β1-subunit–induced structural rearrangements of the Ca 2+ - and voltage-activated K + (BK) channel

Large-conductance Ca 2+ - and voltage-activated K + (BK) channels play many physiological roles, ranging from the maintenance of smooth muscle tone to the modulation of alcohol tolerance. In most cases, this physiological versatility of the BK channel is due to the association of the pore-forming α-...

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Published inProceedings of the National Academy of Sciences - PNAS Vol. 113; no. 23
Main Authors Castillo, Juan P., Sánchez-Rodríguez, Jorge E., Hyde, H. Clark, Zaelzer, Cristian A., Aguayo, Daniel, Sepúlveda, Romina V., Luk, Louis Y. P., Kent, Stephen B. H., Gonzalez-Nilo, Fernando D., Bezanilla, Francisco, Latorre, Ramón
Format Journal Article
LanguageEnglish
Published 07.06.2016
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Abstract Large-conductance Ca 2+ - and voltage-activated K + (BK) channels play many physiological roles, ranging from the maintenance of smooth muscle tone to the modulation of alcohol tolerance. In most cases, this physiological versatility of the BK channel is due to the association of the pore-forming α-subunit with β-subunits. Therefore, it is of importance to know what the structural consequences of this association are. Here, using lanthanide-based resonance energy transfer, we were able to determine the extracellular position of transmembrane segments S0–S2 with and without the β1-subunit and the position of the two transmembrane segments of the β1 subunit in the α/β1-subunit complex. We concluded that β1 produces rearrangements of the BK voltage sensor domain. Large-conductance Ca 2+ - and voltage-activated K + (BK) channels are involved in a large variety of physiological processes. Regulatory β-subunits are one of the mechanisms responsible for creating BK channel diversity fundamental to the adequate function of many tissues. However, little is known about the structure of its voltage sensor domain. Here, we present the external architectural details of BK channels using lanthanide-based resonance energy transfer (LRET). We used a genetically encoded lanthanide-binding tag (LBT) to bind terbium as a LRET donor and a fluorophore-labeled iberiotoxin as the LRET acceptor for measurements of distances within the BK channel structure in a living cell. By introducing LBTs in the extracellular region of the α- or β1-subunit, we determined ( i ) a basic extracellular map of the BK channel, ( ii ) β1-subunit–induced rearrangements of the voltage sensor in α-subunits, and ( iii ) the relative position of the β1-subunit within the α/β1-subunit complex.
AbstractList Large-conductance Ca 2+ - and voltage-activated K + (BK) channels play many physiological roles, ranging from the maintenance of smooth muscle tone to the modulation of alcohol tolerance. In most cases, this physiological versatility of the BK channel is due to the association of the pore-forming α-subunit with β-subunits. Therefore, it is of importance to know what the structural consequences of this association are. Here, using lanthanide-based resonance energy transfer, we were able to determine the extracellular position of transmembrane segments S0–S2 with and without the β1-subunit and the position of the two transmembrane segments of the β1 subunit in the α/β1-subunit complex. We concluded that β1 produces rearrangements of the BK voltage sensor domain. Large-conductance Ca 2+ - and voltage-activated K + (BK) channels are involved in a large variety of physiological processes. Regulatory β-subunits are one of the mechanisms responsible for creating BK channel diversity fundamental to the adequate function of many tissues. However, little is known about the structure of its voltage sensor domain. Here, we present the external architectural details of BK channels using lanthanide-based resonance energy transfer (LRET). We used a genetically encoded lanthanide-binding tag (LBT) to bind terbium as a LRET donor and a fluorophore-labeled iberiotoxin as the LRET acceptor for measurements of distances within the BK channel structure in a living cell. By introducing LBTs in the extracellular region of the α- or β1-subunit, we determined ( i ) a basic extracellular map of the BK channel, ( ii ) β1-subunit–induced rearrangements of the voltage sensor in α-subunits, and ( iii ) the relative position of the β1-subunit within the α/β1-subunit complex.
Author Hyde, H. Clark
Sánchez-Rodríguez, Jorge E.
Kent, Stephen B. H.
Sepúlveda, Romina V.
Bezanilla, Francisco
Latorre, Ramón
Zaelzer, Cristian A.
Aguayo, Daniel
Luk, Louis Y. P.
Gonzalez-Nilo, Fernando D.
Castillo, Juan P.
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  givenname: Romina V.
  surname: Sepúlveda
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  organization: Universidad Andrés Bello, Center for Bioinformatics and Integrative Biology, Facultad de Ciencias Biológicas, Santiago 8370146, Chile
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  givenname: Louis Y. P.
  surname: Luk
  fullname: Luk, Louis Y. P.
  organization: Department of Chemistry, University of Chicago, Chicago, IL 60637
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  givenname: Stephen B. H.
  surname: Kent
  fullname: Kent, Stephen B. H.
  organization: Department of Biochemistry and Molecular Biology, University of Chicago, Chicago, IL 60637;, Department of Chemistry, University of Chicago, Chicago, IL 60637
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  givenname: Fernando D.
  surname: Gonzalez-Nilo
  fullname: Gonzalez-Nilo, Fernando D.
  organization: Centro Interdisciplinario de Neurociencias de Valparaíso, Facultad de Ciencias, Universidad de Valparaíso, Valparaiso 2360103, Chile;, Universidad Andrés Bello, Center for Bioinformatics and Integrative Biology, Facultad de Ciencias Biológicas, Santiago 8370146, Chile
– sequence: 10
  givenname: Francisco
  surname: Bezanilla
  fullname: Bezanilla, Francisco
  organization: Centro Interdisciplinario de Neurociencias de Valparaíso, Facultad de Ciencias, Universidad de Valparaíso, Valparaiso 2360103, Chile;, Department of Biochemistry and Molecular Biology, University of Chicago, Chicago, IL 60637
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  givenname: Ramón
  surname: Latorre
  fullname: Latorre, Ramón
  organization: Centro Interdisciplinario de Neurociencias de Valparaíso, Facultad de Ciencias, Universidad de Valparaíso, Valparaiso 2360103, Chile
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Snippet Large-conductance Ca 2+ - and voltage-activated K + (BK) channels play many physiological roles, ranging from the maintenance of smooth muscle tone to the...
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Title β1-subunit–induced structural rearrangements of the Ca 2+ - and voltage-activated K + (BK) channel
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