Calcium‐induced calcium release in proximity to hair cell BK channels revealed by PKA activation

Abstract Large‐conductance calcium‐activated potassium (BK) channels play a critical role in electrical resonance, a mechanism of frequency selectivity in chicken hair cells. We determine that BK currents are dependent on inward flow of Ca2+, and intracellular buffering of Ca2+. Entry of Ca2+ is fur...

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Main Authors: Jun‐ping Bai, Na Xue, Omolara Lawal, Anda Nyati, Joseph Santos‐Sacchi, Dhasakumar Navaratnam
Format: Article
Language:English
Published: Wiley 2020-08-01
Series:Physiological Reports
Subjects:
Online Access:https://doi.org/10.14814/phy2.14449
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spelling doaj-12ce0286fa1b4ce595b1307512ed881a2020-11-25T03:40:02ZengWileyPhysiological Reports2051-817X2020-08-01815n/an/a10.14814/phy2.14449Calcium‐induced calcium release in proximity to hair cell BK channels revealed by PKA activationJun‐ping Bai0Na Xue1Omolara Lawal2Anda Nyati3Joseph Santos‐Sacchi4Dhasakumar Navaratnam5Department of Neurology Yale School of Medicine New Haven CT USADepartment of Otolaryngology‐Head and Neck Surgery Shanghai Ninth People's HospitalShanghai Jiaotong University School of Medicine Shanghai ChinaDepartment of Neurology Yale School of Medicine New Haven CT USAUndergraduate Program Johns Hopkins University Baltimore MD USADepartment of Surgery Yale School of Medicine New Haven CT USADepartment of Neurology Yale School of Medicine New Haven CT USAAbstract Large‐conductance calcium‐activated potassium (BK) channels play a critical role in electrical resonance, a mechanism of frequency selectivity in chicken hair cells. We determine that BK currents are dependent on inward flow of Ca2+, and intracellular buffering of Ca2+. Entry of Ca2+ is further amplified locally by calcium‐induced Ca2+ release (CICR) in close proximity to plasma membrane BK channels. Ca2+ imaging reveals peripheral clusters of high concentrations of Ca2+ that are suprathreshold to that needed to activate BK channels. Protein kinase A (PKA) activation increases the size of BK currents likely by recruiting more BK channels due to spatial spread of high Ca2+ concentrations in turn from increasing CICR. STORM imaging confirms the presence of nanodomains with ryanodine and IP3 receptors in close proximity to the Slo subunit of BK channels. Together, these data require a rethinking of how electrical resonance is brought about and suggest effects of CICR in synaptic release. Both genders were included in this study.https://doi.org/10.14814/phy2.14449BK channelsCICRHair CellSTORM imaging
collection DOAJ
language English
format Article
sources DOAJ
author Jun‐ping Bai
Na Xue
Omolara Lawal
Anda Nyati
Joseph Santos‐Sacchi
Dhasakumar Navaratnam
spellingShingle Jun‐ping Bai
Na Xue
Omolara Lawal
Anda Nyati
Joseph Santos‐Sacchi
Dhasakumar Navaratnam
Calcium‐induced calcium release in proximity to hair cell BK channels revealed by PKA activation
Physiological Reports
BK channels
CICR
Hair Cell
STORM imaging
author_facet Jun‐ping Bai
Na Xue
Omolara Lawal
Anda Nyati
Joseph Santos‐Sacchi
Dhasakumar Navaratnam
author_sort Jun‐ping Bai
title Calcium‐induced calcium release in proximity to hair cell BK channels revealed by PKA activation
title_short Calcium‐induced calcium release in proximity to hair cell BK channels revealed by PKA activation
title_full Calcium‐induced calcium release in proximity to hair cell BK channels revealed by PKA activation
title_fullStr Calcium‐induced calcium release in proximity to hair cell BK channels revealed by PKA activation
title_full_unstemmed Calcium‐induced calcium release in proximity to hair cell BK channels revealed by PKA activation
title_sort calcium‐induced calcium release in proximity to hair cell bk channels revealed by pka activation
publisher Wiley
series Physiological Reports
issn 2051-817X
publishDate 2020-08-01
description Abstract Large‐conductance calcium‐activated potassium (BK) channels play a critical role in electrical resonance, a mechanism of frequency selectivity in chicken hair cells. We determine that BK currents are dependent on inward flow of Ca2+, and intracellular buffering of Ca2+. Entry of Ca2+ is further amplified locally by calcium‐induced Ca2+ release (CICR) in close proximity to plasma membrane BK channels. Ca2+ imaging reveals peripheral clusters of high concentrations of Ca2+ that are suprathreshold to that needed to activate BK channels. Protein kinase A (PKA) activation increases the size of BK currents likely by recruiting more BK channels due to spatial spread of high Ca2+ concentrations in turn from increasing CICR. STORM imaging confirms the presence of nanodomains with ryanodine and IP3 receptors in close proximity to the Slo subunit of BK channels. Together, these data require a rethinking of how electrical resonance is brought about and suggest effects of CICR in synaptic release. Both genders were included in this study.
topic BK channels
CICR
Hair Cell
STORM imaging
url https://doi.org/10.14814/phy2.14449
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AT naxue calciuminducedcalciumreleaseinproximitytohaircellbkchannelsrevealedbypkaactivation
AT omolaralawal calciuminducedcalciumreleaseinproximitytohaircellbkchannelsrevealedbypkaactivation
AT andanyati calciuminducedcalciumreleaseinproximitytohaircellbkchannelsrevealedbypkaactivation
AT josephsantossacchi calciuminducedcalciumreleaseinproximitytohaircellbkchannelsrevealedbypkaactivation
AT dhasakumarnavaratnam calciuminducedcalciumreleaseinproximitytohaircellbkchannelsrevealedbypkaactivation
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