TRIC-B channels display labile gating: evidence from the TRIC-A knockout mouse model

Elisa Venturi, Antoni W Matyjaszkiewicz, Samantha J Pitt, Krasimira Tsaneva-Atanasova, Miyuki Nishi, Daiju Yamazaki, Hiroshi Takeshima, Rebecca Sitsapesan

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Abstract

Sarcoplasmic/endoplasmic reticulum (SR) and nuclear membranes contain two related cation channels named TRIC-A and TRIC-B. In many tissues, both subtypes are co-expressed, making it impossible to distinguish the distinct single-channel properties of each subtype. We therefore incorporated skeletal muscle SR vesicles derived from Tric-a-knockout mice into bilayers in order to characterise the biophysical properties of native TRIC-B without possible misclassification of the channels as TRIC-A, and without potential distortion of functional properties by detergent purification protocols. The native TRIC-B channels were ideally selective for cations. In symmetrical 210 mM K+, the maximum (full) open channel level (199 pS) was equivalent to that observed when wild-type SR vesicles were incorporated into bilayers. Analysis of TRIC-B gating revealed complex and variable behaviour. Four main sub-conductance levels were observed at approximately 80 % (161 pS), 60 % (123 pS), 46 % (93 pS), and 30 % (60 pS) of the full open state. Seventy-five percent of the channels were voltage sensitive with Po being markedly reduced at negative holding potentials. The frequent, rapid transitions between TRIC-B sub-conductance states prevented development of reliable gating models using conventional single-channel analysis. Instead, we used mean-variance plots to highlight key features of TRIC-B gating in a more accurate and visually useful manner. Our study provides the first biophysical characterisation of native TRIC-B channels and indicates that this channel would be suited to provide counter current in response to Ca2+ release from the SR. Further experiments are required to distinguish the distinct functional properties of TRIC-A and TRIC-B and understand their individual but complementary physiological roles.
Original languageEnglish
Pages (from-to)1135-1148
JournalPflügers Archiv: European Journal of Physiology
Volume465
DOIs
Publication statusPublished - Aug 2013

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Venturi, E., Matyjaszkiewicz, A. W., Pitt, S. J., Tsaneva-Atanasova, K., Nishi, M., Yamazaki, D., Takeshima, H., & Sitsapesan, R. (2013). TRIC-B channels display labile gating: evidence from the TRIC-A knockout mouse model. Pflügers Archiv: European Journal of Physiology, 465, 1135-1148. https://doi.org/10.1007/s00424-013-1251-y