALITY CONTROL;

PROTEINS;

CARBOXY TERMINUS OF HSP70 INTERACTING PROTEIN; CHAPERONE; HEAT SHOCK PROTEIN 40; HEAT SHOCK PROTEIN 70; HEAT SHOCK PROTEIN 90; HSP70 HSP90 ORGANIZER PROTEIN; SODIUM CHLORIDE COTRANSPORTER; THIAZIDE DIURETIC AGENT; UBIQUITIN PROTEIN LIGASE E3; UNCLASSIFIED DRUG;

ANIMAL CELL; ARTICLE; BIOGENESIS; CARBOXY TERMINAL SEQUENCE; CELL STRAIN HEK293; COMPLEX FORMATION; CONTROLLED STUDY; ENDOPLASMIC RETICULUM ASSOCIATED DEGRADATION; MASS SPECTROMETRY; MDCK CELL; MUTANT; NONHUMAN; PRIORITY JOURNAL; PROTEIN FOLDING; PROTEIN FUNCTION; QUALITY CONTROL; REGULATORY MECHANISM; TEMPERATURE; WILD TYPE;

CHLORIDE TRANSPORT; ER-ASSOCIATED DEGRADATION; HEAT SHOCK PROTEIN; HSP70; HSP90; NCC; SODIUM TRANSPORT;

ANIMALS; CELL LINE; DOGS; ENDOPLASMIC RETICULUM; HSP70 HEAT-SHOCK PROTEINS; HSP90 HEAT-SHOCK PROTEINS; HUMANS; MICE; MULTIPROTEIN COMPLEXES; PROTEIN FOLDING; PROTEOLYSIS; RECEPTORS, DRUG; SYMPORTERS; UBIQUITIN-PROTEIN LIGASES;

MAMMALIA;

EID: 84877116653     PISSN: 00219258     EISSN: 1083351X     Source Type: Journal    
DOI: 10.1074/jbc.M113.455394     Document Type: Article

References (52)

1. Gamba, G. (2005) Molecular physiology and pathophysiology of electroneutral cation-chloride cotransporters. Physiol. Rev. 85, 423-493
2. ALLHAT Officers and Coordinators for the ALLHAT Collaborative Research Group (2002) Major outcomes in high-risk hypertensive patients randomized to angiotensin-converting enzyme inhibitor or calcium channel blocker vs diuretic. The Antihypertensive and Lipid-Lowering Treatment to Prevent Heart Attack Trial (ALLHAT). JAMA 288, 2981-2997
3. Simon, D. B., Nelson-Williams, C., Bia, M. J., Ellison, D., Karet, F. E., Molina, A. M., Vaara, I., Iwata, F., Cushner, H. M., Koolen, M., Gainza, F. J., Gitleman, H. J., and Lifton, R. P. (1996) Gitelman's variant of Bartter's syndrome, inherited hypokalaemic alkalosis, is caused by mutations in the thiazide-sensitive Na-Cl cotransporter. Nat. Genet. 12, 24-30 (Pubitemid 26011315)
4. Ji, W., Foo, J. N., O'Roak, B. J., Zhao, H., Larson, M. G., Simon, D. B., Newton-Cheh, C., State, M. W., Levy, D., and Lifton, R. P. (2008) Rare independent mutations in renal salt handling genes contribute to blood pressure variation. Nat. Genet. 40, 592-599 (Pubitemid 351601207)
5. Acuña, R., Martínez-de-la-Maza, L., Ponce-Coria, J., Vázquez, N., Ortal-Vite, P., Pacheco-Alvarez, D., Bobadilla, N. A., and Gamba, G. (2011) Rare mutations in SLC12A1 and SLC12A3 protect against hypertension by reducing the activity of renal salt cotransporters. J. Hypertens. 29, 475-483
6. Kunchaparty, S., Palcso, M., Berkman, J., Velázquez, H., Desir, G. V., Bernstein, P., Reilly, R. F., and Ellison, D. H. (1999) Defective processing and expression of thiazide-sensitive Na-Cl cotransporter as a cause of Gitelman's syndrome. Am. J. Physiol. 277, F643-F649 (Pubitemid 29526005)
7. De Jong, J. C., Van Der Vliet, W. A., Van Den Heuvel, L. P., Willems, P. H., Knoers, N. V., and Bindels, R. J. (2002) Functional expression of mutations in the human NaCl cotransporter. Evidence for impaired routing mechanisms in Gitelman's syndrome. J. Am. Soc. Nephrol. 13, 1442-1448 (Pubitemid 34579232)
8. Brodsky, J. L., and Skach, W. R. (2011) Protein folding and quality control in the endoplasmic reticulum. Recent lessons from yeast and mammalian cell systems. Curr. Opin. Cell Biol. 23, 464-475
9. Braakman, I., and Bulleid, N. J. (2011) Protein folding and modification in the mammalian endoplasmic reticulum. Annu. Rev. Biochem. 80, 71-99
10. Needham, P. G., Mikoluk, K., Dhakarwal, P., Khadem, S., Snyder, A. C., Subramanya, A. R., and Brodsky, J. L. (2011) The thiazide-sensitive NaCl cotransporter is targeted for chaperone-dependent endoplasmic reticulum-associated degradation. J. Biol. Chem. 286, 43611-43621
11. 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 (Pubitemid 33044412)
12. Mayer, M. P., and Bukau, B. (2005) Hsp70 chaperones. Cellular functions and molecular mechanism. Cell Mol. Life Sci. 62, 670-684
13. Shaner, L., and Morano, K. A. (2007) All in the family. Atypical Hsp70 chaperones are conserved modulators of Hsp70 activity. Cell Stress Chaperones 12, 1-8 (Pubitemid 47403323)
14. 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
15. Pearl, L. H., and Prodromou, C. (2006) Structure and mechanism of the Hsp90 molecular chaperone machinery. Annu. Rev. Biochem. 75, 271-294 (Pubitemid 44118034)
16. Wandinger, S. K., Richter, K., and Buchner, J. (2008) The Hsp90 chaperone machinery. J. Biol. Chem. 283, 18473-18477
17. Krukenberg, K. A., Street, T. O., Lavery, L. A., and Agard, D. A. (2011) Conformational dynamics of the molecular chaperone Hsp90. Q. Rev. Biophys. 44, 229-255
18. Pratt, W. B., and Toft, D. O. (2003) Regulation of signaling protein function and trafficking by the Hsp90/Hsp70-based chaperone machinery. Exp. Biol. Med. (Maywood) 228, 111-133 (Pubitemid 36187918)
19. Cyr, D. M., Höhfeld, J., and Patterson, C. (2002) Protein quality control. U-box-containing E3 ubiquitin ligases join the fold. Trends Biochem. Sci. 27, 368-375 (Pubitemid 34756520)
20. Subramanya, A. R., Liu, J., Ellison, D. H., Wade, J. B., and Welling, P. A. (2009) WNK4 diverts the thiazide-sensitive NaCl cotransporter to the lysosome and stimulates AP-3 interaction. J. Biol. Chem. 284, 18471-18480
21. Shevchenko, A., Tomas, H., Havlis, J., Olsen, J. V., and Mann, M. (2006) In-gel digestion for mass spectrometric characterization of proteins and proteomes. Nat. Protoc. 1, 2856-2860
22. - cotransporter is mediated by regulation of cotransporter trafficking. Am. J. Physiol. Renal Physiol. 284, F1145-F1154
23. Brodsky, J. L. (2007) The protective and destructive roles played by molecular chaperones during ERAD (endoplasmic-reticulum-associated degradation). Biochem. J. 404, 353-363
24. 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)
25. Younger, J. M., Ren, H. Y., Chen, L., Fan, C. Y., Fields, A., Patterson, C., and Cyr, D. M. (2004) A foldable CFTRΔF508 biogenic intermediate accumulates upon inhibition of the Hsc70-CHIP E3 ubiquitin ligase. J. Cell Biol. 167, 1075-1085 (Pubitemid 40066623)
26. 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 (Pubitemid 32114840)
27. Faresse, N., Ruffieux-Daidie, D., Salamin, M., Gomez-Sanchez, C. E., and Staub, O. (2010) Mineralocorticoid receptor degradation is promoted by Hsp90 inhibition and the ubiquitin-protein ligase CHIP. Am. J. Physiol. Renal Physiol. 299, F1462-F1472
28. 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)
29. McClellan, A. J., Scott, M. D., and Frydman, J. (2005) Folding and quality control of the VHL tumor suppressor proceed through distinct chaperone pathways. Cell 121, 739-748 (Pubitemid 40797596)
30. Felts, S. J., and Toft, D. O. (2003) p23, a simple protein with complex activities. Cell Stress Chaperones 8, 108-113 (Pubitemid 36993176)
31. Whitesell, L., Santagata, S., and Lin, N. U. (2012) Inhibiting HSP90 to treat cancer. A strategy in evolution. Curr. Mol. Med. 12, 1108-1124
32. Bagatell, R., Paine-Murrieta, G. D., Taylor, C. W., Pulcini, E. J., Akinaga, S., Benjamin, I. J., and Whitesell, L. (2000) Induction of a heat shock factor 1-dependent stress response alters the cytotoxic activity of hsp90-binding agents. Clin. Cancer Res. 6, 3312-3318 (Pubitemid 30637762)
33. Ballinger, C. A., Connell, P., Wu, Y., Hu, Z., Thompson, L. J., Yin, L. Y., and 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)
34. Brinker, A., Scheufler, C., Von Der Mulbe, F., Fleckenstein, B., Herrmann, C., Jung, G., Moarefi, I., and Hartl, F. U. (2002) Ligand discrimination by TPR domains. Relevance and selectivity of EEVD-recognition in Hsp70 x Hop x Hsp90 complexes. J. Biol. Chem. 277, 19265-19275 (Pubitemid 34967430)
35. 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 358, 761-764
36. Monette, M. Y., Rinehart, J., Lifton, R. P., and Forbush, B. (2011) Rare mutations in the human Na-K-Cl cotransporter (NKCC2) associated with lower blood pressure exhibit impaired processing and transport function. Am. J. Physiol. Renal. Physiol. 300, F840-F847
37. Wang, X., Koulov, A. V., Kellner, W. A., Riordan, J. R., and Balch, W. E. (2008) Chemical and biological folding contribute to temperature-sensitive ΔF508 CFTR trafficking. Traffic 9, 1878-1893
38. Warmuth, S., Zimmermann, I., and Dutzler, R. (2009) X-ray structure of the C-terminal domain of a prokaryotic cation-chloride cotransporter. Structure 17, 538-546
39. Sabath, E., Meade, P., Berkman, J., de los Heros, P., Moreno, E., Bobadilla, N. A., Vázquez, N., Ellison, D. H., and Gamba, G. (2004) Pathophysiology of functional mutations of the thiazide-sensitive Na-Cl cotransporter in Gitelman disease. Am. J. Physiol. Renal Physiol. 287, F195-F203 (Pubitemid 38943934)
40. Kosano, H., Stensgard, B., Charlesworth, M. C., McMahon, N., and Toft, D. (1998) The assembly of progesterone receptor-Hsp90 complexes using purified proteins. J. Biol. Chem. 273, 32973-32979 (Pubitemid 28557691)
41. Freeman, B. C., Toft, D. O., and Morimoto, R. I. (1996) Molecular chaperone machines. Chaperone activities of the cyclophilin Cyp-40 and the steroid aporeceptor-associated protein p23. Science 274, 1718-1720 (Pubitemid 26414905)
42. Echeverría, P. C., Bernthaler, A., Dupuis, P., Mayer, B., and Picard, D. (2011) An interaction network predicted from public data as a discovery tool. Application to the Hsp90 molecular chaperone machine. PLoS One 6, e26044
43. Yan, F. F., Pratt, E. B., Chen, P. C., Wang, F., Skach, W. R., David, L. L., and Shyng, S. L. (2010) Role of Hsp90 in biogenesis of the β-cell ATP-sensitive potassium channel complex. Mol. Biol. Cell 21, 1945-1954
44. 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 (Pubitemid 28550282)
45. Youker, R. T., Walsh, P., Beilharz, T., Lithgow, T., and Brodsky, J. L. (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)
46. 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, e87-100
47. 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)
48. Buck, T. M., Kolb, A. R., Boyd, C. R., Kleyman, T. R., and Brodsky, J. L. (2010) The endoplasmic reticulum-associated degradation of the epithelial sodium channel requires a unique complement of molecular chaperones. Mol. Biol. Cell 21, 1047-1058
49. Claessen, J. H., Kundrat, L., and Ploegh, H. L. (2012) Protein quality control in the ER. Balancing the ubiquitin checkbook. Trends Cell Biol. 22, 22-32
50. Kundrat, L., and Regan, L. (2010) Balance between folding and degradation for Hsp90-dependent client proteins. A key role for CHIP. Biochemistry 49, 7428-7438
51. Loo, T. W., Bartlett, M. C., and Clarke, D. M. (2008) Correctors promote folding of the CFTR in the endoplasmic reticulum. Biochem. J. 413, 29-36 (Pubitemid 351946859)
52. Krishnamurthy, H., Piscitelli, C. L., and Gouaux, E. (2009) Unlocking the molecular secrets of sodium-coupled transporters. Nature 459, 347-355