Role of the transverse-axial tubule system in generating calcium sparks and calcium transients in rat atrial myocytes

Malcolm M. Kirk, Leighton T Izu, Ye Chen-Izu, Stacey L. McCulle, W. Gil Wier, C. William Balke, Stephen R. Shorofsky

Research output: Contribution to journalArticle

77 Citations (Scopus)

Abstract

Cardiac atrial cells lack a regular system of transverse tubules like that in cardiac ventricular cells. Nevertheless, many atrial cells do possess an irregular internal transverse-axial tubular system (TATS). To investigate the possible role of the TATS in excitation-contraction coupling in atrial myocytes, we visualized the TATS (labelled with the fluorescent indicator, Di-8-ANEPPS) simultaneously with Ca2+ transients and/or Ca2+ sparks (fluo-4). In confocal transverse linescan images of field-stimulated cells, whole-cell Ca2+ transients had two morphologies: 'U-shaped' transients and irregular or 'W-shaped' transients with a varying number of points of origin of the Ca2+ transient. About half (54%, n =289 cells, 13 animals) of the cells had a TATS. Cells with TATS had a larger mean diameter (13.2 ± 2.8 μm) than cells without TATS (11.7 ± 2.0 μm) and were more common in the left atrium (n = 206 cells; left atrium: 76 with TATS, 30 without TATS; right atrium: 42 with TATS, 58 without TATS). Simultaneous measurement of Ca2+ sparks and sarcolemmal structures showed that cells without TATS had U-shaped transients that started at the cell periphery, and cells with TATS had W-shaped transients that began simultaneously at the cell periphery and the TATS. Most (82 out of 102 from 31 cells) 'spontaneous' (non-depolarized) Ca2+ sparks occurred within 1 μm of a sarcolemmal structure (cell periphery or TATS), and 33% occurred within 1 pixel (0.125 μm). We conclude that the presence of a sarcolemmal membrane either at the cell periphery or in the TATS in close apposition to the sarcoplasmic reticulum is required for the initiation of an evoked Ca2+ transient and for spontaneous Ca2+ sparks.

Original languageEnglish (US)
Pages (from-to)441-451
Number of pages11
JournalJournal of Physiology
Volume547
Issue number2
DOIs
StatePublished - Mar 1 2003
Externally publishedYes

Fingerprint

Calcium Signaling
Muscle Cells
Calcium
Heart Atria
Excitation Contraction Coupling
Sarcoplasmic Reticulum

ASJC Scopus subject areas

  • Physiology

Cite this

Role of the transverse-axial tubule system in generating calcium sparks and calcium transients in rat atrial myocytes. / Kirk, Malcolm M.; Izu, Leighton T; Chen-Izu, Ye; McCulle, Stacey L.; Gil Wier, W.; Balke, C. William; Shorofsky, Stephen R.

In: Journal of Physiology, Vol. 547, No. 2, 01.03.2003, p. 441-451.

Research output: Contribution to journalArticle

Kirk, Malcolm M. ; Izu, Leighton T ; Chen-Izu, Ye ; McCulle, Stacey L. ; Gil Wier, W. ; Balke, C. William ; Shorofsky, Stephen R. / Role of the transverse-axial tubule system in generating calcium sparks and calcium transients in rat atrial myocytes. In: Journal of Physiology. 2003 ; Vol. 547, No. 2. pp. 441-451.
@article{6a5056a543314e928527d9e40dd52944,
title = "Role of the transverse-axial tubule system in generating calcium sparks and calcium transients in rat atrial myocytes",
abstract = "Cardiac atrial cells lack a regular system of transverse tubules like that in cardiac ventricular cells. Nevertheless, many atrial cells do possess an irregular internal transverse-axial tubular system (TATS). To investigate the possible role of the TATS in excitation-contraction coupling in atrial myocytes, we visualized the TATS (labelled with the fluorescent indicator, Di-8-ANEPPS) simultaneously with Ca2+ transients and/or Ca2+ sparks (fluo-4). In confocal transverse linescan images of field-stimulated cells, whole-cell Ca2+ transients had two morphologies: 'U-shaped' transients and irregular or 'W-shaped' transients with a varying number of points of origin of the Ca2+ transient. About half (54{\%}, n =289 cells, 13 animals) of the cells had a TATS. Cells with TATS had a larger mean diameter (13.2 ± 2.8 μm) than cells without TATS (11.7 ± 2.0 μm) and were more common in the left atrium (n = 206 cells; left atrium: 76 with TATS, 30 without TATS; right atrium: 42 with TATS, 58 without TATS). Simultaneous measurement of Ca2+ sparks and sarcolemmal structures showed that cells without TATS had U-shaped transients that started at the cell periphery, and cells with TATS had W-shaped transients that began simultaneously at the cell periphery and the TATS. Most (82 out of 102 from 31 cells) 'spontaneous' (non-depolarized) Ca2+ sparks occurred within 1 μm of a sarcolemmal structure (cell periphery or TATS), and 33{\%} occurred within 1 pixel (0.125 μm). We conclude that the presence of a sarcolemmal membrane either at the cell periphery or in the TATS in close apposition to the sarcoplasmic reticulum is required for the initiation of an evoked Ca2+ transient and for spontaneous Ca2+ sparks.",
author = "Kirk, {Malcolm M.} and Izu, {Leighton T} and Ye Chen-Izu and McCulle, {Stacey L.} and {Gil Wier}, W. and Balke, {C. William} and Shorofsky, {Stephen R.}",
year = "2003",
month = "3",
day = "1",
doi = "10.1113/jphysiol.2002.034355",
language = "English (US)",
volume = "547",
pages = "441--451",
journal = "Journal of Physiology",
issn = "0022-3751",
publisher = "Wiley-Blackwell",
number = "2",

}

TY - JOUR

T1 - Role of the transverse-axial tubule system in generating calcium sparks and calcium transients in rat atrial myocytes

AU - Kirk, Malcolm M.

AU - Izu, Leighton T

AU - Chen-Izu, Ye

AU - McCulle, Stacey L.

AU - Gil Wier, W.

AU - Balke, C. William

AU - Shorofsky, Stephen R.

PY - 2003/3/1

Y1 - 2003/3/1

N2 - Cardiac atrial cells lack a regular system of transverse tubules like that in cardiac ventricular cells. Nevertheless, many atrial cells do possess an irregular internal transverse-axial tubular system (TATS). To investigate the possible role of the TATS in excitation-contraction coupling in atrial myocytes, we visualized the TATS (labelled with the fluorescent indicator, Di-8-ANEPPS) simultaneously with Ca2+ transients and/or Ca2+ sparks (fluo-4). In confocal transverse linescan images of field-stimulated cells, whole-cell Ca2+ transients had two morphologies: 'U-shaped' transients and irregular or 'W-shaped' transients with a varying number of points of origin of the Ca2+ transient. About half (54%, n =289 cells, 13 animals) of the cells had a TATS. Cells with TATS had a larger mean diameter (13.2 ± 2.8 μm) than cells without TATS (11.7 ± 2.0 μm) and were more common in the left atrium (n = 206 cells; left atrium: 76 with TATS, 30 without TATS; right atrium: 42 with TATS, 58 without TATS). Simultaneous measurement of Ca2+ sparks and sarcolemmal structures showed that cells without TATS had U-shaped transients that started at the cell periphery, and cells with TATS had W-shaped transients that began simultaneously at the cell periphery and the TATS. Most (82 out of 102 from 31 cells) 'spontaneous' (non-depolarized) Ca2+ sparks occurred within 1 μm of a sarcolemmal structure (cell periphery or TATS), and 33% occurred within 1 pixel (0.125 μm). We conclude that the presence of a sarcolemmal membrane either at the cell periphery or in the TATS in close apposition to the sarcoplasmic reticulum is required for the initiation of an evoked Ca2+ transient and for spontaneous Ca2+ sparks.

AB - Cardiac atrial cells lack a regular system of transverse tubules like that in cardiac ventricular cells. Nevertheless, many atrial cells do possess an irregular internal transverse-axial tubular system (TATS). To investigate the possible role of the TATS in excitation-contraction coupling in atrial myocytes, we visualized the TATS (labelled with the fluorescent indicator, Di-8-ANEPPS) simultaneously with Ca2+ transients and/or Ca2+ sparks (fluo-4). In confocal transverse linescan images of field-stimulated cells, whole-cell Ca2+ transients had two morphologies: 'U-shaped' transients and irregular or 'W-shaped' transients with a varying number of points of origin of the Ca2+ transient. About half (54%, n =289 cells, 13 animals) of the cells had a TATS. Cells with TATS had a larger mean diameter (13.2 ± 2.8 μm) than cells without TATS (11.7 ± 2.0 μm) and were more common in the left atrium (n = 206 cells; left atrium: 76 with TATS, 30 without TATS; right atrium: 42 with TATS, 58 without TATS). Simultaneous measurement of Ca2+ sparks and sarcolemmal structures showed that cells without TATS had U-shaped transients that started at the cell periphery, and cells with TATS had W-shaped transients that began simultaneously at the cell periphery and the TATS. Most (82 out of 102 from 31 cells) 'spontaneous' (non-depolarized) Ca2+ sparks occurred within 1 μm of a sarcolemmal structure (cell periphery or TATS), and 33% occurred within 1 pixel (0.125 μm). We conclude that the presence of a sarcolemmal membrane either at the cell periphery or in the TATS in close apposition to the sarcoplasmic reticulum is required for the initiation of an evoked Ca2+ transient and for spontaneous Ca2+ sparks.

UR - http://www.scopus.com/inward/record.url?scp=0037335625&partnerID=8YFLogxK

UR - http://www.scopus.com/inward/citedby.url?scp=0037335625&partnerID=8YFLogxK

U2 - 10.1113/jphysiol.2002.034355

DO - 10.1113/jphysiol.2002.034355

M3 - Article

C2 - 12562899

AN - SCOPUS:0037335625

VL - 547

SP - 441

EP - 451

JO - Journal of Physiology

JF - Journal of Physiology

SN - 0022-3751

IS - 2

ER -