Differential regulation of action potentials by inactivating and noninactivating BK channels in rat adrenal chromaffin cells

Biophysical Journal

Volumn 97, Issue 7, 2009, Pages 1832-1842

  Sun, Liang ^a   Xiong, Yu ^a   Zeng, Xuhui ^b   Wu, Ying ^a   Pan, Na ^a   Lingle, Christopher J ^b   Qu, Anlian ^a   Ding, Jiuping ^a  

^a HUAZHONG UNIVERSITY OF SCIENCE AND TECHNOLOGY   (China)

^b WASHINGTON UNIVERSITY SCHOOL OF MEDICINE   (United States)

Author keywords

[No Author keywords available]

Indexed keywords

BKI CHANNEL; BKS CHANNEL; CALCIUM; LARGE CONDUCTANCE CALCIUM ACTIVATED POTASSIUM CHANNEL; UNCLASSIFIED DRUG;

ACTION POTENTIAL; AFTERHYPERPOLARIZATION; ANIMAL CELL; ARTICLE; CHROMAFFIN CELL; CONTROLLED STUDY; CYTOSOL; HYPERPOLARIZATION; MATHEMATICAL MODEL; MEMBRANE POTENTIAL; NONHUMAN; POTASSIUM CURRENT; RAT; REGULATORY MECHANISM; SIGNAL TRANSDUCTION; SODIUM CURRENT;

RATTUS;

ACTION POTENTIALS; ADRENAL MEDULLA; ANIMALS; CALCIUM; CELL MEMBRANE; CHROMAFFIN CELLS; CYTOSOL; ELECTRIC CONDUCTIVITY; KINETICS; LARGE-CONDUCTANCE CALCIUM-ACTIVATED POTASSIUM CHANNELS; MODELS, BIOLOGICAL; POTASSIUM CHANNELS, VOLTAGE-GATED; RATS; SODIUM;

EID: 70350006755     PISSN: 00063495     EISSN: 15420086     Source Type: Journal    
DOI: 10.1016/j.bpj.2009.06.042     Document Type: Article

References (57)

1. Saito, M., C. Nelson, L. Salkoff, and C. J. Lingle. 1997. A cysteine-rich domain defined by a novel exon in a slo variant in rat adrenal chromaffin cells and PC12 cells. J. Biol. Chem. 272:11710-11717.
2. Dworetzky, S. I., J. T. Trojnacki, and V. K. Gribkoff. 1994. Cloning and expression of a human large-conductance calcium-activated potassium channel. Brain Res. Mol. Brain Res. 27:189-193.
3. Tseng-Crank, J., J. A. Yao, M. F. Berman, and G. N. Tseng. 1993. Functional role of the NH2-terminal cytoplasmic domain of a mammalian A-type K channel. J. Gen. Physiol. 102:1057-1083.
4. Orio, P., P. Rojas, G. Ferreira, and R. Latorre. 2002. New disguises for an old channel: MaxiK channel b-subunits. News Physiol. Sci. 17:156-161.
5. Salkoff, L., A. Butler, G. Ferreira, C. Santi, and A. Wei. 2006. Highconductance potassium channels of the SLO family. Nat. Rev. Neurosci. 7:921-931.
6. + signaling. Science. 314:615-620.
7. 2+ entry in anterior pituitary cells. J. Neurosci. 21:5902-5915.
8. + (BK) channel inactivation contributes to spike broadening during repetitive firing in the rat lateral amygdala. J. Physiol. 552:483-497.
9. + current in rat adrenal chromaffin cells. J. Neurosci. 15:6110-6123.
10. Lovell, P. V., and D. P. McCobb. 2001. Pituitary control of BK potassium channel function and intrinsic firing properties of adrenal chromaffin cells. J. Neurosci. 21:3429-3442.
11. + channel inactivation: a comparative study between pancreatic islet β-cells and adrenal chromaffin cells in rat. J. Physiol. 548:191-202.
12. Zhou, Z., and S. Misler. 1995. Action potential-induced quantal secretion of catecholamines from rat adrenal chromaffin cells. J. Biol. Chem. 270:3498-3505.
13. Duan, K., X. Yu, C. Zhang, and Z. Zhou. 2003. Control of secretion by temporal patterns of action potentials in adrenal chromaffin cells. J. Neurosci. 23:11235-11243. (Pubitemid 37548960)
14. Lovell, P. V., J. T. King, and D. P. McCobb. 2004. Acute modulation of adrenal chromaffin cell BK channel gating and cell excitability by glucocorticoids. J. Neurophysiol. 91:561-570.
15. Lingle, C. J., C. R. Solaro, M. Prakriya, and J. P. Ding. 1996. Calcium-activated potassium channels in adrenal chromaffin cells. Ion Channels. 4:261-301.
16. Inoue, M., K. Harada, H. Matsuoka, T. Sata, and A. Warashina. 2008. Inhibition of TASK1-like channels by muscarinic receptor stimulation in rat adrenal medullary cells. J. Neurochem. 106:1804-1814.
17. Fenwick, E. M., A. Marty, and E. Neher. 1982. Sodium and calcium channels in bovine chromaffin cells. J. Physiol. 331:599-635.
18. 2+ channels in rat chromaffin cells. J. Neurophysiol. 81:2267-2278.
19. Marty, A., and E. Neher. 1985. Potassium channels in cultured bovine adrenal chromaffin cells. J. Physiol. 367:117-141. (Pubitemid 16195382)
20. + channel in rat PC12 cells by hypoxia. J. Physiol. 502:293-305.
21. + channels: role of the Kv1.2-subunit in mediating the hypoxic response. J. Physiol. 524:783-793.
22. Neely, A., and C. J. Lingle. 1992. Two components of calcium-activated potassium current in rat adrenal chromaffin cells. J. Physiol. 453:97-131.
23. + channels in cultured rat adrenal chromaffin cells. J. Physiol. 481:555-570.
24. Ding, J. P., Z. W. Li, and C. J. Lingle. 1998. Inactivating BK channels in rat chromaffin cells may arise from heteromultimeric assembly of distinct inactivation-competent and noninactivating subunits. Biophys. J. 74:268-289.
25. Wei, A., C. Solaro, C. Lingle, and L. Salkoff. 1994. Calcium sensitivity of BK-type KCa channels determined by a separable domain. Neuron. 13:671-681. (Pubitemid 24300171)
26. 2+- and voltage-dependent BK channels in adrenal chromaffin cells and rat insulinoma tumor cells. J. Neurosci. 19:5255-5264.
27. + current during mAChR activation in rat adrenal chromaffin cells. J. Physiol. 485:297-318.
28. 2+ from intracellular stores in rat chromaffin cells. J. Neurosci. 16:4344-4359.
29. Morgan, K., E. B. Stevens, B. Shah, P. J. Cox, A. K. Dixon, et al. 2000. β3: an additional auxiliary subunit of the voltage-sensitive sodium channel that modulates channel gating with distinct kinetics. Proc. Natl. Acad. Sci. USA. 97:2308-2313.
30. + channels must deactivate to recover from inactivation. Neuron. 12:819-829.
31. + currents and depolarizes neonatal rat adrenal chromaffin cells. J. Physiol. 512:421-434.
32. + channels in immortalised rat chromaffincell- derived MAH cells. J. Physiol. 545:807-818.
33. Steidl, J. V., and A. J. Yool. 1999. Differential sensitivity of voltage-gated potassium channels Kv1.5 and Kv1.2 to acidic pH and molecular identification of pH sensor. Mol. Pharmacol. 55:812-820.
34. + channels, types Kv1.1, 1.2, 1.3, 1.5, and 3.1, stably expressed in mammalian cell lines. Mol. Pharmacol. 45:1227-1234.
35. Rezazadeh, S., H. T. Kurata, T. W. Claydon, S. J. Kehl, and D. Fedida. 2007. An activation gating switch in Kv1.2 is localized to a threonine residue in the S2-S3 linker. Biophys. J. 93:4173-4186. (Pubitemid 350294466)
36. Neshatian, L., Y. M. Leung, Y. Kang, X. Gao, H. Xie, et al. 2007. Distinct modulation of Kv1.2 channel gating by wild type, but not open form, of syntaxin-1A. Am. J. Physiol. Gastrointest. Liver Physiol. 292:G1233-G1242.
37. 2+ channels. J. Neurophysiol. 84:1123-1135.
38. Bournaud, R., J. Hidalgo, H. Yu, E. Jaimovich, and T. Shimahara. 2001. Low threshold T-type calcium current in rat embryonic chromaffin cells. J. Physiol. 537:35-44. (Pubitemid 33076952)
39. 2+ channels in hippocampal mossy fiber boutons. J. Neurosci. 27:13420-13429.
40. 2+ and BK channels underlies functional coupling in rat brain. J. Cell Sci. 120:985-995.
41. 2+ channels in hippocampal neurons. Nature. 395:900-905.
42. Berkefeld, H., and B. Fakler. 2008. Repolarizing responses of BKCa-Cav complexes are distinctly shaped by their Cav subunits. J. Neurosci. 28:8238-8245.
43. Marcantoni, A., P. Baldelli, J. M. Hernandez-Guijo, V. Comunanza, V. Carabelli, et al. 2007. L-type calcium channels in adrenal chromaffin cells: role in pace-making and secretion. Cell Calcium. 42:397-408. (Pubitemid 47264008)
44. Beeler, G. W., and H. Reuter. 1977. Reconstruction of the action potential of ventricular myocardial fibres. J. Physiol. 268:177-210. (Pubitemid 8115094)
45. + channels. J. Neurosci. 22:1550-1561.
46. 2+ binding and channel opening in large conductance (BK) potassium channels. J. Gen. Physiol. 120:267-305.
47. + channel. J. Gen. Physiol. 110:257-281.
48. Ding, J., and C. Lingle. 2002. Steady-state and closed-state inactivation properties of inactivating BK channels. Biophys. J. 82:2448-2465. (Pubitemid 34441284)
49. Zeng, X.-H., X.-M. Xia, and C. J. Lingle. 2003. Redox-sensitive extracellular gates formed by auxiliary β subunits of calcium-activated potassium channels. Nat. Struct. Biol. 10:448-454.
50. Lingle, C. J., X.-H. Zeng, J.-P. Ding, and X.-M. Xia. 2001. Inactivation of BK channels mediated by the N-terminus of the β3b auxiliary subunit involves a two-step mechanism: possible separation of binding and blockade. J. Gen. Physiol. 117:583-605.
51. Solaro, C. R., J. P. Ding, Z. W. Li, and C. J. Lingle. 1997. The cytosolic inactivation domains of BKi channels in rat chromaffin cells do not behave like simple, open-channel blockers. Biophys. J. 73:819-830.
52. Benzinger, G. R., X. M. Xia, and C. J. Lingle. 2006. Direct observation of a preinactivated, open state in BK channels with β2 subunits. J. Gen. Physiol. 127:119-131.
53. + channels: a transmembrane β-subunit homolog. Proc. Natl. Acad. Sci. USA. 96:4137-4142.
54. 2+ signal for phasic transmitter release at the rat calyx of Held. J. Physiol. 547:665-689.
55. Wu, Y. C., and R. Fettiplace. 1996. A development model for generating frequency maps in the reptilian and avian cochleas. Biophys. J. 70:2557-2570.
56. + channels in spike broadening during repetitive firing in rat hippocampal pyramidal cells. J. Physiol. 521:135-146.
57. Zeng, X. H., X. M. Xia, and C. J. Lingle. 2005. Divalent cation sensitivity of BK channel activation supports the existence of three distinct binding sites. J. Gen. Physiol. 125:273-286.