Specific serine proteases selectively damage KCNH2 (hERG1) potassium channels and IKr

American Journal of Physiology - Heart and Circulatory Physiology

Volumn 290, Issue 3, 2006, Pages

  Rajamani, Sridharan ^a   Anderson, Corey L ^a   Valdivia, Carmen R ^a   Eckhardt, Lee L ^a   Foell, Jason D ^a   Robertson, Gail A ^b   Kamp, Timothy J ^a,b   Makielski, Jonathan C ^a,b   Anson, Blake D ^a   January, Craig T ^a,b,c  

^a UNIVERSITY OF WISCONSIN SCHOOL OF MEDICINE AND PUBLIC HEALTH   (United States)

^b UNIVERSITY OF WISCONSIN MADISON   (United States)

^c University of Wisconsin Health   (United States)

Author keywords

Enzymes; Myocyte isolation; Rapidly activating delayed rectifier potassium current

Indexed keywords

POTASSIUM CHANNEL HERG; PROTEIN KNCH2; SERINE PROTEINASE; UNCLASSIFIED DRUG; KCNH2 PROTEIN, HUMAN; POTASSIUM;

ARTICLE; CELL ISOLATION; CELL STRAIN HEK293; ELECTROPHYSIOLOGY; MUSCLE CELL; PRIORITY JOURNAL; PROTEIN DEGRADATION; ANIMAL; CELL CULTURE; CELL MEMBRANE POTENTIAL; CHANNEL GATING; COMPARATIVE STUDY; DOG; DRUG EFFECT; HEART MUSCLE CELL; METABOLISM; PHYSIOLOGY;

ANIMALS; CELLS, CULTURED; DOGS; ETHER-A-GO-GO POTASSIUM CHANNELS; ION CHANNEL GATING; MEMBRANE POTENTIALS; MYOCYTES, CARDIAC; POTASSIUM; SERINE ENDOPEPTIDASES;

EID: 33645729724     PISSN: 03636135     EISSN: 15221539     Source Type: Journal    
DOI: 10.1152/ajpheart.00777.2005     Document Type: Article

References (58)

1. Anson BD, Ackerman MJ, Tester DJ, Will ML, Delisle BP, Anderson CL, and January CT. Molecular and functional characterization of common polymorphisms in HERG (KCNH2) potassium channels. Am J Physiol Heart Circ Physiol 286: H2434-H2441, 2004.
2. Armstrong CE and Roberts WM. Electrical properties of frog saccular hair cells: distortion by enzymatic dissociation. J Neurosci 18: 2962-2973, 1998.
3. Armstrong CM, Bezanilla F, and Rojas E. Destruction of sodium conductance inactivation in squid axons perfused with pronase. J Gen Physiol 62: 375-391, 1973.
4. Ks cardiac potassium current. Nature 384: 78-80, 1996.
5. + currents in isolated human ventricular myocytes from patients with terminal heart failure. Circ Res 73: 379-385, 1993.
6. h) in neocortical neurons is blocked by external proteolysis and internal TEA. J Neurophysiol 72: 2737-2742, 1994.
7. Chapman RE and Spinale FG. Extracellular protease activation and unraveling of the myocardial interstitium: critical steps toward clinical applications. Am J Physiol Heart Circ Physiol 286: H1-H10, 2004.
8. Cohen AW, Hnasko R, Schubert W, and Lisanti MP. Role of caveolae and caveolins in health and disease. Physiol Rev 84: 1341-1379, 2004.
9. Dani AM, Cittadini A, Flamini G, Festuccia G, and Terranova T. Preparation and some properties of isolated beating myocytes from adult rabbit heart. J Mol Cell Cardiol 9: 777-784, 1977.
10. Delisle BP, Anderson CL, Balijepalli RC, Anson BD, Kamp TJ, and January CT. Thapsigargin selectively rescues the trafficking defective LQT2 channels G601S and F805C. J Biol Chem 278: 35749-35754, 2003.
11. Donaldson SH, Hirsh A, Li DC, Holloway G, Chao J, Boucher RC, and Gabriel SE. Regulation of the epithelial sodium channel by serine proteases in human airways. J Biol Chem 277: 8338-8345, 2002.
12. Ebeling W, Hennrich N, Klockow M, Metz H, Orth HD, and Lang H. Proteinase K from Tritirachium album Limber. Eur J Biochem 47: 91-97, 1974.
13. Eckhardt LL, Hammill D, Tester DJ, Rajagopal HN, Rodriguez E, Kanter R, Glatter K, Park JK, Makielski JC, and Ackerman MJ. Molecular and functional characterization of a novel KCNJ2 mutation, R82W, associated with a distinct arrhythmogenic phenotype. Circulation 108: 120, 2003.
14. Ellgaard L, Molinari M, and Helenius A. Setting the standards: quality control in the secretory pathway. Science 286: 1882-1888, 1999.
15. Farmer BB, Harris RA, Jolly WW, Hathaway DR, Katzberg A, Watanabe AM, Whitlow AL, and Besch HR Jr. Isolation and characterization of adult rat hearts cells. Arch Biochem Biophys 179: 545-558, 1977.
16. Foell JD, Balijepalli RC, Delisle BP, Yunker AM, Robia SL, Walker JW, McEnery MW, January CT, and Kamp TJ. Molecular heterogeneity of calcium channel β-subunits in canine and human heart: evidence for differential subcellular localization. Physiol Genomics 17: 183-200, 2004.
17. Gong Q, Anderson CL, January CT, and Zhou Z. Role of glycosylation in cell surface expression and stability of HERG potassium channels. Am J Physiol Heart Circ Physiol 283: H77-H84, 2002.
18. Gong Q, Keeney DR, Molinari M, and Zhou Z. Degradation of trafficking-defective long QT syndrome type II mutant channels by the ubiquitin-proteasome pathway. J Biol Chem 280: 19419-19425, 2005.
19. Green WN. Ion channel assembly: creating structures that function. J Gen Physiol 113: 163-170, 1999.
20. Hamill OP, Marty A, Neher E, Sakmann B, and Sigworth FJ. Improved patch-clamp techniques for high-resolution current recording from cells and cell-free membrane patches. Pflügers Arch 391: 85-100, 1981.
21. Harary I and Farley B. In vitro studies of single isolated beating heart cells. Science 131: 1674-1675, 1960.
22. + channel inactivation gating. Circ Res 75: 114-122, 1994.
23. Haworth RA, Goknur AB, Warner TF, and Berkoff HA. Some determinants of quality and yield in the isolation of adult heart cells from rat. Cell Calcium 10: 57-62, 1989.
24. Herzberg IM, Trudeau MC, and Robertson GA. Transfer of rapid inactivation and sensitivity to the class III antiarrhythmic drug E-4031 from HERG to M-eag channels. J Physiol 511: 3-14, 1998.
25. Hoshi T, Zagotta WN, and Aldrich RW. Biophysical and molecular mechanisms of Shaker potassium channel inactivation. Science 250: 533-538, 1990.
26. Kr channels minimally comprise hERG 1a and 1b subunits. J Biol Chem 279: 44690-44694, 2004.
27. + currents in nonfailing human hearts. Similarities between right septal subendocardial and left subepicardial ventricular myocytes. Circulation 92: 1179-1187, 1995.
28. Kraut J. Serine proteases: structure and mechanism of catalysis. Annu Rev Biochem 46: 331-358, 1977.
29. + current in human ventricular myocytes. Circ Res 78: 689-696, 1996.
30. Lippincott-Schwartz J. Dynamics of secretory membrane trafficking. Ann NY Acad Sci 1038: 115-124, 2004.
31. Ks contributes to the longer action potential of the M cell. Circ Res 76: 351-365, 1995.
32. Liu J, Zhang M, Jiang M, and Tseng GN. Structural and functional role of the extracellular s5-p linker in the HERG potassium channel. J Gen Physiol 120: 723-737, 2002.
33. Lopez-Otin C and Overall CM. Protease degradomics: a new challenge for proteomics. Nat Rev Mol Cell Biol 3: 509-519, 2002.
34. Mitra R and Morad M. A uniform enzymatic method for dissociation of myocytes from hearts and stomachs of vertebrates. Am J Physiol Heart Circ Physiol 249: H1056-H1060, 1985.
35. Pardo-Lopez L, Zhang M, Liu J, Jiang M, Possani LD, and Tseng GN. Mapping the binding site of a human ether-a-go-go-related gene-specific peptide toxin (ErgTx) to the channel's outer vestibule. J Biol Chem 277: 16403-16411, 2002.
36. Peeters GA, Sanguinetti MC, Eki Y, Konarzewska H, Renlund DG, Karwande SV, and Barry WH. Method for isolation of human ventricular myocytes from single endocardial and epicardial biopsies. Am J Physiol Heart Circ Physiol 268: H1757-H1764, 1995.
37. Kr channels in rat, mouse, and human heart. Trends Cardiovasc Med 11: 286-294, 2001.
38. Rajamani S, Kilby J, Slind J, Balijepalli RC, Anderson CL, Anson BD, Kamp TJ, and January CT. N-linked glycosylation is not obligatory for rescue of trafficking-defective LQT2 mutations. Pacing Clin Electrophysiol 2, Suppl 1: S107, 2005.
39. + channel long-QT2 mutations: human ethera-go-go-related gene rescue without block. Circulation 105: 2830-2835, 2002.
40. Kr and KCNH2 (HERG) channels by extracellular proteases (Abstract). Biophys J 86: 134A, 2004.
41. Rawlings ND, O'Brien E, and Barrett AJ. MEROPS: the protease database. Nucleic Acids Res 30: 343-346, 2002.
42. Robertson GA, Warmke JM, and Ganetzky B. Potassium currents expressed from Drosophila and mouse eag cDNAs in Xenopus oocytes. Neuropharmacology 35: 841-850, 1996.
43. Ks potassium channel. Nature 384: 80-83, 1996.
44. Kr potassium channel. Cell 81: 299-307, 1995.
45. + current. Differential sensitivity to block by class III antiarrhythmic agents. J Gen Physiol 96: 195-215, 1990.
46. Schaffer P, Pelzmann B, Bernhart E, Lang P, Machler H, Rigler B, and Koidl B. Repolarizing currents in ventricular myocytes from young patients with tetralogy of Fallot. Cardiovasc Res 43: 332-343, 1999.
47. Sheets MF, January CT, and Fozzard HA. Isolation and characterization of single canine cardiac purkinje cells. Circ Res 53: 544-548, 1983.
48. Stauber WT, January CT, and Schottelius BA. Potentials in mammalian skeletal muscle from collagenase-treated tissue. Experientia 33: 1614-1615, 1977.
49. Swiatecka-Urban A, Duhaime M, Coutermarsh B, Karlson KH, Collawn J, Milewski M, Cutting GR, Guggino WB, Langford G, and Stanton BA. PDZ domain interaction controls the endocytic recycling of the cystic fibrosis transmembrane conductance regulator. J Biol Chem 277: 40099-40105, 2002.
50. Trudeau MC, Warmke JW, Ganetzky B, and Robertson GA. HERG, a human inward rectifier in the voltage-gated potassium channel family. Science 269: 92-95, 1995.
51. Vahouny GV, Wei R, Starkweather R, and Davis C. Preparation of beating heart cells from adult rats. Science 167: 1616-1618, 1970.
52. Valdivia CR, Ackerman MJ, Tester DJ, Wada T, McCormack J, Ye B, and Makielski JC. A novel SCN5A arrhythmia mutation, M1766L, with expression defect rescued by mexiletine. Cardiovasc Res 55: 279-289, 2002.
53. Warmke JW and Ganetzky B. A family of potassium channel genes related to eag in Drosophila and mammals. Proc Natl Acad Sci USA 91: 3438-3442, 1994.
54. + channel from human atrium. Circ Res 76: 343-350, 1995.
55. Yue L, Feng J, Li GR, and Nattel S. Transient outward and delayed rectifier currents in canine atrium: properties and role of isolation methods. Am J Physiol Heart Circ Physiol 270: H2157-H2168, 1996.
56. Zhang S, Rajamani S, Chen Y, Gong Q, Rong Y, Zhou Z, Ruoho A, and January CT. Cocaine blocks HERG, but not KvLQT1 + minK, potassium channels. Mol Pharmacol 59: 1069-1076, 2001.
57. Zhou Z, Gong Q, Epstein ML, and January CT. HERG channel dysfunction in human long QT syndrome. Intracellular transport and functional defects. J Biol Chem 273: 21061-21066, 1998.
58. Zhou Z, Gong Q, Ye B, Fan Z, Makielski JC, Robertson GA, and January CT. Properties of HERG channels stably expressed in HEK 293 cells studied at physiological temperature. Biophys J 74: 230-241, 1998.