Cardiolipin binding enhances KcsA channel gating via both its specific and dianion-monoanion interchangeable sites
Summary: KcsA is a potassium channel with a plethora of structural and functional information, but its activity in the KcsA-producing actinomycete membranes remains elusive. To determine lipid species involved in channel-modulation, a surface plasmon resonance (SPR)-based methodology, characterized...
| Main Authors: | , , , , , |
|---|---|
| Format: | Article |
| Language: | English |
| Published: |
Elsevier
2023-12-01
|
| Series: | iScience |
| Subjects: | |
| Online Access: | http://www.sciencedirect.com/science/article/pii/S2589004223025488 |
| _version_ | 1797388771395633152 |
|---|---|
| author | Masayuki Iwamoto Masayuki Morito Shigetoshi Oiki Yudai Nishitani Daisuke Yamamoto Nobuaki Matsumori |
| author_facet | Masayuki Iwamoto Masayuki Morito Shigetoshi Oiki Yudai Nishitani Daisuke Yamamoto Nobuaki Matsumori |
| author_sort | Masayuki Iwamoto |
| collection | DOAJ |
| description | Summary: KcsA is a potassium channel with a plethora of structural and functional information, but its activity in the KcsA-producing actinomycete membranes remains elusive. To determine lipid species involved in channel-modulation, a surface plasmon resonance (SPR)-based methodology, characterized by immobilization of membrane proteins under a membrane environment, was applied. Dianionic cardiolipin (CL) showed extremely higher affinity for KcsA than monoanionic lipids. The SPR experiments further demonstrated that CL bound not only to the N-terminal M0 helix, a lipid-sensor domain, but to the M0 helix-deleted mutant. In contrast, monoanionic lipids interacted primarily with the M0 helix. This indicates the presence of an alternative CL-binding site, plausibly in the transmembrane domain. Single-channel recordings demonstrated that CL enhanced channel opening in an M0-independent manner. Taken together, the action of monoanionic lipids is exclusively mediated by the M0 helix, while CL binds both the M0 helix and its specific site, further enhancing the channel activity. |
| first_indexed | 2024-03-08T22:45:38Z |
| format | Article |
| id | doaj.art-d15636ac956e4f708caf31747d51e325 |
| institution | Directory Open Access Journal |
| issn | 2589-0042 |
| language | English |
| last_indexed | 2024-03-08T22:45:38Z |
| publishDate | 2023-12-01 |
| publisher | Elsevier |
| record_format | Article |
| series | iScience |
| spelling | doaj.art-d15636ac956e4f708caf31747d51e3252023-12-17T06:40:55ZengElsevieriScience2589-00422023-12-012612108471Cardiolipin binding enhances KcsA channel gating via both its specific and dianion-monoanion interchangeable sitesMasayuki Iwamoto0Masayuki Morito1Shigetoshi Oiki2Yudai Nishitani3Daisuke Yamamoto4Nobuaki Matsumori5Department of Molecular Neuroscience, Faculty of Medical Sciences, University of Fukui, Fukui 910-1193, Japan; Corresponding authorDepartment of Chemistry, Graduate School of Science, Kyushu University, Fukuoka 819-0395 JapanBiomedial Imaging Research Center, University of Fukui, Fukui 910-1193, JapanDepartment of Applied Physics, Faculty of Science, Fukuoka University, Fukuoka 814-0180, JapanDepartment of Applied Physics, Faculty of Science, Fukuoka University, Fukuoka 814-0180, JapanDepartment of Chemistry, Graduate School of Science, Kyushu University, Fukuoka 819-0395 Japan; Corresponding authorSummary: KcsA is a potassium channel with a plethora of structural and functional information, but its activity in the KcsA-producing actinomycete membranes remains elusive. To determine lipid species involved in channel-modulation, a surface plasmon resonance (SPR)-based methodology, characterized by immobilization of membrane proteins under a membrane environment, was applied. Dianionic cardiolipin (CL) showed extremely higher affinity for KcsA than monoanionic lipids. The SPR experiments further demonstrated that CL bound not only to the N-terminal M0 helix, a lipid-sensor domain, but to the M0 helix-deleted mutant. In contrast, monoanionic lipids interacted primarily with the M0 helix. This indicates the presence of an alternative CL-binding site, plausibly in the transmembrane domain. Single-channel recordings demonstrated that CL enhanced channel opening in an M0-independent manner. Taken together, the action of monoanionic lipids is exclusively mediated by the M0 helix, while CL binds both the M0 helix and its specific site, further enhancing the channel activity.http://www.sciencedirect.com/science/article/pii/S2589004223025488Biological sciencesBiochemistryMembrane architecture |
| spellingShingle | Masayuki Iwamoto Masayuki Morito Shigetoshi Oiki Yudai Nishitani Daisuke Yamamoto Nobuaki Matsumori Cardiolipin binding enhances KcsA channel gating via both its specific and dianion-monoanion interchangeable sites iScience Biological sciences Biochemistry Membrane architecture |
| title | Cardiolipin binding enhances KcsA channel gating via both its specific and dianion-monoanion interchangeable sites |
| title_full | Cardiolipin binding enhances KcsA channel gating via both its specific and dianion-monoanion interchangeable sites |
| title_fullStr | Cardiolipin binding enhances KcsA channel gating via both its specific and dianion-monoanion interchangeable sites |
| title_full_unstemmed | Cardiolipin binding enhances KcsA channel gating via both its specific and dianion-monoanion interchangeable sites |
| title_short | Cardiolipin binding enhances KcsA channel gating via both its specific and dianion-monoanion interchangeable sites |
| title_sort | cardiolipin binding enhances kcsa channel gating via both its specific and dianion monoanion interchangeable sites |
| topic | Biological sciences Biochemistry Membrane architecture |
| url | http://www.sciencedirect.com/science/article/pii/S2589004223025488 |
| work_keys_str_mv | AT masayukiiwamoto cardiolipinbindingenhanceskcsachannelgatingviabothitsspecificanddianionmonoanioninterchangeablesites AT masayukimorito cardiolipinbindingenhanceskcsachannelgatingviabothitsspecificanddianionmonoanioninterchangeablesites AT shigetoshioiki cardiolipinbindingenhanceskcsachannelgatingviabothitsspecificanddianionmonoanioninterchangeablesites AT yudainishitani cardiolipinbindingenhanceskcsachannelgatingviabothitsspecificanddianionmonoanioninterchangeablesites AT daisukeyamamoto cardiolipinbindingenhanceskcsachannelgatingviabothitsspecificanddianionmonoanioninterchangeablesites AT nobuakimatsumori cardiolipinbindingenhanceskcsachannelgatingviabothitsspecificanddianionmonoanioninterchangeablesites |