Role of Hsp90 in biogenesis of the β-cell ATP-sensitive potassium channel complex

Molecular Biology of the Cell

Volumn 21, Issue 12, 2010, Pages 1945-1954

  Yan, Fei Fei ^a,b   Pratt, Emily B ^a   Chen, Pei Chun ^a   Wang, Fang ^a   Skach, William R ^a   David, Larry L ^a   Shyng, Show Ling ^a  

^a OREGON HEALTH AND SCIENCE UNIVERSITY   (United States)

^b SIBS Novo Nordisk Translational Research Centre for PreDiabetes   (China)

Author keywords

[No Author keywords available]

Indexed keywords

ADENOSINE TRIPHOSPHATE; HEAT SHOCK PROTEIN 40; HEAT SHOCK PROTEIN 70; HEAT SHOCK PROTEIN 90; INWARDLY RECTIFYING POTASSIUM CHANNEL SUBUNIT KIR6.2; POTASSIUM CHANNEL; SULFONYLUREA RECEPTOR 1; ABC TRANSPORTER; ABCC8 PROTEIN, RAT; ADENOSINE TRIPHOSPHATE SENSITIVE POTASSIUM CHANNEL; BENZOQUINONE DERIVATIVE; DRUG RECEPTOR; INWARDLY RECTIFYING POTASSIUM CHANNEL; MACROCYCLIC LACTAM; MUTANT PROTEIN; PROTEIN BINDING; PROTEIN SUBUNIT; SULFONYLUREA RECEPTOR; TANESPIMYCIN;

ARTICLE; BIOGENESIS; CELL MEMBRANE; COMPLEX FORMATION; CONTROLLED STUDY; GENE MUTATION; IMMUNOPRECIPITATION; NUCLEOTIDE SEQUENCE; PRIORITY JOURNAL; PROTEIN ANALYSIS; PROTEIN EXPRESSION; ANIMAL; ANTAGONISTS AND INHIBITORS; BIOSYNTHESIS; DRUG EFFECTS; GENETIC TRANSFECTION; HAMSTER; METABOLISM; PANCREAS ISLET BETA CELL; PROTEIN SUBUNIT; RAT;

ANIMALS; ATP-BINDING CASSETTE TRANSPORTERS; BENZOQUINONES; CELL MEMBRANE; CRICETINAE; HSP90 HEAT-SHOCK PROTEINS; INSULIN-SECRETING CELLS; KATP CHANNELS; LACTAMS, MACROCYCLIC; MUTANT PROTEINS; POTASSIUM CHANNELS, INWARDLY RECTIFYING; PROTEIN BINDING; PROTEIN SUBUNITS; RATS; RECEPTORS, DRUG; SULFONYLUREA RECEPTORS; TRANSFECTION;

EID: 77953507086     PISSN: 10591524     EISSN: None     Source Type: Journal    
DOI: 10.1091/mbc.E10-02-0116     Document Type: Article

References (43)

1. Aguilar-Bryan, L., and Bryan, J. (1999). Molecular biology of adenosine triphosphate-sensitive potassium channels. Endocr. Rev. 20, 101-135.
2. Ashcroft, F. M. (2005). ATP-sensitive potassium channelopathies: focus on insulin secretion. J. Clin. Invest. 115, 2047-2058.
3. Balch, W. E., Morimoto, R. I., Dillin, A., and Kelly, J. W. (2008). Adapting proteostasis for disease intervention. Science 319, 916-919.
4. Cartier, E. A., Conti, L. R., Vandenberg, C. A., and Shyng, S. L. (2001). Defective trafficking and function of KATP channels caused by a sulfonylurea receptor 1 mutation associated with persistent hyperinsulinemic hypoglycemia of infancy. Proc. Natl. Acad. Sci. USA 98, 2882-2887.
5. Chene, P. (2002). ATPases as drug targets: learning from their structure. Nat. Rev. 1, 665-673.
6. Conti, L. R., Radeke, C. M., Shyng, S. L., and Vandenberg, C. A. (2001). Transmembrane topology of the sulfonylurea receptor SUR1. J. Biol. Chem. 276, 41270-41278.
7. 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. Circulation Res. 92, e87-e100.
8. Flanagan, S. E., Clauin, S., Bellanne-Chantelot, C., de Lonlay, P., Harries, L. W., Gloyn, A. L., and Ellard, S. (2009). Update of mutations in the genes encoding the pancreatic beta-cell K(ATP) channel subunits Kir6.2 (KCNJ11) and sulfonylurea receptor 1 (ABCC8) in diabetes mellitus and hyperinsulinism. Hum. Mutat. 30, 170-180.
9. Higgins, C. F. (1995). The ABC of channel regulation. Cell 82, 693-696.
10. Hohmeier, H. E., BeltrandelRio, H., Clark, S. A., Henkel-Rieger, R., Normington, K., and Newgard, C. B. (1997). Regulation of insulin secretion from novel engineered insulinoma cell lines. Diabetes 46, 968-977. (Pubitemid 27220996)
11. Inagaki, N., Gonoi, T., Clement, J.P.t., Namba, N., Inazawa, J., Gonzalez, G., Aguilar-Bryan, L., Seino, S., and Bryan, J. (1995). Reconstitution of IKATP: an inward rectifier subunit plus the sulfonylurea receptor. Science 270, 1166-1170.
12. Kamal, A., Thao, L., Sensintaffar, J., Zhang, L., Boehm, M. F., Fritz, L. C., and Burrows, F. J. (2003). A high-affinity conformation of Hsp90 confers tumour selectivity on Hsp90 inhibitors. Nature 425, 407-410.
13. Keller, A., Nesvizhskii, A. I., Kolker, E., and Aebersold, R. (2002). Empirical statistical model to estimate the accuracy of peptide identifications made by MS/MS and database search. Anal. Chem. 74, 5383-5392.
14. Lin, C. W., Lin, Y. W., Yan, F. F., Casey, J., Kochhar, M., Pratt, E. B., and Shyng, S. L. (2006). Kir6.2 mutations associated with neonatal diabetes reduce expression of ATP-sensitive K+ channels: implications in disease mechanism and sulfonylurea therapy. Diabetes 55, 1738-1746.
15. Lin, C. W., Yan, F., Shimamura, S., Barg, S., and Shyng, S. L. (2005). Membrane phosphoinositides control insulin secretion through their effects on ATP-sensitive K+ channel activity. Diabetes 54, 2852-2858.
16. Lin, Y. W., Bushman, J. D., Yan, F. F., Haidar, S., MacMullen, C., Ganguly, A., Stanley, C. A., and Shyng, S. L. (2008). Destabilization of ATP-sensitive potassium channel activity by novel KCNJ11 mutations identified in congenital hyperinsulinism. J. Biol. Chem. 283, 9146-9156.
17. 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)
18. Minami, K., Miki, T., Kadowaki, T., and Seino, S. (2004). Roles of ATP-sensitive K+ channels as metabolic sensors: studies of Kir6.x null mice. Diabetes 53 (suppl 3), S176-S180.
19. Nathan, D. F., Vos, M. H., and Lindquist, S. (1997). In vivo functions of the Saccharomyces cerevisiae Hsp90 chaperone. Proc. Natl. Acad. Sci. USA 94, 12949-12956.
20. Neagoe, I., and Schwappach, B. (2005). Pas de deux in groups of four-the biogenesis of KATP channels. J. Mol. Cell. Cardiol. 38, 887-894.
21. Nesvizhskii, A. I., Keller, A., Kolker, E., and Aebersold, R. (2003). A statistical model for identifying proteins by tandem mass spectrometry. Anal. Chem. 75, 4646-4658.
22. Nichols, C. G. (2006). KATP channels as molecular sensors of cellular metabolism. Nature 440, 470-476.
23. Pearl, L. H., and Prodromou, C. (2000). Structure and in vivo function of Hsp90. Curr. Opin. Struct. Biol. 10, 46-51.
24. Pearl, L. H., and Prodromou, C. (2006). Structure and mechanism of the Hsp90 molecular chaperone machinery. Annu. Rev. Biochem. 75, 271-294.
25. Powers, E. T., Morimoto, R. I., Dillin, A., Kelly, J. W., and Balch, W. E. (2009). Biological and chemical approaches to diseases of proteostasis deficiency. Annu. Rev. Biochem. 78, 959-991.
26. Pratt, E. B., Yan, F. F., Gay, J. W., Stanley, C. A., and Shyng, S. L. (2009). Sulfonylurea receptor 1 mutations that cause opposite insulin secretion defects with chemical chaperone exposure. J. Biol. Chem. 284, 7951-7959.
27. Rowe, S. M., Miller, S., and Sorscher, E. J. (2005). Cystic fibrosis. N. Engl. J. Med. 352, 1992-2001.
28. Shyng, S. L., Ferrigni, T., Shepard, J. B., Nestorowicz, A., Glaser, B., Permutt, M. A., and Nichols, C. G. (1998). Functional analyses of novel mutations in the sulfonylurea receptor 1 associated with persistent hyperinsulinemic hypoglycemia of infancy. Diabetes 47, 1145-1151.
29. Solit, D. B., and Rosen, N. (2006). Hsp 90, a novel target for cancer therapy. Curr. Top. Med. Chem. 6, 1205-1214.
30. Sreedhar, A. S., Kalmar, E., Csermely, P., and Shen, Y. F. (2004). Hsp90 isoforms: functions, expression and clinical importance. FEBS Lett. 562, 11-15.
31. Taschenberger, G., Mougey, A., Shen, S., Lester, L. B., LaFranchi, S., and Shyng, S. L. (2002). Identification of a familial hyperinsulinism-causing mutation in the sulfonylurea receptor 1 that prevents normal trafficking and function of KATP channels. J. Biol. Chem. 277, 17139-17146.
32. Tucker, S. J., Gribble, F. M., Zhao, C., Trapp, S., and Ashcroft, F. M. (1997). Truncation of Kir6.2 produces ATP-sensitive K+ channels in the absence of the sulphonylurea receptor. Nature 387, 179-183.
33. Tusnady, G. E., Sarkadi, B., Simon, I., and Varadi, A. (2006). Membrane topology of human ABC proteins. FEBS Lett. 580, 1017-1022.
34. Vasiliou, V., Vasiliou, K., and Nebert, D. W. (2009). Human ATP-binding cassette (ABC) transporter family. Hum. Genomics 3, 281-290.
35. Walker, V. E., Atanasiu, R., Lam, H., and Shrier, A. (2007). Co-chaperone FKBP38 promotes HERG trafficking. J. Biol. Chem. 282, 23509-23516.
36. Wang, X., et al. (2006). Hsp90 cochaperone Aha1 downregulation rescues misfolding of CFTR in cystic fibrosis. Cell 127, 803-815.
37. Welch, W. J. (2004). Role of quality control pathways in human diseases involving protein misfolding. Semin. Cell Dev. Biol. 15, 31-38.
38. Yan, F., Lin, C. W., Weisiger, E., Cartier, E. A., Taschenberger, G., and Shyng, S. L. (2004). Sulfonylureas correct trafficking defects of ATP-sensitive potassium channels caused by mutations in the sulfonylurea receptor. J. Biol. Chem. 279, 11096-11105.
39. Yan, F. F., Lin, C. W., Cartier, E. A., and Shyng, S. L. (2005). Role of ubiquitin-proteasome degradation pathway in biogenesis efficiency of {beta}-cell ATP-sensitive potassium channels. Am J. Physiol. Cell Physiol. 289, C1351-C1359.
40. Yan, F. F., Lin, Y. W., MacMullen, C., Ganguly, A., Stanley, C. A., and Shyng, S. L. (2007). Congenital hyperinsulinism associated ABCC8 mutations that cause defective trafficking of ATP-sensitive K+ channels: identification and rescue. Diabetes 56, 2339-2348.
41. Yang, B., Zhao, D., and Verkman, A. S. (2009). Hsp90 inhibitor partially corrects nephrogenic diabetes insipidus in a conditional knock-in mouse model of aquaporin-2 mutation. FASEB J. 23, 503-512.
42. Young, J. C., Moarefi, I., and Hartl, F. U. (2001). Hsp 90, a specialized but essential protein-folding tool. J. Cell Biol. 154, 267-273.
43. Zerangue, N., Schwappach, B., Jan, Y. N., and Jan, L. Y. (1999). A new ER trafficking signal regulates the subunit stoichiometry of plasma membrane K(ATP) channels. Neuron 22, 537-548. (Pubitemid 29159852)