The hERG channel is dependent upon the Hsp90α isoform for maturation and trafficking

Molecular Pharmaceutics

Volumn 9, Issue 6, 2012, Pages 1841-1846

  Peterson, Laura B ^a   Eskew, Jeffrey D ^b   Vielhauer, George A ^b,c   Blagg, Brian S J ^a  

^a UNIVERSITY OF KANSAS   (United States)

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

^c UNIVERSITY OF KANSAS CANCER CENTER   (United States)

Author keywords

hERG; Hsp90; isoform

Indexed keywords

HEAT SHOCK PROTEIN 90 INHIBITOR; POTASSIUM CHANNEL HERG;

ARTICLE; CARDIOTOXICITY; CELL MATURATION; CELL MIGRATION; CONTROLLED STUDY; HUMAN; HUMAN CELL; IMMUNOPRECIPITATION; NUCLEOTIDE SEQUENCE; PRIORITY JOURNAL;

BLOTTING, WESTERN; CELL LINE; DENSITOMETRY; ETHER-A-GO-GO POTASSIUM CHANNELS; HSP90 HEAT-SHOCK PROTEINS; HUMANS; IMMUNOPRECIPITATION; MASS SPECTROMETRY; MODELS, BIOLOGICAL; PROTEIN BINDING; PROTEIN ISOFORMS; PROTEIN TRANSPORT; RNA, SMALL INTERFERING;

EID: 84862004190     PISSN: 15438384     EISSN: 15438392     Source Type: Journal    
DOI: 10.1021/mp300138n     Document Type: Article

References (28)

1. Bishop, S. C.; Burlison, J. A.; Blagg, B. S. J. Hsp90: a novel target for the disruption of multiple signaling cascades. Curr. Cancer Drug Targets 2007, 7, 369-388. (Pubitemid 46849241)
2. Kim, Y. S.; Alarcon, S. V.; Lee, S.; Lee, M. J.; Giaccone, G.; Neckers, L.; Trepel, J. B. Update on Hsp90 inhibitors in clinical trial. Curr. Top. Med. Chem. 2009, 9, 1479-1492.
3. Biamonte, M. A.; Van de Water, R.; Arndt, J. W.; Scannevin, R. H.; Perret, D.; Lee, W. Heat shock protein 90: inhibitors in clinical trials. J. Med. Chem. 2010, 53, 3-17.
4. Chen, B.; Piel, W. H.; Gui, L.; Bruford, E.; Monteiro, A. The HSP90 family of genes in the human genome: Insights into their divergence and evolution. Genomics 2005, 86, 627-637. (Pubitemid 41752943)
5. Johnson, J. L. Evolution and function of diverse Hsp90 homologs and cochaperone proteins. Biochim. Biophys. Acta, Mol. Cell Res. 2012, 1823, 607-613.
6. Perrin, M. J.; Subbiah, R. N.; Vandenberg, J. I.; Hill, A. P. Human ether-a-go-go related gene (hERG) K+ channels: Function and dysfunction. Prog. Biophys. Mol. Biol. 2008, 98, 137-148.
7. Vandenberg, J. I.; Walker, B. D.; Campbell, T. J. HERG K+ channels: friend and foe. Trends Pharmacol. Sci. 2001, 22, 240-246.
8. Ficker, E.; Dennis, A. T.; Wang, L.; Brown, A. M. Role of the cytosolic chaperones Hsp70 and Hsp90 in maturation of the cardiac potassium channel hERG. Circ. Res. 2003, 92, e87-e100.
9. Nanduri, J.; Bergson, P.; Wang, N.; Ficker, E.; Prabhakar, N. R. Hypoxia inhibits maturation and trafficking of hERG K+ channel protein: Role of Hsp90 and ROS. Biochem. Bioph. Res. Commum. 2009, 388, 212-216.
10. Fermini, B.; Fossa, A. A. The impact of drug-induced QT interval prolongation on drug discovery and development. Nat. Rev. Drug Discovery 2003, 2, 439-447. (Pubitemid 37361725)
11. Brown, A. M. hERG Assay, QT Liability, and Sudden Cardiac Death. In Cardiac Safety of Noncardiac Drugs; Humana Press: 2005; pp 67-81.
12. Wible, B. A.; Hawryluk, P.; Ficker, E.; Kuryshev, Y. A.; Kirsch, G.; Brown, A. M. HERG-Lite: A novel comprehensive high-throughput screen for drug-induced hERG risk. J. Pharmacol. Toxicol. 2005, 52, 136-145. (Pubitemid 41008637)
13. Zhou, Z.; Gong, Q.; Ye, B.; Fan, Z.; Makielski, J. C.; Robertson, G. A.; January, C. T. Properties of HERG channels stably expressed in HEK 293 cells studied at physiological temperature. Biophys. J. 1998, 74, 230-241. (Pubitemid 28041752)
14. Walker, V. E.; Atanasiu, R.; Lam, H.; Shrier, A. Co-chaperone FKBP38 Promotes HERG Trafficking. J. Biol. Chem. 2007, 282, 23509-23516. (Pubitemid 47311946)
15. Ficker, E.; Dennis, A. T.; Kuryshev, Y. A.; Wible, B. A.; Brown, A. M. hERG channel trafficking. Novartis Found. Symp. 2005, 266, 57-74.
16. Petrecca, K.; Atanasiu, R.; Akhavan, A.; Shrier, A. N-linked glycosylation sites determine HERG channel surface membrane expression. J. Physiol. 1999, 515, 41-48. (Pubitemid 29092619)
17. Gong, Q.; Anderson, C. L.; January, C. T.; Zhou, Z. Role of glycosylation in cell surface expression and stability of HERG potassium channels. Am. J. Physiol. 2002, 283, H77-H84. (Pubitemid 34705326)
18. Riggs, D. L.; Cox, M. B.; Cheung-Flynn, J.; Prapapanich, V.; Carrigan, P. E.; Smith, D. F. Functional Specificity of Co-Chaperone Interactions with Hsp90 Client Proteins. Crit. Rev. Biochem. Mol. Biol. 2004, 39, 279-295. (Pubitemid 40089517)
19. Dmochewitz, L.; Lillich, M.; Kaiser, E.; Jennings, L. D.; Lang, A. E.; Buchner, J.; Fischer, G.; Aktories, K.; Collier, R. J.; Barth, H. Role of CypA and Hsp90 in membrane translocation mediated by anthrax protective antigen. Cell. Microbiol. 2011, 13, 359-373.
20. Kaiser, E.; Kroll, C.; Ernst, K.; Schwan, C.; Popoff, M.; Fischer, G.; Buchner, J.; Aktories, K.; Barth, H. Membrane Translocation of Binary Actin-ADP-Ribosylating Toxins from Clostridium difficile and Clostridium perfringens Is Facilitated by Cyclophilin A and Hsp90. Infect. Immun. 2011, 79, 3913-3921.
21. Didelot, C.; Lanneau, D.; Brunet, M.; Bouchot, A.; Cartier, J.; Jacquel, A.; Ducoroy, P.; Cathelin, S.; Decologne, N.; Chiosis, G.; Dubrez-Daloz, L.; Solary, E.; Garrido, C. Interaction of heat-shock protein 90β isoform (HSP90β) with cellular inhibitor of apoptosis 1 (c-IAP1) is required for cell differentiation. Cell Death Differ. 2008, 15, 859-866. (Pubitemid 351524428)
22. Houlihan, J. L.; Metzler, J. J.; Blum, J. S. HSP90α and HSP90β Isoforms Selectively Modulate MHC Class II Antigen Presentation in B Cells. J. Immunol. 2009, 182, 7451-7458.
23. Kunisawa, J.; Shastri, N. Hsp90α Chaperones Large CTerminally Extended Proteolytic Intermediates in the MHC Class I Antigen Processing Pathway. Immunity 2006, 24, 523-534. (Pubitemid 43728158)
24. Voss, A. K.; Thomas, T.; Gruss, P. Mice lacking HSP90β fail to develop a placental labyrinth. Development 2000, 127, 1-11. (Pubitemid 30064383)
25. Eustace, B. K.; Sakurai, T.; Stewart, J. K.; Yimlamai, D.; Unger, C.; Zehetmeier, C.; Lain, B.; Torella, C.; Henning, S. W.; Beste, G.; Scroggins, B. T.; Neckers, L.; Ilag, L. L.; Jay, D. G. Functional proteomic screens reveal an essential extracellular role for hsp90α in cancer cell invasiveness. Nat. Cell Biol. 2004, 6, 507-514. (Pubitemid 38786593)
26. Chadli, A.; Felts, S. J.; Toft, D. O. GCUNC45 is the first Hsp90 co-chaperone to show α/β isoform specificity. J. Biol. Chem. 2008, 283, 9509-9512.
27. Millson, S. H.; Prodromou, C.; Piper, P. W. A simple yeastbased system for analyzing inhibitor resistance in the human cancer drug targets Hsp90α/β. Biochem. Pharmacol. 2010, 79, 1581-1588.
28. Millson, S. H.; Truman, A. W.; Rácz, A.; Hu, B.; Panaretou, B.; Nuttall, J.; Mollapour, M.; Söti, C.; Piper, P. W. Expressed as the sole Hsp90 of yeast, the α and β isoforms of human Hsp90 differ with regard to their capacities for activation of certain client proteins, whereas only Hsp90β generates sensitivity to the Hsp90 inhibitor radicicol. FEBS J. 2007, 274, 4453-4463.